Abstract
Laboratory investigations on Galba truncatula experimentally infected with Calicophoron daubneyi were carried out to study the influence of natural light and sky nebulosity on cercarial emergence in snails subjected every week outdoors to a thermal shock (a mean of 12 °C for 3 h) during the patent period. The same study was also performed in G. truncatula naturally infected with Haplometra cylindracea according to the same protocol. Compared to infected controls always reared indoors at 20 °C, the number of cercariae emerging from snails subjected outdoors to a thermal shock was significantly greater, whatever parasite species. Natural light had an effect on snails releasing C. daubneyi cercariae after the thermal shock because their numbers were significantly higher between 601 and 1,200 lx and for the highest nebulosity values (7–8 octas). In contrast, the type of light used during thermal shock did not influence cercarial emergence of H. cylindracea because the numbers of cercariae per shedding snail noted under natural light or a 3,000-lx artificial light did not significantly differ from each other. Most snails releasing H. cylindracea cercariae were significantly more numerous for light levels higher than 3,000 lx. As for Fasciola hepatica cercariae, natural light had a significant influence on cercarial emergence of C. daubneyi, and this behavioural particularity for cercariae of both digeneans might be due to the fact that both species develop in the same ruminants and the same snail host.
Similar content being viewed by others
References
Abrous M. (1999) Les mollusques hôtes et les formes larvaires de Paramphistomum daubneyi Dinnik, 1962 (Trematoda) dans le centre de la France. Influence d'une co-infestation avec Fasciola hepatica Linné, 1758. Doctorate thesis, Univ Limoges, p 278
Abrous M, Rondelaud D, Dreyfuss G (1999a) Influence of low temperatures on the cercarial shedding of Paramphistomum daubneyi from the snail Lymnaea truncatula. Parasite 6:85–88
Abrous M, Rondelaud D, Dreyfuss G (1999b) Paramphistomum daubneyi and Fasciola hepatica: influence of low temperatures on the shedding of cercariae from dually infected Lymnaea truncatula. Parasitol Res 85:765–769
Audousset JC, Rondelaud D, Dreyfuss G, Vareille-Morel C (1989) Les émissions cercariennes de Fasciola hepatica L. chez le mollusque Lymnaea truncatula Müller. A propos de quelques observations chronobiologiques. Bull Soc Fr Parasitol 7:217–224
Augot D, Abrous M, Rondelaud D, Dreyfuss G (1996) Paramphistomum daubneyi and Fasciola hepatica: the redial burden and cercarial shedding in Lymnaea truncatula submitted to successive unimiracidial cross-exposures. Parasitol Res 82:623–627
Combes C (1995) Interactions durables. Ecologie et évolution du parasitisme. Masson, Paris, p 544
Díaz P, Pedreira J, Sánchez-Andrade R, Suárez JL, Arias MS, Francisco I, Fernandez G, Díez-Baños P, Morrondo P, Paz-Silva A (2007a) Risk periods of infection by Calicophoron daubneyi (Digenea: Paramphistomata) in cattle from oceanic climate areas. Parasitol Res 101:339–342
Díaz P, Paz-Silva A, Sánchez-Andrade R, Suárez JL, Pedreira J, Arias M, Díez-Baños P, Morrondo P (2007b) Assessment of climatic and orographic conditions on the infection by Calicophoron daubneyi and Dicrocoelium dendriticum in grazing beef cattle (NW Spain). Vet Parasitol 149:285–289
Düşen S, Öz M (2013) Helminth fauna of the Eurasian marsh frog, Pelophylax ridibundus (Pallas, 1771) (Anura: Ranidae), collected from Denizli Province, Inner-West Anatolia Region, Turkey. Helminthologia 50:57–66
Ginetsinkaya TA (1988) Trematodes, their life-cycles, biology and evolution. Amerind Publishing Co, Pvt Ltd, New Delhi, p 559
Goumghar MD, Abrous M, Ferdonnet D, Dreyfuss G, Rondelaud D (2000) Prevalence of Haplometra cylindracea infection in three species of Lymnaea snails in central France. Parasitol Res 86:337–339
Graczyk TK, Fried B (1999) Development of Fasciola hepatica in the intermediate host. In: Dalton JP (ed) Fasciolosis. CABI Publishing, Oxon, pp 31–46
Hodasi JKM (1972) The output of cercariae of Fasciola hepatica by Lymnaea truncatula and the distribution of metacercariae on grass. Parasitology 65:431–436
Kendall SB (1965) Relationships between the species of Fasciola and their molluscan hosts. Adv Parasitol 3:59–98
Kendall SB, McCullough FS (1951) The emergence of the cercariae of Fasciola hepatica from the snail Limnaea truncatula. J Helminthol 25:77–92
Mage C, Bourgne H, Toullieu JM, Rondelaud D, Dreyfuss G (2002) Fasciola hepatica and Paramphistomum daubneyi: changes in prevalences of natural infections in cattle and in Lymnaea truncatula from central France over the past 12 years. Vet Res 33:439–447
Malone JB, Yilma JM (1999) Predicting outbreaks of fasciolosis: from Ollerenshaw to satellites. In: Dalton JP (ed) Fasciolosis. CABI Publishing, Oxon, pp 151–183
Mas-Coma S, Valero MA, Bargues MD (2009) Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Vet Parasitol 163:264–280
Moukrim A, Oviedo J, Vareille-Morel C, Rondelaud D, Mas-Coma S (1993) Cercarial sheddings of Haplometra cylindracea. About several observations in Lymnaea truncatula during single or dual infections. Res Rev Parasitol 53:57–61
Navarro P, Lluch J (2006) Helminth communities of two green frogs (Rana perezi and Rana saharica) from both shores of the Alboran Sea. Parasite 13:291–297
Okulewicz A, Hildebrand J, Łysowski R, Buńkowska K, Perec-Matysiak A (2014) Helminth communities of green and brown frogs from Poland (Lower Silesia region). J Herpetol 48:34–37
Ollerenshaw CB (1971) Some observations on the epidemiology of fascioliasis in relation to the timing of molluscicide applications in the control of the disease. Vet Rec 88:152–164
Ollerenshaw CB, Smith LP (1969) Meteorological factors and forecast of helminthic diseases. Adv Parasitol 7:283–323
Rondelaud D (2004) Cressonnières naturelles du Limousin et risques de distomatose humaine à Fasciola hepatica. Ann Sci Limousin 15:1–14, Published online in Ann Sci Naturaliste (2012)
Rondelaud D, Fousi M, Vignoles P, Moncef M, Dreyfuss G (2007) Optimization of metacercarial production for three digenean species by the use of Petri dishes for raising lettuce-fed Galba truncatula. Parasitol Res 100:861–865
Rondelaud D, Vignoles P, Dreyfuss G (2009) La Limnée tronquée, un mollusque d’intérêt médical et vétérinaire. PULIM, Limoges, p 283
Rondelaud D, Titi A, Vignoles P, Mekroud A, Dreyfuss G (2013) Consequence of temperature changes on cercarial shedding from Galba truncatula infected with Fasciola hepatica or Paramphistomum daubneyi. Parasite 20:10
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611
Szmidt-Adjidé V, Abrous M, Adjidé CC, Dreyfuss G, Lecompte A, Cabaret J, Rondelaud D (2000) Prevalence of Paramphistomum daubneyi infection in cattle in central France. Vet Parasitol 87:133–138
Théron A (1984) Early and late shedding patterns of Schistosoma mansoni cercariae: ecological significance in transmission to human and murine hosts. J Parasitol 70:652–655
Théron A (1989) Hybrids between Schistosoma mansoni and S. rodhaini: characterization by cercarial emergence rhythms. Parasitology 99:225–228
Vignoles P, Rondelaud D, Dreyfuss G (2007) The populations of Galba truncatula, known for their natural infections with Haplometra cylindracea (Digenea, Plagiorchioidea), are better intermediate hosts for metacercarial production of Fasciola hepatica. Parasitol Res 100:1371–1373
Vignoles P, Dreyfuss G, Rondelaud D (2011) Haplometra cylindracea: variation in the dates of cercarial shedding for overwintering Galba truncatula. Parasite 18:181–184
Vignoles P, Titi A, Rondelaud D, Mekroud A, Dreyfuss G (2014) Fasciola hepatica: effect of natural light level on parasite cercarial emergence from temperature-challenged Galba truncatula. Parasite 21:8
Acknowledgments
The authors gratefully thank F. Marguerat, Meteo France, Limoges, for providing data on sky nebulosity during the time of their experiments on snails.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Titi, A., Rondelaud, D., Mekroud, A. et al. Natural light influences cercarial emergence of Calicophoron daubneyi but not that of Haplometra cylindracea from temperature-challenged Galba truncatula . Parasitol Res 113, 3557–3563 (2014). https://doi.org/10.1007/s00436-014-4021-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-014-4021-7