Cryptokotyle lühe, 1899 (trematoda: heterophyidae): special characteristics of developmental biology and epizootiology

  • S. Honcharov The National University of Life and Environmental Sciences of Ukraine, 15, Heroyiv Oborony Str., Kyiv, 03041
  • N. Soroka The National University of Life and Environmental Sciences of Ukraine, 15, Heroyiv Oborony Str., Kyiv, 03041
  • A. Dubovyi Department of Molecular Medicine and Pathology, The University of Auckland, 85 Park Road, Auckland, Grafton1023, New Zealand
  • M. Galat The National University of Life and Environmental Sciences of Ukraine, 15, Heroyiv Oborony Str., Kyiv, 03041
Keywords: cryptocotylosis, biohelminth, zoonosis, intermediate hosts, definitive hosts

Abstract

This review presents the scientific studies data on the special characteristics of developmental biology and epizo- otiology of Cryptocotyle trematodes, which belong to Heterophyidae family and pose a threat to the health of the endotherms, including humans, i.e., it is a typical zoonosis. These trematodes are predominantly widespread in the Mediterranean region, namely, in the western Mediterranean region and the Aegean province. The trematodes of Cryptocotyle genus are found in Europe, Asia, North and South America, and Antarctica. They are typical bio- helminths, i.e., they have a complicated life cycle, where the initial intermediate hosts are mollusks, the second ones – fish of different species, the definitive and final hosts are piscivorous birds, carnivorous animals (foxes, wolves, dogs, cats, etc.), and humans. Cryptocotylosis is remarkable for its seasonal prevalence, which depends on the climatic zoning of territories. For instance, in the territorial waters of Ukraine, the highest indices of crypto- cotylosis invasion among Agonidae fish are mainly observed in summer and autumn, but the peak of the invasion comes in autumn. The parasitizing of Cryptocotyle trematodes in the organism of mollusks impacts the reproduc- tion ability and behavioral specificities (motility) of the latter. The invaded fish have black pigment spots on the surface of their bodies – these are metacercariae. In the organism of definitive hosts, the agent is localized in the gastrointestinal tract and may cause inflammatory processes in the mucous membrane of the intestines and changes in parenchymatous organs, which demonstrates the toxic effect of the parasite on the host organism. The diagnos- tics of cryptocotylosis is based on detecting the agent in the host organism and its further taxonomic identification by its anatomic and morphological specificities. The pollution of the aqueous medium with organic and inorganic residues impacts the organisms of both hosts and parasites.

References

Babbott FL, Frye WW, Gordon JE (1961) Intestinal parasites of man in Arctic Greenland. Amer J Trop Med Hygiene 10:185–190. https://doi.org/10.4269/ajtmh.1961.10.185.

Bakke TA (1972) Studies of the helminth fauna of Norway XXII: The common gull, Larus canus L., as final host for Digenea (Platyhelminthes). I. The ecology of the common gull and the infection in relation to season and the gulls habitat. Norw J Zool 20:165–188.

Benjamin LR, James BL (1987) The development of the metacercaria of Maritrema linguilla Jäg., 1908 (Digenea: Microphallidae) in the intermediate host, Ligia oceanica (L.). Parasitology 94(2):221–231. https://doi.org/10.1017/S0031182000053907.

Borges JN, Skov J, Bahlool QZM, Møller OS, Kania PW, Santos CP, Buchmann K (2015) Viability of Cryptocotyle lingua metacercariae from Atlantic cod (Gadus morhua) after exposure to freezing and heating in the temperature range from 80°С to 100°С. Food control 50:371–377. https://doi.org/10.1016/j.foodcont.2014.09.021.

Broek van den WLF (1979) Infection of estuarine fish populations by Cryptocotyle lingua (Creplin). J Fish Biol 14(4):395–402. https://doi.org/10.1111/j.1095-8649.1979.tb03534.x

Buchmann K (1986) Prevalence and intensity of infection of Cryptocotyle lingua (Creplin) and Diplostomum spathaceum (Rudolphi)-parasitic metacercariae of Baltic cod (Gadus morhua L.). Nord Vet Med 38(5):303–307.

Cable RM (1931) Studies on the Germ-cell Cycle of Cryptocotyle lingua. I. Gametogenesis in the Adult. Quart Journ Micr Sci 74:563–590.

Cable RM (1934) Studies on the Germ-cell Cycle of Cryptocotyle lingua. J Cell Sci 76:573–614.

Carpenter S (2008) Littorina litorea infection by Cryptocotyle lingua at Nahant, MA: an investigation of possible behavior changes. J Marine Ecol 1(2):90–94.

Casalins L, Arbetman M, Viozzi G, Flores V (2020) A New Species of Cryptocotyle (Digenea: Heterophyidae) Infecting Kelp Gull and a Galaxiid Fish in Patagonian Freshwater Environments: Morphological and Molecular Analyses. J Parasitol 106:203–210. https://doi.org/10.1645/18-44.

Chai J, Shin E, Lee S, Rim H (2009) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47:69–102. https://doi.org/10.3347/kjp.2009.47.S.S69.

Chai JY, Bahk YY, Sohn WM (2013) Trematodes recovered in the small intestine of stray cats in the Republic of Korea. Korean J Parasitol 51(1):99–106. https://doi.org/10.3347/kjp.2013.51.1.99.

Chai JY, Jung BK (2017) Fishborne zoonotic heterophyid infections: An update. Food Waterbor Parasitol 8–9:33–63. https://doi.org/10.1016/j.fawpar.2017.09.001.

Chapman H, Wilson R (1973) The propulsion of the cercariae of Himasthla secunda (Nicoll) and Cryptocotyle lingua. Parasitol 67(1):1–15. https://doi.org/10.1017/S0031182000046242.

Chapman HD (1974) The behaviour of the cercaria of Cryptocotyle lingua. Z F Parasitenkunde 44:211–226. https://doi.org/10.1007/BF00328763.

Chernyshenko AS (1949) New helminths of fishes of the Black Sea. Proceedings of the Odessa University Series Biology 4(57):79–91. (In Russian)

Chernyshenko AS (1955) Materials on the parasitic fauna of the Odessa Bay fish. Proceedings of the Odessa University Series Biol 145(7):211–222. (In Russian)

Ching H (1978) New marine hosts for Parorchis acanthus, Cryptocotyle lingua, Maritrema megametrios, and Maritrema gratiosum, trematodes of birds from British Columbia, Canada. Canad J Zool 56:1877–1879. https://doi.org/10.1139/z78-254.

Christensen N, Roth H (1946) Investigations in gastrointestinal parasites of cats. Kongelige Veterinær og Landbohøjskole Aarsskrift 114–144.

Christensen N, Roth H (1949) Investigations on internal parasites of dogs. Kongelige Veterinær og Landbohøjskole Aarsskrift 1–73.

Christensen ND, Skirnisson K, Nielsen OK (2015) The parasite fauna of the gyrfalcon (Falco rusticolus) in Iceland. J Wildl Dis 51:929–933. https://doi.org/10.7589/2015-01-022.

Ciurea I (1924) Heterophyides de la faune parasitaire de la Roumanie. Parasitol 16:1–21. https://doi.org/10.1017/S003118200001982X. (In French)

Ciurea J (1915a) Über einige neue Distomen aus dem Darm unserer Haustiere und des Pelikans für welche die Fische als Infektionsquelle zu betrachten sind. Ztschr f Infektionskr d Haustiere XVI:445–458. (In German)

Ciurea J (1915b) Nachtrag zu meiner Arbeit: “Über einige neue Distomen aus dem Darm unserer Haustiere und des Pelikans usw.” Ztschr f Infektionskr d Haustiere XVII:108–112. (In German)

Cottrell B (1977) The immune response of plaice (Pleuronectes platessa L.) to the metacercariae of Cryptocotyle lingua and Rhipidocoytle johnstonei. Parasitol 74(1):93–107. PMID: 402627.

Cross MA, Irwin SW, Fitzpatrick SM (2001) Effects of heavy metal pollution on swimming and longevity in cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitol 123(5):499–507. https://doi.org/10.1017/s0031182001008708.

Cross MA, Irwin SW, Fitzpatrick SM (2005) Effects of host habitat quality on the viability of Cryptocotyle lingua (Trematoda: Digenea) cercariae. Parasitol 130(2):195–201. https://doi.org/10.1017/s0031182004006419.

Davies M, Knowles AJ (2001) Effects of trematode parasitism on the behaviour and ecology of a common marine snail (Littorina littorea (L.)). J Exper Marine Biol Ecol 260:155–167. https://doi.org/10.1016/s0022-0981(01)00250-7.

Davis DS, Farley J (1973) The effect of parasitism by the trematode Cryptocotyle lingua (Creplin) on the digestive efficiency in the snail host, Littorina saxatilis (olivi). Parasitol 66(1):191–197. https://doi.org/10.1017/S003118200004453X.

Deblock S (1980) Inventaire des trematodes larvaires parasites des mollusques Hydrobia (Prosobranches) des côtes de France. Parassitolog 22:100–105. (In French)

Declerck D (1992) Voorkomen van de trematode Cryptocotyle lingua bij wijting (Merlangius merlangus) op het Belgisch continentaal plat en de zuidelijke Noordzee. Landbouwtijdschrift (Belgium) 45(6):1221–1229. (In German)

Dogel VA (1962) General parasitology. Leningrad: Leningrad State University 464. (In Russian)

El-Darsh H, Whitfield P (1999) Digenean metacercariae (Timoniella spp., Labratrema minimus and Cryptocotyle concava) from the flounder, Platichthys flesus, in the tidal Thames. J Helminthol 73:103–113. https://doi.org/10.1017/S0022149X99000165.

El-Mayas H, Kearn G (1995) In vitro excystment of the metacercaria of Cryptocotyle concavum from the common goby Pomatoschistus microps. J Helminthol 69(4):285–297. https://doi.org/10.1017/S0022149X00014851.

Esch GW, Fernandez JC (1993) A Functional Biology of Parasitism: Ecological and evolutionary implications. Springer Science Business Media B.V. 336 p.

Faust EC, Nishigori M (1926) The life cycles of two new species of Heterophyidae, parasitic in mammals and birds. J Parasit 13(2):91–128. https://doi.org/10.2307/3271705.

Fish JD, Fish S (1974) The breeding cycle and growth of Hydrobia ulvae in the Dovey Estuary. J Mar Biol Ass U K 54:685–697. https://doi.org/10.1017/s0025315400022852.

Forzan M de J (2001) Pathological effects of Cryptocotyle lingua in double-crested cormorants (Phalacrocorax auritus) treated with dexamethasone. Dissertation. University of Prince Edward Island Department of Pathology and Microbiology Faculty of Veterinary Medicine 1–147. https://islandscholar.ca/islandora/object/ir:21544/datastream/PDF/download/citation.pdf.

Galaktionov K, Irwin S, Prokofiev V, Saville H, Nikolaev K, Levakin I (2006) Trematode Transmission in Coastal Communities – Temperature Dependence and Climate Change Perspectives. Medimond International Proceedings 85–90. https://www.researchgate.net/publication/262935645. (In Russian)

Gardner LS, Thew PT (2006) Redescription of Cryptocotile thapari (Trematoda: Heterophiidae) in the River Otter Lutra longicaudis from Bolivia. Comparative Parasitol 73(1):20–23. https://doi.org/10.1654/0001.1.

Gibson D, Jones A, Bray A (2002) Keys to the Trematoda Vol. 1. Wallingford: CABI Publ 521 p. https://doi.org/10.14411/fp.2003.010.

Jones A, Bray RA, Gibson DI (2005) Keys to the Trematoda Vol. 2. Wallingford: CABI Publ 768 p. https://doi.org/10.14411/fp.2005.044.

Bray RA, Gibson D, Jones A (2008) Keys to the Trematoda Vol. 3. Wallingford: CABI Publ 824 p. https://doi.org/10.1186/1756-3305-2-9.

Golovin PV, Ivanov MV, Ivanova TS, Rybkina EV, Lyus DL (2020) Characteristics of threespined stickleback (Gasterosteus aculeatus L.) infection with metacercariae of Cryptocotyle spp. Trematodes during the spawning season in the White Sea. Proceedings of the Karelian Scientific Center of the Russian Academy of Sciences. https://doi.org/10.17076/eco1299. (In Russian)

Goncalves MLC, Araújo A, Ferreira LF (2003) Human intestinal parasites in the past. New findings and a review. Mem Inst Oswaldo Cruz Rio de Janeiro 98(I):103–118. https://doi.org/10.1590/S0074-02762003000900016.

Goncharov SL, Soroka NM, Pryima OB, Dubovyi AI (2017) Distribution of Trematodes Cryptocotyle (Trematoda, Heterophyidae) in Fish of the Family Gobiidae in Estuary Waters and the Black Sea in Southern Ukraine. Vestnik Zoologii 51(5):393–400. https://doi.org/10.1515/vzoo-2017-0046.

Gorbushin AM (1997) Field evidence of trematode-induced gigantism in Hydrobia ssp. (Gastropoda: Prosobranchia). J Mar Biol Ass U K 77:785–800.

Gorman AM, Moring JR (1982) Occurrence of Cryptocotyle lingua (Creplin, 1825) (Digenea: Heterophyidae) in the rock gunnel, Pholis gunnellus (L.). Canad J Zoolog 60:2526–2528. https://doi.org/10.1139/z82-322.

Granovitch AI, Johannesson K (2000) Digenetic trematodes in four species of Littorina from the West Coast of Sweden. Ophelia 53:55–65. https://doi.org/10.1080/00785326.2000.10409435.

Guildal JA (1968) Investigations on the endoparasitic fauna of the Scandinavian Baltic population of the black-headed gull (Larus ridibundus L.). Kongelige Veterinær og Landbohøjskole Aarsskrift 59–78.

Heuch PA, Jansen PA, Hansen H, Sterud E, MacKenzie K, Haugen P, Hemmingsen W (2011) Parasite faunas of farmed cod and adjacent wild cod populations in Norway: a comparison. Aquaculture Environment Interactions 2:1–13. https://doi.org/10.3354/aei00027.

Honcharov SL (2017b) Pathological anatomic changes in experimental cryptocotylosis of ducklings. Problems of zooengineering and veterinary medicine Collection of scientific papers 35(2):31–34. (In Ukrainian)

Honcharov SL (2017a) Experimental infection of ducklings with trematodes Cryptocotyle Lühe 1899 metacercariae (Trematoda: Heterophyidae). Scientific Messenger of Lviv National University of Veterinary Medicine and Biotechnologies 19(78):112–117. https://doi.org/10.15421/nvlvet7823. (In Ukrainian)

Honcharov SL (2018) Morphological changes in the blood of the fishes of Gobiidae family during cryptocotylosis. Ukr J Veterin Sci 9(1):12–19. https://doi.org/10.31548/ujvs2019.01.012. (In Ukrainian)

Honcharov SL (2019a) Age dynamics of infection of fish of the family Gobiidae with trematodes Cryptokotyle Lühe 1899 (Trematoda: Heterophyidae) in estuary waters and the Black Sea in southern Ukraine. Bulletin of the Poltava State Agrarian Academy 3:207–214. https://doi.org/10.31210/visnyk2019.03.28. (In Ukrainian)

Honcharov SL (2019b) Distribution of Cryptokotyle Lühe 1899 (Trematoda: Heterophyidae) metacercariae in the body of fish of the family Gobiidae. Scientific bulletin LNUVMB named after S.Z. Gzhitsky 21(95):9–14. https://doi.org/10.32718/nvlvet9502. (In Ukrainian)

Honcharov SL (2019c) Influence of some biotic and abiotic factors on the state of parasitofauna of aquatic organisms of natural reservoirs of the South of Ukraine. Scientific Bulletin of Veterinary Medicine 2:60–70. https://doi.org/10.33245/2310-4902-2019-152-2-60-70. (In Ukrainian)

Honcharov SL (2019d) Seasonal dynamics of invasion by trematodes Cryptokotyle Lühe 1899 (Trematoda: Heterophyidae) in fishes of the Gobiidae family in the estuary and water area of the Black Sea in the South of Ukraine. Anim Biol 21(3):21–27. https://doi.org/10.15407/animbiol21.03.021.

Honcharov SL (2019e) Violation of the biochemical homeostasis of the blood of goby fish in case of defeat by metacercariae of the family Heterophyidae. Agrarian Bulletin of the Black Sea region Veterinary Science 93:172–181. (In Ukrainian)

Huxham M, Raffaelli D, Pike A (1993) The influence of Cryptocotyle lingua (Digenea:Platyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda:Prosobranchia); an ecological approach. J Exper Marine Biol Ecol 168(2):223–238. https://doi.org/10.1016/0022-0981(93)90262-M.

Irwin S, Threadgold L, Howard N (1978) Cryptocotyle lingua (Creplin) (Digenea: Heterophyidae): Observations on the morphology of the redia, with special reference to the birth papilla and release of cercariae. Parasitol 76(2):193–199. https://doi.org/10.1017/S0031182000047776.

Isaychikov IM (1924) On the fauna of parasitic worms of domestic carnivores of the Crimea. I. Parasitic worms of dogs. Scientific works of the Siberian vet. institute 6:47–106. (In Russian)

Isaychikov IM (1925) On the fauna of parasitic worms of domestic rodents of the Crimea. Scientific works of the Siberian vet. institute 1(6):105–125. (In Russian)

Iskova NI (1966) Detection of trematodes Cryptocotyle concavum Creplin 1825 and Paramonostomum pseudoalveatum Price 1931 in domestic ducks. Probl parasitology Kyiv: Naukova dumka 6:78–82. (In Russian)

Korniychuk J, Martynenko I (2009) Some peculiarities of Cryptocotyle metacercariae (Heterophyidae) distribution on the body surface of the Roung goby Apollonia (Neogobius) melanostomus. Ecology of the Sea 79:11–14. (In Russian)

Kornyushin VV, Malyshko EI, Malega OM (2013) Domestic dogs and cats as the reservoir of natural nidi and zoonotic helminthoses under present conditions in Ukraine. Veterinary Medicine: Parasitolog 97:383–387. (In Ukrainian)

Kozlov DP (1967) To the study of the helminth fauna of carnivorous mammals in the river basin Pechory. Proceedings of the Helminthological Laboratory Academy of Sciences of the USSR 20:71–78. (In Russian)

Kristoffersen R (1992) Occurrence of the digenean Cryptocotyle lingua in farmed Arctic charr Salvelinus alpinus and periwinkles Littorina littorea sampled close to charr farms in northern Norway. Diseases of Aquatic Organisms Disease Aquat Org 12(1):59–65. https://doi.org/10.3354/dao012059.

Krupa P, Cousineau G, Bal A (1968) Ultrastructural and Histochemical Observations on the Body Wall of Cryptocotyle lingua Rediae (Trematoda). J Parasitol 54(5):900–908.

Krupa PL, Bal AK, Cousineau GH (1967) Ultrastructure of the redia of Cryptocotyle lingua. J Parasitol 53(4):725–734. PMID: 6035711.

Kuklin V, Kuklina M, Ezhov A (2019) Helminths of the Barents Sea Northern Fulmar (Fulmarus glacialis Procellariiformes Procellariidae): Composition, Impact on Host, and Indicator Properties. Biol Bull 46(8):804–813. https://doi.org/10.1134/S1062359019080077.

Kvach Y (2000) The metazoan parasites of gobiids in the Dniester estuary (Black Sea) depending on water salinity. Oceanolog Hydrobiolog Studies 33:47–56. https://www.researchgate.net/publication/200451590.

Kvach Y (2001) Helminthes of gobies from the Tuzly’s Lagoons (North-Western part of the Black Sea). Oceanolog Studies 30:103–113. https://www.researchgate.net/publication/200451597.

Kvach Y (2004) Helminth fauna of gobiid fishes (Gobiidae) of the Tyligul Estuary of the Black Sea. Bulletin of Lviv University 37:144–148. https://www.researchgate.net/publication/200451601. (In Ukrainian)

Kvach Y, Korniychuk J, Mierzejewska K, Rubtsova N, Yurakhno V, Grabowska J, Ovcharenko M (2014) Parasitization of invasive gobiids in the eastern part of the Central trans-European corridor of invasion of Ponto-Caspian hydrobionts. Parasitol Res 113:1605–1624. https://doi.org/10.1007/s00436-014-3791-2.

Kvach YV, Zamorov VV, Kudrenko SA (2000) Infestation of the sand goby by the parasite Ligula pavlovskii Dubinina in the lower reaches of the Khadzhibey estuary. Vestn Odessa in-that Biol 5(1):181–185. (In Russian)

Kvach YV (2007) Helminth fauna of gobies (Gobiidae) of the Odessa Gulf of the Black Sea. Vestnik zoologii 41(3):207–211. (In Ukrainian)

Lambert W, Corliss E, Sha J, Smalls J (2012) Trematode Infections in Littorina littorea on the New Hampshire Coast. Northeastern Naturalist 19:461–474. https://www.jstor.org/stable/41684254.

Lambert TC, Farley J (1968) The effect of parasitism by the trematode Cryptocotyle lingua (Creplin) on zonation and winter migration of the common periwinkle, Littorina littorea (L.). Canad J Zool 46(6):1139–1147. https://doi.org/10.1139/z68-164.

Landis SH, Kalbe M, Reusch TB, Roth O (2012) Consistent pattern of local adaptation during an experimental heat wave in a pipefish-trematode host-parasite system. PLoS One 7(1):1–7. https://doi.org/10.1371/journal.pone.0030658.

Lang T, Bade T, Dethlefsen V (2001) Trends in the occurrence of selected parasites of North Sea Dab (Limanda limanda) and Whiting (Merlangius merlangus). Working group on pathology and diseases of marine organisms Santiago de Compostela Spain 13–17 March 2001 28–36.

Lee Y, Seo M, Chai J (2020) Intestinal Flukes Recovered from a Herring Gull, Larus argentatus, in the Republic of Korea. Korean J Parasitol 58:81–86. https://doi.org/10.3347/kjp.2020.58.1.81.

Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and departure dates. Advan Ecol Res 35:1–31. https://doi.org/10.1016/S0065-2504(04)35001-4.

Levakin IA (2004) The influence of infections with Trematodes Bunocotyle progenetica (Hemiuridae) and Cryptocotyle cancavum (Heterophiidae) onto mortality of littoral mollusks Hydrobia ulvae (Gastropod: Prosobranchia) in condition of extremely high temperature. Parasitolog 38(4):352–358. PMID: 15493287. (In Russian)

Linton E (1915) Tocotrema lingua (Creplin) the adult stage of a skin parasite of the cunner and other fishes of the Woods Hole region. J Parasitolog 1(3):128–134. https://doi.org/10.2307/3271116.

Lothar WR (2002) Parasitäre Würmer (Helminthen) von Seevögeln der Ostseeküste. Seevögel Zeitschrift Verein Jordsand 23(3):66–76. (In German)

Lysne D, Skorping AA, Hemmingsen W (1998) Transmission of Cryptocotyle lingua cercariae in natural environments: a field experiment. J Fish Biol 53(4):879–885. https://doi.org/10.1111/j.1095-8649.1998.tb01840.x.

Lysne DA, Hemmingsen W, Skorping A (1994) The distribution of Cryptocotyle spp. metacercariae in the skin of caged Atlantic cod (Gadus morhua). J Fish Biol 45(2):352–355. https://doi.org/10.1111/j.1095-8649.1994.tb01315.x.

Malek M (2001) Effects of the digenean parasites Labratrema minimus and Cryptocotyle concavum on the growth parameters of Pomatoschistus microps and P. minutus from Southwest Wales. Parasitol Res 87(4):349–355. https://doi.org/10.1007/pl00008591.

Martynenko I (2017) On the taxonomic status of the species Cryptocotyle ransomii Isaitshikow 1924 (Trematoda: Heterophyidae). Parasitolog 50(3):261–265. https://www.researchgate.net/publication/320432330. (In Russian)

Martynenko I (2016) The geographical distribution of the genus Cryptocotyle Lühe 1899 (sensu stricto). Proceedings of the Center for Parasitology: Fauna and ecology of parasites XLIX 63–65. https://doi.org/10.13140/RG.2.2.23261.03045. (In Russian)

Martynenko I (2018) The dynamics of invasion of the Herring gull (Larus cachinnans) by the trematode Cryptocotyle jejuna in the Kerch strait. All-Russian scientific and practical conference: Aquatic biological resources and aquaculture of the South of Russia 162–163. https://www.researchgate.net/publication/348606724. (In Russian)

Martynenko IM, Kornyychuk YM (2013) Trematodes Cryptocotyle jejuna in mollusks Hydrobia acuta in the Kerch Strait. XV conference of Ukrainian Scientific Society of Parasitologists Chernivtsi 58. (In Russian)

Martynenko IM (2012) On the finding of Cryptocotyle jejuna (Nicoll 1907) Ransom 1920 in the Kerch Strait. Abstracts of the Conference of Young Researchers– Zoologists 2012 (Kyiv Institute of Zoology of the National Academy of Sciences of Ukraine April 18–19 2012):21. (In Russian)

Matskasi I (1976) The occurrence of Cryptocotyle jejunum (Nicoll 1907), (trematodes) in the dog in Hungary. Parasitolog Hungarica 9:37–39.

Mattheus PM, Montgomery WI, Hanna REB (1985) Infestation of littorinids by larval Digenea around a small fishing port. Parasitolog 90:277–287.

Matthews RA, Matthews BF (1993) Cryptocotyle lingua in mullet, Chelon labrosus; significance of metacercarial excretory proteins in the stimulation of the immune response. J Helminthol 67(1):1–9. https://doi.org/10.1017/s0022149x00012785.

McDaniel JS, Dixon KE (1967) Utilization of exogenous glucose by the rediae of Parorchis acanthus (Digenea: philophthalmidae) and Cryptocotyle lingua (Digenea: heterophyidae). Biol Bull 133(3):591–599. https://doi.org/10.2307/1539920.

McDaniel SJ (1969) Littorina littorea: lowered heat tolerance due to Cryptocotyle lingua. Exp Parasitol 25(1):13–15. https://doi.org/10.1016/0014-4894(69)90048-4.

McTaggart H (1958) Cryptocotyle lingua in British Mink. Nature 181:651.

Mellegaard S, Lang T (1999) Diseases and parasites of Baltic cod (Gadus morhua) from the Mecklenburg Bight to the Estonian coast. ICES J Marine Sci 56(2):164–168. https://doi.org/10.1006/jmsc.1999.0466.

Morozov FN (1952) Trematodes of the superfamily Heterophyoidea. In the book: K. I. Scriabin (ed.). Trematodes of animals and humans. Publishing house of the Academy of Sciences of the USSR 6:153–615. (In Russian)

Moshu A (2014) Helminths of fish ponds between the rivers Dniester and Prut, potentially dangerous to human health. Eco-Tiras Kishineu 88 p. (In Russian)

Naidenova NN (1974) Parasites Fauna of fishes of the family Gobiidae of the Black Sea and Sea of Azov. Naukova Dumka Kyiv 184 p. (In Russian)

Nardi E (1962) Identificazione di un altro trematode del genere Cryptocotyle parassita intestinale del cane: Cryptocotyle jejunum (Nicoll 1907). Atti delia Societe Italiana delie Scienze Veterinarie 16(2):399–402. (In Italian)

Nicoll W (1923) A reference list of the trematode parasites of British birds. Parasit 15(2):151–202. https://doi.org/10.1017/S0031182000014645.

Pichura VI, Potravka LO, Skok SV (2019) Ecological condition of the Dnieper-river water area in the zone of the impact of urbosystems (exemplified by Kherson). Aquatic bioresources and aquaculture 2:19–34. https://doi.org/10.32851/wba.2019.2.2. (In Ukrainian)

Prokofiev VV (2006) Strategies for Infection of Host Animals with Trematode Cercariae: An Analysis Experience in Ecosystems of the Coastal Seas and Lakes of Northwest Russia: Author’s abstract Diss doct biol sciences St. Petersburg: ZIN RAN 26. (In Russian)

Prokofiev VV, Berger VI, Galaktionov KV (2001) Respiration and motor activity of cercariae of three trematode species from the intertidal shell Littorina littorea L (Gastropoda) from the White Sea. Parasitolog 35(4):325–332. PMID: 11605457. (In Russian)

Radulescu I, Vasiliu N (1951) Infestatie masiva cu ectoparaziti la stronghil (Neogobius melanostomus Pall). Bull Inst Cer Pesc 10(4):59–66. (In Romanian)

Ransom B (1920) Synopsis of the Trematode family Heterophyidae with descriptions of a new genus and five new species. Proc US Natur Mus Washington 57:527–573. https://doi.org/10.5479/si.00963801.57-2322.527.

Rausch RL, Scott EM, Rausch VR (1967) Helminths in Eskimo in western Alaska, with particular reference to Diphyllobothrium infection and anemia. Transactions of the Royal Society of Tropical Medicine and Hygiene 61:351–357. https://doi.org/10.1016/0035-9203(67)90008-9.

Rea J, Irwin S (1991) Behavioural responses of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae) to computer-controlled shadow sequences. Parasitolog 103(3):471–477. https://doi.org/10.1017/s0031182000059990.

Rea J, Irwin S (1992a) The effects of age, temperature, light quantity, and wavelength on the swimming behavior of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitolog 105(1):131–137. https://doi.org/10.1017/S0031182000073789.

Rea J, Irwin S (1992b) The effects of computer-controlled shadow stimuli on the success of cercarial transmission by Cryptocotyle lingua (Digenea: Heterophyidae). Parasitolog 105(2):243–246. https://doi.org/10.1017/S0031182000074163.

Read AF, Barnard CJ, Behnke JM (1990) Parasites and the evolution of host sexual behaviour. Parasitism and Host Behaviour 117–157.

Rees FG (1974) The ultrastructure of the body wall and associated structures of the cercaria of Cryptocotyle lingua (Creplin) (Digenea: Heterophyidae) from Littorina littorea (L.). Z Parasitenkd 44(3):239–265. https://doi.org/10.1007/BF00328765.

Rees FG (1975a) Studies on the pigmented and unpigmented photoreceptors of the cercaria of Cryptocotyle lingua (Creplin) from Littorina littorea (L.). Proc R Soc Lond B Biol Sci 188(1091):121–138. https://doi.org/10.1098/rspb.1975.0007.

Rees FG (1975b) The arrangement and ultrastructure of the musculature, nerves, and epidermis, in the tail of the cercaria of Cryptocotyle lingua (Creplin) from Littorina littorea (L.). Proc Roy Soc London B Biological Sci 190(1099):165–186. https://doi.org/10.1098/rspb.1975.0085.

Rees FG (1977) The development of the tail and the excretory system in the cercaria of Cryptocotyle lingua (Creplin) (Digenea: heterophyidae) from Littorina littorea (L.). Proc R Soc Lond B Biol Sci 195(1121):425–452. https://doi.org/10.1098/rspb.1977.0019.

Rees FG (1979) The morphology and ultrastructure of the female reproductive ducts in the metacercaria and adult of Cryptocotyle lingua (Creplin) (Digenea: Heterophyida). Z Parasitenkd 60(2):157–176. https://doi.org/10.1007/BF00927972.

Reimer LW (1970) Digene Trematoden und Cestoden der Ostseefische als naturliche Fischmarken. Fischer Jena 144.

Robson E, Williams I (1971) Relationships of Some Species of Digenea with the Marine Prosobranch Littorina littorea (L.) III. The Effect of Larval Digenea on the Glycogen Content of the Digestive Gland and Foot of L. littorea. J Helminthol 45(4):381–401. https://doi.org/10.1017/S0022149X0000064X.

Rosenqvist G, Johansson K (1995) Male avoidance of parasitized females explained by direct benefits in a pipefish. Anim Behav 49(4):1039–1045. https://doi.org/10.1006/anbe.1995.0133.

Rothschild M (1938) Preliminary note on the life-history of Cryptocotyle jejuna Nicoll 1907 (Trematoda). Ann Magaz Nat Histor 1(2):238–239. https://doi.org/10.1080/00222933808526760.

Saeed I, Maddox-Hyttel C, Monrad J, Kapel CM (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–179. https://doi.org/10.1016/j.vetpar.2006.02.015.

Sarabeev VL, Domnich IF (2001) Parasites of fishes of the family Gobiidae in the North-Western part of the Azov Sea. Problems of Ichthyopathology UAAS Kyiv 100–104. (In Russian)

Seaman B, Briffa M (2015) Parasites and personality in periwinkles (Littorina littorea): Infection status is associated with mean-level boldness but not repeatability. Behav Proc 115:132–134. https://doi.org/10.1016/j.beproc.2015.03.014.

Sekhar SC, Threlfall W (1970) Helminth Parasites of the Gunner, Tautogolabrus adspersus (Walbaum) in Newfoundland. J Helminthol 44(2):169–188. https://doi.org/10.1017/S0022149X00021726.

Shchepkina AM (1981) The effect of Cryptocotyle concavum metacercariae on the lipid content of the tissue of Gobius melanostomus. Parazitolog 15:185–187. (In Russian)

Sindermann CJ, Farrin AE (1962) Ecological studies of Cryptocotyle lingua (Trematoda: Heterophyidae) whose larvae cause “pigment spots” of marine fish. Ecology 43(1):69–75.

Sindermann CJ, Rosenfeld A (1954) Diseases of fishes of the Western North Atlantic III. Mortalities of sea herring (Clupea harengus) caused by larval trematode invasion. Maine Dept Sea and Shore Fish Res Bull 21:1–16.

Sindermann CJ (1964) Larval ecology of the Trematode Cryptocotyle lingua. Proc First Inter Congress Parasitol Pergamon 1:12–13. https://doi.org/10.1016/b978-1-4832-2913-3.50017-4.

Skuratovskaya EN, Yurakhno VM, Chesnokova II (2020) Biochemical response of two fish species of Gobiidae (Gobiiformes) to Cryptocotyle (Opisthorchiida, Heterophyidae) metacercariae infection from the mouth of the river Chernaya (Black Sea). Ecologica Montenegrina 38:158–165. https://doi.org/10.37828/em.2020.38.24.

Smith GM (1935) A Hyperplastic Epidermal Disease in the Winter Flounder Infected with Cryptocotyle lingua (Creplin). Amer Assoc Cancer Res 25(1):108–112. https://doi.org/10.1158/ajc.1935.108.

Smith HJ (1977) Parasites of red foxes in New Brunswick and Nova Scotia. J Wildlife Dis 14:366–370. https://doi.org/10.7589/0090-3558-14.3.366.

Smith HJ (1978) Cryptocotyle lingua infection in a Bald Eagle (Haliaeetus leucocephalus). J Wildlife Dis 14(2):163–134. https://doi.org/10.7589/0090-3558-14.2.163.

Sohn WM, Chai J (2005) Infection status with helminths in feral cats purchased from a market in Busan, Republic of Korea. Korean J Parasitol 43(3):93–100. https://doi.org/10.3347/kjp.2005.43.3.93.

Soroka N, Goncharov S Patent № 103347 Ukraine, MPK (2015, 10) Method of allocation metacercariae trematodes Paracoenogonimus ovatus; Applicant and Patentee the National University of Life and Environmental Sciences stated 25.06.2015; Bjul 12.10.2015 (in Ukraine)

Sousa WP, Gleason M (1989) Does parasitic infection compromise host survival under extreme environmental conditions? The case of Cerithidea californica (Gastropoda: Prosobranchia). Oecologa 80:456–464. https://doi.org/10.1007/BF00380066.

Sousa WP (1983) Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. J Exp Mar Biol Ecol 73(3):273–296. https://doi.org/10.1016/0022-0981(83)90051-5.

Sten’ko RP (1985) Sensory system of two species of cercariae of the genus Cryptocotyle (Trematoda, Heterophyidae). Parazitolog 19(5):403–406. PMID: 4069748. (In Russian)

Stunkard HW, Willey CH (1929) The Development of Cryptocotyle (Heterophyidae) in its Final Host. Amer J Tropical Medicine 1–9(2):117–128.

Stunkard HW (1929) The excretory system of Cryptocotyle (Heterophyidae). J Parasitol 15:259–266.

Stunkard HW (1930) Life history of Cryptocotyle lingua (Crepl.) with notes on the physiology of the metacercariae. J Morph Physiol 50:143–191. https://doi.org/10.1002/jmor.1050500106.

Tatonova YV, Besprozvannykh VV (2019) Description of a new species, Cryptocotyle lata sp. nov., and discussion of the phylogenetic relationships in Opisthorchioidea, Parasitology International 72:101939. https://doi.org/10.1016/j.parint.2019.10193.

Terenina NB, Tolstenkov OO, Gustafsson MKS, Kuklin VV, Kuklina MM (2010) Nerve-muscle system of cercariae and adult of trematodes Cryptocotyle lingua and C. concavum (Heterophyidae). Rus Parasitol J 1:22–29. (in Russian)

Threlfall W (1982) Endoparasites of the Double-crested Cormorant (Phalacrocorax auritus) in Florida. Proc Helminthol Soc Wash 49(1):103–108.

Tolonen A, Karlsbakk E (2003) The parasite fauna of the Norwegian spring spawning herring (Clupea harengus L.). ICES J Marine Sci 60:77–84. https://doi.org/10.1006/jmsc.2002.1307.

Tolstenkov OO, Prokofiev VV, Terenina NB, Galaktionov KV (2010) Effect of some pharmacological substances on the motility of the Cryptocotyle lingua cercaria (Heterophiidae). Parasitolog 44(4):364–370. PMID: 21061596. (In Russian)

Torres P, Schlatter R, Montefusco A, Gesche W, Ruiz E, Contreras A (1993) Helminth parasites of piscivorous birds from lakes in the south of Chile. Memorias do Instituto Oswaldo Cruz 88:341–343. https://doi.org/10.1590/s0074-02761993000200028.

Van Hoey G, Hostens K, Parmentier K, Robbens J, Bekaert K, Backer A, Derweduwen J, Devriese L, Hillewaert H, Hoffman S (2009) Biological and chemical effects of the disposal of dredged material in the Belgian part of the North Sea (period 2007–2008). Report ILVO-Animal Sciences-Fisheries 1–101. https://www.researchgate.net/publication/259004910.

Vernberg WB, Vernberg FJ (1963) Influence of parasitism on thermal resistance of the mudflat snail Nassa obsoleta Say. Exp Parasitol 14(3):330–332. https://doi.org/10.1016/0014-4894(63)90039-0.

Wood B, Matthews R (2006) The immune response of the thick-lipped grey mullet, Chelon labrosus (Risso, 1826), to metacercarial infections of Cryptocotyle lingua (Creplin, 1825). J Fish Biol 31(sA):175–183. https://doi.org/10.1111/j.1095-8649.1987.tb05310.x.

Wood BP (1990) The immune response of the grey mullet, Chelon labrosus (Risso, 1826), to Cryptocotyle lingua (Creplin, 1825), (Digenea). Thesis of Doctor of Philosophy 1–221 p.

Wootton DM (1957) The life history of Cryptocotyle concavum (Creplin, 1825) Fischoeder, 1903 (Trematoda: Heterophyidae). J Parasitol 43:271–279. https://doi.org/10.2307/3274345.

Yamaguti S (1975) A synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval forms. Keigaku Tokyo 590.

Yoshimira K (1965) On the trematode species Phocitrema fusiforme Goto and Ozaki 1930 and Cryptocotyle lingua (Creplin, 1825). Japan J Veterin Res 13(2):15–18. https://doi.org/10.14943/jjvr.13.2.15.

Yurakhno MV, Stryukov AA (2006) Helminth fauna of the sea lion (Eumetopias jubatus) inhabiting the western and central parts of the Bering Sea. Marine mammals of the Holarctic 569–571. (In Russian)

Zander CD, Kesting V (1996) The indicator properties of parasite communities of gobies (Teleostei, Gobiidae) from Kiel and Lübeck Bight, SW Baltic Sea. Appl Parasitol 37(3):186–204.

Zander CD, Kollra HG, Antholz B, Meyer W, Westphal D (1984) Small-sized euryhaline fish as intermediate hosts of the digenetic trematode Cryptocotyle concavum. Helgoländer Meeresuntersuchungen 37(1–4):433–443.

Zander CD, Reimer LW, Barz K, Dietel G, Strohbach U (2000) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea) II. Guild communities, with special regard to snails, benthic crustaceans, and small-sized fish. Parasitol Res 86(5):359–372. https://doi.org/10.1007/s004360050681.

Zander CD, Reimer LW, Barz K, Bight È (1999) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). I. Structure and dynamics of communities of littoral fish, especially small-sized fish. Parasitol Res 85(5):356–372. https://doi.org/10.1007/s004360050562.

Zander CD (1998) Ecology of Host Parasite Baltic Sea. Naturwissenschaften Rev Artic 85:426–436. https://doi.org/10.1007/s001140050526.

Zavras ET, Hugo AJ (1979) Carotenoids found in Littorina littorea and their relationship to parasitic infection by larva trematodes. J Invert Pathol 34(3):276–284. https://doi.org/10.1016/0022-2011(79)90074-0.

Zdzitowiecki K, Niewiadomska K, Drozdz J (1989) Trematodes of birds and mammals in the environs of H. Arctowski Station South Shetlands, Antarctic. Acta Parasitol Polon 34(3):247–257.

Zimmerman MR, Smith GS (1975) A probable case of occidental inhumation of 1600 years ago. Bull NY Acad Med 51(7):828–837. PMID: 19312928.

Zimmerman MR (1980) Disease in ancient Egypt. In A. Cockburn E. Cockburn, T.A. Reyman (eds), Mummies, Disease & Ancient Cultures, 2nd ed., Cambridge University, Cambridge, 138–153.

Published
2022-08-03
How to Cite
Honcharov, S., Soroka, N., Dubovyi, A., & Galat, M. (2022). Cryptokotyle lühe, 1899 (trematoda: heterophyidae): special characteristics of developmental biology and epizootiology. Agricultural Science and Practice, 9(1), 50-74. https://doi.org/10.15407/agrisp9.01.050