Seasonal evolution of faecal egg output by gastrointestinal worms in goats on communal farms in eastern Namibia

KUMBA, F.F., KATJIVENA, H., KAUTA, G. & LUTAAYA, E. 2003. Seasonal evolution of faecal egg output by gastrointestinal wotmS in goats on communal farms in eastern Namibia. Onderstepoort Journal of Veterinaty Research, 70:265-271 As a more detailed continuation 01 a previous sludy, faecal samples for worm egg counts were col· lected per rectum from ten marlted adult animals in selected ftocks of goats. In each 01 six villages evenly spread out in the communal farming district of Okakarara in eastern Namibia. The study was conducted on a monthly basis from August 1999 to July 2000. Average faecal worm egg counts (FECs) were highest during lhe warm-wet season, much lower during the coId-dry months and mod· erate during the hot-dry season. Least square means 01 FECs were 2140. 430 and 653 per gram of faeces for the three seasons, respectively. Seasonal variation in egg counts was significant (P < 0.(001). Gastrointestinal strongyles, and to a lesser extent Strongyloides species, were the predominant parasite groups identified in goats. Kidding rates peaked in the cold-dry season and mor· tality rates in the hot-dry season. Results 01 this study suggest that gastrointestinal parasitism may be a problem that accentuates the effect of poor nutrition on small ruminants during the season of food shortages in the east of Namibia and lhal the use of FECs per sa to assess the severity of gastrointestinal parasitic infection in goalslollowed by chemoprophylactic strategic aod/or tactical treat· ment, may not be the best approach to addressing the WOfTTl problem under resource·poor condi· lions. The use of the FAMACHAO system lhatldenlilies severely affected animals for treatment is technlcaltya better option for communal farmers. KeYWOfda: Faecal egg counts, FAMACHAO system, gastrointestinal nematodes, goats, seasonal occurrence


INTRODUCTION
Infection by gastrointestinal parasites is one of the most serious problems affecting small ruminant populations worldwide (Pugh, Hilton & Mobini 1998;Waller 1999).In many parts of Africa heavy worm burdens have often been demonstrated in small ruminants (Connor, Munyuku, Mackyao & Halliwell 1990;Huart, Dungu, Matatu & Schandevyl 1993;Ndao, Belot, Zinsstag & Pfister 1995;Vassilev 1995;Kusiluka, Kambarage, Harrison, Daborn & Matthewman 1998;Ameh, Egwu & Tijjani 2000).Goats are an important source of livelihood for smallholder farmers in southern Africa (Donkin & Boyazoglu 2000) but appear especially vulnerable to the negative effects of gastrointestinal parasitism (Pomroy 1985;Radostitis, Blood & Gay 1994).Tactical and strategic prophylactic treatments of flocks with anthelmintic preparations are measures recommended by parasitologists for the control of gastrointestinal parasites (Biggs & Anthonissen 1982;Radostits et al. 1994;Vassilev 1995;Garcia-Perez, Hurtado, Oregui & Juste 2002).For instance in the Basque country in Spain, two tactical annual treatments based on the physiological status of the animal and season have recently been recommended in dairy sheep (Garcia-Perez et al. 2002).Frequent tactical and strategic treatment is blamed for the emergence, in recent years, of rapid development of anthelmintic resistance to nearly all available drugs, posing serious threats to the small ruminant industry (Barton 1983;Rowlands, 1993;Boersema & Pandey 1997;Van Wyk, Bath & Malan 1998;Van Wyk, Stenson, Van der Merwe, Vorster & Viljoen 1999;Van Wyk 2001).In southern Africa, most smallholder farmers in communal grazing areas are resource-poor, hence are often unable to pay for veterinary services including recommended tactical or strategic anthelmintic treatments.In Namibia, faecal egg count (FEC) is still the main technique used to determine the severity of gastrointestinal parasitic infection in livestock.Output of eggs by intestinal worms is known to fluctuate depending on various factors including the physiological status of the host animal (Pandey, Ndao & Kumar 1994;Nuvor, Assoku & Agyei 1997) and seasonal changes in local environmental conditions (Mukaratirwa, Hove & Kyvsgaard 1997;Arosemena, Bevilaqua, Melo & Girao 1999) besides, FEC is a highly specialized technique.The aim of this study was to determine the evolution of the parasitic burden in goats in the eastern communal area of Namibia and to recommend sustainable worm control protocols that are affordable and manageable by communal farmers themselves to estimate and combat parasitic infection in small ruminants.It is a continuation of a previous study of the same nature in the same area (Kumba, Undi, Katjivena, Kauta, Hengua & Tjiteere 2000).

The study area
This study was carried out in the district of Okakarara (20°0'-21°4' S; 17°30'-18°25' E, altitude 1 050 m), which forms part of the vast eastern communal agricultural area of Namibia.The area is semi-arid with an erratic annual rainfall of 250-550 mm that is usually almost totally confined to the warm-wet season (January to April), although in the year of study, rainfall pattern deviated considerably from the usual norm.The mean minimum tempera-ture is low (6 °C) during May to September, the cold-dry season.By contrast the mean maximum temperature is high (31 °C) during October to December, the hot-dry season.
Okakarara district is sparsely populated, with most villages composed of just a few families.Cattle, goat and sheep farming constitute the main subsistence activity for the communal farmers but goats are the predominant species owned by the poorest farmers.All animals, especially small ruminants, in a particular village are exposed to the same environmental conditions because the same grazing land is communally utilized all year round.Significant demographic increases in recent years demanded that livestock numbers are increased to meet the nutritional needs of the rapidly increasing population in the eastern communal area.As a result, tremendous pressure is exerted on the limited grazing resource leading to overgrazing and seasonal shortages of animal feed, particularly during the hot-dry season.Frequent droughts have only added to the difficulty.The meteorological data for rainfall (1986)(1987)(1988)(1989)(1990)(1991)(1992)(1993)(1994)(1995)(1996)(1997)(1998)(1999)(2000) and temperature (1999/2000) used in this study were obtained from a station in the neighbouring Omaruru communal farming district.

Animals
Six villages (Okatuhoro, Okanjokomukona, Omatupa, Oruvize, Otjimati and Otjiyere) were selected by virtue of their proximity to six points evenly marked on the district map.Herds of goats belonging to a randomly selected household in each village were used for the one-year study period.Households were selected from a list available at the district agricultural extension office at Okakarara but were included in the investigation if they were willing to participate, and had goat flocks that had not received any anthelmintic treatment within 12 months prior to commencement of the study.Selected farmers agreed not to deworm the goats or to dispose of any marked animal for the duration of the study.In total, selected households owned 425 adult goats at the beginning of the study, with between 12-96 goats per household.Of these 299 animals (70 %) were females and 126 animals (30 %) were males.Most flocks consisted of indigenous goat breeds or crosses of indigenous animals and Boer goats.For this study, ten adult animals, both males and females, randomly selected by the researchers within each flock, were earmarked by notching the left ear.No attempt was made to balance selected animals as regards to sex nor to distinguish if selected males were intact or castrated.
Experimental animals were herded during the day and housed at night in unroofed kraals together with the rest of the flock, separate from other domestic species.In all goat flocks from which animals were selected for study, the owners agreed to keep record of newborn animals and animals that died due to disease or non-identified causes, such as loss in the veld.Seven experimental animals that died during the study were promptly replaced with animals randomly selected within the same flock.

Parasitological analysis
During the first week of each month, between August 1999 and July 2000, three faecal pellets (about 2-3 g) were collected, from the rectum of each experimental animal as described by Reinecke (1983).Faecal samples were pooled per flock in plastic bags, stored on ice in cold boxes and dispatched to the laboratory for composite FECs by the modified McMaster technique (Reinecke 1983).The collection of faecal samples in the field lasted for three days each month and sample analysis was completed within a week after delivery of samples to the laboratory.Samples were stored at 4 °C pending coprological analysis in the laboratory.Morphological features of parasite eggs were used to identify groups of parasites (Reinecke 1983;Urquhart, Armour, Duncan, Dunn & Jennings 1996).

Statistical analysis
The data on average FECs was analyzed by the SAS GLM procedure (Anon. 1996).The model included influence of season (January to April = 1, May to September = 2, October to December = 3) and village, where the latter was used as a blocking factor.In randomized complete block designs it is assumed that there is no interaction between treatments and blocks (Lentner & Bishop 1993).However, in this study, samples were collected monthly from the same flock over any given season, hence constituting sub-samples.Thus a season x village interaction was included in the model and was used to test the significance of the main effect (season).
Residual analysis indicated one outlying observation, which was dropped in subsequent analyses because the farmer in question may have predisposed his goats to greater risks of parasitic infection in a marshy area, in the search for pasture.The residual analysis also indicated a non-constant variance.Data was thus transformed using natural logarithms and this resulted in a better-fitting model.Least square means were tested for significance using the t-test, then back-transformed.

RESULTS
Average FECs in goats varied from one village to another, and from month to month in the same village (Table 1).The FECs followed a three-pronged trend, being highest in January, February, March and April (the warm-wet season) in most villages, much lower in May to September (the cold-dry season), and intermediate for October to December (the hot-dry months) (Fig. 1).As indicated in Fig. 2, the rainfall during the period of study was much greater than usual, with some unusually high downpours particularly in December.It is interesting to note the similarity in the pattern between rainfall and faecal egg output (Fig. 2 and 3).Strongyles 267 F.F. KUMBA et al. and to a lesser extent Strongyloides predominated during all seasons in all experimental flocks (Fig. 3).Other parasite eggs seen in one farm were those of ascarids.No trematode eggs were found, probably because of the unfavourable environment in the east of Namibia for the proliferation of their molluscan intermediate hosts.The apparent absence of cestode eggs might be an indication that the flotation method used at the Grootfontein veterinary laboratory is not suitable for detection of cestode eggs.
Kidding peaked in June and declined gradually thereafter towards the end of the hot-dry season in December (Table 2).No newborn kids were reported during February-April.Table 2 also shows that mortalities occurred mostly among kids and > 80 % of mortalities occurred in the cold-dry and hot-dry seasons (September to December), with almost no deaths occurring in the warm-wet season.Farmers were of the opinion that morbidity was lowest in the warm-wet season and relatively high in the other seasons, especially during the hot-dry months, and that the predominant clinical manifestations encountered were due to gastrointestinal helminth infection and intoxications attributed to plant poisoning.They described gastrointestinal parasitism as mainly sporadic conditions characterized by general poor body condition, emaciation and/or diarrhoea, often affecting few animals in flocks.
Note that rainfall during period of study was higher than usual especially in December 1999 in this study) in the communal area administered anthelmintic preparations to the more severely affected animals in their flocks.
Analysis of variance showed highly significant differences (P < 0.0001) in seasonal average FECs.An unusually high FEC was recorded in the flock at Oruvize during November (Table 1), probably because farmers in this village moved their animals to a neighbouring marshy area in search of better grazing.This abnormal record was excluded from the statistical analyses.Least square means of average FEC across all flocks were 2 140, 430 and 653 for seasons 1, 2 and 3 respectively, and were significantly different (P < 0.05).

DISCUSSION AND CONCLUSIONS
In this study the evolution of monthly FECs followed the well-known pattern influenced primarily by temperature and moisture (Biggs & Anthonissen 1982;Radostits et al. 1994;Urquhart et al. 1996;Arosemena et al. 1999) as they were highest in the wet season (which is warm), moderate in the hot-dry season and lowest in the cold-dry season.It seems unlikely that the phenomenon of peri-parturient rise (Nuvor et al. 1997) could have played a role since the FECs were at their lowest levels when most kidding occurred.On the other hand, it is possible that the so-called spring rise in FEC [from maturation of hypobiotic L 4 larvae (Blitz & Gibbs 1972)] may have been responsible for the observed rise in FECs before the rains came at the beginning of the warm-wet season.Another possibility is the early rains at some villages that may have had an influence.In the village of Oruvize very high average FECs were recorded during November when the animals were grazed on marshy land (Table 1), probably due to the ample moisture that was available.
Many authors have reported Haemonchus spp. as of paramount importance in small ruminants in many parts of southern Africa, including Namibia (Biggs & Anthonissen 1982;Pandey et al. 1994;Vassilev 1995;Vatta,   in the east of Namibia, or else the animals have been selected naturally for the ability to withstand worms, or both.
Over the past few decades it has become conventional for helminthologists to base worm management strategy largely on use of chemicals in such a way that worms are practically excluded as a factor in animal production.However, they lost sight of the fact that methods such as strategic drenching at a time when there are few worms in refugia, or drenching animals before they are moved to uninfected, or lightly infected pasture, strongly select for drug resistance.Furthermore, such methods require routine drenching of all the animals in the flock or herd, and/or facilities such as a variety of separate paddocks-approaches that require resources unavailable to most if not all communal farmers.
Fortunately, because worms are grossly over-dispersed in any given host population (Barger 1985), only a small minority of animals is badly affected in most outbreaks of worm infection.Therefore, a practical approach is to treat only the stragglers that are unable to withstand heavy worm challenge unaided.Faecal worm egg counts are impractical because all individuals need to be tested to identify the few that are heavily infected, and this facility is seldom readily available to all resource-poor farming communities.However, recently Malan & Van Wyk (1992), Van Wyk, Malan & Bath (1997) and Malan, Van Wyk & Wessels (2001) developed and refined the FAMACHA© system whereby haemonchosis is evaluated clinically according to the colour of the ocular mucous membrane, which varies from nearly red in the healthy animals to practically white in those that are terminally anaemic.The system was particularly thoroughly tested in sheep (Van Wyk & Bath 2002), but also in goats of resourcepoor farmers (Vatta et al. 2001(Vatta et al. , 2002)).Very importantly, it was found that even poorly literate persons are able to apply the FAMACHA© system to good effect.
In conclusion, therefore, it is recommended that the FAMACHA© system is introduced through proper training to the resource-poor farmers of eastern Namibia.It is easy to apply and enables the farmer with very small financial outlay to salvage animals badly affected by haemonchosis and possibly other haematophagus gastrointestinal parasites.The system appears to fit in well with traditional African approach to deal with disease in animals, by treating only the individuals that are obviously affected.
In the process both costs and selection for anthelmintic resistance are greatly reduced.

FIG. 1 FIG. 2
FIG. 1 Average seasonal FECs per gram of faecal sample from goats in six selected villages in Okakarara district, eastern Namibia (August 1999 to July 2000)

TABLE 1
Monthly average FECs per gram of faecal sample from goats in six selected villages in Okakarara district, eastern Namibia (August 1999 to July 2000).Note the very high egg count recorded at Oruvize in November.This was excluded from subsequent analyses FIG. 3 Average monthly FECs per gram of faecal sample from goats in six villages in Okakarara district, eastern Namibia (August 1999 to July 2000).Note that low FECs were recorded in May through September, the cold-dry season.It is obvious that Strongyles were the main parasite group found in goats in the area

TABLE 2
The number of kids born as well as mortalities among young and adult goats due to disease and non-specific causes in all goat-flocks in which animals were selected for study during 1999-2000 in six villages in Okakarara district