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EFFECT OF GENETIC TYPE, LACTATION AND MANAGEMENT ON HELMINTH INFECTION OF EWES IN AN INTENSIVE GRAZING SYSTEM ON IRRIGATED PASTURE L. GRUNER,* J.Bourx,tJ.CABARET, *C.

§CNEVA,

BOULARD,*J.CORTET,* C.SAUVE,* G.MOLENAT$ M.CALAMEL$

*INRA,Station de Pathologie Aviaire et de Parasitologie, 37380 Nouzilly, France TINRA, Station d’AmClioration Genetique des Animaux. BP 27, 31326 Auzeville, France fDomaine INRA-ENSA du Merle, Route d’Arles, 13350 Salon de Provence, France Laboratoire de Pathologie des Petits Ruminants et des Abeilles, Route des Colles, Sophia Antipolis, France (Received

29 January

1992; accepted

I8 June

and

06410 Biot,

1992)

Abstract- GRUNER L., BOUIXJ., CABARETJ., BOULARDC.. CORTETJ., SAUVEC., MOLENAT G. and CALAMEL M. 1992. Effect of genetic type, lactation and management on helminth infection of ewes in an intensive grazing system on irrigated pasture. International Journal ,for Parasitology 22: 919-925. A survey of helminth infection was conducted in a flock of 290 ewes distributed into Romanov (R), Merinos d’Arles (M) and Romanov x Merinos (R x M) genetic types, grazing irrigated pasture in the south of France. Faecal egg and larval counts were done seven times per year from 198 I to 1984 on homogeneous groups of ewes and then individually once to four times every autumn from 1985 to 1988. Helminth fauna was diverse and more abundant during autumn. High levels of strongyle infection occurred in the ewes that remained on the same irrigated pastures during summer. Moving to Alpian pastures during the summer lowered autumnal infection. Significant differences between genotypes in intensity of infection were observed in the order R> R x M > M for strongyles (Tekadorsagia circumcincta and/or Trichosirongylus vitrinus, Chabertia ovina and/ or Oesophagostomum venulosum, Nematodirus spp.). Moniezia spp. and Dict.vocaulusjilaria. The hierarchy was reversed for Fasciola hepafica infection and not consistent from one year to another for protostrongylid infections. The effect of lactation intensity on the postparturient rise was studied by equilibrating number of ewes according to reproductive status (zero, one or two lambs in lactation). Merino ewes with two lambs in lactation, as well as primiparous Romanov ewes, had significantly higher strongyle infections than the others. The repeatabilities of the larval and egg counts between the four trial years were 0.24,0.23 and 0.16, respectively, for protostrongyles, Nemarodirus and strongyles, with higher intra-annual values for protostrongyles and inconsistently significant results for strongyles due to the presence of several species. INDEX KEY WORDS: Sheep helminths; Telador.sagia; Tricho.rlronR?/u.s: Dictyocaulus; liver flukes: breed; lactation; irrigated pasture: faecal excretion: repeatability.

INTRODUCTION IN

the Mediterranean

climatic

region

protostrongyles:

In this study, the flocks were intensively managed and grazed on irrigated pasture. Parasitism was very diverse and high levels of infections occurred (Gruner & Cabaret, 1985). The aim of this experiment was firstly to compare intensity of helminth infection between categories of ewes, and secondly to study the individual response to parasites.

of south-eastern

France, Merinos d’Ar1es is the commonest breed, and is well adapted to the local conditions. Attempts are being made to increase flock productivity by introducing the highly prolific Romanov breed. To assess the adaptative potential of this breed in Mediterranean conditions, experimental flocks composed of Romanov (R), Merino (M) and Romanov x Merino (R x M) ewes are established in different ecological situations and at different levels of productivity. On irrigated pasture, infection is less dependent on climatic conditions than in non-irrigated pasture and the soil is the reservoir of infective larvae during the main part of the grazing season (Gruner, Mounport & Suryahadi. 1987).

MATERIALSANDMETHODS The investigations were performed at ‘Domaine du Merle’ (Salon de Provence) in the southern part of France. The climate is a humid Mediterranean one (640 mm of annual rainfall, with an average temperature of 6°C in January and 22.5”C in July). The flock was composed of 290 ewes equally distributed between Merinos d’Arles, Romanov and their cross. The three lambing periods were February, June and 919

920

L. TABLE

I-VARIABLES

Abbreviated name Parasitological GIS NEM DICT DICR PRO Factors GENO AGE LITT LALA LLIN LACT MOVI YEAR IND

GRUNER

et

al.

AND FACTORS TAKEN INTO ACCOUNT FOR EXPERIMENT

Expression

Designation

variables gastro-intestinal strongyles other than Nematodirus Nemotodirus spp. Dictyocaulus sp. Dicrocoelium sp. protostrongyles

faecal egg counts egg presence-absence egg presence-absence egg presence-absence faecal larval counts

genotype age of the ewes litter size for individual ewes number of lambs in lactation litter-lactation index milk production of the ewe estimated on lamb weight gains moving to Alpian pasture year of sampling individual ewe

September~to~r. The ewes were set stocked together for 2 years at the beginning of the experiment, on irrigated pasture at 20 ewes ha-‘. Paddocks were flooded every 10 days from April to October. During the winter, ewes were totally or partly housed. Irrigated pastures were grazed from March to December. Lambs grazed with their dams and received supplementary feed for finishing. During summer, one-half (1981 to 1986) or the entire flock (in 1987 and in 1988) moved to Alpian pasture located from 1500 to 2000 m above sea level, from June to the end of September. The remainder continued grazing irrigated pasture. After lambing in October, ewes grazed nine irrigated paddocks in two flocks; lactating ewes and non-lactating ewes. Culling rate of the ewes was 20% per year. The permanent pasture was composed of SO-60% of grasses (mostly hcfj’h gfumerara and Arrhenathcrum elutiu.7). 25-30% of legumimous plants (Trfolium pratense and Lotus cornicufatus) and 1S-20% of various plants (Plantago lanceolatum, Taraxacum c#icinaie, etc.). Hay was made from excess grass in each year on some of the paddocks. Two successive investigations were performed from the end of 198 1to the end of 1988. Experiment 1 (I 98 I1984): the flock was sampled seven to eight times per year from November 1981 to June 1984. Faeces were coilected from five ewes per reproductive category (dry to first month pregnancy or pre-lambing to lactating ewes) and per genotype (R, M or Rx M). Experiment 2 (1985-1988): to study the parasite excretion of eggs at the individual level, egg counts were done on every ewe of the flock at the principal lambing period (September-October) and at the end of the grazing season (beginning of December). The sampling dates were: December 1985. December 1986, September, October, November and December 1987, September and December 1988. In December 1986. only dry ewes were sampled. To study the relations between parturition, lactation and helminth

2

I= M,Z= RxM,3= R l=land2to8= 9yrsormore I= Oto4= 3ormorelambs I= 0 to 3 = 2 lambs see details in Table 3 IO-30 days bodyweight gain I = sedentary, 2 = moving l= 1985to4= 1988 I-509th sampled ewe

infection, four flocks were sampled in 1987, each grazing its own two paddocks during autumn: non-lactating dry ewes (n = 48) with Romanov (R), Romanov x Merino (R x M) and Merino (M) genotypes, non-lactating ewes weaned at lambing (n = 59), with M and R x M, lactating ewes feeding one lamb (n = 75), with M, R and R x M and iactating ewes feeding two lambs (n = 53), with M, R and R x M. In 1988, the number of ewes with zero, one or two lambs were also balanced between the genotypes, but ewes were managed in two flocks, lactating and non-lactating. In all cases, pastures were grazed during the summer with a naturally infected flock. Variables and factors taken into account in Experiment 2 are summarized in Table I. Paras~zo~o~~cait~~r~nique.~.Egg and larval counts were processed with the technique of Caiamel & Soule (1975) in Experiment 1. In Experiment 2, 3 g of faeces was Baermannized to collect the lungworm larvae; 5 g was processed in potassium and mercuric iodide for egg counts in McMaster slides. Individual cultures were processed in December 1985 and 1986 for larval identification. Infective larvae were categorized as Te~ador.~a~io circumcin~~~i Trie~~Jsrrong~iu.~ vizrinus, Chaberria ovinu and N~rna~od~ru.~ spp. In 1985 and 1986 a serum ELlSA test was processed for liver fluke diagnosis (Boulard, Bouvry & Argente. 1985). Nematode species were identified according to Durette-Desset (1979. 1989) and Rossi (1983) on adults sampled from 12 necropsied ewes. ~~~f~r~c~~ analysis. During the second experiment, a total of 1866 faecal samples were collected. The parasitological variables were: LoglO-transformed faecal egg or larval counts or presence-absence, for gastrointestinal strongyles (GIS), Nematodiru.r (NEM), Dicrocoelium (DICR), protostrongyles (PRO) and Dic~yocaulus (DICT). Several variance analyses were tested (with or without interactions) by using

Variability

in helminth

Amance software (Bachacou, Masson & Millier, 1981). The repeatability of the faecal egg counts of the ewes was calculated between years (509 ewes were examined one to four times in December from 1985 to 1988) or within year between lambing time and December. Two linear models were used for each parasitological variable(Y). The betweenyear model was

Yijklmno = u + YEARi

t

GENOm

+ MOVlj + AGEk + LALAl lNDmn + Eijklrnno,

+

where u = overall mean YEARI‘, i= 14, was the fixed effect of the ith level of YEAR MOVIj, j= l-2, was the fixed effect of thejth level of MOVI AGEk, k = 1-8, was the fixed effect of the kth level of AGE LALAI, I= I-3, was the fixed effect of the Ith level of LALA GENOm,m= I-3,was thefixedeffectofthemthlevel ofGEN0 INDn, n = l-509, was the random effect of the nth individual. Y~jklmno and ~~k~~~~o were, respectively. the value of the observation and of the residual of the 0th measure of the nth individual with GENOm, LALAI, AGEk, MOVIj and YEARI‘. For within year and LALA value, the model was

Yijk = u + (MOW

x AGE

x GENO)I’

t INDik + E[jk,

where (MOW x AGE x GENO)i was the combination of the three fixed effects for i corresponding to i x j x k of the previous model. In these models, interactions between fixed effects were also studied. For these two models, repeatability r was

Y = var(lND)

/ ( var(lND)

+ var(E) ).

where var(lND) was the individual component variance and var(E) was the residual variance.

infections

921

of ewes

TABLE ~---COMPAR~~~N~~FTHEFAE~ALEC~GO~LARVAL FOR THE MAJOR HELMINTHS

BETWEEN CATEGORlES

Parasite

Ewe categories comparisons Lactating Romanov RxMvsM RvsRxM

vs non lact. Rvs Merinos

M

COUNTS

OF EWES

Excretion

GIS

PRO

DICR

Fu~iola

S S S NS

NS NS NS HS

NS NS NS NS

NS NS NS NS

R, Romanov; M, Merinos of Arles; NS, non-signifi~nt~ S and HS, significant for P~0.05 and PiO.01 respectively. Other abbreviations as for Table 1.

and R x M genotypes compared with M. Differences were not significant between R and RX M and between all the groups for the other major he~minths. Individual variation of the helminth egg and larval excretion (Experiment 2) The relative importance of the significant source of variation for the strongyles and for the protostrongyles were different (Fig. 1, Tabie 3). For the strongyles, the litter-lactation index, the year and the genotype were more important than for the protostrongyles. For the latter, ewe effect (509 ewes in total), age (oldest ewes were more infected), moving during the summer (lowerexcretion forewes which moved) were relatively more important, a third of the variance remaining unexplained.

of the

The fauna was particularly diversified with the liver (Fasciola heputica and Dicrocoelium ianceolatum), Cestodes (Moniezia spp.) and nematodes. Protostrongyle species were Neostrongy/us linearis, Protostrongylus rufescens, Cystocaulus oc’rectus and Mueilerius capillaris. DictyocauIusJilaria was also present. In the digestive tract. Te~adorsa~ia ~~rcu~zc~n~ta (and its morph T. tri&rcata), and Trichostrongylus vitrinus were the major species. Minor species were Nematodirus f N. spathiger, N. jilicoNis, N. chabaudi and N. abnormalis), Chabertia ovina and Oesophagostomum venulosum. For the sedentary flock, strongyle egg output was high ti~roughout the year and drenching was necessary to limit it. infection with protostrongyles and flukes was higher during autumn and winter. The comparison of strongyle egg counts between categories of ewes (Table 2) revealed significantly higher counts in lactating compared with non-lactating ewes, and in R flukes

STRONQYLES

PROTOSTRONGYLES

FIG. I. Relative importance of significant factors acting on the egg and larval counts at the end of the grazing season (percentage of adjusted sum of squares).

The variance analyses with highest (R’) values (percentage of explained variance) were those done on GIS and PRO after logarithmic transformation and on the presenceeabsence data for NEM and DICT. Ewes that moved during the summer experienced lower autumnal infection with strongyles and protostrongyles than the sedentary ones. Older ewes experienced lower infection for GIS and NEM and higher for PRO compared with younger ones. No effect of LITT or LACT was observed when GENO, LALA and YEAR were taken into account. For the four variables, the

922

L.

GRUNER

et al.

TABLE ~-~ALUESOPTHEPARAS~TOLOG~CALVAR~ABLESASADJUSTEI)GEOMETRICMEANEGGORLARYALCOUNTS PERGRAMOFFAECESFORGISAND

Factor

Class

I= 2= 3= I= 2= 3= 4= I= 2= I= 2= 3= 4= 5= 6= 7=

GENO

YEAR

MOVI AGE

8 =

M RxM R 1985 1986 1987 1988 sedent. moving < 3 years 3 years 4 years 5 years 6 years 7 years 8 years 9 and more

1 = Oborn 2= lborn 3= 2born

LLIN

4= 5= 6= 7= 8= 9=

Olact. llact.

llact. Zborn Zlact. 3born llact. 3born Zlact. >ObornOlact. 1born Olact. (1987) Zborn Olact. (1987)

PROoa

MEANPREVALENCESFOR

NEM,DICRANDDICT

No. of samples

GIS

PRO

epg

lpg

NEM

Prevalence DICR

DICT

293 355 352 283 181 217 219 233 667 79 184 199 106 159 94 39 40 437 160 47 116 22 44 28 34 12

57 94 124 37 246 70 135 122 76 124 108 63 94 73 91 136 67 36 226 229 422 393 371 65 10 13

10 12 15 13 32 15 4 30 9 2 8 14 19 19 17 24 20 I 18 16 25 39 39 9 4 I

43.4 57.7 70.1 60.6 44.9 58.2 59.3 57.2 56.3 90.2 61.3 55.2 48.1 53.5 47.5 52.5 34.5 47.7 70.3 62.0 67.7 75.7 76.3 51.2 25.6 61.2

58.6 64.6 53.9 87.2 96.5 24.9 28.1 61.6 59.0 53.6 63.5 59.3 60.7 62.8 55.8 52.5 56.5 61.1 65.0 60.5 55.3 78.7 52.9 62.4 34.0 31.9

21.8 32.8 44.7 8.9 60.3 29.8 42.9 29.6 33.6 28.2 30.4 31.2 39.8 33.0 34.9 24.8 39.1 20.5 43.6 42.2 54.5 52.5 49.1 40.9 88.1 26.7

See Table 1 for abbreviations

interaction GENO x LALA was significant; GENO x LALA x YEAR was significant for GIS, NEM and DICT. The effects of GENO, YEAR, and LALA on the GIS infection (Fig. 2) revealed the importance of lactation. Non-lactating ewes had lower egg counts than lactating ones, without any difference between dry ewes and those which were weaned at lambing time (in 1987). GENO was a very significant variable (P< 0.01) for non-lactating ewes, and the infection hierarchy was M < R x M < R. GENO was non-significant for ewes feeding one or two lambs. In 1987 and 1988 the size of GENO-LALA groups of ewes were balanced: in these years, the infection hierarchy was M > R x M > R for LALA = 2, especially in 1987. In 1988, nearly all R ewes were primiparous ones; their egg output was very high (Fig. 2), but this age effect was taken into account in the model The individual cultures done in 1985 and 1986 revealed that the significant (P

Effect of genetic type, lactation and management on helminth infection of ewes in an intensive grazing system on irrigated pasture.

A survey of helminth infection was conducted in a flock of 290 ewes distributed into Romanov (R), Merinos d'Arles (M) and Romanov x Merinos (R x M) ge...
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