INVENTORY OF WILD RODENTS A N D LAGOMORPHS AS NATURAL HOSTS OF FASCIOLA HEPATICA O N A FARM LOCATED I N A HUMID AREA
I N LOIRE ATLANTIQUE (FRANCE)
MÉNARD A.*, L'HOSTIS M.*, LERAY G.**, MARCHANDEAU S.**, PASCAL M.***, ROUDOT N.*, MICHEL V.**** & CHAUVIN A.*
Summary:
With the objective of studying the role of wild fauna in the epidemiology of fasciolosis disease, a definitive wild-host inventory was carried out in a french farm where infected domestic hosts (cows) cohabit with wild potential ones. Liver flukes, faecal eggs and antibodies were looked for in lagomorphs (Oryctolagus cuniculus) and rodents (Myocastor coypus, Ondatra zybethicus, Rattus norvegicus, Arvicola sapidus and micromammal species) trapped in the study area. Presence of Fasciola hepatica was detected in two species: O. cuniculus and M. coypus. Infection rates were respectively 34 % (42/124) and 55 % (106/193).
Liver flukes were found in 78 M. coypus (n = 192) and 1 1 O. cuniculus (n = 35). No other species was infected by F. hepática. The number of animals shedding fluke eggs was higher in M. coypus (49 out of 1 27 sampled; 38.6 %) than in O. cuniculus (two out of 17 sampled; 11.7 %). The results indicate that M. coypus may play a role in the maintenance and the dissemination of F. hepatica in various environments and open a discussion on the role of other natural wild hosts.
KEY WORDS : epidemiology, Fasciola hepatica, Loire Atlantique, Myocostor coypus, Oryctolagus cuniculus, rodents, wild fauna.
Résumé :
INVENTAIRE DES PETITS MAMMIFÈRES SAUVAGES HÔTES NATURELS DE FASCIOLA HEPATICA DANS UNE EXPLOITATION AGRICOLE SITUÉE DANS UNE ZONE HUMIDE DE LOIRE ATLANTIQUEAfin d'étudier le rôle de la faune sauvage dans l'épidémiologie de la fasciolose, un inventaire des rongeurs et des lagomorphes hôtes sauvages de Fasciola hepatica a été effectué dans une ferme française où des bovins infestés cohabitent avec des animaux sauvages potentiellement hôtes. La présence de douves hépatiques, d'oeufs dans les fèces et d'anticorps sanguins a été recherché chez des lagomorphes (Oryctolagus cuniculus) des rongeurs (Myocastor coypus, Ondatra zybethicus, Rattus
norvegicus, Arvicola sapidus et micromammifères) capturés sur la zone d'étude. La présence de Fasciola hepatica a été observée chez deux espèces : O. cuniculus et M. coypus. Les taux d'infestation sont respectivement de 34 % (42/124) et 55 % (106/193). Des douves ont été isolées dans 78 foies de M. coypus (n = 192) et 11 foies de O. cuniculus (n = 35).
Aucune autre espèce n'est infestée. Le nombre d'animaux infestés excréteurs d'oeufs est plus élevé chez M. coypus (49 sur les
127 échantillonnés ; 38,6%) que chez O. cuniculus (2 sur les 17 échantillonnées; 11,7 %). Les résultats témoignent du rôle possible de M. coypus dans le maintien et la dissémination de F. hepatica et permettent de discuter du rôle des autres hôtes sauvages.
MOTS CLES :
épidémiologie, Fasciola hepatica, faune sauvage, Loire Atlantique, Myocastor coypus, Oryctolagus cuniculus, rongeurs.INTRODUCTION
F asciola hepatica is an e u r y x e n e parasite found in m a n y d o m e s t i c s p e c i e s [ b o v i n e s , o v i n e s , JL c a p r i n e s ( R e d d i n g t o n et al., 1986)] a n d wild s p e c i e s like rodents ( D e l e c o l e , 1 9 8 2 ; Molan & Hus- sein, 1 9 8 8 ; M a s - C o m a et al, 1 9 8 8 a n d 1 9 8 9 ) , l a g o - m o r p h s ( B a i l e n g e r et al, 1 9 6 5 ; T e r r a c c i a n o et al., 1 9 8 8 ) , suidae ( B o l l o et al., 1 9 9 3 ) a n d wild ruminants
* UMR ENVN/INRA "Interactions Hôte-Parasite-Milieu", École Natio- nale Vétérinaire de Nantes, BP 40706, 44307 Nantes, France.
** Office National de la Chasse, 53, rue Russeil, 44000 Nantes, France.
*** Département hydrobiologique et faune sauvage, Université Rennes I, 35042 Rennes Cedex, France.
**** Laboratoire de pathologie infectieuse, École Nationale Vétérinaire de Nantes, BP 40706, 44307 - Nantes, France.
Correspondence: Alexandre Ménard.
Tél. : 33 (0)2 40 68 77 00 - Fax : 33 (0)2 40 68 77 51.
( B a r r a s , 1 9 8 2 ; J o h a n n s e n et al, 1 9 8 9 ; Alcouffe et al., 1 9 9 2 ) , a n d e v e n in Man. T h e e c o n o m i c c o n s e q u e n c e s o f d o m e s t i c ruminant infestation ( M a g e et al., 1 9 8 9 ; Mage, 1 9 9 0 ) and the increase o f the n u m b e r o f human c o n t a m i n a t i o n s w o r l d w i d e ( M a s - C o m a et al., 1 9 9 9 ) warrant an effective c o n t r o l o f fasciolosis. T h e use o f fasciolicide m o l e c u l e s is r e c o m m e n d e d to stop the laying o f adult parasites p r e s e n t in cattle. T h e e x i s - t e n c e o f infested wild animals c a n b e a limit to this strategy b y allowing the pursuit o f the parasitic life c y c l e a n d t h e reinfestation o f s y m p a t r i c potential hosts like d o m e s t i c animals or man. Dreyfuss et al, in 1 9 9 4 , d e m o n s t r a t e d h u m a n c o n t a m i n a t i o n s in w a t e r c r e s s b e d s l o c a t e d in plots outside o f cattle pre- s e n c e but w h e r e t h e p r e s e n c e o f wild rodents a n d l a g o m o r p h s w a s reported. T o establish the real impact o f wild fauna in fasciolosis e p i d e m i o l o g y , it is impor- tant to k n o w w h i c h s p e c i e s are s u s c e p t i b l e to the parasite a n d w h i c h o n e s h a v e a m o r e durable rela- tionship with it.
Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/2000072077
MÉNARD A., L'HOSTIS M., LERAY G., MARCHANDFAU S., PASCAL M., ROUDOT N., MICHEL V. & CHAUVIN A.
T h e aim o f this study is to list the wild small mammals species infested by F. hepática o n a small scale in France, where wild and domestic animals live in sympatry, and to discuss the nature o f the relationships established bet
w e e n these species and F. hepática to consider their role in the parasite's maintenance and dissemination.
MATERIALS AND METHODS
DESCRIPTION OF THE STUDY AREA AND COW-BREEDING
T
h e study w a s carried out o n the Massereau reserve (Loire Atlantique, F r a n c e ) m a n a g e d b y the National Hunting Office (Office National de la Chasse; O N C ) , from 1 9 9 5 to 1 9 9 8 . T h e total surface o f the reserve is 3 9 3 hectares (982.5 acres). A study area o f 45 hectares (112.5 acres) was defined (area 1, Fig. 1).A s e c o n d area o f 19 hectares ( 4 7 . 5 acres), ecologically similar to the first, had to b e defined to increase the size o f our samples (area 2, Fig. 1). Each o f these two areas consisted o f three ecologically different environ
ments: clamp m e a d o w s (environment 1 ) surrounded b e l o w by slimy calcareaous borders (environment 2 )
Fig. 1. - S t u d y a r e a t o p o g r a p h y .
o n e part o f which is flooded during the floods o f the river (la Loire) (environment 3 ) . T h e s e three environ
ments are potential Lymnaea truncatula habitats.
T h e results will b e dealt with d e p e n d i n g o n the three environments and not o n the areas.
Eighteen c o w s (Nantaise b r e e d ) grazed in area 1.
Cattle w e r e treated yearly with triclabendazole ( F a s - c i n e x ND). T h e serological infection rate o f cattle w a s m e a s u r e d b y ELISA m e t h o d to 9 0 % (n = 1 2 ) ( B o u l a r d et al, 1 9 9 5 ) .
Foot print observation proved the presence o f wild ani
mals sympatric with c o w s .
SAMPLING OF THE WILD SPECIES
A total o f 2 5 0 traps o f INRA and Sherman traps and rat-trap-Manufrance-for-capture-of-small-rodents types w e r e set every three months, according to the method described by Spitz ( 1 9 6 5 ) , in the three area 1 environ
ments from N o v e m b e r 1 9 9 6 to N o v e m b e r 1997, and in the three area 2 environments, in N o v e m b e r 1 9 9 6 and July 1997 (Fig. 1). Trappings using rat-trap-Manufrance- for-capture-of-small-rodents w e r e pursued in the third environment o f the area 1 until n o v e m b e r 1999, at the same periodicity. Thirty traps for the capture o f medium size and big rodents w e r e set every three months from N o v e m b e r 1 9 9 6 to J u l y 1 9 9 8 , and divided out a m o n g the three area 1 environments (Fig. 1 ) .
All the animals captured w e r e euthanasied.
A line o f 55 rabbit traps w e r e set in part o f area 1 with the highest concentration o f rabbits (Oryctolagus cuni- culus), from N o v e m b e r 1 9 9 6 to March 1 9 9 8 . A study carried out b y ONC necessitated the release o f the Oryctolagus cuniculus trapped. T o demonstrate the fluke carrying by O. cuniculus, O. cuniculus shooting w e r e also carried out b y ONC, in the s a m e place. T h e carcasses w e r e c o l l e c t e d monthly.
INFECTION DIAGNOSIS IN THE SAMPLED SPECIES Table I summarizes the four methods o f infestation dia
gnosis used for e a c h s p e c i e s .
T h e animal autopsies included a meticulous e x p l o r a tion o f the c h o l e d o c canal and biliary ducts followed by a fine cut o f the liver.
Bile was extracted after puncturing the gall bladder.
T h e bile was o b s e r v e d to l o o k for fluke eggs.
T h e c o p r o s c o p i c diagnosis w a s carried out using a iodomercurate potassium flotation m e t h o d ( K n a p p &
Presidente, 1 9 7 1 ) .
Serological infestation was established using an ELISA m e t h o d (Boulard, 1 9 9 5 ) , adapted for e a c h s p e c i e s .
STATISTICS
T h e m e a n values w e r e subjected to Anova or to the c o m p a r i s o n test o f experimental frequencies.
78 Mémoire P a r a s i t e , 2 0 0 0 , 7, 7 7 - 8 2
Autopsy Bile examination Coproscopy Serology
Infected Adult Bile- Faecal
Captures animals Realized worms Reali/ed eggs Realized eggs Realized Positives
C. capreohts 3 2 0 0 0 0 2 2 3 2
O. cuniculus 124 42 3 5 1 1 27 10 17 2 6 8 3 3
M. coypus 193 1 0 6 192 78 1-') 8 8 127 4 9 167 133
O. zybethicus 22 2 22 0 13 0 14 2 0 0
R. norvegicus 6 5 ( 3 2 + 3 3 ) * 0 65 ( 3 2 + 3 3 ) * 0 0 0 0 0 3 5 (15 + 2 0 ) * 0
A. sapidus 1 0 1 ü 1 0 0 0 0 0
A. sylvaticus 361 0 3 6 1 0 0 0 0 o 0 0
M. arvalis 89 0 89 0 0 0 0 0 0 0
M. agrestis 4 0 4 0 0 0 0 0 0 0
C. glareolus 16 0 1 6 0 0 0 0 0 0 0
* Total of the Rattus norvegicus captured (number of Rattus norvegicus captured between november 1997 and november 1998 + number of Rattus norvegicus captured between november 1998 and november 1999).
Table I. - Number of infected animals depending on the species and the screening method.
O. cuniculus M. coypus O. zybeticus
C a p t u r e s A B
c
s C a p t u r e s A B C S C a p t u r e s A B cN % N % N % N % N % N % N % N % N % N % N %
H u m i d m e a d o w s e n v i r o n m e n t 1
2 2 0 2 0 2 0 1 1 0 0 4 8 4 7 15 Í2 24 3 7 1 6 4 6 3 0 8 8 0 0 5 0
N % N % N % N % N % N % N % N % N % N % N %
S w a m p s b o r d e r e n v i r o n m e n t 2
122 3 2 3 4 2 5 3 7 15 1 3 6 7 4 8 6 9 6 9 4 1 6 2 4 8 4 3 4 2 4 5 4 9 3 3 0 2 (1 2 0
N % N % N % N % N % N % N % N % N % N % N %
S w a m p s e n v i r o n m e n t 3
0 0 0 0 0 0 0 0 0 7 6 7 6 5 6 4 8 6 4 4 7 5 3 4 3 7 2 11 11 II 4 II 7 2 9
RESULTS
EVALUATION OF THE CAPTURES
T
a b l e I gives the n u m b e r o f trapped animals p e r species. Nine s p e c i e s w e r e sampled in the study areas: four aquatic rodent s p e c i e s , four micro- m a m m a l rodent s p e c i e s a n d o n e l a g o m o r p h s p e c i e s . Four s p e c i e s w e r e captured m o r e often: 3 6 l Apodemus sylvaticus, 193 Myocastor coypus, 124 Oryctolagus cuniculus a n d 8 9 Microtus arvalis.
T a b l e II gives the repartition o f the captures b a s e d o n the environment. T h e n u m b e r o f trapped M. coypus w a s not significantly different in the three environments ( 3 9 % o f M. coypus trapped w e r e captured in envi
r o n m e n t 1, 3 6 % in environment 2, 25 % in environ
ment 3 ) . T h e results w e r e the s a m e for O. zybethicus 0 6 . 4 % o f O. zybethicus trapped w e r e captured in envi
r o n m e n t 1, 13-6 % in e n v i r o n m e n t 2 and 5 0 % in envi
r o n m e n t 3 ) . O n l y two Rattus norvegicus w e r e trapped
in the driest b i o t o p e (environment 1 ) ( 6 . 2 % out o f the 32 R. norvegicus trapped a m o n g the three environ
m e n t s ) against 4 0 . 6 % in environment 2 and 53-2 % in environment 3- O n the contrary, m i c r o m a m m a l s w e r e trapped m o r e frequently in dry biotopes: 5 6 . 4 % in the environment 1 and 4 2 . 6 % in environment 2 against 1 % in environment 3- T h e trapping and the shooting o f O. cuniculus w e r e carried out in only o n e envi
ronment.
DIAGNOSIS OF FLUKE INFECTION
T h e results o f the infection diagnosis per s p e c i e s are summarized in T a b l e I. W e o b s e r v e two s p e c i e s for which all the screening methods used show fluke infec
tion: M. coypus and O. cuniculus. In these two species, fluke stages w e r e detected [liver flukes in 7 8 M. coypus (n = 1 9 2 ) and H O . cuniculus (n = 3 5 ) ; faecal eggs in 4 9 M. coypus (n = 1 2 7 ) and two O. cuniculus (n = 17)1 a n d a n t i b o d i e s w e r e o b s e r v e d in b l o o d s a m p l e s [133 M. coypus (n = 167) and 33 O. cuniculus (n = 68)].
NATURAL H O S T S O F FACIÓLA HEPÁTICA
A = a u t o p s y ; B = b i l e o b s e r v a t i o n ; C = c o p r o s c o p i c s c r e e n i n g ; S = s e r o l o g y ; N = s a m p l e s i z e .
T a b l e II. - F. hepatica i n f e c t i o n rate d e p e n d i n g o n t h e s p e c i e s , t h e s c r e e n i n g m e t h o d s a n d t h e e n v i r o n m e n t s .
MENARD A., L'HOSTIS M., LERAY G., MARCHANDEAU S., PASCAL M., ROUDOT N.. MICHEL V. & CHAUVIN A.
T h e infection rates m e a s u r e d (all screening m e t h o d s c o m b i n e d ) in these s p e c i e s are 55 % in M. coypus and 3 4 % in O. cuniculus. T h e difference is not significant.
O n the contrary, the frequency o f faecal egg shedding w a s significantly higher (p < 0 . 0 0 1 ) in M. coypus than in O. cuniculus ( 4 9 / 1 2 7 and 2 / 2 respectively instead o f 2 / 1 7 for O. cuniculus).
In O. zybethicus, the diagnosis w e r e not the s a m e depending o n the screening m e t h o d used: two animals s h e d faecal e g g s but n o autopsy revealed fluke livers and n o antibodies w e r e detected in b l o o d samples.
None o f the 6 5 R. norvegicus trapped w e r e infested.
T h e ELISA m e t h o d used in 35 b l o o d samples did not detect any fluke antibodies.
No animal out o f the four m i c r o m a m m a l s p e c i e s sam
pled w e r e s h o w n to h a v e fluke livers.
T a b l e II gives infection rates depending o n the spe
cies and the environment w h e r e they w e r e trapped.
Infected M. coypus w e r e d e t e c t e d in the three envi
ronments. T h e p r e v a l e n c e m e a s u r e d in environment 3 was significantly higher (p < 0 . 0 0 1 ) than the o n e m e a sured in e n v i r o n m e n t o n e ( 5 6 % out o f the 7 6 M. coy
pus trapped in s w a m p s w e r e infected c o m p a r e d to 15 % in humid m e a d o w s ) .
DISCUSSION
T
h e present sampling o f the herbivorous mammals a g r e e s with t h o s e carried out b y ONC ( u n p u b l i s h e d data). O n l y Micromys minutus, w h o s e p r e s e n c e has b e e n reported by ONC, w a s not trapped in o u r study. T h e trapping p r o t o c o l e ( e x h a u s tive trapping in area 1 and sampling trapping in area 2 ) gives a g o o d representation o f the potential F. hepá
tica hosts present.
T h e results confirm the e x i s t e n c e o f various wild spe
cies infected by F. hepática-, lagomorphs ( O . cuniculus) and rodents CM. coypus).
O. cuniculus infection has b e e n reported for a long time ( O l s e n , 1 9 4 8 ) and has b e e n o b s e r v e d in several different countries: in F r a n c e ( B a i l e n g e r et al., 1 9 6 5 ; Hubard, 1 9 8 5 ; Biadi & Le Gall, 1 9 9 3 ) , in England, USA and Australia ( B a i l e n g e r et al, 1 9 6 5 ) , as well as in Rumania (Nesterov et al, 1 9 7 3 ) , in Czechoslovakia, in Italy and in Chile (Rubilar et al, 1 9 8 7 ) . T h e average infection rate measured in our study was in a c c o r d a n c e with those reported b y the various authors.
In spite o f a large potential host spectrum, F. hepática only forms o n e rodent s p e c i e s CM. coypus).
T h e positivity o f the c o p r o s c o p i c diagnosis in t w o faecal samples c o l l e c t e d in O. zybethicus d o e s not prove the infestation o f the population. C o p r o s c o p i c diagnosis is not a specific screening m e t h o d and it c a n b e difficult to r e c o g n i z e fluke eggs o f another e n d o -
parasite eggs (like Alaria spp...). Also, a e x o g e n origin o f the faecal eggs c a n n o t b e e x c l u d e d : O. zybethicus is a c a e c o t r o p h and the quantity o f faecal e g g s found w a s l o w ( 0 . 6 and 2.8 eggs per g r a m m e ( e p g ) ) . T h e a b s e n c e o f liver flukes and antibodies s e e m s to s h o w that the population sampled is not infested b y F. hepá
tica. T h e s e results confirm t h o s e o f B o u s s i n e s q w h o e x p l o r e d , in 1 9 8 6 , the F. hepática susceptibility o f a O. zybethicus population in area w h e r e M. coypus infestation was s h o w n . N o n e o f the 7 0 animals autop- sied w e r e infested b y the parasite. T h e specific ali
mentary behavior, w h i c h differs strongly from that o f M. coypus (Perry, 1 9 8 2 ) , m a y provide an explanation for the resistance of O. zybethicus to F. hepática.
N o n e R. norvegicus n o r m i c r o m a m m a l s p e c i e s w e r e infected. T h e a b s e n c e o f R. norvegicus and micro- m a m m a l s infected in an infected F. hepática area s e e m s to confirm that parasite carrying is not frequent in these s p e c i e s . R. norvegicus infection has only b e e n o b s e r v e d in Irak by Molan & Hussein ( 1 9 8 8 ) and the p r e v a l e n c e m e a s u r e d w a s l o w (7 % ) . O n l y o n e micro
m a m m a l infection was detected, in Mus musculus, a s p e c i e s not trapped in our study, b y Mas-Coma et al.
( 1 9 8 8 ) , in Corsica. Mas-Coma s h o w e d that, like the Rattus rattus fluke infection, this p h e n o m e n o n is the c o n s e q u e n c e o f insularity c o n c e r n i n g n i c h e widening in b o t h host and parasite s p e c i e s (Mas-Coma et al, 1 9 8 9 ) . It appears that the carrying o f F. hepática by Rattus s p p . and m i c r o m a m m a l s m a y only o c c u r under certain circumstances, in particular environments.
M. coypus infection is, o n the contrary, m o r e w i d e s pread. It has b e e n reported in France ( D e l e c o l e , 1982;
R o s o u x , 1 9 8 4 ; B o u s s i n e s q , 1 9 8 6 ) , in USSR (Zakariev, 1 9 7 7 ) and in Brazil, in its native habitat, by Santos et al. ( 1 9 9 2 ) . T h e results s h o w that M. coypus infection o c c u r s in various e n v i r o n m e n t s ( s w a m p s , humid m e a d o w s ) and the infection rate c a n b e e x c e e d i n g l y high (serological p r e v a l e n c e is 7 2 % in s w a m p ) . In a pre
vious study (unpublished data) earned out in 10 watery areas in Loire Atlantique, w e o b s e r v e d that M. coypus infection rates varied b e t w e e n 0 and 50 % ( m e a n = 9 % ) in the different areas but it reached a m e a n rate o f 42 % in F. hepática infected areas. F. hepática carrying seems to b e frequent in M. coypus and is c o m m o n p l a c e in many populations, in several different environments.
Relationships b e t w e e n wild fauna and F. hepática are different depending o n the s p e c i e s . S o m e wild small m a m m a l s s p e c i e s d o not s e e m to b e naturally sus
ceptible to the parasite and m a y play n o role in fas- ciolasis disease CO. zybethicus).
O t h e r small mammals s p e c i e s are only able to harbour fluke livers in particular e n v i r o n m e n t a l c o n d i t i o n s (Rattus spp., m i c r o m a m m a l s ) and serve, as the black rat Rattus rattus in Corsica, as a reservoir o f fasciolosis in these specific b i o t o p e s (Valero et al, 1 9 9 8 ) [Mas-
80 Mémoire P a r a s i t e , 2 0 0 0 , 7, 7 7 - 8 2
NATURAL, HOSTS OF FACIOLA HEPATICA
Coma ( 1 9 8 8 ) measured an infection rate equal to 48.5 % in Corsica Rattus rattus].
Finally, s o m e wild s p e c i e s are frequently natural hosts o f F. hepática (O. cuniculus, M. coypus). T h e e p i d e - miological role o f t h e s e wild hosts vary d e p e n d i n g o n the nature o f t h e definitive host a n d the environment.
In fact, O. cuniculus is a favourable host c o n c e r n i n g the duration a n d t h e intensity o f F. hepática infection but s e e m s to b e less favourable c o n c e r n i n g the pur- suit o f life parasitic cycle: the n u m b e r o f infected shedding O. cuniculus is generally l o w ( 1 8 % in o u r study, T a b l e I ) , fluke e g g s eclosability a n d d e v e l o p - mental s u c c e s s a r e p o o r ( B o r a y , 1969; Rondelaud &
Dreyfuss, 1 9 9 5 ) . T h e s e results w o u l d tend to r e d u c e the impact o f O. cuniculus infection in the fasciolosis e p i d e m i o l o g y . O n the contrary, notwithstanding e c l o - sability a n d d e v e l o p m e n t s u c c e s s o f faecal fluke e g g s h a v e not b e e n studied yet, high n u m b e r o f infected a n d shedding M. coypus (fluke e g g s s h e d b y 8 0 % o f infected animals) c o m b i n e d with high population den- sity, opportunistic b e h a v i o r a n d w i d e s p r e a d distribu- tion (Jouventin et al, 1996), suggest that M. coypus pro- b a b l y plays a major e p i d e m i o l o g i c a l role in fasciolosis.
This role is c o m p o u n d e d b y t h e fact that this rodent is amphibious a n d used to defaecate in water and shed fluke e g g s c l o s e t o habitats o f snails w h i c h a r e p o t e n - tial intermediate hosts; a b e h a v i o r very m u c h to the benefit o f the parasite a n d its life c y c l e .
T h e s e results demonstrate that rodents play a m o r e c o m p l e x e p i d e m i o l o g i c a l role in the fasciolosis epi- d e m i o l o g y than that reported b y M a c k o & B a s a n d a ( 1 9 7 7 ) w h o thought that rodents w e r e just scattering agents o f F. hepática, a n d i n c r e a s e the interest that veterinary r e s e a r c h h a v e to b e a r o n it. T h e variations o f the infestation rate a c c o r d i n g to t h e e n v i r o n m e n t also s h o w that its role c a n b e different according to the b i o t o p e incriminated.
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