IN FRANCE

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COCCIDIOSIS OF THE WILD RABBIT

(ORYCTOLAGUS CUNICULUS)

IN FRANCE

G R È S V . * , VOZA T . * . C H A B A U D A.* & L A N D A U I.*

Summary :

In 1 9 9 8 - 1 9 9 9 a survey of coccidiosis in wild rabbits was carried out in six different localities in France. About five individuals were caught monthly in each locality and a total of 2 5 4 wild rabbits was examined. Ten species of Coccidia were identified: Eimeria perforans, E. flavescens, E. piriformis, E. exigua, E. media, E. magna, E. coecicola, E. stiedai, E. roobroucki, E. inteslinalis.

Intensity of infection in young individuals was higher than in adults. Intensity was highest in winter but, as there are no young rabbits in winter, in young individuals it was higher in spring and autumn than in summer. Intensities were higher in the northern rather than in southern localities. Ranking of prevalence was remarkably stable, in contrast to the variability of the parasitic load. The equilibrium between congeneric species of rabbit coccidia (stable prevalence rank, variable parasitic load) is thought to be probably the consequence of the opportunistic feeding habits of rabbits

K E Y W O R D S : Eimeria, wild rabbit, congeneric species.

Résumé : LA COCCIDIOSE DU LAPIN DE GARENNE (ORYCTOLAGUS CUNICULUS) EN FRANCE

En 1998-1999, nous avons mené une étude sur la coccidiose du lapin de garenne dans six localités différentes en France. Pour chaque site, cinq individus environ ont été capturés mensuellement et un total de 254 lapins a été examiné. Dix espèces de

Coccidies ont pu être identifiées : Eimeria perforans, E. flavescens, E. piriformis, E. exigua, E. media, E. magna , E. coecicola, E. stiedai, E. roobroucki, E. intestinalis. Chez les jeunes lapins, l'intensité de l'infection apparaît plus élevée que chez les adultes. C'est en hiver que l'intensité de l'infection des adultes est la plus élevée. Par contre, chez les juvéniles, qui n'apparaissent qu'au printemps, l'infection est plus importante au printemps et à l'automne qu'en été. Les sites du nord présentent les intensités les plus élevées. L'ordre des prévalences apparaît remarquablement stable comparé à la variabilité de la charge parasitaire. L'équilibre entre les espèces congénériques de coccidies de lapins (ordre des prévalences stable, charge

parasitaire variable) pourrait être la conséquence du comportement alimentaire opportuniste du lapin de garenne.

MOTS CLÉS : Eimeria, lapin de garenne, espèces congénériques.

INTRODUCTION

R

a b b i t Eimeria h a v e b e e n e x t e n s i v e l y u s e d as e x p e r i m e n t a l m o d e l s , b e c a u s e o f t h e small s i z e o f their host, its g r e a t f e c u n d i t y a n d e c o - n o m i c i m p o r t a n c e . I n f o r m a t i o n o n this g r o u p o f parasites is e x c e p t i o n a l l y e x t e n s i v e a n d p r e c i s e ( C o u - dert et al., 1 9 9 5 ) , but it mainly c o n c e r n s t h e d o m e s t i c rabbit. T h e p r e s e n t w o r k is an a t t e m p t to c o m p a r e t h e fauna o f wild and d o m e s t i c rabbits a n d to unders- tand t h e t y p e o f b a l a n c e a c h i e v e d b e t w e e n t h e parasite s p e c i e s . Results w e r e c o m p a r e d with r e p o r t s from t h e few o t h e r c o u n t r i e s w e r e similar s u r v e y s w e r e p e r f o r m e d .

* M u s é u m N a t i o n a l d ' H i s t o i r e N a t u r e l l e . É q u i p e P a r a s i t o l o g i e c o m - p a r é e et m o d è l e s e x p é r i m e n t a u x a s s o c i é e à l ' I N S E R M , U 5 6 7 et L a b o r a t o i r e d e P r o t o z o o l o g i e et P a r a s i t o l o g i e c o m p a r é e ( E P H E ) , 6 1 , rue B u f f o n . 7 5 2 3 1 P a r i s C e d e x 0 5 , F r a n c e .

C o r r e s p o n d e n c e : I r è n e L a n d a u .

T e l . : + 3 3 ( 0 ) 1 4 0 79 3 5 0 0 - F a x : + 3 3 ( 0 ) 1 4 0 7 9 3 4 9 9 . E-mail: l a n d a u @ c i m r s 1 . m n h n . f r

MATERIALS AND METHODS

S T U D Y AREAS

T h e survey w a s carried out in six study areas.

Arjuzanx reserve c o v e r s 2 , 4 5 2 ha in t h e south-west o f France (department o f Landes, 4 4 ° 0 0 ' N, 0° 5 1 ' W ) . T h e climate is o c e a n i c , the m e a n annual rainfall is 1,016 mm a n d t h e m e a n annual t e m p e r a t u r e 12.9° C. Rabbits w e r e caught in m e s o p h i l i c land c o l o n i s e d by Ilex euro- peus, Caluna v u l g a r i s , Erica cinerea and Erica sco- paria.

C h è v r e l o u p arboretum o c c u p i e s 2 0 0 ha in Versailles near Paris (department o f Yvelines, 4 8 ° 5 0 ' N. 0 2 ° 0 6 ' E ) . T h e climate is o c e a n i c with continental influence, the m e a n annual rainfall is 6 0 6 mm and the m e a n annual temperature 1 0 . 3 ° C. T h e terrain is m e s o p h i l i c grass- land.

D o n z è r e - M o n d r a g o n reserve c o v e r s 1.545 ha in the south-east o f F r a n c e (departments o f D r o m e a n d Vau- cluse, 4 4 ° 2 6 ' N, 4° 4 2 ' E ) . T h e climate is mediterra- n e a n with continental influence. T h e m e a n annual rain-

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Mémoire 51

Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/2003101p51

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GRÈS V., VOZA T., CHABAUD A. & LANDA'

fall is 8 6 0 m m and the m e a n annual t e m p e r a t u r e 12.8° C. It is very diversified xerophilic wasteland sup- porting G r a m i n a c e a e , F a b a c e a e and Compositae and s o m e shrubs, mainly Cornus sanguined, Populus alba.

P. nigra. Crataegus monogyna and Robinia pseuda- cacia.

Massereau reserve covers 3 9 3 ha in the west o f F r a n c e (department o f Loire-Atlantique 4 7 ° 14' N, 0 1 ° 5 5 ' W ) . T h e climate is o c e a n i c , the m e a n annual rainfall is 7 8 0 m m and the mean annual temperature 1 1 . 7 ° C . It comprises mesophilic m e a d o w l a n d with mainly Agros- tis sp., Oleus lanatus and Trifolium spp., a canal border with Iris spp, Joncus spp, Pbragmites communis and a dam bordering a s w a m p , with Primus spinosa and R u b u s fructicosus.

Gerstheim reserve has an area o f 2,630 ha; it is located in the east o f F r a n c e ( d e p a r t m e n t o f B a s - R h i n ) ( 4 8 ° 22' N, 7 ° 4 2 ' E ) . T h e climate is continental, the m e a n annual rainfall is 6 5 0 mm and the m e a n annual tem- p e r a t u r e is 1 0 ° C. T h e r e g i o n u s e d for t r a p p i n g c o n s i s t e d o f three artificial sites with small s h r u b b y vegetation o f the m e s o b r o m e t u m o r m e s o x e r o b r o - m e t u m type.

B e n i g u e t island reserve has an area o f 6 4 ha and is l o c a t e d three miles off C o n q u e t in Brittany ( 4 8 ° 2 1 ' N, 0 4 ° 5 1 ' W ) . T h e c l i m a t e is o c e a n i c , the m e a n annual rainfall is 8 0 0 m m and t h e m e a n annual temperature is 1 1 . 8 ° C . T h e terrain c o m p r i s e s x e r o p h i l i c d u n e s c o v e r e d w i t h Armeria maritima, Festuca rubra, Senecio jacobaea, Silenae matitima and Carex are- naria.

It was not possible to evaluate, in the various reserves, the rabbits density per hectare.

SAMPLING

Five rabbits w e r e usually caught e a c h month from February 1998 to February 1 9 9 9 in the five mainland areas.

Twenty rabbits w e r e caught on a single occasion in the Beniguet reserve, on the 23 and 24th o f September 1998.

Caecal contents were diluted with two volumes o f 2.5 % potassium dichromate solution and samples w e r e kept for three days at r o o m temperature o f 2 4 ° C, in large Petri dishes to allow maturation o f the oocysts. T h e faecal s u s p e n s i o n s w e r e then filtered through sieves o f decreasing m e s h size ( 4 0 0 µm, 2 0 0 urn, 100 µm).

Oocysts were isolated by magnesium sulphate flotation, identified and counted with the aid o f a MacMaster cell.

Results are e x p r e s s e d as the n u m b e r o f oocysts per gram o f c a e c a l contents. T h e a g e o f rabbits w a s eva- luated by weighing the crystalline lenses, previously fixed with formaldehyde solution. Rabbits w e r e clas- sified as young (crystalline lenses weighing less than 100 m g ) or adult (crystalline lenses weighing more than 100 m g ) according to Myers & Gilbert ( 1 9 6 8 ) .

Sporulated oocysts w e r e identified according to the published morphological criteria, particularly t h o s e o f Coudert et al. ( 1 9 9 5 ) .

RESULTS

T

en s p e c i e s w e r e identified: Eimeria perforans (Leuckart, 1879); E. f l a v e s c e n s Marotel & Guilhon, 194T, E. piriformis Kotlan & P ô s p e s c h 1 9 3 4 ; E. exigua Yakimoff, 1 9 3 4 ; E. media K e s s e l , 1 9 2 9 ; E. magna Pérard, 1925; E. intestinalis Cheissin, 1948;

E. stiedai (Lindemann, 1 8 6 5 ) ; E. coecicola Cheissin, 1947 and E. roobroucki d e s c r i b e d recently by Grès, Marchandeau & Landau ( 2 0 0 2 ) . No specific hare c o c - cidia w e r e identified.

Detailed figures o f prevalence and parasite load have b e e n recorded in a b o o k (LV) deposited in our labora- tory (Parasitologie comparée et modèles expérimentaux) at the Muséum National d'Histoire Naturelle in Paris.

T h e s e x o f the animals had n o impact on infections which varied with the age o f the rabbits, the season and the locality.

T a b l e s I to IV and figures 1 to 4 summarize our results.

It was not possible to publish here all the detailed

Arjuzanx B é n i g u e t Chèvreloup D o n z è r e - M . Massereau Gerstheim

( n = 4 4 ) (n = 1 9 ) ( n = 1 9 ) (n = 5 3 ) ( n = 3 9 ) ( n = 4 3 )

E. perforans 9 2 3 ± 5 4 5 1 8 9 ± 7 3 1 1 . 4 9 9 ± 5 . 4 4 9 2 2 8 ± 5 2 5 9 6 ± 1 2 3 2 . 0 6 9 ± 7 3 3 E. flavescens 2 7 6 ± 5 9 2 2 1 ± 6 2 4 , 5 8 3 ± 2 , 2 4 6 1 9 3 ± 3 9 3 2 7 ± 7 0 1,183 ± 4 8 5 E. media 125 ± 7 2 2 7 0 ± 1 4 6 2 , 8 9 7 ± 1,423 4 0 ± 14 7 3 3 ± 4 3 3 1,490 ± 1.106 E. exigua 8 ± 2 3 ± 2 1,937 ± 1 . 1 2 1 5 ± 3 3 9 ± 14 5 8 5 ± 5 4 4 E. piriformis 7 0 ± 2 0 170 ± 1 3 8 5 , 5 9 6 ± 2 , 8 1 7 6 7 ± 2 3 4 5 6 ± 2 0 7 7 ± 2 5 E. stiedai 10 ± 1 0 7 ± 5 5 4 ± 4 0 0 . 4 ± 0 . 4 5 ± 4 6 ± 6

E. magna 1 ± 0 . 3 15 ± 7 8 4 ± 6 5 2 ± 1 5 ± 3 In + 5

E. coecicola 17 ± 1 4 0.4 ± 0.4 6 6 5 ± 4 8 6 11 ± 6 1 8 ± 1 5 1 1 0 ± 5 4

E. intestinalis 0 3 8 ± 3 4 3,151 ± 2 , 8 4 2 0 0.1 ± 0.1 13 ± 13

E. roobroucki 2 ± 1 0.7 ± 0 . 4 0 0.1 ± 0.1 2 ± 2 1 ± 1

T a b l e I. - M e a n p a r a s i t i c l o a d of adult r a b b i t s a c c o r d i n g t o locality ( ± s t a n d a r d d e v i a t i o n ) .

52 Parasite, 2003, 10. 51-57

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EIMERIA O F W I L D R A B B F T S

Arjuzanx Béniguet Chèvreloup Donzère-M. Massereau Gerstheim

( n = 9 ) ( n = 1 ) ( n = 9 ) ( n = 7 ) ( n = 1) ( n = 1 0 )

E. perforans 1 6 . 8 4 0 ± 7 , 4 1 5 1 6 4 1 6 7 , 5 4 5 ± 8 0 , 7 9 3 1 3 , 7 6 3 ± 1 0 , 3 7 0 4 , 4 5 3 1 0 7 . 2 3 6 ± 6 9 , 3 8 1 E. flavescens 4 , 5 2 9 ± 2 . 3 9 0 1 5 7 6 , 5 3 3 ± 4 3 , 8 0 7 3 , 0 2 1 ± 1 . 2 6 9 4 , 5 9 3 4 3 , 3 7 2 ± 4 1 , 7 3 8 E. media 1 9 , 9 3 5 ± 1 3 , 5 6 6 0 1 9 . 8 8 5 ± 1 6 . 6 8 9 1 , 3 5 0 ± 1,071 0 4 9 , 9 2 3 ± 2 8 , 4 1 4 E. exigua 8 7 4 ± 6 5 2 0 1.988 ± 1,196 2 8 5 ± 1 7 9 0 2 , 5 1 2 ± 2 . 1 3 9 E. piriformis 4 ± 4 140 1 1 , 1 2 1 ± 6 , 3 9 9 2 3 4 ± 1 0 6 7 3 0 E. stiedai 9 , 5 7 5 ± 9 , 4 0 8 0 7 2 . 1 1 2 ± 5 0 , 9 6 6 1 4 . 0 2 5 ± 1 2 , 6 2 1 3 4 7 4 5 , 7 6 8 ± 2 7 , 3 2 7 E. magna 1 , 7 8 5 ± 1 . 5 6 6 6 5 2 , 0 1 4 ± 5 1 , 4 8 3 9 7 5 ± 7 8 0 1 2 0 2 0 . 9 9 5 ± 1 3 , 2 6 5 E. coecicola 3 8 ± 3 8 0 3 8 , 9 4 1 ± 2 5 , 5 3 6 5 3 ± 5 3 1 9 3 3 2 . 9 3 3 ± 1 6 . 0 5 5

E. intestinalis 0 0 1 6 , 7 3 2 ± 1 0 , 8 1 0 0 0 0

E. roobroucki 0 0 0 0 0 0

T a b l e II. - M e a n p a r a s i t i c l o a d o f j u v e n i l e r a b b i t s , a c c o r d i n g t o l o c a l i t y ( ± s t a n d a r d d e v i a t i o n ) .

Spring ( n = 5 2 ) Summer ( n = 4 0 ) A u t u m n ( n = 6 7 ) Winter ( n = 5 8 )

E. perforans 783 ± 1 8 9 4 9 3 ± 2 3 0 1.109 ± 5 3 4 4 , 3 4 9 ± 1 . 8 9 0 E. flavescens 2 9 3 ± 48 1.333 ± 9 8 6 7 7 5 ± 2 6 7 9 7 9 ± 4 3 6

E. media 5 2 6 ± 3 2 3 1 3 9 ± 9 7 6 0 3 ± 3 0 1 1,50.3 ± 8 8 9

E. exigua 4 8 ± 1 9 2 6 ± 14 4 1 7 ± 3 5 3 5 6 2 ± 3 7 7

E. piriformis 102 ± 3 7 2 4 9 ± 1 8 3 6 0 9 ± 3 6 9 1,132 ± 8 8 0

E. stiedai 1 ± 0 . 6 1 9 ± 13 19 ± 15 5 ± 5

E. magna 5 ± 3 2 ± 1 10 ± 4 2 8 ± 2 2

E. coecicola 2 2 ± 13 7 0 ± 4 0 4 6 ± 3 7 2 1 3 ± 1 5 9

E. intestinalis 0 0 1 0 6 ± 8 4 9 3 2 ± 9 3 2

E. roobroucki 3 ± 2 0 0.2 ± 0.1 0.4 ± 0 . 2

T a b l e III. - M e a n p a r a s i t i c l o a d o f adult r a b b i t s a c c o r d i n g t o s e a s o n ( ± s t a n d a r d d e v i a t i o n ) .

Spring ( n = 9 ) Summer ( n = 1 8 ) Autumn ( n = 9 )

E. perforans 6 8 , 5 9 7 ± 2 7 , 7 3 0 56,2.32 ± 3 7 , 7 3 8 1 3 3 . 5 5 4 ± 8 5 , 9 8 0 E. flavescens 5 2 , 3 3 3 ± 4 4 , 4 2 2 1 1 , 1 1 8 ± 8 . 0 2 6 5 7 . 2 5 0 ± 4 5 , 5 0 2 E. media 5 0 . 2 1 1 ± 2 8 , 6 1 7 3 , 2 3 9 ± 1.906 3 9 , 4 4 7 ± 2 3 , 8 6 8

E. exigua 4 , 1 2 4 ± 2 , 4 4 9 4 4 8 ± 3 3 2 8 3 3 ± 5 7 9

E. piriformis 1 , 7 9 6 ± 1 , 7 2 6 4 , 0 7 5 ± 3 , 3 6 8 1,353 ± 6 5 8 E. stiedai 9 2 , 7 8 9 ± 5 1 . 5 3 3 4 . 9 8 3 ± 4 , 6 9 8 4 0 . 5 1 8 ± 2 5 , 4 3 1 E. magna 8 . 6 2 8 ± 8 , 2 2 4 3 4 , 4 4 2 ± 2 6 , 1 2 0 3 8 5 ± 1 9 6

E. coecicola 0 1 8 , 1 2 0 ± 9 , 4 0 7 3 9 , 5 3 2 ± 2 5 , 7 4 4

E. intestinalis 0 5 . 0 3 5 ± 5 , 0 3 5 6 , 6 6 3 ± 5 , 6 7 7

E. roobroucki 0 0 0

T a b l e IV. - M e a n p a r a s i t i c l o a d o f j u v e n i l e r a b b i t s a c c o r d i n g t o s e a s o n ( ± s t a n d a r d d e v i a t i o n ) .

tables and graphs. T h e y m a y h o w e v e r b e found in V. Grès thesis ( 2 0 0 1 ) :

i) the m e a n parasite load o f adult ( T a b l e I) and young ( T a b l e I I ) rabbits from e a c h locality (for all s e a s o n s together);

ii) the m e a n parasite load o f adult ( T a b l e III) and y o u n g ( T a b l e IV) rabbits at different s e a s o n s ;

iii) p r e v a l e n c e s o f the different s p e c i e s in e a c h study area throughout the year, in adult (Fig. 1) a n d young (Fig. 2 ) rabbits; and

iv) prevalences o f the different s p e c i e s in adult (Fig. 3 ) and young (Fig. 4 ) rabbits a c c o r d i n g to the s e a s o n . T h e r e w e r e n o y o u n g rabbits present in winter.

INTENSITY O F INFECTION

Parasite l o a d w a s variable in y o u n g rabbits, possibly d e p e n d i n g o n the uncertain c h a n c e o f their b e c o m i n g infected.

In adult rabbits, intensity o f infection was generally highest in winter. In young animals it was higher in spring and autumn than in s u m m e r e x c e p t for E. piri- formis and E. magna.

In adult rabbits, the intensity o f infection was g e n e - rally highest in winter.

T h e principal feature determining the intensity o f infection was the geographical location. Parasite load w a s

P a r a s i t e , 2 0 0 3 . 10. 5 1 - 5 7

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GRÈS V., VOZA T., CHABAUD A. & LANDAU I.

Fig. 1. - P r e v a l e n c e s o f t h e Eimeria s p e c i e s in adult r a b b i t s , a c c o r d i n g to locality.

Fig. 2. - P r e v a l e n c e s of t h e Eimeria s p e c i e s in j u v e n i l e r a b b i t s , a c c o r d i n g t o locality.

5 4 Mémoire P a r a s i t e , 2 0 0 3 , 10, 5 1 - 5 7

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EIMERIA O F W I L D R A B B I T S

Fig. 3. - P r e v a l e n c e s of Eimeria s p e c i e s in adult r a b b i t s , a c c o r d i n g t o s e a s o n .

Fig. 4. - P r e v a l e n c e s of Eimeria s p e c i e s in j u v e n i l e r a b b i t s , a c c o r d i n g t o s e a s o n .

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ORES V., VOZA T., CHABAUD A. & LANDAU I.

high in the humid and relatively c o l d localities (Ile de France and Alsace), lower along the Atlantic littoral (Loire and Landes) and lower still in the dryer and war- m e r areas ( R h o n e valley).

PREVALENCES

In adult rabbits, prevalence was highest with two spe- cies, E. perforans and E.

flavescens;

it was moderately high with E. media and E. piriformis, and generally low with the six o t h e r s p e c i e s .

Results from y o u n g rabbits w e r e available (Figs 2 and 4 ) from only four locations ( s e v e n to 10 rabbits e x a - mined from e a c h ) : Arjuzanx, Chevreloup, D o n z è r e - Mondragon and Gershteim. E. roobrouki was absent and E. intestinalis was found only in Chevreloup.

Prevalences were, with few e x c e p t i o n s , remarkably similar in the different localities: nearly 100 % with E. perforans and E. flavescens and 7 0 % with the six o t h e r s p e c i e s . T w o e x c e p t i o n s w e r e E. piriformis, absent from Gerstheim, and E. exigua and E. coecicola, which had low prevalences (around 1 0 - 3 0 % ) in Arju- z a n x and D o n z è r e - M o n d r a g o n .

The histogram o f prevalence (Fig. 4 ) according to season s h o w s least variability in autumn c o m p a r e d with spring and summer, i.e. E. perforans and E. flavescens around 100 % and the six other species around 7 0 %.

With the adult rabbits, in contrast with the variability o f parasite load according to location (Fig. 1), w e o b s e r v e d stable prevalences: E. perforans and E. fla- vescens, 9 0 - 1 0 0 %; E. piriformis, 70-95 %; E. exigua, 3 2 - 7 2 %; E. media. 2 9 - 6 9 %; E. magna, 17-42 %;

E. coecicola. 5-32 %; E. stiedai, 4-21 %; E. roobrouck, 0-21 %; and E. intestinalis, 0-16 %. Even m o r e striking, in all localities, the ranked order o f prevalence o f e a c h s p e c i e s w a s remarkably stable: E. perforans and E. fla- vescens, 1-2; E. piriformis, 3; E. exigua, 4-5 (with low- parasite loads); E. media, 4-5; E. magna. 6; coeci- cola and E. stiediai, 7-9; E. roobroucki and E. intesti- nalis. 9 - 1 0 .

DISCUSSION

COMPARISON O F C O C C I D I O S I S O F WILD AND D O M E S T I C RABBITS

F

or this type o f study, precise specific identifica- tion is necessary but the systematics o f Coccidia are difficult. C o n g e n e r i c s p e c i e s are frequent with the Nematodes, for e x a m p l e , and their morpho- logy is varied with many differential characters, while with Eimeria the m o r p h o l o g y o f the oocyst, w h i c h is the main criterion is a w e a k character. Confusion bet- w e e n s p e c i e s is always possible and it is disturbing to find in the literature different biological characters

assigned to the s a m e s p e c i e s by reliable authors. In the s a m e way the origin o f strains is not always s p e - cified, and biological differences o b s e r v e d amongst strains may in fact represent subspeciation.

T h e parasitism o f domestic rabbits differs from that in the wild: Zundel ( 1 9 7 9 ) carried out a survey in b r e e - ding c o l o n i e s in different parts o f France and listed nine intestinal s p e c i e s . T w o o f the s p e c i e s recorded, although designated by different names, correspond to s p e c i e s found by us in the wild: Eimeria sp. sensu Zundel = E. flavescens. and E. neoleporis sensu Zun- del = E. coecicola. His list differs from ours by the pre- s e n c e o f E. irresidua and the a b s e n c e o f E. exigua and E. roobroucki. T h e p e r c e n t a g e s o f p r e v a l e n c e ( P ) and parasite load (PL) w e r e a p p r o x i m a t e l y as follows:

E. perforans: P 8 7 % , PL 37 %; E. media: P 55 %, PL 10 %; E. magna: P 53 %, PL 37 %; flavescens:

P 3 0 %, PL 1 %; E. irresidua: P 25 % , PL 1 %; E. intes- tinalis-. P 21 %, PL 10 %; E. piriformis: P 13 %, PL 1 %;

and E. coecicola: P 11 %, PL 10 %. H o w e v e r , contraty to what w e o b s e r v e d with wild rabbits, the ranking o f p r e v a l e n c e varied from o n e region to the other.

T h e p r e d o m i n a n c e in breeding c o l o n i e s of d o m e s t i c rabbits o f the three s p e c i e s E. perforans, E. media and E. magna has also b e e n reported in Italy (Gallazzi, 1 9 7 7 ) , England ( C a t c h p o l e & Norton, 1979), B e l g i u m (Peeters & G e e r o m s , 1981), Saudi Arabia (Kasim & Al- Shawa, 1 9 8 7 ) , Nigeria ( O k e w o l e , 1 9 9 0 ) , and India (Souza et al., 1 9 9 3 ) . T h e s e s p e c i e s remained dominant in the industrial breeding c o l o n i e s after d e v e l o p i n g resistance to robenidine.

In contrast to these observations, in the wild rabbit in its natural environment, in south-west Australia, H o b b s

& Twigg ( 1 9 9 8 ) found p r e v a l e n c e s to b e very similar to ours in France: E. perforans, 8 4 %; E. flavescens, 6 0 %; E. piriformis, 5 0 %; E. exigua, 62 %; E. media, 45 %; E. magna, 33 %; E. coecicola, 7 %; E. stiedai, 26 %; and E. intestinalis, 19 %. T h e only important dif- ference w a s the p r e s e n c e in Australia of E. irresidua ( 9 % ) and the a b s e n c e o f E. roobroucki. This w a s not true, however, for the parasite intensities.

THE BALANCE B E T W E E N CONGENERIC SPECIES

Several factors have influenced speciation o f Eimeria in rabbits: a long evolutionary period, the Lagomorpha having e v o l v e d little s i n c e the E o c e n e and having retained their parasitic fauna, and geographical isola- tion together with m o n o x e n o u s life c y c l e s and oocysts which appear to b e (Coudert & Ivoré, 1973) fragile and destroyed b y heat.

Rabbits are strictly herbivorous, but they are opportunistic feeders w h i c h a c c o u n t s for the variability o f parasite intensity from e a c h individual. H o w e v e r the stability o f the rank o f p r e v a l e n c e indicates an ancient and highly stable equilibrium.

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EìMERIA O F W I L D R A B B I T S

ACKNOWLEDGEMENTS

T

his study was supported by a grant from the Office National de la Chasse et de la Faune Sau- vage (ONCFS). W e are very grateful to F. Biady, director o f CNERA for allowing our work to b e carried out in the national reserves o f ONCFS and to the colleagues w h o collected the biological material, particularly S. Avignon, G. Delacour, J . C . Gauclin, F. B e r - nard and G. Leray. W e are m u c h indebted to A. R o o - brouck for his help in the w o r k performed at Versailles and to S. M a r c h a n d e a u for his c o n s t a n t h e l p and advice throughout this study. Many thanks to J o h n B a k e r and Jean-Charles Gantier for their great help.

Z U N D E L E. Coccidies et coccidioses intestinales du lapin - étude bibliographique, enquête épidémiologique. Veterinary thesis, Créteil University, 1 9 7 9 .

Reçu le 13 juillet 2 0 0 2 Accepté le 1 2 décembre 2 0 0 2

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