Hostname: page-component-77c89778f8-rkxrd Total loading time: 0 Render date: 2024-07-19T16:19:28.683Z Has data issue: false hasContentIssue false

No time to relax: Age-dependent infectivity of cercariae in marine coastal ecosystems

Published online by Cambridge University Press:  22 December 2023

Kirill E. Nikolaev*
Affiliation:
White Sea Biological Station, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
Daniil D. Fedorov
Affiliation:
Laboratory for the Study of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
Anna A. Vinogradova
Affiliation:
Laboratory for the Study of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
Ivan A. Levakin
Affiliation:
Laboratory for the Study of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
Kirill V. Galaktionov
Affiliation:
Laboratory for the Study of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia
*
Corresponding author: Kirill E. Nikolaev; Email: kirill.nicolaev@gmail.com

Abstract

Age dynamics of the ability of cercariae of two digenean species, Himasthla elongata (Himasthlidae) and Renicola parvicaudatus (Renicolidae), to infect the second intermediate host (SIH), mussels (Mytilus edulis), was investigated experimentally. This is the first study of this kind made on cercariae transmitted in the intertidal of the northern seas. The larvae of all tested ages (from 0.5 to 6 hr) were equally successful in infecting mussels. This finding disagrees with the literature data on cercariae of several freshwater digeneans, which are practically incapable of infecting the SIH during the first 1–3 hr of life. The presence of a time delay before the attainment of the maximum infectivity (TDMI) may be associated with the need for physiological maturation of cercariae in the very beginning of their life in the environment, the need for their broad dispersion, and the prevention of superinfection of the downstream host. The absence of TDMI in the cercariae examined in our study could be associated with the instability of environmental factors in the marine intertidal (wave impact, tidal currents). These factors promote a broad dispersion of cercariae in the intertidal biotope and prevent superinfection of potential SIHs. Biological and behavioural features may also play a role. We hypothesize that the presence or absence of TDMI does not depend on the taxonomic affiliation of the cercariae but is determined by the transmission conditions.

Type
Short Communication
Copyright
© The Author(s), 2023. 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

Alberson, NR, Rosser, TG, King, DT, Woodyard, ET, Khoo, LH, Baumgartner, WA, Wise, DJ, Pote, LM, Cunningham, FL and Griffin, MJ (2022) Experimental elucidation of the life cycle of Drepanocephalus spathans (Digenea: Echinostomatidae) with notes on the morphological plasticity of D. spathans in the United States. Journal of Parasitology 108, 141158. https://doi.org/10.1645/19-157CrossRefGoogle ScholarPubMed
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. https://doi.org/10.1017/S0031182000052082Google Scholar
Anderson, RM, Whitfield, PJ and Mills, CA (1977) An experimental study of the population dynamics of an ectoparasitic digenean, Transversotrema patialense: The cercarial and adult stages. Journal of Animal Ecology 46, 555580. https://www.semanticscholar.org/paper/An-Experimental-Study-of-the-Population-Dynamics-of-Anderson-Whitfield/47360b57c575774d6e0d93301c5560e8ccec3a4e.Google Scholar
Ataev, GL (2010) The influence of Echinostoma caproni metacercariae (Trematoda) on the survival of Biomphalaria molluscs (Pulmonata). Parazitologiya 44(6), 481495 (in Russian). https://pubmed.ncbi.nlm.nih.gov/21427957/.Google Scholar
Beaver, PC (1941) Studies on the life history of Euparyphium melis (Trematoda: Echinostomidae). Journal of Parasitology 27, 3544. https://www.semanticscholar.org/paper/Studies-on-the-Life-History-of-Euparyphium-melis-Beaver/66bf789e9bd6457e3ad485459a94edc03b2b0866.CrossRefGoogle Scholar
Born-Torrijos, A, van Beest, GS, Vyhlidalova, T, Knudsen, R, Kristoffersen, R, Amundsen, P- A, Thieltges, DW and Soldanova, M (2022) Taxa-specific activity loss and mortality patterns in freshwater trematode cercariae under subarctic conditions. Parasitology 149, 457468. https://doi.org/10.1017/S0031182021002006CrossRefGoogle 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. https://doi.org/10.1017/S0031182000085048CrossRefGoogle ScholarPubMed
de Montaudouin, X, Wegeberg, 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. https://www.int-res.com/articles/dao/34/d034p063.pdf.CrossRefGoogle Scholar
de Montaudouin, X, Blanchet, H, Desclaux-Marchand, C, Lavesque, N and Bachelet, G (2016) Cockle infection by Himasthla quissetensis − I. From cercariae emergence to metacercariae infection. Journal of Sea Research 113, 99107. https://doi.org/10.1016/j.seares.2015.02.008CrossRefGoogle Scholar
Evans, NA and Gordon, DM (1983) Experimental studies on the transmission dynamics of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 87, 167174. https://doi.org/10.1017/S0031182000052513CrossRefGoogle Scholar
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Larval swimming overpowers turbulent mixing and facilitates transmission of marine parasite. Ecology 84, 25022515. https://doi.org/10.1890/02-4035CrossRefGoogle Scholar
Fried, B, Idris, N and Ohsawa, T (1995) Experimental infection of juvenile Biomphalaria glabrata with cercariae of Echinostoma trivolvis. Journal of Parasitology 81, 308310. https://doi.org/10.2307/3283941CrossRefGoogle ScholarPubMed
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.Google Scholar
Galaktionov, KV, Solovyeva, AI and Miroliubov, A (2021) Elucidation of Himasthla leptosoma (Creplin, 1829) Dietz, 1909 (Digenea, Himasthlidae) life cycle with insights into species composition of the north Atlantic Himasthla associated with periwinkles Littorina spp. Parasitology Research 120, 16491668. https://doi.org/10.1007/s00436-021-07117-8Google Scholar
Galaktionov, KV, Solovyeva, AI, Blakeslee, AMH and Skirnisson, K (2023) Overview of renicolid digeneans (Digenea, Renicolidae) from marine gulls of northern Holarctic with remarks on their species statuses, phylogeny and phylogeography. Parasitology 150, 5577. https://doi.org/10.1017/S0031182022001500CrossRefGoogle Scholar
Ginetsinskaya, TA (1968) Trematodes, Their Life Cycles, Biology and Evolution. Leningrad: Nauka. (in Russian) (Translated in 1988 by Amerind Publ Co Pvt Ltd, New Delhi)Google Scholar
Haas, W (2003) Parasitic worms: Strategies of host finding, recognition and invasion. Zoology 106, 349364. https://doi.org/10.1078/0944-2006-00125CrossRefGoogle ScholarPubMed
Karvonen, A, Paukku, S, Valtonen, ET and Hudson, PJ (2003) Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217224. https://doi.org/10.1017/S0031182003003561CrossRefGoogle ScholarPubMed
Kostadinova, A (2005) Family Echinostomatidae Looss, 1899. In Jones, A, Bray, RA and Gibson, DI (eds), Keys to the Trematoda , Vol. 2. Oxford, UK: CABI Publishing, 964.CrossRefGoogle Scholar
Kulatchkova, VG (1985) Parasites of blue mussels – the aquaculture object in the White Sea. In Lukanin, VV (ed), Investigation of the Blue Mussel of the White Sea. Zoological Institute, Leningrad, 8897 (in Russian).Google Scholar
Kuris, AM and Warren, J (1980) Echinostome cercarial penetration and metacercarial encystment as mortality factors for a second intermediate host, Biomphalaria glabrata. Journal of Parasitology 66, 630635. https://doi.org/10.1645/GE-321RCrossRefGoogle ScholarPubMed
Lafferty, KD and Kuris, AM (2005) Parasitism and environmental disturbances. In Thomas, F, Renaud, F and Guégan, J-F (eds), Parasitism and Ecosystems. Oxford: Oxford University Press, 113123.CrossRefGoogle Scholar
Lauckner, G (1983) Diseases of Mollusca: Bivalvia. In Kinne, O (ed), Diseases of Marine Animals . Vol. 2. Hamburg: Biologishe Anstalt Helgoland, 632961.Google Scholar
Levakin, IA, Losev, EA, Nikolaev, КE and Galaktionov, KV (2013) In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the hemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. Journal of Helminthology 87, 180188. https://doi.org/10.1017/S0022149X1200017XGoogle Scholar
Lezin, PA, Agat’eva, NA and Khalaman, VV (2006) A comparative study of the pumping activity of some fouling animals from the White Sea. Russian Journal of Marine Biology 32, 245249. https://doi.org/10.1134/S1063074006040079Google Scholar
Lo, CT and Cross, JH (1975) Obsevations on the host–parasite relations between Echinostoma revolutum and lymnaeid snails. Chinese Journal of Microbiology 8, 241252. https://www.semanticscholar.org/paper/Observations-on-the-host-parasite-relations-between-Lo-Cross/74f9638116fb450054a87bdf8b2f666a11c82d0d.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. https://doi.org/10.1017/s0031182000077775CrossRefGoogle ScholarPubMed
Malek, EA (1977) Geographical distribution, hosts, and biology of Schistosomatium douthitti (Cort, 1914) Price, 1931. Canadian Journal of Zoology 55, 661671. https://doi.org/10.1139/z77-087Google Scholar
Marcogliese, DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 13311352. https://doi.org/10.1139/cjz-79-8-1331CrossRefGoogle Scholar
McCarthy, AM (1999) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383388. https://doi.org/10.1017/s003118209900400xCrossRefGoogle ScholarPubMed
Miller, HM Jr and McCoy, OR (1930) An experimental study of the behavior of Cercaria floridensis in relation to its fish intermediate host. Journal of Parasitology 16, 185197. https://doi.org/10.2307/3271513Google Scholar
Morley, NJ (2011). Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 14421452. https://doi.org/10.1017/S0031182011001272CrossRefGoogle Scholar
Muñoz-Antoli, 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. https://www.researchgate.net/publication/239588603_Survival_and_infectivity_of_Echinostoma_friedi_Trematoda_Echinostomatidae_miracidia_and_cercariae_under_experimental_conditions.Google Scholar
Nikolaev, KE, Prokofiev, VV, Levakin, IA and Galaktionov, KV (2017) How the position of mussels at the intertidal lagoon affects their infection with the larvae of parasitic flatworms (Trematoda: Digenea): A combined laboratory and field experimental study. Journal of Sea Research 128, 3240. https://doi.org/10.1016/j.seares.2017.07.010CrossRefGoogle Scholar
Paller, VGV, Kimura, D and Uga, S (2007) Infection dynamics of Centrocestus armatus cercariae (Digenea: Heterophyidae) to second intermediate fish hosts. Journal of Parasitology 93, 436439. https://doi.org/10.1645/GE-997R.1Google 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. https://doi.org/10.1017/S0031182000081920CrossRefGoogle Scholar
Pekkarinen, M (1987) The cercaria of Lacunovermis macomae (Lebour, 1908) (Trematoda: Gymnophallidae), and its penetration into the bivalve Macoma balthica (L.) in experimental conditions. Annales Zoologici Fennici 24, 101121. https://www.jstor.org/stable/23734457Google Scholar
Pietrock, M and Marcogliese, DJ (2003) Free-living endohelminth stages: At the mercy of environmental conditions. Trends in Parasitology 19, 293299. https://doi.org/10.1016/S1471-4922(03)00117-XCrossRefGoogle ScholarPubMed
Prokofiev, VV (2002) Vertical migration of cercariae of the littoral trematode Renicola thaidus (Trematoda: Renicolidae) in the water layer. Parazitologiya 36(4), 314321 (in Russian). https://www.researchgate.net/publication/11116068_Vertical_migration_of_cercariae_of_the_littoral_trematode_Renicola_thaidus_Trematoda_Renicolidae_in_the_water_layer.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. https://doi.org/10.1016/j.seares.2015.07.007Google Scholar
Radev, V, Kanev, I, Hrusanov, D and Fried, B (2009) Reexamination of the life cycle of Isthmiophora melis (Trematoda: Echinostomatidae) on material from Southeast Europe). Parazitologiya 43(6), 445453 (in Russian). https://pubmed.ncbi.nlm.nih.gov/20198963/.Google ScholarPubMed
Sokal, RR and Rohlf, FJ (1995) Biometry: The Principles and Practice in Statistics in Biological Researches. 3rd edn. New York: WH Freeman and company.Google Scholar
Stirewalt, MA and Fregeau, WA (1968) Effect of selected experimental conditions on penetration and maturation of cercariae of Schistosoma mansoni in mice. II. Parasite-related conditions. Experimental Parasitology 22, 7395. https://doi.org/10.1016/0014-4894(68)90081-7Google Scholar
Stunkard, HW and Shaw, CR (1931) The effect of dilution of sea water on the activity and longevity of certain marine cercariae, with descriptions of two new species. The Biological Bulletin 61, 242271. https://www.journals.uchicago.edu/doi/10.2307/1537015.Google Scholar
Thieltges, DW (2006) Effect of infection by the metacercarial trematoda Renicola roscovita on growth in intertidal blue mussel Mytilus edulis. Marine Ecology Progress Series 319, 129134. https://www.jstor.org/stable/24870782.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. https://doi.org/10.3354/dao073063Google ScholarPubMed
Tkach, VV, Kudlai, O and Kostadinova, A. (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology 46, 171185. https://doi.org/10.1016/j.ijpara.2015.11.001CrossRefGoogle ScholarPubMed
Toledo, R, Munoz-Antoli, C, Perez, M and Esteban, JG (1999) Survival and infectivity of Hypoderaeum conoideum and Euparyphium albuferensis cercariae under laboratory conditions. Journal of Helminthology 73, 177182. https://pubmed.ncbi.nlm.nih.gov/10431379/.CrossRefGoogle ScholarPubMed
Underwood, AJ (1997) Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge: Cambridge University PressGoogle Scholar
Werding, B (1969) Morphologie, entwicklung und ökologie digener trematoden-larven der strandschpecke Littorina littorea. Marine Biology 3, 306333. https://doi.org/10.1007/BF00698861CrossRefGoogle Scholar
Wetzel, EJ and Esch, GW (1995) Effect of age on infectivity of cercariae of Halipegus occidualis (Digenea: Hemiuridae) to their second intermediate host. Invertebrate Biology 114, 205210. https://doi.org/10.2307/3226875Google Scholar
Whitfield, PJ, Bartlett, A, Khammo, N and Clothier, RH (2003) Age-dependent survival and infectivity of Schistosoma mansoni cercariae. Parasitology 127, 2935. https://doi.org/10.1017/s0031182003003263CrossRefGoogle ScholarPubMed
Zimmer, RK, Fingerut, JT and Zimmer, CA (2009) Dispersal pathways, seed rains, and the dynamics of larval behavior. Ecology 90, 19331947. https://www.jstor.org/stable/25592702.CrossRefGoogle ScholarPubMed