Strategies of search behaviuor in trematode Cercariae

V.V. Prokofiev and K.V. Galaktionov

Proceedings of the Zoological Institute RAS, 2009, 313(3): 308–318   ·   https://doi.org/10.31610/trudyzin/2009.313.3.308

Full text  

Abstract

On the base of analysis of original and literature data four basic strategies were distinguished in host-search behaviour of trematode cercariae. There are active search (1), passive waiting (2), active waiting (3) and prey mimetism (4). Many of the Xiphidiocercaria, cercariae of some Echinostomatidae, Psilostomatidae, Acanthocolpidae and Lepocreadiidae as well as cercariae of Fasciolidae, Haploporidae, Notocotylidae, Pronocephalidae, Gladorchiidae and some Haplosplanchnidae encysting on surface of underwater substrates follow the first strategy. These cercariae demonstrate a continuous swimming and photo-, geo- and sometimes chemoreactivity. The second strategy is characteristic for cercariae of Microcerca group with ambuscade behaviour. These cercariae exhibit pronounced oscilloreactions whereas other orienting reactions are feebly marked or even absent. Cercariae of Bucephalidae and Hemiuroidea which float passively in the water column also follow the strategy of passive waiting. The strategy of active waiting is characteristic of cercariae (Furcocercaria, Pleurolophocerca, Parapleurolophocerca, etc.) with an intermittent type of locomotion, where periods of active movement alternate regularly with periods of repose. These cercariae demonstrate a wide range of orienting reactions. The pray mimetism strategy exhibit cercariae of some trematodes (Azygiidae, Bivesiculidae, some Echinostomatidae, Heterophyidae, Lepocreadiidae, Gyliauchinidae, etc.) infecting their hosts passively per os. The active searching cercariae (strategy 1) usually infect sedentary animals or mobile ones but during periods of their minimal locomotory activity. The cercariae exploiting strategies 2–4 predominantly infect mobile animals. It was emphasized that the model of foraging strategies produced by Schoener (1971) and Huey and Pianka (1981) for free-living animals could be applied to analysis of cercarial hostsearch behaviour.

Key words

orientation reactions, parasites, host-search behaviour, foraging strategies, trematodes, cercariae

Submitted February 10, 2009  ·  Accepted June 1, 2009  ·  Published September 25, 2009

References

Галактионов К.В. 1993. Жизненные циклы трематод как компоненты экосистем (опыт анализа на примере представителей семейства Microphallidae). Издательство Кольского научного центра РАН, Апатиты, 190 с.

Галактионов К.В. 1996. Экспериментальное исследование необычного жизненного цикла Parvatrema sp. (Trematoda: Gymnophallidae). Паразитология, 30(6): 487–494.

Галактионов К.В. и Добровольский А.А. 1998. Происхождение и эволюция жизненных циклов трематод. Наука, Санкт-Петербург, 404 с.

Гинецинская Т.А. 1968. Трематоды, их жизненные циклы, биология и эволюция. Наука, Ленинград, 410 с.

Курочкин Ю.В. 1987. Трематоды фауны СССР. Прагонимиды. Наука, Москва, 152 с.

Панин В.Я. 1984. Трематоды дикроцелииды мировой фауны. Наука, Алма-Ата, 248 с.

Панин В.Я. 1986. Циклы развития трематод надсемейства Dicrocoeliidae. В кн.: Е.В. Гвоздев и З. Ждярска (Ред.). Функциональная морфология личинок трематод и цестод. Наука, Алма-Ата: 10–17.

Прокофьев В.В. 1994. «Засадный» тип поведения церкарий некоторых морских трематод. Зоологический журнал, 73(5): 13–20.

Прокофьев В.В. 1997. Реакции на свет церкарий морских литоральных трематод Cryptocotyle sp. (Heterophyidae) и Maritrema subdolum (Microphallidae). Зоологический журнал, 76(3): 275–280.

Прокофьев В.В. 2001. Реакции на свет церкарий морской литоральной трематоды Renicola thaidus (Trematoda; Renicolidae). Паразитология, 35(3): 429–435.

Прокофьев В.В. 2002. Особенности вертикальной дисперсии в толще воды церкарий морской литоральной трематоды Renicola thaidus (Trematoda: Renicolidae). Паразитология, 36(4): 316–323.

Прокофьев В.В. 2003. Характер вертикального распределения в толще воды церкарий трематод Cryptocotyle concavum (Heterophyidae) и Maritrema subdolum (Microphallidae). Паразитология, 37(3): 207–215.

Прокофьев В.В. 2005. Особенности плавания церкарий некоторых видов трематод. Паразитология, 39(3): 250–261.

Прокофьев В.В. 2006. Стратегии заражения животных-хозяев церкариями трематод: опыт анализа в экосистемах прибрежья морей и озер северо-запада России. Диссертация доктора биологических наук. Зоологический институт РАН, Санкт-Петербург, 545 с.

Прокофьев В.В. 2008. Стратегии заражения хозяина церкариями трематод. В кн.: Материалы IV Всероссийского съезда Паразитологического общества при РАН «Паразитология в XXI веке – проблемы, методы, решения» (20–25 октября 2008, Санкт-Петербург). Т. 3. ЛЕМА, Санкт-Петербург: 57–62.

Тихомиров И.А. 1980. Жизненный цикл Philophthalmus rhionica sp. nov. (Trematoda: Philophthalmidae). Автореферат диссертации кандидата биологических наук. Ленинградский государственный университет, Ленинград, 24 с.

Соболева Т.Н. 1986. Циклы развития трематод надсемейства Brachylaimoidea. В кн.: Е.В. Гвоздев и З. Ждярска (Ред.). Функциональная морфология личинок трематод и цестод. Наука, Алма-Ата: 70–75.

Bartoli P. and Combes C. 1986. Stratégies de dissémination des cercaires de trématodes dans un écosystème marin littoral. Acta Ecologica, 7: 101–114.

Cable R.M. 1956. Marine cercariae of Puerto Rico. Scientific Survey of Puerto Rico and Virgin Islands, 61: 491–577.

Campbell J.F. and Lewis E.E. 2002. Entomopathogenic nematode host-search strategies. In E.E. Lewis, J.F. Campbell and M.V.K. Sukhdeo (Eds). The behavioural ecology of parasites. CABI Publ., Wallingford, New York: 13–38. https://doi.org/10.1079/9780851996158.0013

Chapman H.D. 1974. The behaviour of the cercaria of Cryptocotyle lingua. Zeitschrift für Parasitenkunde, 44: 211–226. https://doi.org/10.1007/BF00328763

Combes C. 1980. Les mécanismes de recrutement chez les métazoaires parasites et leur interprétation en termes de stratégies démographiques. Vie Milieu, 30: 55–63.

Combes C. 2001. Parasitism. The ecology and evolution of intimate interactions. The University of Chicago Press, Chicago and London, 728 p.

Combes C., Fournier A., Moné H. and Théron A. 1994. Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology, 109 (Suppl.): S3–S13. https://doi.org/10.1017/S0031182000085048

Combes C., Bartoli P. and Théron A. 2002. Trematode transmission strategies. In: E.E. Lewis, J.F. Campbell and M.V.K. Sukhdeo (Eds). The behavioural ecology of parasites. CABI Publ., Wallingford, New York: 1–12. https://doi.org/10.1079/9780851996158.0001

Evans N.A. and Gordon D.M. 1983. Experimental observations on the specificity of Echinoparyphium recurvatum toward second intermediate host. Zeitschrift für Parasitenkunde, 69: 217–222. https://doi.org/10.1007/BF00926956

Feiler W. and Haas W. 1988a. Host-finding in Trichobilharzia ocellata cercariae: swimming and attachment to the host. Parasitology, 96: 493–505. https://doi.org/10.1017/S0031182000080136

Feiler W. and Haas W. 1988b. Trichobilharzia ocellata: chemical stimuli of duck skin for cercarial attachment. Parasitology, 96: 507–517. https://doi.org/10.1017/S0031182000080148

Fried B. and King W. 1989. Attraction of Echinostoma revolutum cercariae to Biomphalaria glabrata dialysate. Journal of Parasitology, 75: 55–57. https://doi.org/10.2307/3282935

Galaktionov K.V. and Dobrovolskij A.A. 2003. The biology and evolution of trematodes. An essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Kluwer Academic Publishers, Boston, Dordrecht, London, 620 p.

Galaktionov K.V., Irwin S.W.B. and Saville D.H. 2006. One of the most complex life cycles among digenetic trematodes: a description of Parvatrema margaritense (Ching, 1982) n. comb. (Gymnophallidae) possessing parthenogenetic metacercariae. Parasitology, 132(5): 733–746. https://doi.org/10.1017/S0031182005009765

Haas W. 1992. Physiological analysis of cercarial behaviour. Journal of Parasitology, 78: 243–255. https://doi.org/10.2307/3283471

Haas W. 1994. Physiological analysis of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology, 109 (Suppl.): S15–S29. https://doi.org/10.1017/S003118200008505X

Haas W. and Haberl B. 1997. Host recognition by trematode miracidia and cercariae. In: Fried B. and Graczyk T.K. (Eds.) Advances in Trematode Biology. CRC Press, Boca Raton, New York: 197–227.

Haas W., Körner M. Hutterer E., Wegner M. and Haberl B. 1995. Finding and recognition of the snail intermediate hosts by 3 species of echinostome cercariae. Parasitology, 110: 133–142. https://doi.org/10.1017/S0031182000063897

Huey R.B. and Pianka E.R. 1981. Ecological consequences of foraging mode. Ecology, 62: 991–999. https://doi.org/10.2307/1936998

Køie M. 1976. On the morphology and life-history of Zoogonoides viviparus (Olsson, 1868) Odhner, 1902 (Trematoda, Zoogonidae). Ophelia, 15(1): 1–14. https://doi.org/10.1080/00785326.1976.10425444

Køie M. 1979. On the morphology and life-history Monascus [= Haplocladus] filiformis (Rudolphi, 1819) Loos, 1907 and Steringophorus furciger (Olsson, 1868) Odhner, 1905 (Trematoda, Fellodistomidae). Ophelia, 18(1): 113–132. https://doi.org/10.1080/00785326.1979.10425494

Køie M. 1985. On the morphology and life-history of Lepidapedon elongatum (Lebour, 1908) Nicoll, 1910 (Trematoda, Lepocreadiidae). Ophelia, 24: 135–153. https://doi.org/10.1080/00785326.1985.10429724

Körner M. and Haas W. 1998a. Chemo-orientation of echinostome cercariae towards their snail-hosts: amino acids signal a low host-specificity. International Journal for Parasitology, 28: 511–516. https://doi.org/10.1016/S0020-7519(97)00196-3

Körner M. and Haas W. 1998b. Chemo-orientation of echinostome cercariae towards their snail-hosts: the stimulating structure of amino acids and other attractants. International Journal for Parasitology, 28: 517–525. https://doi.org/10.1016/S0020-7519(97)00195-1

Le Zotte L.A. 1954. Studies on marine digenetic trematodes of Puerto Rico: the family Bevisiculidae, its biology and affinities. Journal of Parasitology, 40: 148–162. https://doi.org/10.2307/3274295

Lewis M.C., Welsford I.G. and Uglem G.L. 1989. Cercarial emergence of Proterometra macrostoma and P. edneyi (Digenea: Azygiidae): contrasting responses to light: dark cycling. Parasitology, 99: 215–223. https://doi.org/10.1017/S0031182000058662

Maillard C. 1971. Cycle évolutif de Cainocreadium labracis (Dujardin, 1845) (Trematoda, Allocreadiidae). Comptes Rendus de l’Académie des Sciences, Paris, 272: 3303–3306.

Matthews R.A. 1973. The life-cycle of Prosorhynchus crucibulum (Rudolphi, 1819) Odhner, 1905, and a comparison of its cercaria with that of Prosorhynchus squamatus Odhner, 1905. Parasitology, 66: 133–164. https://doi.org/10.1017/S0031182000044504

Matthews R.A. 1974. The life-cycle of Bucephaloides gracilescens (Rudolphi, 1819) Hopkins, 1954 (Digenea: Gasterostomata). Parasitology, 68: 1–12. https://doi.org/10.1017/S0031182000045315

Mas-Coma S. and Montoliu I. 1986. The life cycle of Brachylaima ruminae n. sp. (Trematoda: Brachylaimidae), a parasite of rodents. Zeitschrift für Parasitenkunde, 72: 739–753. https://doi.org/10.1007/BF00925095

Mas-Coma S. and Montoliu I. 1987. The life cycle of Dollfusinus frontalis, a brachylaimid trematode of small mammals (Insectivora and Rodentia). International Journal for Parasitology, 17: 1063–1079. https://doi.org/10.1016/0020-7519(87)90159-7

Mas-Coma S. and Montoliu I. 1995. Life cycle of Pseudoleucochloridium pericardicum n. sp. (Trematoda: Brachylaimidae), a parasite of shrews (Insectivora: Soricidae) in the Oriental Pyrenees. Research and Reviews in Parasitology, 55: 155–171.

Olson P.D., Cribb T.H., Tkach V.V., Bray R.A. and Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33: 733–755. https://doi.org/10.1016/S0020-7519(03)00049-3

Poulin R. 2007. Evolutionary ecology of parasites. Princeton University Press, Princeton and Oxford, 332 p. https://doi.org/10.1515/9781400840809

Shiff C.J. and Graczyk T.K. 1994. A chemokinetic response in Schistosoma mansoni cercariae. Journal of Parasitology, 80: 879–883. https://doi.org/10.2307/3283434

Schoener T.W. 1971. Theory of feeding strategies. Annual Review of Ecology and Systematics, 2: 369–404. https://doi.org/10.1146/annurev.es.02.110171.002101

Shostak A.W. and Esch G.W. 1990. Photocycle-dependent emergence by cercariae of Halipegus occidualis from Helisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission. Journal of Parasitology, 76: 790–795. https://doi.org/10.2307/3282796

Stunkard H.W. 1938. Distomum lasium Leidy, 1891 (Syn. Cercariaeum lintoni Miller and Northup, 1926), the larval stage of Zoogonus rubellus (Olsson, 1868) (Syn. Z. mirus Looss, 1901). The Biological Bulletin, 75: 308–334. https://doi.org/10.2307/1537737

Stunkard H.W. 1943. The morphology and life-history of the digenetic trematode, Zoogonoides laevis Linton, 1940. The Biological Bulletin, 85: 227–237. https://doi.org/10.2307/1538224

West A.F. 1961. Studies on the biology of Philophthalmus gralli Mathis and Leger, 1910 (Trematoda: Digenea). American Midland Naturalist, 66: 363–383. https://doi.org/10.2307/2423036

Wardle W.J. 1988. A bucephalid larva, Cercaria pleuromerae n. sp. (Trematoda: Digenea), parasitizing a deepwater bivalve from the Gulf of Mexico. Journal of Parasitology, 74: 692–694. https://doi.org/10.2307/3282191

Wilson R.A. 1987. Cercariae to liver worms: development and migration in the mammalian host. In: Rollinson D. and Simpson A.J.G. (Eds.). The biology of schistosomes. From genes to latrines. Academic Press, London: 115–146.

Wright D.G.S. 1974. Responses of the cercariae of Trichobilharzia ocellata to white light, monochromatic light, and irradiance reduction. Canadian Journal of Zoology, 52: 575–579. https://doi.org/10.1139/z74-074

 

© Zoological Institute of the Russian Academy of Sciences
Last modified: September 11, 2024