IN NATURAL WATERCRESS BEDS IN THE LIMOUSIN REGION (FRANCE)

THE CHEMICAL AND BIOLOGICAL CONTROL OF LYMNAEA TRUNCATULA

IN NATURAL WATERCRESS BEDS IN THE LIMOUSIN REGION (FRANCE)

RONDELAUD D.*, VAREILLE-MOREL C.**

Summary :

The snails present in 17 natural watercress beds have been trea­

ted during 1 or 2 years by a control associating the use of a mol- luscicide (СuCl2) and the introduction of a predatory snail, Zonitoides nitidus. Lymnea truncatula was eliminated in only one year of treatment in 14 stations, and in two years in the three others. Elimination of other aquatic pulmonate snails was effected in two years for L. glabra, in 3 years for L. palustris, and in only one year for Physa acuta. Z. nitidus has disappeared from 1 2 watercress beds during the 4th year after treatment ; in the five others, the numbers of this predator increased during 1 or 2 years and then decreased before their disappearance.

F

cating the snail w h i c h acts as intermediate host in t h e p a r a s i t e ' s life c y c l e ( T a y l o r , 1 9 6 4 ) . N u m e r o u s o r g a n i c or c h e m i c a l molluscicidal agents h a v e b e e n p r o p o s e d to date ( r e v i e w e d b y E u z e b y , 1 9 7 1 ) , h o w e v e r , the principal difficulty e n c o u n t e r e d with their u s e c o n c e r n s t h e a m p h i b i o u s n a t u r e o f Lymnaea truncatula w h i c h allows it to e s c a p e toxic s u b s t a n c e s b y l e a v i n g t h e w a t e r a n d s u b s e q u e n t l y r e c o l o n i z e the treated habitats (Rondelaud, 1 9 7 8 a ) . Eradication o f the snail can b e a c c o m p l i s h e d , h o w e ­ ver, b y associating a) a sublethal d o s e o f a c h e m i c a l molluscicidal agent ( С и С У in the water drainage sys­

t e m d u r i n g t h e s p r i n g m a t i n g p e r i o d w i t h b ) t h e introduction o f a land pulmonate, Zonitoides nitidus, w h i c h is an active predator o f L. truncatula in J u n e - July. T h e first trials carried out in the s w a m p y m e a ­ d o w s o f t h e L i m o u s i n r e g i o n ( F r a n c e ) r e s u l t e d in eradication o f the snail from the majority o f its habi­

tats after a single year o f treatment (Rondelaud, 1 9 8 6 , 1 9 8 8 ) .

Since natural watercress b e d s play an important role in the e p i d e m i o l o g y o f h u m a n fasciolosis in the three d e p a r t m e n t s o f t h e L i m o u s i n r e g i o n ( R o n d e l a u d , 1 9 8 0 ; R o n d e l a u d a n d M a g e , 1 9 9 0 ) , w e d e s i r e d to k n o w w h e t h e r the a b o v e - m e n t i o n e d t e c h n i q u e c o u l d

* Laboratoire d'Histopathologie parasitaire, Faculté de Médecine, 2, rue du Docteur-Raymond-Marcland, F 87025 Limoges Cédex.

** Laboratoire de Malacologie Appliquée, Faculté des Sciences, 123, avenue Albert-Thomas, F 87060 Limoges Cédex.

Send correspondence to : Dr. D. Rondelaud , Faculté de Médecine, 87025 Limoges Cédex.

Les limnées présentes dans 17 cressonnières naturelles ont été sou- mises pendant 1 ou 2 années à un contrôle associant l'emploi d'un molluscicide (CuCl2) et l'introduction d'un mollusque prédateur, Zonitoides nifidus. La Limnée tronquée a été éliminée en une seule année de traitement dans 14 stations, en deux ans dans les trois autres. L'élimination des autres Pulmonés aquatiques s'est faite en deux ans pour L. glabra, 3 ans pour L. palustris et en une seule année pour Physa acuta. Le prédateur a disparu de 12 cresson- nières au cours de la 4e année après le traitement; dans les 5

autres, les effectifs de Z . nitidus se sont accrus pendant 1 ou 2 ans avant de diminuer par la suite et de disparaître.

MOTS CLES : Contrôle biologique. Contrôle chimique. Cressonnière.

Fasciolose. Lymnaea truncatula.

control the snail in this particular type o f habitat. T h e present study answers this question b y reporting the results from e x p e r i m e n t s carried out in natural water- cress b e d sites located in the Department o f Haute- V i e n n e ( F r a n c e ) .

T h e subsoil under the watercress b e d s was c o m p r i s e d of granite, diorite, or migmatite. T h e b e d s w e r e found a r o u n d s p r i n g s o r from s t r e a m s w h i c h o r i g i n a t e d from them. Their surface area was less than 20 m², and the w a t e r pH w a s b e t w e e n 6.1 and 6.9 with a free calcium ion concentration ranging from 5 to 15 mg/1.

O u r o b s e r v a t i o n s w e r e m a d e from 2 1 w a t e r c r e s s b e d s , o f w h i c h e l e v e n w e r e solely c o l o n i z e d b y L.

truncatula. F o u r o f t h e s e w e r e u s e d as c o n t r o l s (group 1 ) , and s e v e n w e r e s u b j e c t e d to the e x p e r i - mentation (group 2 ) . T h e ten other b e d s w e r e c o m - prised o f p o p u l a t i o n s o f L. truncatula and a n o t h e r a q u a t i c p u l m o n a t e : L. glabra ( 3 c a s e s , g r o u p 3 ) , L. palustris ( 2 c a s e s , g r o u p 4 ) , o r Physa acuta (5 cases, group 5 ) . T h e watercress b e d s from groups 2 to 5 w e r e t r e a t e d u s i n g c h e m i c a l a n d b i o l o g i c a l m e t h o d ( R o n d e l a u d , 1 9 8 6 ) . Eight liters o f C u C l², 2 H²0 (at 0.1 mg/1) w e r e p o u r e d ( 2 x 4 1) into e a c h area in April during the spring mating p e r i o d o f L.

truncatula. Zonitoides nitidus w a s t h e n i n t r o d u c e d (20 per m²) in J u n e or J u l y and a layer o f freshly-cut grass w a s placed. T h e watercress b e d s from group 2 w e r e treated for o n e year, while those o f the three other groups w e r e treated for t w o or three years until the aquatic pulmonates had disappeared.

P a r a s i t e , 1 9 9 4 , 1, 8 9 - 9 2 Note de recherche -89

KEY WORDS : Biological control. Chemical control. Fasciolosis. Lymnaea truncatula. Watercress bed.

R é s u m é : L E CONTROLE CHIMIQUE E T B I O L O G I Q U E D E LYMNAEA TRUNCA- TULA M Ü L L E R DANS LES CRESSONNIERES NATURELLES D U L I M O U S I N ( F R A N C E ) .

Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1994011089

R O N D E L A U D D . , V A R E I L L E - M O R E L С.

T h r e e series o f observations w e r e carried out in e a c h site: a ) the snails w h i c h had survived the winter w e r e c o u n t e d in April (sampling A), b ) the spring genera­

t i o n w a s c o u n t e d at t h e e n d o f J u n e b e f o r e t h e streams dried (sampling B ) , and c ) a search for survi­

vors was m a d e in S e p t e m b e r during the first post- s u m m e r rains (sampling C). T h e investigations w e r e u n d e r t a k e n o v e r a six-year p e r i o d and involved all snails present in e a c h watercress b e d , comprising a s e a r c h for the following s p e c i e s : L. truncatula, the o t h e r a q u a t i c p u l m o n a t e s , Pisidium casertanum, Succinea putris, and Z. nitidus. All counts w e r e per­

formed b y visual s e a r c h and the snails w e r e left in p l a c e after b e i n g counted.

T h e data o b t a i n e d for e a c h group o f watercress b e d s w e r e then averaged, and standard deviations establi­

s h e d , t a k i n g into a c c o u n t t h e date t h e c o u n t w a s m a d e and the snail s p e c i e s .

T h e n u m b e r s o f L. truncatula w e r e rather constant o v e r the six years in the c o n t r o l s from g r o u p 1. A m e a n o f 37 to 42 overwintering snails w a s c o u n t e d in sampling A ; in sampling В and C, the m e a n num­

bers o f snails w e r e respectively 8 7 - 1 2 4 and 4 1 - 5 7 per w a t e r c r e s s b e d ( F i g . 1 ) . T h e m e a s u r e s t a k e n t o control the snails resulted in snail d i s a p p e a r a n c e at

sampling С during the first year (Figs. 2b and d) or by the p e r s i s t e n c e o f a few survivors during the s a m e sampling from group 2 (2 snails at o n e site, Fig. 2 a ) and group 4 (Fig. 2 c ) . T h e s e snails disappeared natu­

rally (Fig. 2 a ) or w e r e eradicated at the e n d o f the s e c o n d year (Fig. 2 c ) . No recolonization o f the treated sites was observed during the six years o f observation.

T h e r e was considerably m o r e variability in the results from the watercress b e d s o f groups 3 to 5 with the t h r e e o t h e r p u l m o n a t e s . It w a s n e c e s s a r y to a p p l y control measures for t w o years to eliminate L. glabra from its habitats and recolonization o f o n e site w a s o b s e r v e d during the sixth year (Fig. 2 b ) . It t o o k three years to eliminate L. palustris from the sites o f w h i c h o n e w a s a l s o r e c o l o n i z e d d u r i n g t h e s i x t h y e a r (Fig. 2 c ) . Physa acuta w a s e l i m i n a t e d in o n l y o n e year and n o recolonization was o b s e r v e d (Fig. 2 d ) . Pisidium casertanum totally disappeared from the 14 treated watercress b e d s or persisted in reduced num­

bers in three sites from group 2 ( 3 to 24 per m2 o f habitat). T h e n u m b e r o f S. putris d r o p p e d to 5 0 % o f the initial value during a p p l i c a t i o n o f c o n t r o l m e a ­ sures at group 2 and 3 sites, h o w e v e r , it rapidly r e p o - pulated in only o n e y e a r after cessation o f treatment (results not s h o w n ) .

Fig. 1. - Numerical distribution of L. truncatula in control watercress beds during six years. Mean values and standard deviations refer to sampling A, B, and С made respectively in April, at the end of June, and in September.

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CONTROL OF LYMNAEA TRUNCATULA IN WATERCRESS BEDS

Fig. 2. - N u m e r i c a l d i s t r i b u t i o n o f f o u r a q u a t i c s n a i l s in 17 w a t e r c r e s s b e d s s u b j e c t e d t o b i o l o g i c a l a n d c h e m i c a l c o n t r o l m e a s u r e s . M e a n v a l u e s a n d s t a n d a r d d e v i a t i o n s r e f e r t o s a m p l i n g A, В a n d С m a d e r e s p e c t i v e l y in April, at t h e e n d o f J u n e , a n d in S e p t e m b e r .

Fig. 3. - N u m e r i c a l distribution o f Z. nitidus in 17 w a t e r c r e s s b e d s s u b j e c t e d t o b i o l o g i c a l a n d c h e m i c a l c o n t r o l m e a s u r e s ( g r o u p s 2 t o 5 ) . M e a n v a l u e s a n d s t a n d a r d d e v i a t i o n s refer to s a m p l i n g В m a d e just b e f o r e t h e e v e n t u a l i n t r o d u c t i o n o f o t h e r p r e d a t o r s (with t h e e x c e p t i o n o f t h e first y e a r ) . T h e asteriks i n d i c a t e the y e a r s that the habitat c o n t r o l m e a s u r e s w e r e a p p l i e d .

Note de recherche 91

RONDELAUD D., VAREILLE-MOREL С.

T h e n u m b e r s o f Z. nitidus regularly d e c r e a s e d during t h e years following their introduction into g r o u p 2 sites. T h e m e a n value o f 1 0 8 adult snails w h i c h w e r e introduced in e a c h station during the first year drop­

p e d to less than 3 snails p e r site during the 4th year at sampling В (Fig. 3 a ) . T h e regular introduction o f predators in the group 3 and 4 sites for two or three years resulted in increased n u m b e r s w h i c h persisted e v e n o n e o r two years after discontinuing treatment ( F i g s . 3 b a n d c ) . A g r a d u a l d e c r e a s e in n u m b e r s , h o w e v e r , w a s subsequently o b s e r v e d similar to that n o t e d in the group 2 sites. T h e numerical o u t c o m e in the group 5 sites was identical to that n o t e d in group 2 sites, with the d i s a p p e a r a n c e o f predators at the e n d o f the 4th year o f study (Fig. 3 d ) .

T h e results o b t a i n e d with m i x e d treatment o f water­

cress b e d s w e r e partially similar to those o b t a i n e d b y R o n d e l a u d ( 1 9 8 6 , 1 9 8 8 ) w h e n this t e c h n i q u e w a s used in s w a m p y Limousin m e a d o w s . H o w e v e r , three p o i n t s w a r r a n t s p e c i a l c o m m e n t . F i r s t , it t o o k a clearly greater length o f time (2 or 3 years) to eradi­

c a t e L. glabra o r L. palustris from w a t e r c r e s s b e d s than it did to eradicate L. truncatula. T h e time requi­

red for successful biological control o f these t w o s p e ­ c i e s w a s p r e v i o u s l y d e t e r m i n e d w h e n R o n d e l a u d ( 1 9 7 8 b ) indicated that five s u c c e s s i v e years o f treat­

m e n t w e r e r e q u i r e d to eliminate L. glabra from its habitats using Z. nitidus. Although use o f the toxic c h e m i c a l certainly results in i n c r e a s e d mortality o f t h e s e s n a i l s p e c i e s w h i c h g o t h r o u g h t h e w i n t e r (Rondelaud, 1 9 8 6 ) , it is h o w e v e r clear that c h e m i c a l treatment associated with predators is insufficient to e r a d i c a t e t h e s e snails in only o n e year. T h i s result m a y b e e x p l a i n e d b y t h e w a t e r c r e s s b e d s ' g r e a t e r depth and c o n s e q u e n t l y b y stream velocity, w h i c h is generally greater w h e n L. glabra or L. palustris w e r e p r e s e n t . O n e o f t h e p o s s i b l e s o l u t i o n s to c o n s i d e r w o u l d b e to increase the sublethal concentration o f C u C b (0.5 mg/1) a n d / o r increase the v o l u m e o f c h e ­ mical w h i c h is p o u r e d into the treatment sites.

Secondly, recolonization o f the treated habitats by L.

glabra or L. palustris beginning from the 6th year o f study can b e explained by snail migration from areas downstream and from the s a m e water drainage sys­

tem. T h e s e two species would thus b e capable, like L.

truncatula ( M o e n s , 1 9 8 2 ) , o f m i g r a t i n g u p s t r e a m against the water current, requiring a time period (2 to 3 years) that Rondelaud ( 1 9 8 3 ) reported for L. trunca­

tula during reinvasion o f swampy m e a d o w s after the snail was e r a d i c a t e d using b i o l o g i c a l m e t h o d s . T h e a b s e n c e o f habitat recolonization b y L. truncatula can be explained by the time period (7 to 10 years) requi­

red by the snail to invade watercress beds previously treated by a biological method (Ximenes, 1991).

Thirdly, the gradual numerical d e c r e a s e o f Z. nitidus in w a t e r c r e s s b e d s c o l o n i z e d b y L. truncatula

c o n c o r d s with w h a t R o n d e l a u d ( 1 9 8 2 ) r e p o r t e d for b e d s o f rushes o n s l o p e s and river b a n k s treated b y a biological method. O n the other hand, the temporary s p r e a d o f t h e p r e d a t o r in sites c o l o n i z e d b y t w o snails is m o r e difficult to interpret. T h e m o s t plausible hypothesis is that living conditions in t h e s e last sites w e r e most favourable for c o l o n y d e v e l o p m e n t a n d that the final numerical d e c r e a s e w a s linked to the progressive d i s a p p e a r a n c e o f potential prey.

REFERENCES

EUZEBY J . : Les maladies vermineuses des animaux domes­

tiques et leurs incidences sur la pathologie humaine.

Tome II. Fase. 1. Livre 1. Vigot frères, Paris, 1971, 798 p.

MOENS R. : Mécanisme de réinfestation par Lymnaea trun-

catula des terrains propices à la fasciolose. Malacologia, 1982, 22, 29-34.

RONDELAUD D.: Le comportement des Limnées tronquées (Lymnaea (Galba) truncatula Muller) saines ou infestées par Fasciola hepática L. en présence de leurs prédateurs.

Ann. Parasitol. Hum. Сотр., 1978a, 53, 63-74.

RONDELAUD D.: Les effets à long terme d'un contrôle biolo- gique par prédation. Étude expérimentale de la dyna- m i q u e de plusieurs e s p è c e s de M o l l u s q u e s . Ann.

Parasitol. Hum. Сотр., 1978b, 53, 215-222.

RONDELAUD D.: Données épidémiologiques sur la distoma- tose humaine à Fasciola hepática L. dans la région du Limousin, France. Les plantes consommées et les limnées vectrices. Ann. Parasitol. Hum. Сотр., 1980, 55, 393-405.

RONDELAUD D.: Le contrôle biologique par prédation de Lymnaea truncatula Muller. Etude expérimentale de la dynamique de cinq espèces de Mollusques après arrêt du traitement. Malacologia, 1982, 22, 697-700.

RONDELAUD D.: Les réseaux de drainage superficiel et leur colonisation par Lymnaea truncatula Müller. A propos de quatre années d'observations en Haute-Vienne. Ann.

Rech. Vét., 1983, 14, 57-63.

RONDELAUD D.: Le contrôle mixte et alterné de Lymnaea

truncatula Müller par voie chimique et biologique.

Premiers essais expérimentaux sur le terrain. Ann. Rech.

Vet., 1986, 17, 15-20.

RONDELAUD D.: Le contrôle mixte et alterné de Lymnaea

truncatula Müller. A propos de trois techniques pour l'épandage du molluscicide. Ann. Rech. Vét., 1988, 19, 279-282.

RONDELAUD D., MAGE C : The natural watercress ponds in Limousin (France) and their infection by Fasciola hepá- tica. Bull. Soc. Fr. Parasitol., 1990, 8, Suppl. 2, 692.

TAYLOR E.L.: F a s c i o l i a s i s and the liver fluke. F.Α.О.

Agricultural Studies, 1964, n° 64, 234 p.

XIMENES T.: Le contrôle biologique de Lymnaea truncatula

Müller, hôte intermédiaire de Fasciola hepática L.

Possibilités et perspectives. Thèse Doct. Vét., Alfort, 1991, n° 122, 103 p.

Accepté le 2 janvier 1994

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