THE HELMINTHFAUNA OF Oryctolagus cuniculus (LINNAEUS, 1 7 5 8 ) IN THE IBERIAN PENINSULA.
FAUNISTIC AND ECOLOGICAL CONSIDERATIONS
B L A S C O S.*, T O R R E S J . * , F E L I U C.*,**, C A S A N O V A J . C . * , M I Q U E L J . * & M O R E N O S.***
Summary :
Faunistic and ecological analysis of the helminthfauna of the wild rabbit, Oryctolagus cuniculus (Linnaeus, 1758), was undertaken in the Iberian Peninsula. For the first time the helminthfaunas of the two iberian subspecies (O. c. cuniculus and O. c. algirus) are detailed. Fifteen parasite species (1 Digenetic Trematode, 7 Cestodes and 7 Nematodes) were detected. The presence of Leporidotaenia spp. (Cestoda: Anoplocephalidae) is the distinguishable feature between both helminthfaunas. Moreover, qualitative and quantitative differences exist between the two hosts subspecies, often statistically significant. The effect of host sex on the helminthfauna of O. cuniculus in both populations seems to be low.
KEYWORDS : HELMINTHFAUNA, Oryctolagus cuniculus, IBERIAN PENINSULA.
Résumé : L'HELMINTHOFAUNE D' ORYCTOIAGUS CUNICULUS (LINNAEUS, 1758) DANS LA PÉNINSULE IBÉRIQUE. CONSIDÉRATIONS FAUNISTIQUES ET ÉCOLOGIQUES
L'analyse faunistique et écologique de l'helminthofaune du lapin sauvage, Oryctolagus cuniculus (Linnaeus, 1758), de la péninsule ibérique a été effectuée. Cette étude est la première entreprise sur les helminthofaunes d'O. c. cuniculus et O. c. algirus, deux sous- espèces de la péninsule ibérique. Quinze espèces de parasites (1 Trématode, 7 Cestodes et 7 Nématodesj ont été trouvées. La détection de Leporidotaenia spp. est la caractéristique qui permet la différenciation des helminthofaunes entre les deux sous-espèces d'O. cuniculus. De plus, il existe des différences qualitatives et quantitatives, parfois statistiquement significatives, parmi ces helminthofaunes. L'influence du sexe de l'hôte sur l'helminthofaune de O. cuniculus semble peu importante dans les deux sous- espèces hôtes.
MOTS CLES : Helminthofaune, Oryctolagus cuniculus, péninsule ibérique.
INTRODUCTION
The wild rabbit, Oryctolagus cuniculus (Lin- I naeus, 1 7 5 8 ) (Lagomorpha: Leporidae), is a
native m a m m a l from t h e Iberian Peninsula.
Actually, t w o s u b s p e c i e s are recognized: O. cuniculus algirus, restricted to the southwestern o f t h e Iberian Peninsula, a n d O. cuniculus cuniculus in the rest o f Spain, Europe and Australia. B o t h subspecies are g e n e - tically differentiated ( M o n n e r o t et al, 1 9 9 4 ; Ferrand, 1 9 9 5 ; Hardy et al, 1 9 9 5 ) . According to Ferrand ( 1 9 9 5 ) this differentiation h a p p e n e d over the Quaternary gla- ciations. In Europe, there are n u m e r o u s studies about the helminthfauna o f this host ( B o a g , 1 9 7 2 a n d 1987, Mead-Briggs & Page, 1 9 7 5 a n d B o a g & Iason, 1 9 8 6 in Great Britain; Butler, 1 9 9 4 in Ireland; Haupt & Har- tung, 1 9 8 0 a n d 1 9 8 4 in G e r m a n y ; Arm et al, 1 9 6 8 in
* Laboratori de Parasitologia, Departament de Microbiologia i Para- sitologia Sanitàries, Facultat de Farmacia, Universitat de Barcelona, Av. Diagonal, 643. 08028 Barcelona (Spain).
** Institut de Salut Publica, Campus Universitari de Bellvitge, Bar- celona (Spain).
*** Estación Biológica de Doñana, Unidad de Biología de las Espe- cies Cinegéticas y Plaga, Av. Ma Luisa s/n. 41013 Sevilla (Spain).
Tel: (34) 3 4024501. - Fax: (34) 3 4024504. - Email: sblasco@far- macia.far.ub.es
Italy; Horning, 1 9 7 4 in Switzerland; T e n o r a a n d Barus, 1957 in the old C z e c h o s l o v a k i a ; Sugar et al, 1 9 7 8 in Hungary; Theodoridis, 1 9 7 9 in G r e e c e ; etc.). Several studies have also b e e n performed in other continents ( B e r n a r d , 1 9 6 5 in Africa; Courtin et al, 1 9 7 9 a n d Rubilar & Merello, 1987 in South America; Bull, I 9 6 0 and 1 9 6 4 a n d D u n s m o r e , 1 9 7 8 in Australia; e t c . ) . Numerous helminth s p e c i e s have b e e n reported in Oryctolagus in t h e Iberian Peninsula ( C o r d e r o del Campillo et al, 1 9 9 4 ) as a result o f several studies per- formed in different iberian areas (Carvalho Varela,
1 9 6 7 ; Simon V i c e n t e , 1 9 6 9 ; M e n d o n c a a n d Varela, 1 9 7 1 ; Romero-Rodriguez et al, 1 9 7 3 ; T e n o r a et al, 1 9 8 1 - 8 2 ; Afonso-Roque & Barata, 1 9 8 4 ; Reina et al, 1 9 8 7 ; etc.).
T h e present study is the first in analyzing a n d c o m - paring, from a faunistic a n d e c o l o g i c a l point o f view, the h e l m i n t h f a u n a o f t h e t w o i b e r i a n s u b s p e c i e s . Moreover, it is the first study in Continental E u r o p e in w h i c h a characteristic o f host ( s e x ) w a s considered.
Ecological studies have only b e e n described in Great Britain (Mead-Briggs a n d Vaughan, 1973; B o a g , 1985;
B o a g a n d Kolb, 1989), Ireland (Butler, 1994) a n d Aus- tralia (Bull, 1959 a n d 1964; Dudzinski a n d Myky- towycz, 1963; D u n s m o r e , 1966 a, b, c; D u n s m o r e &
Dudzinski, 1968).
Parasite, 1996, 4, 327-333
327 Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1996034327
e x a m i n e d u n d e r s t e r e o s c o p i c m i c r o s c o p a n d t h e r e m o v e d helminths counted, preserved in 7 0 ° a l c o h o l a n d p r o c e s s e d f o l l o w i n g g e n e r a l h e l m i n t h o l o g y methods.
Identification o f the parasite s p e c i e s was performed b a s e d o n previous specific descriptions. A n o p l o c e - phalid Cestodes w e r e identified following descriptions from T e n o r a et al, ( 1 9 8 1 - 8 2 ) , Beveridge ( 1 9 7 8 ) , T e n o r a
& Murai ( 1 9 7 8 ) and G e n o v et ai, ( 1 9 9 0 ) . S p e c i e s belonging to the g e n u s Leporidotaenia w e r e classified following the description o f G e n o v etal, ( 1 9 9 0 ) . Lepo
ridotaenia cf. wimerosa was identified according to the large size o f the strobila ( G e n o v et al, 1 9 9 0 ) . R e c e n t n e w descriptions w e r e u s e d to classify s o m e N e m a todes: Durette-Desset & D e n k e ( 1 9 7 8 ) for Graphidium strigosum; Durette-Desset ( 1 9 7 9 ) for Nematodiroides zembrae, and B a b o s ( 1 9 6 1 ) for Protostrongylus cuni- culorum. Dermatoxys hispaniensis w a s identified fol
lowing the unique descriptions o f Simon Vicente ( 1 9 6 9 ) and Afonso-Roque and Barata ( 1 9 8 4 ) .
T w o different tests w e r e used to perform statistical ana
lysis o f parasite populations. T h e X2 test was used, together with the Y a t e s continuity correction, to carry out a comparative study o f p r e v a l e n c e s . T h e Mann- Whitney « U » statistical was used to c o m p a r e the inten-
Fig. 1. — Number of hosts studied per province in the Iberian Peninsula (B : Barcelona, GE : Gerona, L : Lérida, T : Tarragona, CA: Cádiz, H : Huelva, SE : Sevilla).
MATERIALS AND METHODS
T
w o h u n d r e d and fifteen iberian rabbits from two geographically distant areas w e r e helmin- thologically studied. O n e hundred and fifty- three s p e c i m e n s w e r e c o l l e c t e d b e t w e e n winter 1991 and winter 1 9 9 3 in Catalonia (North-eastern Iberian Peninsula; B a r c e l o n a , Tarragona, Lerida and G e r o n a p r o v i n c e s ) , w h e r e O. cuniculus cuniculus lives; sixty- two w e r e caught during February and April 1 9 9 3 in Andalusia (South-western Peninsula; Huelva, Sevilla and Cadiz p r o v i n c e s ) , w h e r e O. cuniculus algirus is present. T h e n u m b e r o f hosts per province is s h o w n in Figure 1.Hosts w e r e kindly supplied b y the Catalonian Hunting Federation and D o n a n a Biological Station (Andalusia).
T h e available data w e r e the location o f capture and the s e x o f the host. This material arrived to the labo
ratory preserved by freezing. O n l y the digestive tract was studied from the Andalusian hosts. T h e abdominal cavities w e r e e x a m i n e d in the laboratory and the pre
s e n c e o f any cysts recorded. T h e lungs, s p l e e n s and livers w e r e studied separately. Alimentary tract was separated into three regions, stomach, small intestine and large intestine before being analysed. Viscera were
328 Mémoire Parasite, 1996, 4, 327-333
HELMINTHFAUNA OF ORYCTOLAGUS CVNICULUS
sity. Significance level w a s a = 0.05 in both tests. D u e to the a b s e n c e o f information on s e x in hosts sampled, statistic study on s e x influence on infection was d o n e o n a s m a l l e r s a m p l e . T h e r e f o r e , a h u n d r e d a n d seventy-five individuals have b e e n studied: o n e hun
dred and fourteen rabbits from Catalonia (fifty-one males and sixty-three females) and sixty-one rabbits from A n d a l u s i a ( t w e n t y - s i x m a l e s a n d thirty-five females). For e a c h helminth s p e c i e s differences in pre
v a l e n c e and intensity have b e e n analysed in: a) bet
w e e n males and females o f the s a m e host population;
h) b e t w e e n males and females o f general s a m p l e ; and c) b e t w e e n the helmithfaunas o f b o t h populations.
RESULTS
F
ifteen h e l m i n t h s p e c i e s w e r e d e t e c t e d ( o n e Digenetic Trematode, seven Cestodes and seven Nematodes) ; namely: Dicrocoelium dendriticum (Rudolphi, 1 8 1 9 ) ( D i c r o c o e l i i d a e ) ; Taenia pisiformis ( B l o c h , 1 7 8 0 ) larvae ( T a e n i i d a e ) ; Andrya cuniculi ( B l a n c h a r d , 1891 ), Cittotaenia denticulata (Rudolphi, 1 8 0 4 ) , Neoctenotaenia ctenoides (Railliet, 1 8 9 0 ) , Lepo- ridotaenia wimerosa (Moniez, 1 8 8 0 ) , L. pseudowime- rosa ( T e n o r a , Murai, Valero & Cutillas, 1 9 8 1 - 8 2 ) and L. cf. wimerosa (Moniez, 1 8 8 0 ) ( A n o p l o c e p h a l i d a e ) ;Trichuris leporis (Froelich, 1 7 8 9 ) (Trichuridae); Gra- phidium strigosum (Dujardin, 1 8 4 5 ) and Tricbostron- gylus retortaeformis (Zeder, 1 8 0 0 ) (Trichostrongylidae) ;
Nematodiroides zembrae (Bernard, 1 9 6 5 ) (Molineidae);
Passalurus ambiguus (Rudolphi, 1 8 1 9 ) ( O x y u r i d a e ) ; Dermatoxys bispaniensis ( S i m o n Vicente, 1 9 6 9 ) (Hete-
r o x y n e m a t i d a e ) a n d Protostrongylus cuniculorum ( J o y e u x & Gaud, 1 9 4 6 ) (Protostrongylidae).
Distribution o f the helminths in the t w o host popula
tions, p r e v a l e n c e s a n d parasitation intensities are s h o w n in T a b l e I.
Overall prevalences are high in both host populations and n o significant differences can b e observed between them ( T a b l e I ) . However, significant differences are o b s e r v e d in the prevalences b y Cestodes (%2 = 7 . 4 4 ) . Such differences are mainly due to the p r e s e n c e o f Leporidotaenia spp. in the southern population. Com
parative analysis o f prevalences o f the parasite species has demonstrated the e x i s t e n c e o f significant diffe
r e n c e s in most o f them (T.pisiformis larvae, %2 = 4 . 4 3 ; A. cuniculi, %2 = 3-92; C. denticulata, %2 = 1 1 . 7 4 ; L. wimerosa, %2 = 2 7 . 6 0 ; L. pseudowimerosa, %2 = 10.80;
L. cf. wimerosa, %2 = 1 2 . 8 0 ; G. strigosum, %2 = 2 1 . 9 8 ; N. zembrae, %2 = 5 7 . 1 7 ; P. ambiguus, y} = 16.27; D.
bispaniensis, %2 = 67.61). T h e highest infestation pre
v a l e n c e s o f all species, with the e x c e p t i o n o f T. pisi
formis larvae, were detected in the Southern Peninsula.
W h e n comparing parasitation intensities in b o t h host populations, statistically significant differences have only b e e n found in T. retortaeformis (significance level p = 0 . 0 0 4 ) ( T a b l e I).
T a b l e II s h o w s p r e v a l e n c e s and m e a n parasitation intensities in all males and females o f each population.
G e n e r a l N o r t h - E a s t e r n n = 1 5 3 S o u t h - W e s t e r n n = 62
(O. cuniculus cuniculus) (O. cuniculus algirus)
P ( % ) P ( % ) Min. I. Max. I. M e a n I. P ( % ) Min. I. M a x . I. M e a n I.
Dicrocoelium dendriticum 1 7 . 8 1 7 . 8 6 7 0 0 9 4 . 3
T r e m a t o d e s 1 7 . 8 1 7 . 8
Taenia pisiformis larvae 2 8 . 4 3 3 . 3 1 29 4 . 7 16.1 1 31 4 . 7
Andrya cuniculi 1 5 . 4 1 2 . 4 1 4 5 1 0 . 0 2 2 . 6 1 9 2 1 7 . 0
Citlotaenia denticulata 5.1 1.3 2 2 2 . 0 1 4 . 5 1 3 L.8
Neoctenotaenia ctenoides 3 4 . 9 3 5 . 3 1 5 1.7 3 3 . 9 1 2 L.6
Leporidotaenia wimerosa 7 . 0 — — — — 2 4 . 2
ieporidotaenia pseudowimerosa 3.3 — — — — 1 1 . 3 2 6 5 1 9 . 8
Leporidotaenia cf. wimerosa 3.7 — — — — 1 2 . 9
C e s t o d e s 6 7 . 0 6 1 . 4 8 0 . 7
Tricburis leporis 1 4 . 9 17.7 1 6 3 6 . 3 8.1 1 3 1.6
Graphidium strigosum 5 1 . 2 3 9 . 6 1 2 , 8 9 0 2 1 1 . 3 7 9 . 0 1 5 6 8 1 0 1 . 0
Trichostrongylus retortaeform is 7 7 . 7 7 7 . 8 1 2 , 9 0 6 1 8 6 . 7 7 7 . 4 1 1 6 2 4 3 . 2
Nematodimides zembrae 4 7 . 0 3 2 . 6 1 2 1 7 3 7 . 7 8 2 . 3 1 7 7 1 7 1 . 2
Prostostrongylus cuniculorum 1.5 1.5 110 172 1 4 . 0
Passalurus amhiguus 2 0 . 5 11.8 2 1 8 . 7 1 5 2 , 5 8 1 . 7 4 1 . 9 1 9 , 1 1 0 2 . 1 1 7 . 0
Dermatoxys hispaniensis 17.2 2 . 0 1 7 3.0 5 4 . 8 1 1 3 3 2 5 . 5
N e m a t o d e s 9 2 . 1 9 2 . 2 9 1 . 9
H e l m i n t h s 9 4 . 0 9 4 . 8 9 1 . 9
Table I. — Prevalences and intensities in wild rabbits.
P a r a s i t e , 1 9 9 6 , 4, 3 2 7 - 3 3 3 329
BLASCO S., TORRES J . . FELIU C , CASANOVA J.C., MI QUEL J. & MORENO S.
Although prevalences of most species are higher in females, significant differences have only been found in overall prevalence of Cestodes (%2 = 5.02) and A.
cuniculi (%2 = 6.47). No statistically significant diffe
rences have been found in the Northern Peninsula. In the Andalusian population, higher prevalences have b e e n observed in females, but they were only significantly different in Cestodes (%2 = 6.58), A. cuni
culi (X2 = 7.56), T. relortaeformis (%2 = 6.26) and D. bispaniensis (yf = 4.33).
Mean parasitation intensities are also higher in females.
However, statistically significant differences have only been found in the case of T. retortaeformis in the whole population (p = 0.02) and in each area (North p = 0.04; South p= 0.05).
DISCUSSION
T
he helminthfauna o f Oryctolagus cuniculus in the Iberian Peninsula is mainly constituted b y o l i g o x e n o u s s p e c i e s . Therefore, the parasite fauna o f the t w o studied populations s h o w s the s a m econfiguration. Similar results h a v e b e e n d e s c r i b e d in the remaining distribution area o f the host ( T e n o r a a n d Barus, 1 9 5 7 ; Bernard, 1 9 6 5 ; Horning, 1 9 7 4 ; Sugar et al, 1 9 7 8 ; Haupt a n d Hartung, 1 9 8 4 ; B o a g , 1 9 8 5 a n d 1987; Butler, 1 9 9 4 ; etc.). However, the highest n u m b e r o f s p e c i e s , a m o n g the cited helminthfaunas in the dis
tribution area o f the host, has b e e n detected in the Ibe
rian Peninsula. Moreover, s p e c i e s that are a b l e to para
sitize o t h e r Iberian m a m m a l s (D. dendriticum a n d T. retortaeformis) ( C o r d e r o del Campillo et al, 1 9 9 4 ) are also present in the peninsular rabbit a n d s h o w high or very high p r e v a l e n c e s . T h e p e r c e n t a g e o f infesta
tion b y D. dendriticum ( 1 7 . 8 % ) is a m o n g the highest detected in Continental E u r o p e ( C a s a n o v a et al, in p r e s s ) .
T h e comparative study o f the Catalonian a n d Andalu
sian populations s h o w s faunistic a n d e c o l o g i c a l diffe
r e n c e s , w h i c h are often statistically significant. Quali
tatively, the population from Southern Spain c a n b e identified b y the Cestodes o f the g e n u s Leporidotaenia ( T a b l e I ) . D. dendriticum has b e e n o c c a s i o n a l l y found in the liver o f s o m e rabbits from C o t o D o n a n a (Sevilla and Huelva p r o v i n c e s ) . This finding confirms the pre-
General n = 175 North-Eastern n - 114 South-Western n = 6 1
(O. cuniculus cuniculus) (O. cuniculus algi. rus)
Males n = 77 Females » = 9 8 Maies n = 51 Females n = 6 3 Maies n - 26 Females n=35 P (%) Mean I. P(%) Mean I. P (%) Mean I. P (%) Mean I. p (%; Mean I. P (%) Mean I.
Dicrocoeliiim
denâriticum 19.6 96.8 19.1 107.7 19.6 96.8 19.1 107.7
TremaUxles 19.6 19.1 19.6 191
Taenia pisiformis lawac 20.8 4.6 31.6 5.5 25.5 5.3 38.1 5.3 11.5 1.3 20.0 6.1
Andrya cuniculi 6.5 11.0 21.4 13.6 7.8 16.3 12.7 6.0 3.9 1.0 37.1 18.2
Cil toi aa lia den tic it lata S. 1 1.5 6.1 2.0 2.0 2.0 — — 11.5 1.3 17.1 2.0 Neoctenotaenia ctenoides 31.2 1.5 37.8 1.6 31.4 1.5 38.1 1.6 30.8 1.5 37.1 1.6
Leporidotaeiiia uimerosa 9.1 8.2 — — — — 26.9 22.9
Leporidotaenia pseudoivi-
merosa 2.6 14.6 5.1 22.7 — — — — 7.7 14.6 1 13 22.7
Leporidotaenia cf. wime-
rosa 1.3 7.1 — — — — 3.9 20.0
Cestodes 58.4 75.5 54.9 65.1 65.4 94.3
Tricbiirts leporis 11.- 6.6 12.2 7.6 13.7 8.0 14.3 9.6 7.7 1.5 8.6 1.7
Graphidium strigosum (8.1 168.2 61.2 179.3 37.3 235.8 46.0 260.2 69.2 96.8 88.6 103.5 Tricbostroiigy'his retor-
taeformis 70.1 88.6 81.6 189.4 74.5 113.8 76.2 282.0 61.5 28.8 91.4 50.4
Nematodiroides zembrae 36.4 37.1 50.0 73.1 17.7 44.1 27.0 34.9 73.1 33.8 91.4 93.4 Protostrongylus cunicu-
lorutn 2.0 110.0 1.6 172.0 2.0 110.0 1.6 172.0
Passalurus ambiguus 19.5 2,483.0 27.6 1,752.9 9.8 3,905.0 17.5 909.6 38.5 1,772.0 45.7 2,332.7 Dermatoxys bispaniensis 14.3 24.6 25.5 24.2 2.0 7.0 1.6 1.0 38.5 26.4 68.6 25.1
Nematodes 89.6 92.9 90.2 90.5 88.5 97.1
Helminths 90.9 94.9 94.1 93.7 88.5 97.1
Table II. — Prevalences and mean intensities according to sexes.
3 3 0 Parasite, 1996, 4, 327-333
Mémoire
HELMINTHFAUNA OF ORYCTOLAGUS CUNICULUS
s e n c e o f the Trematode in Andalusia (Casanova, unpu
blished data).
O u r results s h o w o n c e again that origin a n d e v o l u tion o f C e s t o d e s b e l o n g i n g to the g e n u s Leporido- taenia are difficult to e x p l a i n ( G e n o v et al, 1 9 9 0 ) . L.
wimerosa and L. cf. wimerosa infest s p e c i e s o f Oryc- tolagus and Lepus in W e s t e r n E u r o p e ( G e n o v et al, 1 9 9 0 ) . H o w e v e r , in the Iberian Peninsula, they h a v e only b e e n found in S o u t h e r n Spain. R e c e n t studies p e r f o r m e d in rabbits from Navarra (Northern Penin
sula) h a v e not s h o w n either the p r e s e n c e o f t h e s e s p e c i e s . O n t h e o t h e r h a n d , L. pseudowimerosa, d e t e c t e d originally in S o u t h e r n Spain ( T e n o r a et al., 1 9 8 1 - 8 2 ) , s e e m s to h a v e a restricted c h o r o l o g y to this area o f t h e Iberian Peninsula. T h e p e n i n s u l a r para
site fauna o f Oryctolagus cuniculus s h o w s the relic- tual trait o f the Iberian helminthfaunas (Hugot a n d Feliu, 1 9 9 0 ) . S u c h c o n d i t i o n is o b s e r v e d in t h e e v o lution o f a g e n u s o f Cestodes (Leporidotaenia), w h i c h has b e e n probably influenced by the peninsular origin o f Oryctolagus. T h e a b s e n c e o f t h e s e A n o p l o c e p h a l i d C e s t o d e s in Australian rabbits (Bull, I 9 6 0 and 1 9 6 4 ; D u n s m o r e , 1 9 7 8 ) substantiates s u c h h y p o t h e s i s . T h e p r e s e n t study d e m o n s t r a t e s for the first time t h e pre
s e n c e o f L. cf. wimerosa in iberian rabbits. T h u s , e v o lution, distribution a n d specificity o f L. wimerosa and L. cf. wimerosa c o u l d b e s i m i l a r ( W e s t e r n E u r o p e / L e p o r i d a e ) . H o w e v e r , L. pseudowimerosa s e e m s t o f o l l o w a d i f f e r e n t p r o c e s s ( S o u t h e r n S p a i n / Oryctolagus).
T h e genetically different Iberian rabbit populations, O. c. cuniculus (north-eastern) and O. c. algirus (south
w e s t e r n ) , can also b e differentiated by their Leporido
taenia s p e c i e s . H o w e v e r , s p e c i e s o f this g e n u s have not b e e n found in Lepus spp. ( C o r d e r o del Campillo et al., 1 9 9 4 ) o f Iberian Peninsula. This surprising fact d o e s not correlate with the range hosts that L. wime
rosa and L. cf. wimerosa s h o w in o t h e r E u r o p e a n c o u n t r i e s ( G e n o v et al., 1 9 9 0 ) . M o r e o v e r , o t h e r e n d e m i c N e m a t o d e s p e c i e s (D. bispaniensis) infest also Iberian rabbits and hares ( S i m o n Vicente, 1 9 6 9 ) .
T.pisiformis (33-3 % in Catalonia/16.1 % in Andalusia;
%2 = 4 . 4 3 ) evolves in the Iberian Peninsula using foxes as definitive hosts. No data exist about infestation o f this Canid in Southern Spain. In Catalonia, the Carni
vore appears to b e infested at low rates b y adult tape
w o r m s (6.1 % ; Miquel et al, 1 9 9 4 ) . D u e to the segre
gation o f the functional s p a c e b e t w e e n f o x e s and lynxes in the studied Andalusian area (Frediani, 1 9 9 3 ) , the cycle o f T. pisiformis could have greater limitations to b e c l o s e d and, therefore, l o w e r rates o f infestation b y larvae in rabbits are detected.
Quantitative results are difficult to e x p l a i n for the remaining s p e c i e s , e x c e p t for the a f o r e - m e n t i o n e d Leporidotaenia spp. T h e data o f s o m e m o n o x e n o u s
p s e u d o g e o h e l m i n t h N e m a t o d e s (P. ambiguus and D. bispaniensis) and g e o h e l m i n t h s (G. strigosum and N. zembrae) are specially controversial. Evidently, humidity and temperature conditions are more adverse for these Nematodes in the Southern regions than in t h e Northern P e n i n s u l a . T h u s , h i g h e r p r e v a l e n c e s should b e e x p e c t e d in the Northern biotopes. Such p h e n o m e n a was described by D u n s m o r e (1966 b) in a study about G. strigosum prevalences in four Aus
tralian areas with different climatic conditions. Lower prevalences w e r e detected in areas with e x t r e m e cli
matic conditions. Lack o f precise information about the biology o f these N e m a t o d e s leads us to the hypothesis that higher density o f wild rabbits in the Southern P e n i n s u l a c o u l d b e t h e m a i n c o n d i t i o n i n g factor influencing our results. Moreover, maximum and mean intensities are, for most Nematode species, higher in the Catalonian population. This would indicate that cli
matic conditions in this area are m o r e advantageous for the majority o f parasite cycles.
T h e effect o f sex, per se, o n the helminthfauna o f O. cuniculus in both populations s e e m s to b e low. In this s e n s e , n o significant differences have b e e n found in Catalonian hosts. Respecting to Andalusian hosts t h r e e s p e c i e s s i g n i f i c a n t l y different (A. cuniculi,
T. retortaeformis, D. bispaniensis) display c o m p l e t e l y different lyfe cycles, which m a k e s difficult to s p e c u late about possible c a u s e s o f their higher prevalences in females.
T h e relationship b e t w e e n helminthfauna and host s e x has always b e e n controversial. Thus, Dudzinski and Myckytowycz ( 1 9 6 3 ) s h o w e d that parasitation intensity d o e s not d e p e n d o n host s e x for T. retortaeformis, but it d o e s for G. strigosum. This N e m a t o d e s e e m s to s h o w higher parasitation in females. D u n s m o r e ( 1 9 7 2 ) cited higher intensities for b o t h species (T. retortae
formis and G. strigosum) in females. However, B o a g and Kolb ( 1 9 8 9 ) described o p p o s i t e results. Mead- Briggs and Vaughan ( 1 9 7 3 ) stated that C. denticulata is m o r e frequent in males. B o a g ( 1 9 8 5 ) and Butler (1994) a g r e e d in that n o significant differences exist b e t w e e n males and females in prevalences by Cestodes and Nematodes. Most authors believe that differences in parasitation intensities o f T. retortaeformis (Bull, 1959; D u n s m o r e , 1 9 6 6 a; D u n s m o r e and Dudzinski, 1 9 6 8 ) , G. strigosum ( D u n s m o r e , 1966 ft) and P. ambi
guus ( D u n s m o r e , 1966 C; D u n s m o r e and Dudzinski, 1 9 6 8 ) b e t w e e n males and females are related to the season. Thus, females s h o w higher rates than males during reproductive periods and an opposite t e n d e n c e is o b s e r v e d during the rest o f the year. T h e influence o f h o r m o n e s in the parasite-host relationship was already described in a study about the influence o f the host reproductive state o n the n u m b e r o f T. retortae
formis and
G. strigosum ( D u n s m o r e , 1 9 6 6 d ) .Parasite, 1996, 4, 527-355
3 3 1Mémoire
B L A S C O S., TORRES J., FELIU C , C A S A N O V A J.C., MIQUEL J. & M O R E N O S.
ACKNOWLEDGEMENTS
T
h e authors want to thank D . Antoni Arrizaba- laga (Granollers, S p a i n ) a n d Dr. R o g e r Pons (Banyuls-sur-Mer, F r a n c e ) for c o n c e d i n g s o m e o f the studied hosts. T h e study has b e e n partially sup- ported by the Spanish D G I C Y T Project P B 9 2 - 0 5 1 7 - C O 2 - 0 2 and the « Comissionat per Universitats i Recerca de la Generalitat d e Catalunya » ( G R Q 9 4 - 1 0 5 7 ) .REFERENCES
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Recu le 11 mars 1996 Accepté le 10 aoüt 1996
Mémoire
