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Parasites in space and time: a novel method to assess and illustrate host-searching behaviour of trematode cercariae

Published online by Cambridge University Press:  05 March 2018

Christian Selbach*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
Robert Poulin
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
Author for correspondence: Christian Selbach, E-mail: [email protected]

Abstract

The transmission from one host to another constitutes a challenging obstacle for parasites and is a key determinant of their fitness. Due to their complex life histories involving several different hosts, the free-living dispersal stages (cercariae) of digenean trematodes show a huge diversity in morphology and behaviour. On a finer scale, we still have an extremely limited understanding of the inter- and intraspecific variation in transmission strategies of many trematode species. Here, we present a novel method to study the movement patterns of cercariae of four New Zealand trematode species (Coitocaecum parvum, Maritrema poulini, Apatemon sp. and Aporocotylid sp. I.) via automated video tracking. This approach allows to quantify parameters otherwise not measurable and clearly illustrates the individual strategies of parasites to search for their respective target hosts. Cercariae that seek out an evasive fish target hosts showed higher swimming speeds (acceleration and velocity) and travelled further distances, compared with species searching for high-density crustacean hosts. Automated video tracking provides a powerful tool for such detailed analyses of parasites’ host-searching strategies and can enhance our understanding of complex host–parasite interactions, ranging from parasite community structure to the transmission of potential disease agents.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Combes, C, Fournier, A, Moné, H and Théron, A (1994) Behaviours in trematode cercariae that enhance parasite transmission: Patterns and processes. Parasitology 109, S3S13.Google Scholar
Cribb, TH, Bray, RA, Olson, PD and Littlewood, DTJ (2003) Life cycle evolution in the digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197254.Google Scholar
Esch, GW, Barger, MA and Fellis, KJ (2002) The transmission of digenetic trematodes: style, elegance, complexity. Integrative and Comparative Biology 42, 304312.Google Scholar
Feiler, W and Haas, W (1988) Host-finding in Trichobilharzia ocellata cercariae: swimming and attachment to the host. Parasitology 96, 493505.Google Scholar
Fenwick, GD (2001) The freshwater amphipoda (Crustacea) of New Zealand: A review. Journal of the Royal Society of New Zealand 31, 341363.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.Google Scholar
Friesen, OC, Poulin, R and Lagrue, C (2017) Differential impacts of shared parasites on fitness components among competing hosts. Ecology and Evolution 7, 46824693.Google Scholar
Galaktionov, KV and Dobrovolskij, AA (2003) The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Dordrecht: Kluwer.Google Scholar
Haas, W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349364.Google Scholar
Haas, W, Beran, B and Loy, C (2008) Selection of the host's habitat by cercariae: from laboratory experiments to the field. Journal of Parasitology 94, 12331238.Google Scholar
Hammer, Ø, Harper, DAT and Ryan, PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 19.Google Scholar
Hannon, ER, Calhoun, DM, Chadalawada, S and Johnson, PTJ (2017) Circadian rhythms of trematode parasites: applying mixed models to test underlying patterns. Parasitology 19. doi: 10.1017/S0031182017001706.Google Scholar
Hechinger, RF (2012) Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa 27, 127.Google Scholar
Kalbe, M, Haberl, B and Haas, W (1997) Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates released from the host snails. Parasitology Research 83, 806812.Google Scholar
Koehler, AV, Brown, B, Poulin, R, Thieltges, DW and Fredensborg, BL (2012) Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evolutionary Ecology 26, 14971512.Google Scholar
Krishnamurthy, D, Katsikis, G, Bhargava, A and Prakash, M (2016) Schistosoma mansoni cercariae swim efficiently by exploiting an elastohydrodynamic coupling. Nature Physics 13, 266271.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 and Lafferty, KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515518.Google Scholar
Lagrue, C and Poulin, R (2015) Spatial covariation of local abundance among different parasite species: the effect of shared hosts. Parasitology Research 114, 36373643.Google Scholar
Lowenberger, CA and Rau, ME (1994) Plagiorchis elegans: emergence, longevity and infectivity of cercariae, and host behavioural modifications during cercarial emergence. Parasitology 109, 6572.Google Scholar
McCarthy, HO, Fitzpatrick, S and Irwin, SWB (2002) Life history and life cycles: production and behavior of trematode cercariae in relation to host exploitation and next-host characteristics. The Journal of Parasitology 88, 910918.Google Scholar
Morley, NJ (2011) Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 14421452.Google Scholar
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 719.Google Scholar
Morley, NJ, Lewis, JW and Hoole, D (2006) Pollutant-induced effects on immunological and physiological interactions in aquatic host–trematode systems: implications for parasite transmission. Journal of Helminthology 80, 137149.Google Scholar
Mouritsen, KN (2001) Hitch-hiking parasite: a dark horse may be the real rider. International Journal for Parasitology 31, 14171420.Google Scholar
Noldus, LPJJ, Spink, AJ and Tegelenbosch, RAJ (2001) Ethovision: a versatile video tracking system for automation of behavioral experiments. Behavior Research Methods, Instruments, & Computers 33, 398414.Google Scholar
Pietrock, M and Marcogliese, DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.Google Scholar
Platt, TR, Burnside, L and Bush, E (2008) The role of light and gravity in the experimental transmission of Echinostoma caproni (Digenea: Echinostomatidae) cercariae to the second intermediate host, Biomphalaria glabrata (Gastropoda: Pulmonata). Journal of Parasitology 95, 512516.Google Scholar
Poulin, R (1998) Evolutionary Ecology of Parasites: From Individuals to Communities. London: Chapman and Hall.Google Scholar
Poulin, R (2011) The many roads to parasitism. Advances in Parasitology 74, 140.Google Scholar
Poulin, R and Lagrue, C (2015) The ups and downs of life: population expansion and bottlenecks of helminth parasites through their complex life cycle. Parasitology 142, 791799.Google Scholar
Presswell, B, Blasco-Costa, I and Kostadinova, A (2014) Two new species of Maritrema Nicoll, 1907 (Digenea: Microphallidae) from New Zealand: morphological and molecular characterisation. Parasitology Research 113, 16411656.Google Scholar
Preston, DL, Orlofske, SA, Lambden, JP and Johnson, PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. Journal of Animal Ecology 82, 509517.Google Scholar
Santos, MJ, Karvonen, A, Pedrot, JC, Faltýnková, A, Seppälä, O and Valtonen, ET (2007) Qualitative and quantitative behavioral traits in a community of furcocercariae trematodes: tools for species separation? Journal of Parasitology 93, 13191323.Google Scholar
Soldánová, M, Selbach, C and Sures, B (2016) The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS ONE 11, e0149678.Google Scholar
Studer, A and Poulin, R (2014) Analysis of trait mean and variability versus temperature in trematode cercariae: is there scope for adaptation to global warming? International Journal for Parasitology 44, 403413.Google Scholar
Thieltges, DW and Rick, J (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 6368.Google Scholar
Thieltges, DW, Jensen, KT and Poulin, R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407426.Google Scholar
Thieltges, DW, Amundsen, PA, Hechinger, RF, Johnson, PT, Lafferty, KD, Mouritsen, KN, Preston, DL, Reise, K, Zander, CD and Poulin, R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122, 14731482.Google Scholar
Thomas, F, Adamo, S and Moore, J (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.Google Scholar
Winterbourn, M (1973) Larval trematoda parasitising the New Zealand species of Potamopyrgus (Gastropoda: Hydrobiidae). Mauri Ora 2, 1730.Google Scholar