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Taxa-specific activity loss and mortality patterns in freshwater trematode cercariae under subarctic conditions

Published online by Cambridge University Press:  11 November 2021

Ana Born-Torrijos
Affiliation:
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 37005 České Budějovice, Czech Republic
Gabrielle S. van Beest
Affiliation:
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 37005 České Budějovice, Czech Republic Cavanilles Institute for Biodiversity and Evolutionary Biology, Science Park, University of Valencia, P.O. Box 22085, 46071 Valencia, Spain
Tereza Vyhlídalová
Affiliation:
Faculty of Science, University of South Bohemia in České Budějovice, Branišovská 31, 37005 České Budějovice, Czech Republic
Rune Knudsen
Affiliation:
Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, N9037 Tromsø, Norway
Roar Kristoffersen
Affiliation:
Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, N9037 Tromsø, Norway
Per-Arne Amundsen
Affiliation:
Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, N9037 Tromsø, Norway
David W. Thieltges
Affiliation:
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, P.O. Box 59, 1790, AB Den Burg, Texel, The Netherlands
Miroslava Soldánová*
Affiliation:
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 37005 České Budějovice, Czech Republic
*
Author for correspondence: Miroslava Soldánová, E-mail: [email protected]

Abstract

Cercarial activity and survival are crucial traits for the transmission of trematodes. Temperature is particularly important, as faster depletion of limited cercarial energy reserves occurs at high temperatures. Seasonal climate conditions in high latitude regions may be challenging to complete trematode life cycle during the 6-month ice-free period, but temperature effects on the activity and survival of freshwater cercariae have not been previously identified. After experimentally simulating natural subarctic conditions during warmer and colder months (13 and 6°C), a statistical approach identifying changes in the tendency of cercarial activity loss and mortality data was used to detect differences in three trematode genera, represented by four taxa (Diplostomum spp., Apatemon spp., small- and large-sized Plagiorchis spp.). A strong temperature-dependent response was identified in both activity loss and mortality in all taxa, with Diplostomum spp. cercariae showing the most gradual changes compared to other taxa. Furthermore, whilst activity loss and mortality dynamics could not be divided into ‘fish- vs invertebrate-infecting cercariae’ groups, the detected taxa-specific responses in relation to life-history traits indicate the swimming behaviour of cercariae and energy allocation among larvae individuals as the main drivers. Cercariae exploit the short transmission window that allows a stable continuance of trematodes’ life cycles in high-latitude freshwater ecosystems.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Anderson, RM and Whitfield, PJ (1975) Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transversotrema patialense (Soparker, 1924). Parasitology 70, 295310CrossRefGoogle Scholar
Bell, AS (1996) Studies on the Biosystematics and Biology of Strigeids (Digenea) Parasitic in Freshwater Fish (PhD thesis). University of Stirling, Scotland.Google Scholar
Blankespoor, HD (1977) Notes on the biology of Plagiorchis noblei Park, 1936 (Trematoda: Plachiorchiidae). Proceedings of the Helminthological Society of Washington 44, 4450.Google Scholar
Born-Torrijos, A, van Beest, GS, Vyhlídalová, T, Knudsen, R, Kristoffersen, R, Amundsen, PA, Thieltges, DW and Soldánová, M (2021) Born-Torrijos et al. Data survival and activity analyses. figshare. Dataset. https://doi.org/10.6084/m9.figshare.17091161.v1CrossRefGoogle Scholar
Born-Torrijos, A, Paterson, R, van Beest, GS, Vyhlídalová, T, Henriksen, EH, Knudsen, R, Kristoffersen, R, Amundsen, P-A and Soldánová, M (2021) Cercarial behaviour alters the consumer functional response of three-spined sticklebacks. Journal of Animal Ecology 90, 978988.10.1111/1365-2656.13427CrossRefGoogle ScholarPubMed
Brassard, P, Curtis, MA and Rau, ME (1982) Seasonality of Diplostomum spathaceum (Trematoda: Strigeidae) transmission to brook trout (Salvelinus fontinalis) in northern Quebec, Canada. Canadian Journal of Zoology 60, 22582263.CrossRefGoogle Scholar
Chapman, HD (1974) The behaviour of the cercariae of Cryptocotyle lingua. Zeitschrift für Parasitenkunde 44, 211226.CrossRefGoogle ScholarPubMed
Combes, C and Theron, A (1981) Les densites cercariennes. Memoires du Museum National d'Histoire Naturelle, Serie A, Zoologie 119, 186196.Google Scholar
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
Crawley, MJ (2013) Survival analysis. In John Wiley & Sons Ltd (eds), The R Book. Chichester, UK: John Wiley & Sons Ltd, pp. 883893.Google Scholar
Dixon, MD (1984) Strategies of Host Location Employed by Larval Trematodes (PhD thesis), University of York, UK.Google Scholar
Evans, NA (1985) The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269275.10.1017/S0031182000050976CrossRefGoogle Scholar
Evans, NA and Gordon, DM (1983) Experimental studies on the transmission dynamics of cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 87, 167174.CrossRefGoogle Scholar
Fenton, A and Hudson, PJ (2002) Optimal infection strategies: should macroparasites hedge their bets? Oikos 96, 92101.10.1034/j.1600-0706.2002.960110.xCrossRefGoogle Scholar
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Patterns and processes of larval emergence in an estuarine parasite system. Biology Bulletin 205, 110120.CrossRefGoogle 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. Boston, Dordrecht & London: Kluwer Academic.CrossRefGoogle Scholar
Ganna, A, Rivadeneira, F, Hofman, A, Uitterlinden, AG, Magnusson, PKE, Pedersen, NL, Ingelsson, E and Tiemeier, H (2013) Genetic determinants of mortality. Can findings from genome-wide association studies explain variation in human mortality? Human Genetics 132, 553561.CrossRefGoogle ScholarPubMed
Ginetsinskaya, TA (1988) Trematodes, Their Life Cycles, Biology and Evolution. New Delhi: Amerind.Google Scholar
Gorman, AM (1980) Studies on the Biology of Pladiorchis elegans (Rudolphi, 1802), (Trematoda: Digenea) in its Mammalian and Molluscan-Hosts (PhD thesis), University of Leeds, UK.Google Scholar
Haas, W, Beran, B and Loy, C (2008) Selection of the hosts’ habitat by cercariae: from laboratory to the field. Journal of Parasitology 94, 12331238.CrossRefGoogle Scholar
Hakalahti, T, Karvonen, A and Valtonen, ET (2006) Climate warming and disease risks in temperate regions – Argulus coregoni and Diplostomum spathaceum as case studies. Journal of Helminthology 80, 9398.CrossRefGoogle ScholarPubMed
Halttunen, E, Gjelland, K-Ø, Hamel, S, Serra-Llinares, RM, Nilsen, R, Arechavala-Lopez, P, Skarðhamar, J, Johnsen, IA, Asplin, L, Karlsen, Ø, Bjørn, P-A and Finstad, B (2017) Sea trout adapt their migratory behaviour in response to high salmon lice concentrations. Journal of Fish Diseases 41, 953967.CrossRefGoogle ScholarPubMed
Karvonen, A, Paukku, S, Valtonen, ET and Hudson, PJ (2003) Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217224.CrossRefGoogle ScholarPubMed
Karvonen, A, Kirsi, S, Hudson, PJ and Valtonen, ET (2004) Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129, 8792.10.1017/S0031182004005281CrossRefGoogle ScholarPubMed
Koprivnikar, J, Lim, D, Fu, C and Brack, SHM (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitology Research 106, 11671177.10.1007/s00436-010-1779-0CrossRefGoogle ScholarPubMed
Kudlai, O, Pantoja, C, O'Dwyer, K, Jouet, D, Skírnisson, K and Faltýnková, A (2021) Diversity of Plagiorchis (Trematoda: Digenea) in high latitudes: species composition and snail host spectrum revealed by integrative taxonomy. Journal of Zoological Systematics and Evolutionary Research 59, 937962.CrossRefGoogle Scholar
Kutz, SJ, Jenkins, EJ, Veitch, AM, Ducrocq, J, Polley, L, Elkin, B and Lair, S (2009) The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host-parasite interactions. Veterinary Parasitology 163, 217228.CrossRefGoogle ScholarPubMed
Lawson, JR and Wilson, RA (1980) The survival of the cercariae of Schistosoma mansoni in relation to water temperature and glycogen utilization. Parasitology 81, 337348.CrossRefGoogle ScholarPubMed
Lo, CT and Lee, KM (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82, 347350.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Lyholt, HCK and Buchmann, K (1996) Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms 25, 169173.CrossRefGoogle Scholar
Mas-Coma, S, Valero, MA and Bargues, MD (2009) Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Veterinary Parasitology 163, 264280.CrossRefGoogle ScholarPubMed
McCarthy, AM (1999 a) Photoperiodic cercarial emergence patterns of the digeneans Echinoparyphium recurvatum and Plagiorchis sp. from a mixed infection in Lymnaea peregra. Journal of Helminthology 73, 5962.CrossRefGoogle Scholar
McCarthy, AM (1999 b) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383388.CrossRefGoogle Scholar
Morley, NJ (2011) Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 14421452.CrossRefGoogle Scholar
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 719.CrossRefGoogle Scholar
Morley, NJ (2020) Cercarial swimming performance and its potential role as a key variable of trematode transmission. Parasitology 147, 13691374.CrossRefGoogle ScholarPubMed
Mouritsen, KN (2002) The Hydrobia ulvaeMaritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76, 341347.CrossRefGoogle ScholarPubMed
Muñoz-Antolí, C, Trelis, M, Espert, A, Toledo, R and Esteban, JG (2002) Survival and infectivity of Echinostoma friedi (Trematoda: Echinostomatidae) miracidia and cercariae under experimental conditions. Helminthologia 39, 149154.Google Scholar
Nikolaev, KE, Levakin, IA and Galaktionov, KV (2020) Seasonal dynamics of trematode infection in the first and the second intermediate hosts: a long-term study at the subarctic marine intertidal. Journal of Sea Research 164, 101931.CrossRefGoogle Scholar
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
Pietrock, M and Marcogliese, DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.CrossRefGoogle ScholarPubMed
Poulin, R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143151.CrossRefGoogle ScholarPubMed
Prokofiev, VV (1999) Influence of temperature and salinity on a life span of cercariae of marine littoral trematodes Cryptocotyle sp. (Heterophyidae), Levinseniella brachysoma and Maritrema subdolum (Microphallidae). Parazitologiya 33, 520526 (in Russian).Google Scholar
Prokofiev, VV (2001) Influence of temperature and salinity on a life span of cercariae of marine littoral trematodes Podocotyle atomon (Opecoealidae) and Renicola thaidus (Renicolidae). Parazitologiya 35, 6976 (in Russian).Google Scholar
Prokofiev, VV, Galaktionov, KV and Levakin, IA (2016) Patterns of parasite transmission in polar seas: daily rhythms of cercarial emergence from intertidal snails. Journal of Sea Research 113, 8598.CrossRefGoogle Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.r-project.org/.Google 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
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
Selbach, C and Poulin, R (2020) Some like it hotter: trematode transmission under changing temperature conditions. Oecologia 194, 745755.CrossRefGoogle ScholarPubMed
Soldánová, M, Georgieva, S, Roháčová, J, Knudsen, R, Kuhn, JA, Henriksen, EH, Siwertsson, A, Shaw, JC, Kuris, AM, Amundsen, P-A, Scholz, T, Laffety, KD and Kostadinova, A (2017) Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology 47, 327345.CrossRefGoogle Scholar
Studer, A and Poulin, R (2013) Cercarial survival in an intertidal trematode: a multifactorial experiment with temperature, salinity and ultraviolet radiation. Parasitology Research 112, 243249.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Studer, A, Thieltges, DW and Poulin, R (2010) Parasites and global warming: net effects of temperature on an intertidal host–parasite system. Marine Ecology Progress Series 415, 1122.CrossRefGoogle Scholar
Therneau, T (2020) A package for survival analysis in R. R package version 3.1-11. Available at https://CRAN.R-project.org/package=survival.Google Scholar
Thieltges, DW and Reise, K (2007) Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150, 569581.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
van Beest, GS, Villar-Torres, M, Raga, JA, Montero, FE and Born-Torrijos, A (2019). In vivo fluorescent cercariae reveal the entry portals of Cardiocephaloides longicollis (Rudolphi, 1819) Dubois, 1982 (Strigeidae) into the gilthead seabream Sparus aurata L. Parasites & Vectors 12, 92.CrossRefGoogle ScholarPubMed
Whitfield, PJ, Anderson, RM and Bundy, DAP (1977) Experimental investigations on the cercariae of an ectoparasitic digenean Transversotrema patialense: general activity patterns. Parasitology 75, 730.CrossRefGoogle ScholarPubMed
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