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Abomasal nematodes in goats from the subtropicalisland of Grand Canary (Spain)

Jm Molina, Ac Gutiérrez, E Rodríguez-Ponce, Ja Viera, S Hernández

To cite this version:Jm Molina, Ac Gutiérrez, E Rodríguez-Ponce, Ja Viera, S Hernández. Abomasal nematodes in goatsfrom the subtropical island of Grand Canary (Spain). Veterinary Research, BioMed Central, 1997, 28(3), pp.259-270. �hal-00902479�

Original article

Abomasal nematodes in goats from the subtropicalisland of Grand Canary (Spain)

JM Molina AC Gutiérrez E Rodríguez-PonceJA Viera S Hernández

1 Deperrtamertto de Patologfa Animal (Perretsitolo!lcr 1. Eijfl.im<.<hiJ<..>. Ptit-tisit(iritis)Facultad de Veterinurlct de la Universidad de Las Palmas de Gron Canaria,

CI Fco, Inglott Artiles, 12-A, 35016 Las Palmas de Gron Canaria;2 I)el,,tirtiiiiento de Pctrusitologia v Enferntedndes !rf;A;!<r/i:<.s.

Facultad de Veterinaria de la Universidad de Ccirdobu,A i’d Medina A!ahara, 14071 Crirdoba, Spain

(Received 17 June 1996; accepted 14 January 1997)

Summary &horbar; The prevalence of gastric nematodes in 151 goats on Grand Canary Island is around 56%,with a mean burden of 691 worms/animal. No significant differences of prevalence and intensitywere found between the four isoclimatic areas of the island [dry-desert (DD); dry-steppe (DS); tem-perate-mild (TM); temperate-cold (TC)]. Five nematode species were identified, the most com-monty-occurring being ’relatlorvtigia circumcincto (observed in 65.8%n of parasitized animals) and Tri-c/M.sfron!v/H.’. axei (51.9°70). The distribution of the two species showed opposing trends: T circumci/lcWwas more prevalent in the coastal areas (DD), diminishing in frequency closer to the centre of the island(TC), while the reverse was true of T!c!fi. The other species identified were Haemonchus c ontnrtus,T trijifrcato and COlllelostro/lgvllls mentulertus: their ranges were restricted to certain areas (H t-oi7-tortus in DS and TM; T trijifrcata in DD, DS and TM; and C mentulatus in DD). To analyse theparasite association under natural conditions of an unusual nematode in goats, C iiiet7ttfl(itl(S, with theusual parasites a principal component analysis (PCA) was used to assess the overall behaviour of thenematode community and to examine the Euclidean distances of the parasite associations. The meanEuclidean distances obtained for C mentulutus showed a tendency to a positive association which hasalso been observed for the other abomasal nematodes.

abomasal nematode / goat / parasite association

Résumé &horbar; Nématodes de la caillette chez les chèvres de l’île subtropicale des Canaries (Espagne).La prévalence des nématodes gastriques chez 151 chèvres de l’île des Canaries est de 56 %, avec une

&dquo; Correspondence and reprints.Tel: (34) 28 45 1 I 06; fax: (34) 28 45 I 1 02.

moyenne de 691 vers/animal. Aucune différence significative de prévalence et d’intensité n’a été trou-vée entre les quatre zones climatiques de l’île (désert, steppe, climat tempéré doux, climat tempéréfroid). Cinq espèces de nématodes ont été identifiées, la plus répandue étant Teladorsa,!ia circumcincta(observées dans 65,8 % des animaux parasités) et Triclmntrnngylus axei (51,9 °/n). La distribution desdeux espèces montre des tendances opposées : pour T circumcincta, elle était plus fréquente dans lazone cotière (désert), et moins fréquente dans le centre de l’île (climat tempéré froid), alors que c’estl’inverse pour T axei. Les autre espèces identifées étaient Haell10nchus conf!rfM.s, T trifurcata etCameLostrongyLus mentulatus ; leur présence était restreinte à certaines zones (H contortus dans le désertet la zone de climat tempéré doux ; T trifÚrcata dans le désert, la steppe et la zone de climat tempérédoux, C mentulatus dans le désert). Pour analyser les associations de parasites dans les conditions natu-relles d’un nématode inhabituel chez les chèvres (C iiienitilaiiis) avec les parasites habituels, uneanalyse en composantes principales (ACP) a été employée. Cette analyse a permis l’évaluation du com-portement global ainsi que l’estimation des distances euclidiennes entre les espèces composant la com-munauté parasitaire de nématodes. Les distances euclidiennes moyennes obtenues pour C lI1entula-tus montrent une tendance vers une association positive ce qui a été aussi observé pour les autresespèces de nématodes de la caillette.

nématode de la caillette / chèvre / association de parasites

INTRODUCTION

The effects of abomasal nematode infectionare well documented, and it is considered amajor cause for production loss (Vercruysseet al, 1988).

Although previous analyses in our labo-ratory have shown that abomasal nematodesare one of the most common parasites inGrand Canary Island goats, no precise datahave hitherto been available regarding theirreal prevalence and their distribution on theisland. The island’s goats may be consid-ered to form a closed indigenous popula-tion, as the importation of small ruminantshas been negligible or non-existent since1980. At the same time, the goat farms couldbe considered isolated from each other, as aresult of the very limited introduction ofnew animals after the establishment of eachfarm. Therefore, parasitological studies ina population of this sort are likely to dis-close factors more closely related to localconditions than in areas where the animal

exchange is more frequent.The purpose of this study was to deter-

mine the prevalence and intensity of abo-masal nematodes in goats on Grand Canary

Island in relation to the four isoclimatic

zones, in order to assess the possible effectof certain environmental factors on infec-tion levels and on the particular speciesinvolved in each case. The paper also exam-ined interspecific associations in these nat-urally acquired nematode communities fol-lowing the tnodel proposed by Hostc andCabaret ( 1992).

MATERIALS AND METHODS

Goat farming and climatology

The herds in Grand Canary Island are composedof 200-500 dairy goats, and the introduction ofnew animals after the initial establishment of theherd is rare. The herd breeding type is semi-inten-sive (grazing on pasture is very limited andlocated in the south of the island) and supple-mented on the farms with corn, wheat bran and

dehydrated lucerne. Antiparasitic treatmentsusing levaillisole are administered very sporad-ically.

All the animals examined in this study wereadult dairy goats of the local breed (Canariangoat) at the end of their production cycle (after the4th-6th lactation, weighing 45-50 kg). Theywere slaughtered at the island’s abattoir betweenOctober 1994 and March 1995. At the abattoir,

information about the origin of each animal wasrecorded. The selected animals belonged to 47different herds.

In Grand Canary Island, following the isocli-matic zone scheme outlined by Rodriguez-Ponceet al ( 1995), two basic climatological zones canbe considered: dry (D) and temperate (T). Theseare further subdivided to give a total of fourzones, as follows:

Dry zones

Dry zones (D) are found below 200 m altitudeon or near the coast, and are divided into:

- dry desert (DD), characterized by low pre-cipitation (< 180 mm per year), an average annualtemperature > 1 R °C and very dry summers. Veg-etation consists primarily of Eul!liorbia spp, cacti,succulents and palms;- dry steppe (DS), with an average annual tem-perature of > 18 °C, and average precipitationlevels of 180-360 mm per year. It can be con-sidered as a steppe-like climate with dry sum-mers, and vegetation similar to that of DD.

Temperate zones

Temperate zones (T) have winter temperatures< 18 °C and considerable winter rainfall. Thesezones are divided into:

- temperate mild (TM), at an altitude of200-800 m, characterized by hot, dry summersand mild winters. Annual precipitation level isaround 400 mm per year;- temperate cold (TC), at over 800 m above sealevel. Conditions are similar to TM, except thatsummer temperatures are lower (< 22 °C), andwinters are also colder. Average annual precip-itation level is between 400 and 800 mm peryear. Vegetation includes the Canary pine andlaurel forests. These isoclimatic areas are

arranged roughly in concentric circles on theisland: the coast (except for the north) is DD;inside this, the isoclimatic zone is DS. The nextzone is TM, and in the centre of the island is theTC zone. Despite small geographic distances,considerable variations between isoclimatic zonesare observed. Several factors such as the Tradewinds or the altitude could be responsible forthose differences.

The total sample (/1 = 151 ) was calculatedtaking into account the Grand Canary Island goatcensus of 1986, where the goats were distributed

among the different isoclimatic areas as follows:

dry-desert (DD) 58%; dry-steppe (DS) 23%; tem-perate-mild (TM) 13%; temperate-cold (TC) 7%.

The number and percentage of investigatedanimals from each isoclimatic zone was 78

(51.6°Io) in DD, 38 (25.2°Io) in DS, 28 (18.5%) inTM and 7 (4.6%) in TC. When necessary, as forexample in the case of the multivariate analysis,the data were grouped to reflect the districts fromwhich the animals were drawn. The distributionof goats according to district and isoclimaticareas is shown in table I.

Recovery and identification of abomasalnematodes

The abomasum contents of the 15 I investigatedanimals were examined using the methods rec-ommended in the Manual of Veterinary Para-sitological Laboratory Techniques (1989).Briefly, the abomasum was ligated and removedfrom the animals. This was cut open and thestomach wall was washed with tap water. Thewash water was collected and made up to a vol-ume of 2 000 mL through the addition of waterand sufficient formalin to give a final concen-tration of 5%. The mixture was agitated and two40 mL samples were removed. Each sample (40mL) was examined and the worms counted usinga dissecting microscope. The total number ofworms counted in both samples were multipliedby 25 to give the number of worms in each abo-masum. The observed males were cleared in lac-

tophenol and identified, and the percentage ofeach species was calculated.

Statistical analysis

Statistical comparison of prevalence and wormburden (overall and per species) between cli-matic zones, and comparisons between goat pop-ulation and sample distribution were performedusing the Pearson homogeneity test (Snedecorand Cochran, 1974).

The most frequent species were determinedusing a mean contrast test (Quesada et al, 1984).

Linear regressions were analysed for wormburden and prevalence, both overall and as afunction of isoclimates. For this latter purpose(linear regressions as a function of isocliiiiates),a numerical value was given to each isoclimatic

zone as follows: DD=1: DS=2: TM=3: TC=4.There were clear relationships between each iso-climatic zone, their geographic distribution onthe island, their altitude above sea level and theiraverage annual precipitation. In our opinion,these relationships made it possible to determinewhether or not there was a proportional increaseor decrease in the prevalence (!70 of parasitizedhosts), frequency (°!n of goats harbouring a nema-tode species) or intensity of abomasal nematodesas one moved from coastal areas (DD) to thecentre of the island (TC) using the proposedmethodology.

A principal component analysis (PCA)(Batista-Foguet and Martinez Arias, 1989) wasperformed on the intensity (actual number ofworms) and frequency (percentage of eachspecies in one abomasum) data to study the inter-specific associations. In order to ensure a greaternumber of observations (rows in the matrix), theresults were classified according to districts ratherthan isoclimatic zones. The variables (columns inthe matrix) were the five nematode species

observed (T trititrmta was considered as a dif-ferent species). Two additional active variableswere incorporated into the intensity analysis asboundary values: the maximum and minimumworm burden.

Data for both studies (frequency and inten-sity) were previously standardized as follows:(-vi X)/(5. (xi = actual value; x = mean value: (5=standard deviation). Only three axes were used inPCA as the percentage of accumulated varianceon three axes was 89% for frequency data and84’’% for intensity data. Mean Euclidean distances(<7) were then calculated in the principal compo-nent space for each district. Further informationwas also gained by calculating the following dis-tances: D2 (for each pair of parasites, the averageof the l2 d values calculated from the results ofthe 12 districts) and D4 (mean distance betweenone species and the other four for the 12 dis-tricts). Distances d, D2 and D4 varied from 0 to2. Values of I or lower were considered posi-tive associations, and values higher than I wereconsidered as negative associations as described

by Hoste and Cabaret (1992). The calculationswere performed using SAS mathematical soft-ware (Statistical Analysis System Institute, 1989).

RESULTS

The prevalence rate of abomasal nematodesamong the goats was 56%, with a maximumburden of 6 278 worms/animal and an arith-metic mean burden of 691 worms/animal.The results for each of the four isoclimaticzones studied is shown in figure 1. Preva-

lences were very similar for all areas below800 m: DD (56.8%), DS (48.5%) and TM(50%); the worm burdens showed a decreasefrom the coastal areas (DD) to the TM zone:DD (710 worms/goat), DS (683 worms/goat) and TM (496 worms/goat). Animals inthe coldest zone (TC) displayed the lowest

worm burden (407 worms/goat) but thehighest prevalence (83.3%). The differencesbetween the four zones analysed, in terms ofprevalence and worm burden were not foundto be statistically significant by the Pearsonhomogeneity test (x2 = 2.04; P = 0.56).

Figure 2 shows the frequency of abo-masal nematodes for each of the climaticzones studied. Five species were recoveredin total. T circumcincta was the most com-mon (65.8%). T axei infection was recordedin 51.9°70 of cases. The mean contrast testshowed that both species together accountedfor the majority of the abomasal worm bur-den of infected animals (P = 0.01 1). Theother nematode species were recovered con-siderably less frequently: H contortu.s wasfound in 15.2°!0 of positive animals, T tri-furcata (although T trif’urcata is a subspecies

of T circumcincta, they were considered asdifferent species to compare with previousstudies) in 8.8% and C mentlilatus in 3.8%.With regards to the isoclimatic zones (fig2), some species were not recorded in certainzones (H coiitoritis in DD and TC, T trifur-cata in TC, C mentulatus in DS, TM andTC). In the isoclimatic zones where thesespecies were observed, statistical compari-son of their frequencies revealed no signif-icant differences (H contortu.s: x’-= 0.23, P= 0.62; T tr(furcata X2 = 1.84, P = 0.39).

The percentage of goats harbouring eachof the two most common species (T cir-cumcincta and T uxei) differed significantlyfor each of the four climatic zones (T cir-cumcincta: xz = 31.67, P = 6.12 2 x t0-! Taxei: X2 = 8.74, P = 0.03). The percentage ofanimals harbouring T circumcinctcs tended to

decrease from dry to temperate zones, whilethe percentage of animals harbouring T axeitended to increase. These tendencies wereobserved for the T axei frequency when alinear regression was performed (P = 0.02;R2 = 0.96).

The intensity of each species (fig 3) fol-lowed a similar pattern to the species fre-quency: the most common parasite species(T cÎrCUl11cÎllcta and T axei) presented higherworm counts (729 and 534 worms/goat,respectively) than the less frequent species(H contortu,s, 326 worms/goat; C mentula-Ius, 270 worms/goat; T tri/Úrcala, 196worms/goat).

Principal component analysis (PCA),based on the frequency and intensity datawas used to study the interspecific associa-tions.

Figure 4 shows the behaviour of distancesbetween each abomasal nematode speciesand the four other parasites (D4) for bothanalyses (frequency data (a) and intensitydata (b)). The observed values for C men-tulatus were 0.78 for frequency data and0.89 for intensity data. The observed D4showed a tendency to positive association,although in some particular cases competi-tion between C mentulatus and the otherabomasal nematodes have been observed

(in the district of Las Palmas de GranCanaria, C mentulatus showed a D4 value of1.88 ± 0.07 and 1.8 ± 0.13 for the frequencyand intensity data respectively) but suchnegative association was not the generaltrend. A very low coefficient of variation

(CV) for C mentulatus D4 and reduced dif-ferences between the maximal and minimal

values of D4 between observed species werealso noted.

Figure 5 represents the D2 distances foreach pair of species according with PCA,which supplemented and confirmed theinformation obtained in the previous analy-sis (D4). The study carried out on frequencydata (fig Sb) showed that C mentulatus wasoften opposed to the other species (three ofthe first four pairs in the figure include thisspecies), but the mean D2 values werealways lower than 1. Higher distances wereobserved when C mentulatus was comparedwith T trifurcata and H contortus.

The results obtained from the intensitydata (fig 5a) showed D2 distances for Cmentulatus lower than 0.8. All the pairswhich included C mentulatus had very sim-

ilar D2 values, but high distances were alsoobserved with H contortus and T tr!fiir(,-at(i.

T circumcincta also showed the high pos-itive associations (the lowest d values), par-ticularly with T axei (both nematodes werethe most frequently observed species) forfrequency data, and with T trifurcata forintensity data.

DISCUSSION

The overall results indicated that the preva-lence of abomasal nematodes in Grand

Canary Island goats reached an intermediatevalue between those observed in neigh-bouring countries such as Mauritania andSenegal. These tended to vary dependingon the season from between 20-30% to

almost 100°!0 of the investigated animals(Jacquiet et al, 1995; Ndao et al, 1995). Thesamples in the present study were collectedduring the wettest season which undoubt-edly favoured the presence of adult worms(Chiejina et a], 1988; Ndao et al, 1995).

A wider variety of species was identifiedin our study than in the other studies fromthe above mentioned countries (Jacquiet etal, I995; Ndao et al, 1995). Species diversityin the present study resembled more closelythe diversity reported in sheep from

Morocco (Pandey et at, 1980) or in goatsfrom the Iberian Peninsula (Garcia-Romeroet at, 1995), perhaps because most of thegoat imports were originally from the Span-ish mainland.

T circumcincta and T axei were the onlyspecies observed in all four climatic zonesstudied, suggesting a greater degree of thesespecies adaptability to local conditions. Theywere also the only species whose prevalencediffered statistically from one isoclimate toanother. The prevalence of T axei wasclosely related to climatic factors, increasinggradually from the coast to the central areaof the island, where the rainfall is greatest.The reverse trend was noted for T circum-cincta.

With regards to the less frequentlyobserved species (some of which wereabsent in certain zones), H contnrtus wasdetected in zones characterized by relativelyhigh humidity and temperature, and by fairlyconstant temperatures throughout the year.

The distribution of T tr!furcata was sim-ilar to that of T circul11cincta, although itwas not observed in the highest areas of theisland. The different frequencies observedfor both nematodes agreed with the obser-vations of Cabaret et at (1986) concerningnematode communities in sheep fromFrance and Morocco, where T trifurc-atawas also much less prevalent than T cir-cumcincta. These authors suggested that Ttrifurcata could have been less abundantbecause of poorer resistence to environ-mental factors or to host defences.

One of the most striking observations inthis study was the presence of C mentulatus,a species typically associated with camelidaeand not hitherto reported in Canarian goats(Cordero del Campillo et al, 1994; Gomez-Calcerrada, 1996). Under experimental con-ditions, the transmissibility of C meiittila-tus to small ruminants seems to be high(Thornton et ai, 1973; Gevrey, 1989). It

could explain why in some countries withlarge camelidae populations, such as Saudi

Arabia or Iraq, C meutulutus is frequentlyobserved in both sheep and goats (Alani andYahay, 1993; EI-Azazy, 1995). This parasitehas also been observed in sheep fromMorocco, but with a lower frequency than inthe aforementioned countries (Pandey et al,1980). Contrary to these observations, inthe neighbouring countries of Mauritaniaand Senegal, where there is also a camelidaepopulation, or on the other islands of theCanarian Archipelago (G6mez-Calcerrada,1996), this nematode is not detected in smallruminants.

Regarding the PCA analysis which wasperformed to study the interspecific associ-ations of abomasal nematodes, in particu-lar for C mentulatus, this study showed thatthree components were sufficient to reflectthe behaviour of the nematode community,with a high accumulated percentage of vari-ance (intensity = 84°l0; frequency = 89%).Neither generic distances (D2; fig 5) norinterspecific distances (D4; fig 4) yieldedvalues greater than I (see Materials andmethods section), indicating a positive asso-ciation in all cases for intensity and fre-quency data. Similar studies by Hoste andCabaret (1992) on gastrointestinal nema-todes and by Diez-Banos et al (1992) onabomasal nematodes in sheep have alsoreported that most of the interspecific asso-ciations observed were not antagonistic. Onrare occasions, these studies noted slightnegative interactions, involving T circum-cincta. In the present study, T circumcincta,in fact, showed the greatest positive inter-action with other species. In the above men-tioned studies, as in the present survey, theresults suggested that parasite populationsare characterized by both a fair degree ofhomogeneity and stability. Low CV valuesand reduced differences between the maxi-mal and minimal distances betweenobserved species (figs 4 and 5) bear out thisconclusion. The stability recorded undernatural conditions has been accounted for, inthe case of ovine gastrointestinal nematodes,by host population factors which tend to

promote positive interactions, thus enhanc-ing the stability of the system (Hoste andCabaret, 1992).

The mean Euclidean distances obtainedfor C mentulatus were always lower than 1,so C mentulatus would show the same gen-eral tendency to a positive association whichwas observed for the other abomasal nema-todes. In the same way, these results con-tribute to the above theory, which states thatunder natural conditions a parasite commu-nity tends towards stability, despite the pres-ence of an uncommon species such as Cmentulatu.s in that community. Althoughthis species showed a general tendency topositive associations, in some cases (ie,when the d values from a particular districtwere considered), the observed resultsshowed a slight negative association (meanEuclidians distances higher than 1 ) betweenthis nematode and others. Although furtherinvestigations would be necessary to explainthis phenomenon, other factors such as man-agement, farm history, etc, could beinvolved in these cases affecting the expres-sion of interspecific association (Cabaretand Gasnier, 1994).

ACKNOWLEDGMENTS

The authors would like to express their appreci-ation to Dr Gonzdlez-Diaz of the ChemistryDepartment of Las Palmas de Gran Canaria Uni-versity, who kindly helped us to define the sta-tistical models utilized.

REFERENCES

Alani AJ, Yahay HQ ( 1993) Observations on the epi-demiology of intestinal helminths in sheep in Nin-crah Province (Iraq). lntJAnim Sci 8, 51-55

Batista Foguet JM, Martinez Arias MR ( 1989) Anali-sis Multivariante. Anblisi,s en Componenies Prin-ci!a/e.B’. Coleeci6n ESADE. (Hispano Europea, SAed), Barcelona, Spain, 10-150

Cabaret J, Morales G, Durette-Desset MC (1986) Car-act6risation de Teladorsagia circwncinctu et T tri-

furcata. II. Aspects morphologiques. Ann Para-sitol Hum Comp 61, 55-64

Cabaret J, Gasnier N ( 1994) Farm history and breedingmanagement influences on the intensity and spe-cific diversity of nematode infection of dairy goats.Vet Parasitol 53, 219-232

Chiejina SN, Fakae BB, Eze BO ( 1988) Arrested devel-opment of gastrointestinal trichostrongylids in goatsin Nigeria. Vet PcarasitoL 28, 103-I 13 3

Cordero del Campillo M, Castanon L, Reguera A( 1994) Indice-Catklogo de zooparásitos ibéricos.2nd ed, Secretariado de Publicaciones, Universi-dad de Le6n, Spain, 201-285

Diez-Bafio; N, Cabaret J, Diez-Banos P ( 1992) Inter-specific interactions in naturally acquired nema-tode communities from sheep abomasum in relationto age of host and season in four areas of Le6n,Spain. IntJ J Parasitol22, 327-334

El-Azazy OME (1995) Seasonal changes and inhib-ited development of the abomasal nematodes ofsheep and goats in Saudi Arabia. Vet Pirasitol 58,91- 98

Garcia Romero C, Miro G, Meana A, Valcarcel F,(1995) Contribucion al mapa parasitol6gico deCastilla-La Mancha: especies de nematodos gas-trointestinales en el ganado caprino. Abstracts ofIV Congreso Iberica de Parasitologia, Santiago deCompostela, Spain, 102

Gevrey J (1989) Lamas et moutons : observationd’intertransmissibilité helminthique. Bull Sac FrPartisitol 7, 245-249

Gomcz-Calcerrada Lopez V (1996) Mapa para-sitologico del ganado caprino en el archipielagoeanario. O Medico Veterinario 47, 29-36

Hostc H, Cabaret J (1992) Intergeneric relationsbetween nematodes of the digestive tract in lambs:a multivariate approach. Ini J Parasitol 22, 173-179

Jacquiet P, Colas F, Cabaret J, Dia ML, Cheikh D,Thiam A (1995) Dry areas: an example of seasonalevolution of helminth infection of sheep and goatsin southern Mauritania. VetParasitol56, 137-148.

Manual af V(,ttritian, Yarn,ritological Liborator!, Tech-niques (1989) Ministry of Agriculture, Fisheriesand Food, London, UK

Ndao M, Belot J, Zinsstag, J, Pfister K ( 1995) !pid6mi-ologic des helminthoses gastro-intestinales despetits ruminants dans la zone sylvo-pastorale auS6n6gal. Vet Res 26, 132-139

Pandcy VS, Cabaret J, Ouhelli H, Dakkak A (1980)Etude des n6inatodes parasites du tube digestif desovins adultes dans deux regions du Maroc. Bull O(1’Int Epizoot 92. 1345-1349

Quesada V, Isidoro A, L<ipez LA (1984) Ctirvo y FJer-c-ic-ios de Estadística. Alhambra cd, Madrid, Spain,336-359

Rodriguez-Ponce E, Molina JM, Hernandez S, (1995)Seroprevalence of goat toxoplasmosis on GrandCanary Island, Spain. Prev Vet Med 24, 229- 234

Snedecor GW, Cochran WG (1974) In: MétodosEstadísticos. Continental Editorial Co, Mexico DC,703

Statistical Analysis System (SAS) Institute Ine ( 1989)Users guide. Cary, NC, USA

Thornton JE, Galvin TJ, Bell RR, Ramsey CW (1973)Transmissibility of gastrointestinal nematodes fromblackbuck antelope to cattle, sheep and goats. J AmVet Med Assoc 163, 554-555

Vercruysse J, Taraschewski H, Voigt WP (1988) Par-asitic diseases of the alimentary system. In: Para-sitology in Focus. Facts and Trends. Melhorn Hed, Springer-Verlag, Berlin, Germany, 481-494