Journal of Helmínthology (1998) 72, 79-82
79
Larval trematode infections in freshwater gastropods from the Albufera Natural ~ Park in Spain ¡
~!
R. Toledo*, C. Muñoz-Antolí, M. Pérez and J.G. Esteban Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain
Abstract
Malacological samplings were made from January 1994 to December 1996 in the Albufera Natural Park (Valencia, Spain) to trace the dynamics of molluscan populations and the prevalence and intensity of infection by larval trematodes. A total of 10,533 freshwater gastropods belonging to seven species (Lymnaea auricularia, L. truncatula, L. palustris, L. peregra, Bithynia tentaculata, Physa acuta and Gyraulus chinensis) was examined, and 110 (1.04%) were found to harbour sorne of the nine distinguishable types of cercariae, namely four echinostome cercariae (Hypoderaeum conoideum, Echinoparyphium recurvatum, Euparyphium albuferensis, and Echinostoma sp.), four furcocercous cercariae, and one xiphidiocercous cercaria. This study shows that the composition of the snail and trematode communities may be determined by the particular environmental conditions present and the human intervention in the area.
Introduction
~1
The Albufera Natural Park, located lükm to the south of the city of Valencia (Spain), is one of the few wet areas remaining in Europe and constitutes a way station for many species of migratory birds. The park covers an area of 21,000 ha and has suffered a prolonged series of various ecological aggressions, beginning with the introduction of rice farming during the last century. Its peculiar geomorphological, edaphic, hydrological, climatic, botanical and fundamentally faunistic characteristics made it possible to declare the zone a Natural Park in 1986. It should be pointed out that two echinostome cercariae, Euparyphium albuferensis Esteban et al., 1997 and Hypoderaeum conoideum (Bloch, 1782), were recently recorded in this Park (Toledo et al., 1996, 1997a; Esteban et al., 1997). However, no more information is available on the larval trematodes and their transmission dynamics in this area.
*Fax: 34 6 3604611
E-mail: rafael.
[email protected]
During studies on the helminth fauna of this area between 1994 and 1996, a proportion of freshwater snails were observed to be infected with larval trematodes. Morever, seasonal changes were recorded in the population densities and the composition of gastropod communities, along with variations in the communities of larval trematodes, these changes probably being related to the variability of the habitat conditions throughout the ye ar. To date, severa! studies have been conducted in Spain, and also in Europe, on the role of the freshwater snails and habitat characteristics on the transmission of larval trematodes. Nevertheless, the majority of this research has been carried out in areas where the soil moisture is constant through the year. The present stud y is an attempt to establish differences in the degree of susceptibility of the molluscan hosts, and to determine the occurrence of larval trematodes and the possible temporal variation in the prevalences of cercariae in the molluscan species occurring in the Albufera Natural Park relative to environmental variations. Moreover, this study constitutes the first contribution to our knowledge of the transmission dynamics of larval trematodes in this area.
R. Toledo et al.
80
Materials and methods The Albufera Natural Park comprises three clearly differentiated ecosystems: (i) the so-called 'Dehesa', with a surface of 850 ha - a littoral sand bar separating the lake from the Mediterranean Sea; (ii) the Albufera Lake, a freshwater lagoon with an area of 2837 ha; and (iii) 12,000 ha of marshes surrounding the lake and characterized by rice fields. These fields are periodica!J.y.flooded from June to August and from November to January, while during the rest of the year remain dry. The climate is typically mediterranean with mild winters (average temperature: 10.8ºC) and long warm rainless summers (average temperature: 25.SºC). The average annual precipitatio.n is 430 mm and the rate of water annual renovahon is lüy- 1. The average solar radiation is 393cal cm- 2 d- 1 . In this area, serious additional aggressions occur due to: (i) industrialization in the neighbouring area; (ii) demographic expansion in outskirting villages; and (iii) touristic urbanization in coastal areas and the construction of a dense road network, which takes up over 40 ha. Waste and sewage from anthropogenic activities are dumped into the irrigation ditches and the lagoon. The excessive use of fertilizers and pesticides are further damaging factors. Despite these problems, the Albufera Natural Park presents a great richness in malacological, entomological, herpetological, piscicological, and mastozoological variety. This park is moreover particularly rich in migratory aquatic avian species, particularly anatids: Monthly snail samples were collected from their natural habitats located in the marsh ecosystem for three successive years from 1994 to 1996. The snails were brought alive to the laboratory, identified, mea~ sured, and then placed individually in separate Petn dishes (5 cm in diameter) containing 5 mi of spring water. In arder to detect emerged or emerging cercariae, the snails were carefully and periodically examined and those snails shedding cercariae were isolated. Others were checked daily for cercarial emission for up to 15 days after collection. At the end of .this period, sn~ils which failed to shed cercariae were d1ssected to confirm the absence of infection. The cercariae were identified according to Frandsen & Christensen (1984) and Schell (1985), and the chaetotaxy of echinostome cercariae were studied and specifically identified after Richard (1971), Grabda-Kazubska & Kiseliene (1989) and Toledo et al., (1997a,b).
Results A total of 10,533 snails belonging to seven species
[Lymnaea auricularia (Linnaeus, 1758), L. truncatula (Müller, 1774), L. palustris (Müller, 1774), L. peregra (Müller, 1774) (Gastropoda: Lymnaeidae), Bithynia tentaculata (Linnaeus, 1758) (Gastropoda: Bithynidae), Physa acuta (Draparnaud, 1805) (Gastropoda: Physidae) and Gyraulus chinensis (Dunker, 1848) (Gastropoda: Planorbidae)] were collected in the Albufera Natural Park during the three years of the study (3487 specimens in 1994, 3707 in 1995 and 3339 in 1996). Physa acuta was the most frequently occurring snail, followed by L. truncatula and L. peregra (table 1). The snail population densities appeared to be uniform throughout
the years considered, although they varied within each year as a function of the hydrological cycle, reaching a maximum in March and mínimum in April, July and November. From the total number of snails examined, only 110 specimens (1.04%) were found to be infected by t~ree morphologically distinguishable types of cercanae. According to the chaetotaxy, echinostome cercariae were identified as Hypoderaeum conoideum (Bloch, 1782), Echinoparyphium recurvatum (Linstow, 1873), ~uparyphium albuferensis Esteban et al., 1997 and Echmostoma sp. Identification of the furcocercous cercariae was not possible, though four different species of the s.trigea cercaria type were observed and they have been des1gned as types 1 to 4. The one xiphidiocercous cercaria recorded corresponds to the Virgulate cercaria type belonging to the family Lecithodendriidae (table 1). However, the snail species did not prove equally efficient as hosts for larval trematodes. The frequency of larval infections was thus highest in L. peregra and only L. auricularia was found to be free of infection. Lymnaea peregra and L. truncatula were found to harbour fou: and two types of cercaría! infections respect~vely,. wh1le L. palustris, P. acuta, B. tentaculata and G. chmenszs showed only one type of cercarial infection (table 1). The occurrence of mixed infections was not recorded. Furcocercous and echinostome cercariae were found to be the most abundant. Moreover, the number of infected snails varied throughout the year, reaching two peaks: one in March (37 specimens infected; 1.0% of the total mfected snails in this month) and another in September (50; 5.2%).
Discussion According to the literature, this is the first time that
Echinoparyphium recurvatum and Echinostoma sp. cer~ariae have been detected in Spain, although metacercanae of the first species were found in naturally infected specimens of L. auricularia and P. acuta (Simón-Vicente, 1963), and adult stages of E. lindoense Sandground & Bonne, 1940 have been recorded in Rattus norvegicus Berkenhout, 1769 (Rodentia: Muridae) (Gállego et al., 1984). Euparyphium albuferensis and H. conoideum cercariae and adults have been previously recorded in the same area of the present study (Toledo et al., 1996, 1997a,b; Esteban et al., 1997) and, also, adults of these species were detected in the Ebro Delta (Spain) (Gállego et al., 1984; Esteban et al., 1997). The rate of infection among different species of snails and their participation in trematode transmission exhibited fluctuations. Lymnaeids play a majar role in the transmission of the larval digeneans. Our results show that the highest frequency of larval infection was detected in L. peregra. This finding contrasts with other European records which point to L. auricularia as the most important first intermediate host for digenetic trematodes (Wesenberg-Lund, 1934; Arystanov, 1970; Adam & Le"".is, 199.3). This observation may be dueto the absence of th1s spec1es in the Albufera Natural Park. Adam & Lewis (1993) suggested that in areas where L auricularia are absent, this species may be replaced by L. peregra as the first intermediate host for severa! species of trematodes. In this sense, severa! species of digenetic trematodes have
Larval trematodes from freshwater gastropods in Spain rl
~
1
1
1
1
o;
1
1
1
1
1
1
1 ("()
1
N
1
1
"'
1
1
1
1
~
"" ""
q o
N
$"'
ci
1
1 1
1
1
1
1
1
1
1
rl
o.. Nci (1)
1
~
q o
81
been found to utilize both snail species as first intermediate hosts (Khan, 1962; Blair, 1977; Adam & Lewis, 1993). Temporal variations in trematode prevalences in a given snail community are common, and are probably related to temperature, the availability of food and host behaviour (Esch & Fernandez, 1993). Several authors (Crews & Esch, 1986; Abdul-Salam et al., 1994, 1997; Mattison et al., 1995) have reported temperature to be the most influential factor in larval trematode transmission, and consequently also the prevalence of infection. In the present paper, cercariae were absent during the hot season (from June to August) but were likewise absent in the cold season (from November to January), following the wet periods. The presence of cercariae coincides with dry spells which follow the periods in which the rice fields remain flooded. In areas where the presence of water is irregular, temperature may be a secondary factor. In this way, the fluctuations recorded in the present study appear to be linked with seasonal fluctuations of the water level in the Albufera Natural Park, probably as a function of irrigation of the rice fields. Our data show that in March and September, the prevalence of infected snails is highest. These peaks occur inmediately after the flooding of the rice fields, i.e. from November to January and from June to August. Only the trematode eggs deposited during these flooding periods may hatch and the miracidia subsequently infect the snail. All these aspects may account for the composition of the trematode fauna of the Albufera Natural Park, and the environmental conditions appear to be adequate for the development of this type of trematode life-cycle.
Acknowledgements
NOOOO
NNN N
\0 00 1..D 1
u)C"-lu)
The present study was supported by Spanish DGICYT Projects PB87-0135 and PB92-0517 of the Ministerio de Educación y Ciencia, Madrid. The authors wish to thank Lic. L. Sánchez (Valencia), for his technical collaboration. Thanks are also due to the Direcció General de la Conselleria de Medi Ambient de la Generalitat Valenciana (Valencia, Spain) for the licence to collect host materials in the field . This work was carried out while the second author (C.M.A.) was in receipt of a predoctoral fellowship from the Conselleria d'Educació i Ciencia de la Generalitat Valenciana (Valencia, Spain).
References Abdul-Salam, J., Sreelatha, B.S. & Ashkanani, H. (1994) Seasonal prevalence of trematode cercariae in Clypeomorus bifasciata (Gastropoda: Prosobranchia) in Kuwait Bay. Folia Parasitologica 41, 247-252. Abdul-Salam, J., Sreelatha, B.S. & Al-Kandari, W. (1997) Temporal variations in the infection of a population of Clypeomorus bifasciata (Gastropoda: Prosobranchia) by a digenean microphallid larva in Kuwait Bay. Journal of Helminthology 71, 1-7. Adam, M.E. & Lewis, J.W. (1993) The role of Lymnaea auricularia (Linnaeus) and Lymnaea peregra (Müller) (Gastropoda: Pulmonata) in the transmission of larval digeneans in the lower Thames Valley. fournal of Molluscan Studies 59, 1-6.
82
R. Toledo et al.
Arystanov, E. (1970) The effect of the ecological factors on the infestation of molluscs with larval digeneans. Parazitologiya 4, 210-218. Blair, D. (1977) A key to cercariae of British strigeids (Digenea) for which the life cycles are known and notes on the characters used. Journal of Helminthology 51, 155-166. Crews, A.E. & Esch, G.W. (1986) Seasonal dynamics of Halipegus occidualis (Trema toda: Hemiuridae) in Helisoma anceps and its impact on fecundi of the snail host. fou rnal of Parasitology 72, 646-651. Esch, G.W. & Femandez, J.C. (1993) Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. American Midland Naturalist 131, 209-237. Esteban, J.G., Toledo, R., Sánchez, L. & Muñoz-Antolí, C. (1997) Life-cycle of Euparyphium albuferensis n . sp. (Trematoda: Echinostomatidae) from rats in Spain. Systematic Parasitology, in press. Frandsen, F. & Christensen, N.O. (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trernatode species of medical and veterinary importance. Acta Tropica 41, 181-202. Gállego, J., Feliu, C. & Torres, J. (1984) Rattus norvegicus Berkenhout, 1769 (Rodentia: Muridae) hospedador de Echinostomátidos en el Delta del Ebro. pp. 367-376 in Aspectos actuales en Biología y Medicina. Libro homenaje al Prof A. Fumarola Busquets. Valladolid. Sever-Cuesta Ed. Grabda-Kazubska, B. & Kiseliene, V. (1989) Chaetotaxy and excretory system of the cercaria of Echinoparyphium recurvatum (Linstow, 1873) (Trematoda, Echinostomatidae). Acta Parasitologica Polonica 34, 325-335. Khan, D. (1962) Studies on larval trematodes infecting freshwater snails in London (UK) and sorne adjoining areas. Part V. Pharyngeal, longifurcate, diastome furcocercariae. Journal of Helminthologi; 36, 59-66. Mattison, R.G., Dunn, T.S., Hanna, R.E.B., Nizami, W.A. &
Ali, Q.M. (1995) Population dynamics of freshwater gastropods and epidemiology of their helminth infections with emphasis on larval paramphistomes in northern India. Journal of Helminthology 69, 125-138. Richard, J. (1971) La chétotaxie des cercaires. Valeur systématique et phylétique. Mémoires du Muséum Na tional d'Histoire Naturelle, Série A, Zoologie, 67, 1-179. Schell, S.C. (1985) Trematodes of North America. 263 pp. Idaho, University of Idaho Press. Simón-Vicente, F. (1963) Lymnaea auricularia (L.) y Physa acuta (Drap.) hospedadores d e metacercarias de Echinoparyphium recurvatum (Linstow, 1873) y de otras formas jóvenes de Digenea. Revista Ibérica de Parasitología 23, 315-324. Toledo, R., Muñoz-Antolí, C., Pérez, M. & Esteban, J.G. (1996) Redescription of the adult stage of Hypoderaeum conoideum (Bloch, 1782) (Trematoda: Echinostomatidae) and a new record in Spain. Research and Review in Parasitology, in press. Toledo, R., Muñoz-Antolí, C., Sánchez, L. & Esteban, J.G. (1997a) Chaetotaxy of the cercaria of Hypoderaeum conoideum (Bloch, 1782) (Trematoda: Echinostomatidae) emitted by Lymnaea peregra (Müller, 1774) in Spain. Research and Review in Parasitology, in press. Toledo, R., Muñoz-Antolí, C., Sánchez, L., BayssadeDufour, C. & Esteban, J.G. (1997b) Cercarial chaetotaxy of Euparyphium albuferensis Esteban et al., 1997 (Trematoda: Echinostomatidae) with a review of sorne genera of Echinostomatinae. Systematic Parasitology, in press. Wesenberg-Lund, C. (1934) Contribution to the development of the trematoda, Digenea. Part II. The biology of freshwater cercariae in Danish freshwaters. Mémoires de l'Académie des Sciences et des Lettres de Danemark 9, 1-223. (Accepted 15 October 1997) © CAB INTERNATIONAL, 1998
