Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T07:02:26.478Z Has data issue: false hasContentIssue false

Cercarial swimming performance and its potential role as a key variable of trematode transmission

Published online by Cambridge University Press:  14 July 2020

Neil J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
*
Author for correspondence: Neil J. Morley, E-mail: n.morley@rhul.ac.uk

Abstract

Trematode transmission in aquatic habitats from molluscan intermediate host to vertebrate or invertebrate target host is typically undertaken by a free-living stage known as cercariae. Active locomotion by cercariae is a key aspect of the transmission process with the swimming speed potentially contributing to infection success. Individual cercarial species swim at different speeds but the significance of this to infection potential has not been determined. This study, using data from the scientific literature, investigates the role of swimming speed in relation to cercarial morphology, host-searching strategies and target host species. Larger cercariae swim faster than smaller ones with tail length being the principal factor controlling locomotion rates. Different cercarial morphotypes swim at different speeds, in particular, furcocercariae, with the exception of the schistosomes, being faster swimmers than mono-tailed cercariae. Host-searching behaviour has a significant influence on swimming speeds with ‘active-searching’ strategies swimming slower than those adopting ‘active-waiting’ or ‘prey mimcry’ strategies. Vertebrate-infecting cercariae swim faster than those infecting invertebrates with species targeting fish demonstrating the highest locomotion rates and those targeting arthropods the slowest speeds. The adaptions of individual cercarial swimming speeds to biological variables and their interactions with the physical processes of aquatic habitats are discussed.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, RM and Whitfield, PJ (1975) Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transversotrema patialensis (Soparker, 1924). Parasitology 70, 295310.CrossRefGoogle Scholar
Beamish, FWH (1978) Swimming capacity. In Hoar, WS and Randall, DJ (Eds), Fish Physiology, vol. 7. London, UK: Academic Press, pp. 101187.Google Scholar
Berkhout, BW, Lloyd, MM, Poulin, R and Studer, A (2014) Variation among genotypes in response to increasing temperature in a marine parasite: evolutionary potential in the face of global warming? International Journal for Parasitology 44, 10191027.CrossRefGoogle Scholar
Cable, RM (1965) Thereby hangs a tail. Journal of Parasitology 51, 312.CrossRefGoogle ScholarPubMed
Chapman, HD and Wilson, RA (1973) The propulsion of the cercariae of Himasthla secunda (Nicoll) and Cryptocotyle lingua. Parasitology 67, 115.CrossRefGoogle ScholarPubMed
Combes, C, Fournier, A, Mone, H and Theron, A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3S13.CrossRefGoogle ScholarPubMed
Cross, MA, Irwin, SWB and Fitzpatrick, SM (2001) Effects of heavy metal pollution on swimming and longevity in cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 123, 499507.CrossRefGoogle Scholar
Cross, MA, Irwin, SWB and Fitzpatrick, SM (2005) Effects of host habitat quality on the viability of Cryptocotyle lingua (Trematoda: Digenea) cercariae. Parasitology 130, 195201.CrossRefGoogle ScholarPubMed
De Montaudouin, X, Wgeberg, AM, Jensen, KT and Sauriau, PG (1998) Infection characteristics of Himasthla elongata cercariae in cockles as a function of water current. Diseases of Aquatic Organisms 34, 6370.CrossRefGoogle Scholar
Dixon, MD (1984) Strategies of Host Location Employed by Larval Trematodes (PhD thesis). University of York, York, UK.Google Scholar
Faltýnková, A (2005) Larval trematodes (Digenea) in molluscs from small water bodies near České Budějovice, Czech Republic. Acta Parasitologica 50, 4955.Google Scholar
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Larval swimming overpowers turbulent mixing and facilitates transmission of a marine parasite. Ecology 84, 25022515.CrossRefGoogle Scholar
Fitzpatrick, KB, Smith, NF and Cohen, JH (2016) Swimming behavior of marine cercariae: effects of gravity and hydrostatic pressure. Journal of Experimental Marine Biology & Ecology 476, 814.CrossRefGoogle Scholar
Galaktionov, K and Dobrovolskij, A (2003) The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Dordrecht, Holland: Kluwer.CrossRefGoogle Scholar
Haas, W (1969) Reizphysiologische Untersuchungen an cercarien von Diplostomum spathaceum. Zeitschrift fur Vergleichende Physiologie 64, 254287.CrossRefGoogle Scholar
Haas, W (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109, S15S29.CrossRefGoogle ScholarPubMed
Hiblish, TJ, Sasada, K, Eyster, LS and Pechenik, JA (1999) Relationship between rates of swimming and growth in veliger larvae: genetic variance and covariance. Journal of Experimental Marine Biology & Ecology 239, 183193.Google Scholar
Horne, AJ and Goldman, CR (1994) Limnology, 2nd Edn. New York, USA: McGraw-Hill, Inc.Google Scholar
Jewsbury, JM (1985) Effects of water velocity on snails and cercariae. Parasitology Today 1, 116117.CrossRefGoogle ScholarPubMed
Lu, D-B, Wang, T-P, Rudge, JW, Donnelly, CA, Fang, G-R and Webster, JP (2009) Evolution in a multi-host parasite: chronobiological circadian rhythm and population genetics of Schistosoma japonicum cercariae indicates contrasting definitive host reservoirs by habitat. International Journal for Parasitology 39, 15811588.CrossRefGoogle Scholar
Maitland, P (1990) Biology of Fresh Waters, 2nd Edn. Glasgow, UK: Blackie & Son Ltd.Google Scholar
Mikheev, VN, Pasternak, AF, Valtonen, ET and Taskinen, J (2014) Increased ventilation by fish leads to a higher risk of parasitism. Parasites & Vectors 7, 281.CrossRefGoogle ScholarPubMed
Mileikovsky, SA (1973) Speed of active movement of pelagic larvae of marine invertebrates and their ability to regulate their vertical position. Marine Biology 23, 1117.CrossRefGoogle Scholar
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 719.CrossRefGoogle Scholar
Morley, NJ and Lewis, JW (2013) Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140, 12111224.CrossRefGoogle ScholarPubMed
Morley, NJ and Lewis, JW (2017) Thermodynamics of egg production, development and hatching in trematodes. Journal of Helminthology 91, 284294.CrossRefGoogle ScholarPubMed
Nanninga, GB and Berumen, ML (2014) The role of individual variation in marine larval dispersal. Frontiers in Marine Science 1, 71.CrossRefGoogle Scholar
Nguyen, KH, Gemmell, BJ and Rohr, JR (2020) Effects of temperature and viscosity on miracidial and cercarial movement of Schistosoma mansoni: ramifications for disease transmission. International Journal for Parasitology 50, 153159.CrossRefGoogle ScholarPubMed
Pechenik, JA and Fried, B (1995) Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology 111, 373378.CrossRefGoogle Scholar
Peters, RH (1983) The Ecological Implications of Body Size. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Pineda, J and Reyns, N (2018) Larval transport in the coastal zone: biological and physical processes. In Carrier, TJ, Reitzel, AM and Heyland, A (Eds), Evolutionary Ecology of Marine Invertebrate Larvae. Oxford, UK: Oxford University Press, pp. 145163.Google Scholar
Prokofiev, VV (2005) Patterns of swimming of cercariae in some trematode species. Parazitologiya 39, 204220. [In Russian].Google Scholar
Prokofiev, VV and Galaktionov, KV (2009) Strategies of search behaviour in trematode cercariae. Proceedings of the Zoological Institute of the Russian Academy of Sciences 313, 308318. [In Russian].Google Scholar
Rea, JG and Irwin, SWB (1992) The effects of age, temperature, light quality and wavelength on the swimming behaviour of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 105, 131137.CrossRefGoogle Scholar
Rea, JG and Irwin, SWB (1995) The effects of age, temperature and shadow stimuli on activity patterns of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 111, 95101.CrossRefGoogle Scholar
Rea, JG and Irwin, SWB (2001) Fun with flukes: the use of ICT in the study of larval trematode behaviour. Journal of Biological Education 36, 3541.CrossRefGoogle Scholar
Santos, MJ, Karvonen, A, Pedro, JC, Faltynkova, A, Seppala, O and Valtonen, ET (2007) Qualitative and quantitative behavioural traits in a community of furcocercariae trematodes: tools for species separation? Journal of Parasitology 93, 13191323.CrossRefGoogle Scholar
Selbach, C and Poulin, R (2018) Parasites in space and time: a novel method to assess and illustrate host-searching behaviour of trematode cercariae. Parasitology 145, 14691474.CrossRefGoogle ScholarPubMed
Semyenova, SK, Khrisanfova, GG, Korsunenko, AV, Voronin, MV, Beer, SV, Vodvanitskaya, SV, Serbina, EA and Yurlova, NI (2007) Multilocus variation in cercariae, parthenogenetic progeny of different species of the class Trematoda. Doklady Biological Sciences 414, 235238.CrossRefGoogle ScholarPubMed
Soldánová, M, Faltýnková, A, Scholtz, T and Kostadinova, A (2011) Parasites in a man-made landscape: contrasting patterns of trematode flow in a fishpond area in central Europe. Parasitology 138, 789807.CrossRefGoogle Scholar
Stables, JN and Chappell, LH (1986) Diplostomum spathaceum (Rud. 1819): effects of physical factors on the infection of rainbow trout (Salmo gairdneri) by cercariae. Parasitology 93, 7179.CrossRefGoogle ScholarPubMed
Styczynska-Jurewicz, E (1966) Astatic-water bodies as characteristic habitat of some parasites of man and animals. Verhandlungen des Internationalen Vereinigung fur theoretische und angewandte Limnologie 16, 604611.Google Scholar
Upatham, ES (1973) Effect of a waterfall on the infectivity of St. Lucian Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine & Hygiene 67, 884885.CrossRefGoogle ScholarPubMed
Upatham, ES (1974a) Studies on the effects of cercarial concentration and length of exposure on the infection of mice by St Lucian Schistosoma mansoni cercariae in a natural running-water habitat. Parasitology 68, 155159.CrossRefGoogle Scholar
Upatham, ES (1974b) Dispersion of St Lucian Schistosoma mansoni cercariae in natural standing and running waters determined by cercaia counts and mouse exposure. Annals of Tropical Medicine & Parasitology 68, 343352.CrossRefGoogle Scholar
Verber, JL (1967) Lake Currents. Technical Report of the Federal Water Pollution Control Administration. Chicago, USA: Federal Water Pollution Control Administration.Google Scholar
Whyte, SK, Secombes, CJ and Chappell, LH (1991) Studies on the infectivity of Diplostomum spathaceum in rainbow trout (Oncorhynchus mykiss). Journal of Helminthology 65, 169178.CrossRefGoogle Scholar
Young, CM (1995) Behavior and locomotion during the dispersal phase of larval life. In McEdward, L (Ed.), Ecology of Marine Invertebrate larvae. Boca Raton, USA: CRC Press, pp. 249277.Google Scholar
Zdárská, Z (1964) The influence of the biotope on the extensity of invasion of freshwater snails by the larval stages of trematodes in conditions of Czechoslovakia. In Ergens, R and Rysavy, B (Eds), Parasitic Worms and Aquatic Conditions. Prague, Czech Republic: Czechoslovak Academy of Sciences, pp. 6972.Google Scholar
Supplementary material: File

Morley supplementary material

Morley supplementary material 1

Download Morley supplementary material(File)
File 39.4 KB
Supplementary material: File

Morley supplementary material

Morley supplementary material 2

Download Morley supplementary material(File)
File 39.3 KB