Hostname: page-component-745bb68f8f-grxwn Total loading time: 0 Render date: 2025-01-14T19:36:37.041Z Has data issue: false hasContentIssue false
  • English
  • Français

The effects of host size and temperature on the emergence of Echinoparyphium recurvatum cercariae from Lymnaea peregra under natural light conditions

Published online by Cambridge University Press:  15 January 2010

N.J. Morley ,
M.E. Adam  and
J.W. Lewis
N.J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, SurreyTW20 0EX, UK
M.E. Adam
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, SurreyTW20 0EX, UK
J.W. Lewis
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, SurreyTW20 0EX, UK
*
*E-mail: n.morley@rhul.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

The production of cercariae from their snail host is a fundamental component of transmission success in trematodes. The emergence of Echinoparyphium recurvatum (Trematoda: Echinostomatidae) cercariae from Lymnaea peregra was studied under natural sunlight conditions, using naturally infected snails of different sizes (10–17 mm) within a temperature range of 10–29°C. There was a single photoperiodic circadian cycle of emergence with one peak, which correlated with the maximum diffuse sunlight irradiation. At 21°C the daily number of emerging cercariae increased with increasing host snail size, but variations in cercarial emergence did occur between both individual snails and different days. There was only limited evidence of cyclic emergence patterns over a 3-week period, probably due to extensive snail mortality, particularly those in the larger size classes. Very few cercariae emerged in all snail size classes at the lowest temperature studied (10°C), but at increasingly higher temperatures elevated numbers of cercariae emerged, reaching an optimum between 17 and 25°C. Above this range emergence was reduced. At all temperatures more cercariae emerged from larger snails. Analysis of emergence using the Q10 value, a measure of physiological processes over temperature ranges, showed that between 10 and 21°C ( ≈ 15°C) Q10 values exceeded 100 for all snail size classes, indicating a substantially greater emergence than would be expected for normal physiological rates. From 14 to 25°C ( ≈ 20°C) cercarial emergence in most snail size classes showed little change in Q10, although in the smallest size class emergence was still substantially greater than the typical Q10 increase expected over this temperature range. At the highest range of 21–29°C ( ≈ 25°C), Q10 was much reduced. The importance of these results for cercarial emergence under global climate change is discussed.

Type
Research Papers
Information
Journal of Helminthology , Volume 84 , Issue 3 , September 2010 , pp. 317 - 326
Copyright
Copyright © Cambridge University Press 2010

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

Adam, M.E. & Lewis, J.W. (1992) Sites of encystment by the metacercariae of Echinoparyphium recurvatum in Lymnaea peregra. Journal of Helminthology 66, 96–99.Google Scholar
Al-Habbib, W.M.S. & Grainger, J.N.R. (1983) The effect of constant and changing temperature on the rate of development of the eggs and the larval stages of Fasciola hepatica. Proceedings of the Royal Irish Academy 83B, 281–290.Google Scholar
Anderson, P.A., Nowsielski, J.W. & Croll, N.A. (1976) The emergence of cercariae of Trichobilharzia ocellata and its relationship to the activity of its snail host Lymnaea stagnalis. Canadian Journal of Zoology 54, 1481–1487.Google Scholar
Asch, H.L. (1972) Rhythmic emergence of Schistosoma mansoni cercariae from Biomphalaria glabrata: control by illumination. Experimental Parasitology 31, 350–355.Google Scholar
Bryant, C. & Flockhart, H.A. (1986) Biochemical strain variation in parasitic helminths. Advances in Parasitology 25, 275–319.Google Scholar
Chernogorenko, M.I. (1982) Periodicity, diurnal rhythm and ecologic factors influencing the rate of issuance of cercariae from mollusc hosts. Hydrobiological Journal 18, (3), 64–72.Google Scholar
Christensen, N.O., Frandsen, F. & Roushdy, M.Z. (1980) The influence of environmental conditions and parasite-intermediate host-related factors on the transmission of Echinostoma liei. Zeitschrift für Parasitenkunde 63, 47–63.CrossRefGoogle Scholar
Combes, C., Fournier, A., Mone, H. & Theron, A. (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–S13.Google Scholar
De Souza, C.P., Araujo, N., Jannotti-Passos, L.K. & Guimaraes, C.T. (1994) Production of Schistosoma mansoni cercariae by Biomphalaria glabrata from a focus in Belo Horizonte, Minas Gerais. Revista do Instituto de Medicina tropical de Sao Paulo 36, 485–489.Google Scholar
Dinnik, J.A. & Dinnik, N.N. (1964) The influence of temperature on the succession of redial and cercarial generations of Fasciola gigantica in a snail host. Parasitology 54, 59–65.CrossRefGoogle Scholar
Duerr, F.G. (1967) Changes in the size–metabolic rate relationship of Lymnaea stagnalis appressa Say produced by digenetic trematode parasitism. Comparative Biochemistry and Physiology 20, 391–398.Google Scholar
Evans, N.A. (1982) Effect of copper and zinc upon the survival and infectivity of Echinoparyphium recurvatum cercariae. Parasitology 85, 295–303.Google Scholar
Evans, N.A. (1985) The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269–275.Google Scholar
Evans, N.A. & Gordon, D.M. (1983a) Experimental observations on the specificity of Echinoparyphium recurvatum toward second intermediate hosts. Zeitschrift für Parasitenkunde 69, 217–222.Google Scholar
Evans, N.A. & Gordon, D.M. (1983b) Experimental studies on the transmission dynamics of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 87, 167–174.Google Scholar
Galaktionov, K. & Dobrovolskij, A. (2003) The biology and evolution of trematodes: An essay on the biology, morphology, life cycles, transmissions, and evolution of digenetic trematodes. 620 pp. Dordrecht, Kluwer.Google Scholar
Getting, P.A. (1985) Neural control of behaviour in gastropods. pp. 269–334in Willow, A.O.D. (Ed.) The Mollusca, Vol. 8 Neurobiology and behaviour, Part 1. New York, Academic Press.Google Scholar
Ginetsinskaya, T.A. (1988) Trematodes, their life cycles, biology and evolution. 559 pp. New Delhi, Amerind Publishing Company.Google Scholar
Graham, A.L. (2003) Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. Journal of Parasitology 89, 458–463.CrossRefGoogle ScholarPubMed
Kawashima, K., Blas, B.L. & Santos, A.T. Jr (1985) The cercarial emergence of Schistosoma japonicum from Oncomelania quadrasi under outdoor conditions in the Philippines. Journal of Helminthology 59, 225–231.CrossRefGoogle ScholarPubMed
Keas, B.E. & Esch, G.W. (1997) The effect of diet and reproductive maturity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis (Trematoda). Journal of Parasitology 83, 96–104.Google Scholar
Lim, H.K. & Lie, K.J. (1969) The redial population of Paryphostomum segregatum (Trematoda: Echinostomatidae) in the snail Biomphalaria glabrata. Zeitschrift fur Parasitenkunde 32, 112–119.Google Scholar
McCarthy, A.M. (1990) The influence of second intermediate host dispersion pattern upon the transmission of cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 101, 43–47.Google Scholar
McCarthy, A.M. (1999a) The influence of second intermediate host species on the infectivity of metacercarial cysts of Echinoparyphium recurvatum. Journal of Helminthology 73, 143–145.Google Scholar
McCarthy, A.M. (1999b) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383–388.CrossRefGoogle ScholarPubMed
McCarthy, A.M. (1999c) Phototactic responses of the cercariae of Echinoparyphium recurvatum during phases of sub-maximal and maximal infectivity. Journal of Helminthology 73, 63–65.Google Scholar
McCarthy, A.M. (1999d) Photoperiodic cercarial emergence patterns of the digeneans Echinoparyphium recurvatum and Plagiorchis sp. from a mixed infection in Lymnaea peregra. Journal of Helminthology 73, 59–62.Google Scholar
Morley, N.J., Crane, M. & Lewis, J.W. (2002) Toxic effects of cadmium and zinc on the transmission of Echinoparyphium recurvatum cercariae. Journal of Helminthology 76, 157–163.Google Scholar
Morley, N.J., Crane, M. & Lewis, J.W. (2003a) Cadmium toxicity and snail–digenean interactions in a population of Lymnaea spp. (Gastropoda: Pulmonata). Journal of Helminthology 77, 49–55.Google Scholar
Morley, N.J., Crane, M. & Lewis, J.W. (2003b) Effects of cadmium and zinc toxicity to the orientation behaviour of Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae. Diseases of Aquatic Organisms 56, 89–92.Google Scholar
Morley, N.J., Crane, M. & Lewis, J.W. (2004a) Influence of cadmium exposure on the incidence of first intermediate host encystment by Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae in Lymnaea peregra. Journal of Helminthology 78, 329–332.Google Scholar
Morley, N.J., Lewis, J.W. & Adam, M.E. (2004b) Metacercarial utilisation of a naturally infected single species (Lymnaea peregra) snail community by Echinoparyphium recurvatum. Journal of Helminthology 78, 51–56.Google Scholar
Morley, N.J., Leung, K.M.Y., Morritt, D. & Crane, M. (2004c) Toxicity of anti-fouling biocides to encysted metacercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae) and their snail hosts. Chemosphere 56, 353–358.Google Scholar
Morley, N.J., Adam, M.E. & Lewis, J.W. (2007) Effects of temperature on the transmission and establishment of Echinoparyphium recurvatum (Trematoda: Echinostomatidae) metacercariae in Lymnaea peregra (Gastropoda: Pulmonata). Journal of Helminthology 81, 311–315.Google Scholar
Niemann, G.M. & Lewis, F.A. (1990) Schistosoma mansoni: influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production. Experimental Parasitology 70, 286–292.Google Scholar
Poulin, R. (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.Google Scholar
Prosser, C.L. (1973) Comparative animal physiology. Philadelphia, Saunders.Google Scholar
Randall, D., Burggren, W. & French, K. (2001) Eckert animal physiology. 5th edn.New York, Freeman and Company.Google Scholar
Rao, K.P. & Bullock, T.H. (1954) Q 10 as a function of size and habitat temperature in poikilotherms. American Naturalist 88, 33–44.Google Scholar
Rees, F.G. (1932) An investigation into the occurrence, structure and life histories of the trematode parasites of four species of Lymnaea (Lymnaea truncatula (Mull), Lymnaea palustris (Mull), and Lymnaea stagnalis (Linne)), and Hydrobia jenkinsi (Smith) in Glamorgan and Monmouth. Proceedings of the Zoological Society of London 1932, 1–32.Google Scholar
Richards, C.S. & Shade, P.C. (1987) The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. Journal of Parasitology 73, 1146–1151.Google Scholar
Russell Hunter, W.D. (1964) Physiological aspects of ecology in non-marine mollusca. pp. 83–126in Wilbur, K.M. & Yonge, C.M. (Eds) Physiology of Mollusca. New York, Academic Press.Google Scholar
Theron, A. (1981a) Dynamics of larval populations of Schistosoma mansoni in Biomphalaria glabrata. I. Rhythmic production of cercariae in monomiracidial infections. Annals of Tropical Medicine and Parasitology 75, 71–77.Google Scholar
Theron, A. (1981b) Dynamics of larval populations of Schistosoma mansoni in Biomphalaria glabrata. II. Chronobiology of the intramolluscan larval development during the shedding period. Annals of Tropical Medicine and Parasitology 75, 547–554.Google Scholar
Toledo, R., Munoz-Antoli, C. & Esteban, J.G. (1999) Production and chronobiology of emergence of the cercariae of Euparyphium albuferensis (Trematoda: Echinostomatidae). Journal of Parasitology 85, 263–267.Google Scholar
Toledo, R., Munoz-Antoli, C. & Fried, B. (2007) The use of echinostomes to study host–parasite relationships between larval trematodes and invertebrate and cold-blooded vertebrate hosts. Parasitology Research 100, 1177–1185.Google Scholar
Vernberg, W.B. (1969) Adaptations of host and symbionts in the intertidal zone. American Zoologist 9, 357–365.Google Scholar
Zischke, J.A. (1967) Redial populations of Echinostoma revolutum developing in snails of different sizes. Journal of Parasitology 53, 1200–1204.Google Scholar
Zischke, J.A. (1968) Reproduction of Echinostoma revolutum rediae when transferred to uninfected snails of different sizes. Journal of Parasitology 54, 39–42.Google Scholar