Skip to main content
    • Aa
    • Aa

The role of biotic factors in the transmission of free-living endohelminth stages

  • D. W. THIELTGES (a1), K. T. JENSEN (a2) and R. POULIN (a1)

The transmission success of free-living larval stages of endohelminths is generally modulated by a variety of abiotic and biotic environmental factors. Whereas the role of abiotic factors (including anthropogenic pollutants) has been in focus in numerous studies and summarized in reviews, the role of biotic factors has received much less attention. Here, we review the existing body of literature from the fields of parasitology and ecology and recognize 6 different types of biotic factors with the potential to alter larval transmission processes. We found that experimental studies generally indicate strong effects of biotic factors, and the latter emerge as potentially important, underestimated determinants in the transmission ecology of free-living endohelminth stages. This implies that biodiversity, in general, should have significant effects on parasite transmission and population dynamics. These effects are likely to interact with natural abiotic factors and anthropogenic pollutants. Investigating the interplay of abiotic and biotic factors will not only be crucial for a thorough understanding of parasite transmission processes, but will also be a prerequisite to anticipate the effects of climate and other global changes on helminth parasites and their host communities.

Corresponding author
*Corresponding author: Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand. E-mail:
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

M. F. Achinelly , M. V. Micielli and J. J. Garciía (2003). Pre-parasitic juveniles of Strelkovimermis spiculatus Poinar & Camino, 1986 (Nematoda: Mermithidae) predated upon by freshwater copepods (Crustacea: Copepoda). Nematology 5, 885888.

M. A. Barger and B. B. Nickol (1998). Structure of Leptorhynchoides thecatus and Pomphorhynchus bulbocolli (Acanthocephala) eggs in habitat partitioning and transmission. Journal of Parasitology 84, 534537.

P. Bartoli and C.-F. Boudouresque (1997). Transmission failure of parasites (Digenea) in sites colonized by the recently introduced invasive alga Caulerpa taxifolia. Marine Ecology Progress Series 154, 253260.

P. F. Basch and L. Altomar Jr. (1969). Penetration of strigeid cercariae into Chaetogaster limnaei. Transactions of the American Microscopical Society 88, 593595.

J. A. Basualdo , M. L. Ciarmela , P. L. Sarmiento and M. C. Minvielle (2000). Biological activity of Paecilomyces lilacinus genus against Toxocara canis eggs. Parasitology Research 86, 854859.

M. A. Baudena , M. R. Chapman , M. Larsen and T. R. Klei (2000). Efficacy of the nematophagous fungus Duddingtonia flagrans in reducing equine cyathostome larvae on pasture in south Louisiana. Veterinary Parasitology 89, 219230.

L. W. Bone , K. P. Bottjer and S. S. Gill (1985). Trichostrongylus colubriformis: egg lethality due to Bacillus thuringiensis crystal toxin. Experimental Parasitology 60, 314322.

L. W. Bone , K. P. Bottjer and S. S. Gill (1986). Trichostrongylus colubriformis: isolation and characterization of ovicidal activity from Bacillus thuringiensis israelensis. Experimental Parasitology 62, 247253.

L. W. Bone , K. P. Bottjer and S. S. Gill (1987). Alteration of Trichostrongylus colubriformis egg permeability by Bacillus thuringiensis israelensis toxin. Journal of Parasitology 73, 295299.

K. P. Bottjer , L. W. Bone and S. S. Gill (1985). Nematoda: susceptibility of the egg to Bacillus thuringiensis toxins. Experimental Parasitology 60, 239244.

R. P. Bryan (1973). The effects of dung beetle activity on the numbers of parasitic gastrointestinal helminth larvae recovered from pasture samples. Australian Journal of Agricultural Research 24, 161168.

R. P. Bryan (1976). The effect of the dung beetle, Onthophagus gazella, on the ecology of the infective larvae of gastrointestinal nematodes of cattle. Australian Journal of Agricultural Research 27, 567574.

R. P. Bryan and J. D. Kerr (1989). Factors affecting the survival and migration of the free-living stages of gastrointestinal nematode parasites of cattle in Central Queensland. Veterinary Parasitology 30, 315326.

E. Chernin (1968). Interference with the capacity of Schistosoma mansoni miracidia to infect the molluscan host. Journal of Parasitology 54, 509516.

E. Chernin and J. M. Perlstein (1969). Further studies on interference with the host-finding capacity of Schistosoma mansoni miracidia. Journal of Parasitology 55, 500508.

E. Chernin and J. M. Perlstein (1971). Protection of snails against miracidia of Schistosoma mansoni by various aquatic invertebrates. Journal of Parasitology 57, 217219.

M. L. Ciarmela , P. Sanchez Thevenet , H. M. Alvarz , M. C. Minvielle and J. A. Basualdo (2005). Effect of Paecilomyces lilacinus on the viability of oncospheres of Taenia hydatigena. Veterinary Parasitology 131, 6164.

C. Combes and H. Moné (1987). Possible mechanisms of decoy effect in Schistosoma mansoni transmission. International Journal for Parasitology 17, 971975.

A. W. English (1979). The effects of dung beetles (Coleoptera-Scarabaeinae) on the free-living stages of strongylid nematodes of the horse. Australian Veterinary Journal 55, 315321.

N. A. Evans and D. M. Gordon (1983). Experimental observations on the specificity of Echinoparyphium recurvatum toward second intermediate hosts. Zeitschrift fuer Parasitenkunde 69, 217222.

B. O. Fagbemi (1984). The effects of environmental factors on the development, behaviour and survival of Paramphistomum microbothrium miracidia. Veterinary Parasitology 16, 7181.

A. S. Fernández , M. Larsen , P. Nansen , J. Grønvold , S. A. Henriksen and J. Wolstrup (1997). Effect of the nematode-trapping fungus Duddingtonia flagrans on the free-living stages of horse parasitic nematodes: a plot study. Veterinary Parasitology 73, 257266.

J. Fernandez , T. M. Goater and G. W. Esch (1991). Population dynamics of Cheatogaster limnaei limnaei (Oligochaeta) as affected by a trematode parasite in Helisoma anceps (Gastropoda). American Midland Naturalist 125, 195205.

G. T. Fincher (1973). Dung beetles as biological control agents for gastrointestinal parasites of livestock. Journal of Parasitology 59, 396399.

G. T. Fincher (1975). Effects of dung beetle activity on the number of nematode parasites acquired by grazing cattle. Journal of Parasitology 61, 759762.

R. J. Glaudel and F. J. Etges (1973). Toxic effects of freshwater turbellarians on schistosome miracidia. Journal of Parasitology 59, 7476.

J. Grønvold (1987). Field experiment on the ability of earthworms (Lumbricidae) to reduce the transmission of infective larvae of Cooperia oncophora (Trichostrongylidae) from cow pats to grass. Journal of Parasitology 73, 11331137.

J. Grønvold , C. Sommer , P. Hotter and P. Nansen (1992). Reduced splash dispersal of bovine parasitic nematodes from cow pats by the dung beetle Diastellopalpus quinquedens. Journal of Parasitology 78, 845848.

C. D. Harvell , C. E. Mitchell , J. R. Ward , S. Altizer , A. P. Dobson , R. S. Ostfeld and M. D. Samuel (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 21582162.

M. M. Ibrahim (2007). Population dynamics of Chaetogaster limnaei (Oligochaeta: Naididae) in the field populations of freshwater snails and its implications as a potential regulator of trematode larvae community. Parasitology Research 101, 2533.

F. Keesing , R. D. Holt and R. S. Ostfeld (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485498.

J. K. Ketzis , J. Vercruysse , B. E. Stromberg , M. Larsen , S. Athanasiadou and J. G. M. Houdijk (2006). Evaluation of efficacy expectations for novel and non-chemical helminth control strategies in ruminants. Veterinary Parasitology 139, 321335.

R. A. Khan and J. Thulin (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201238.

S. E. Knapp (1964). Relationship of different species of forage to the survival and infectivity of Haemonchus contortus in lambs. Journal of Parasitology 50, 144148.

S. E. Knapp , N. L. Baldwin and P. J. Presidente (1972). Experimental transmission of an isolate of Nosema strigeoideae Hussey 1971 to Fasciola hepatica. Journal of Parasitology 58, 12061207.

M. Krakau , D. W. Thieltges and K. Reise (2006). Native parasites adopt introduced bivalves of the North Sea. Biological Invasions 8, 919925.

K. D. Lafferty (1997). Environmental parasitology: what can parasites tell us about human impact on the environment? Parasitology Today 13, 251255.

K. D. Lafferty , A. P. Dobson and A. M. Kuris (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences, USA 103, 1121111216.

H. Lýsek (1963). Effect of certain soil organisms on the eggs of parasitic roundworms. Nature, London 199, 925.

K. MacKenzie (1999). Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 38, 955959.

K. MacKenzie , H. H. Williams , B. Williams , A. H. McVicar and R. Siddall (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85144.

D. J. Marcogliese (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 13311352.

K. S. McCann (2000). The diversity-stability debate. Nature, London 405, 228233.

J. van der Meer (2006). Metabolic theories in ecology. Trends in Ecology and Evolution 21, 136140.

E. H. Michelson (1964). The protective action of Chaetogaster limnaei on snails exposed to Schistosoma mansoni. Journal of Parasitology 50, 441444.

H. Möller (1987). Pollution and parasitism in the aquatic environment. International Journal for Parasitology 17, 353361.

N. J. Morley and J. W. Lewis (2004). Free-living endohelminths: the influence of multiple factors. Trends in Parasitology 20, 114115.

R. A. Moss and A. Vlasshoff (1993). Effect of herbage species on gastro-intestinal roundworm populations and their distribution. New Zealand Journal of Agricultural Research 36, 371375.

K. N. Mouritsen and R. Poulin (2003). The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135, 131137.

P. Nansen , M. Larsen , A. Roepstorff , J. Grønvold , J. Wolstrup and A. A. Henriksen (1996). Control of Oesophagostomum dentatum and Hyostrongylus rubidus in outdoor-reared pigs by daily feeding with the microfungus Duddingtonia flagrans. Parasitology Research 82, 580584.

J. H. Niezen , W. A. G. Charleston , J. Hodgson , C. M. Miller , T. S. Waghorn and H. A. Robertson (1998). Effect of plant species on the larvae of gastrointestinal nematodes which parasitise sheep. International Journal for Parasitology 28, 791803.

M. J. Novacek and E. E. Cleland (2001). The current biodiversity extinction event: scenarios for mitigation and recovery. Proceedings of the National Academy of Sciences, USA 98, 54665470.

J. Oliver-González (1946). The possible role of the guppy, Lebistes reticulatus, on the biological control of Schistosomiasis mansoni. Science 104, 605.

R. S. Ostfeld and F. Keesing (2000). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722728.

A. F. Pasternak , K. Pulkkinen , V. N. Mikheev , T. Hasu and E. T. Valtonen (1999). Factors affecting abundance of Triaenophorus infection in Cyclops strenuus, and parasite-induced changes in host fitness. International Journal for Parasitology 29, 17931801.

M. Pietrock and D. J. Marcogliese (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.

R. Poulin (1992). Toxic pollution and parasitism in freshwater fish. Parasitology Today 8, 5861.

D. Pramer (1964). Nematode-trapping fungi. Science 144, 382388.

J. K. Rodgers , G. J. Sandlan , S. R. Joyce and D. J. Minchella (2005). Multi-species interactions among a commensal (Chaetogaster limnaei limnaei), a parasite (Schistosoma mansoni), and an aquatic snail host (Biomphalaria glabrata). Journal of Parasitology 91, 709712.

J. Rössner (1981). Einfluss von Regenwürmern auf phytoparasitäre Nematoden. Nematologica 27, 340348.

S. M. Silangwa and A. C. Todd (1964). Vertical migration of trichostrngylid larvae on grasses. Journal of Parasitology 50, 278285.

E. Thébault and M. Loreau (2005). Trophic interactions and the relationship between species diversity and ecosystem stability. American Naturalist 166, E95E114.

C. D. Thomas , A. Cameron , R. E. Green , M. Bakkenes , L. J. Beaumont , Y. C. Collingham , B. F. N. Erasmus , M. F. de Siqueira , A. Grainger , L. Hannah , L. Hughes , B. Huntley , A. S. van Jaarsveld , G. F. Midgley , L. Miles , M. A. Ortega-Huerta , A. T. Peterson , O. L. Phillips and S. E. Williams (2004). Extinction risk from climate change. Nature, London 427, 145148.

G. L. Uglem (1972). The life cycle of Neoechinorhynchus cristatus Lynch, 1936 (Acanthocephala) with notes on the hatching of eggs. Journal of Parasitology 58, 10711074.

G. L. Uglem and O. R. Larson (1969). The life history and larval development of Neoechinorhynchus saginatus Van Cleave and Bangham, 1949 (Acanthocephala: Neoechinorhynchidae). Journal of Parasitology 55, 12121217.

E. S. Upatham (1972). Interference by unsusceptible aquatic animals with the capacity of the miracidia of Schistosoma mansoni Sambon to infect Biomphalaria glabrata (Say) under field-simulated conditions in St. Lucia, West Indies. Journal of Helminthology 46, 277283.

E. S. Upatham and R. F. Sturrock (1973). Field investigations on the effect of other aquatic animals on the infection of Biomphalaria glabrata by Schistosoma mansoni miracidia. Journal of Parasitology 59, 448453.

R. L. Uznanski and B. B. Nickol (1976). Structure and function of the fibrillar coat of Leptorhynchoides thecatus eggs. Journal of Parasitology 62, 569573.

P. M. Vitousek (1994). Beyond global warming: ecology and global change. Ecology 75, 18611876.

M. Voge and M. Graiwer (1964). Development of oncospheres of Hymenolepis diminuta, hatched in vivo and in vitro, in the larvae of Tenebrio molitor. Journal of Parasitology 50, 267270.

T. S. Waghorn , D. M. Leathwick , L.-Y. Chen , R. A. J. Gray and R. A. Skipp (2002). Influence of nematophagous fungi, earthworms and dung burial on development of the free-living stages of Ostertagia (Teladorsagia) circumcincta in New Zealand. Veterinary Parasitology 104, 119129.

P. J. Waller and S. M. Thamsborg (2004). Nematode control in ‘green’ ruminant production systems. Trends in Parasitology 20, 493497.

K. S. Warren and P. A. Peters (1968). Cercariae of Schistosoma mansoni and plants – attempt to penetrate Phaseolus vulgaris and Hedychium coronarium produces a cercaricide. Nature, London 217, 647648.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 9
Total number of PDF views: 43 *
Loading metrics...

Abstract views

Total abstract views: 177 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 28th June 2017. This data will be updated every 24 hours.