TICKS AND TICKBORNE HAEMOPARASITES OF SHEEP AND GOATS
Seasonal distribution in Mozambique

• R.M. Arnold and J.A. Travassos Santos Dias

Savannah of Acacia spp. - Movene Station

• Dr Arnold was a member of the FAO/MONAP Project, “Strengthening the Veterinary Institute, Mozambique” (MONAP LI-13). His present address is: Piedra del Sol, San Diego, Torreguadiaro, La Línea, Cádiz, Spain. Dr Travassos Santos Dias was Professor of Parasitology and Parasitic Diseases of the Faculty of Veterinary Medicine, University Eduardo Mondlane, Maputo, Mozambique, and now lives at Quinta da Galiza, Lote 23, 5°D, 2765, S. Joao do Estoril, Portugal. Support of the work by the Director of the Veterinary Research Institute (INIVE) and the staff of the Section of Parasitology is gratefully acknowledged.

In many areas in Africa, tickborne diseases including heartwater (Cowdria ruminantium infection) cause a high rate of mortality and loss in cattle, sheep and goats.

Of the various tick species present in Mozambique, Amblyomma hebraeum, the vector of heartwater, was found to be of the greatest significance in sheep and goats. The work described in this article is therefore of considerable interest since it indicates the practical measures which can be taken in the case of these animals to reduce the incidence of heartwater and other tickborne diseases and to minimize losses arising directly from tick infestation. The effectiveness of foot-baths in this respect is of particular interest.

Although the ticks infesting animals in Mozambique have been catalogued by Travassos Dias (1952, 1954, 1960), there have been no detailed studies of their bionomics throughout the years and, apart from a graph giving a schematic seasonal distribution of five species in cattle, no publications on the subject are known to the authors.

Elsewhere in East Africa, such studies have been made in Tanzania (Yeoman, 1966, 1967), (McCulloch et al., 1968) and in Kenya (Barnett and Bailey, 1951 and Newsom, 1975), but these were directed mainly at Rhipicephalus appendiculatus with a view to elucidating the epidemiology of East Coast Fever.

The present studies were undertaken on sheep and goats during 1978 and 1979 at the “Centre for Small Ruminant Production” in Movene, Maputo Province, Mozambique. The work was initiated to determine the importance of ticks in the causation of foot abscesses (which had often led to generalized infections, permanent lameness and death of animals), and in the transmission of heartwater, a serious cause of mortality.

At the beginning of 1978, there were approximately 300 sheep and 600 goats at the Centre. The main herd was dipped from time to time, with the exception of the test group. The animals were housed at night in a variety of adapted buildings and grazed extensively over areas of planted grass, regenerating scrub-land and riverine bush - formerly an extensively managed dairy farm. The Centre itself is situated along the Movene River, a tributary of the Umbeluzi River, in a semi-arid region where rainfall rarely exceeds 800 mm per annum.

The Movene River is a seasonal stream with pools in the dry season and supports a scanty riverine gallery forest composed mostly of Ficus sycomorus, Mimusops caffra, Afzelia guanzensis, Breonadia microcephala, Phoe- nix reclinata, Diospyros mespiliformia, Spirotachys africana, etc. Away from the river, there were extensive areas which had been partly cleared and where regeneration was taking place with xerophytic vegetation of the savannah type such as Sclerocarya caffra, Peltophorum africanum and Lannea discolor, Acacia nigrescens, A. xantrophloea, Acacia spp., Dichrostachys cinerea and Combretum spp., these being the predominant tree species. This process had advanced to the exclusion of most grasses. There were also some areas of established grassland planted with Panicum maximum, Themeda trianda and Urochloa mocambicensis. Soils were red-brown, self-mulching of average fertility, except along the river banks where fertility is higher.

The gallery vegetation of the Movene River: Acacia xanthophloea, Ficus sycomorus, Mimusops caffra etc.

Bushland of Acacia spp., Sclerocarya caffra etc.

During early 1977 the animals were brought together from a number of farms in the Province of Maputo and Gaza where they had been kept under very varied conditions of management (particularly with regard to tick-control) and nutrition. They were of a variety of breeds but Landim and Black Head Persian crossbred sheep and Landim and Boer goats predominated. These same animals, by means of weekly faecal sampling, were also used to study the seasonal incidence of helminth parasites; the results of which were elaborated by Specht (1981). A selection of 20 sheep and 20 goats was originally made in January 1978 and samples taken from sheep and goats alternately every two weeks throughout 1978 and 1979. Blood slides were made, stained by Giemsa method, and parasites, found in approximately 3 000 erythrocytes (minimum 10 fields), were recorded. The slides were then scanned for trypanosomes. Complete tick collections were at first made from all animals but this proved to be too onerous and the number was reduced to ten and later to four head. Sometimes lack of time, unavailability of animals or bad light reduced numbers sampled.

Arnold and Travassos Santos Dias

Figure 1. Mean tick numbers collected from sheep and goats by months and species with meteorological data

Tick collections were as complete as circumstances would allow. Animals were examined on a table and ticks were removed, counted and dropped into 70 percent alcohol for later identification. Separate collections were made from the head, trunk (including peri-anal region) and feet. The light in the sheds was sometimes inadequate and it is probable that collections of larval stages, especially from the sheep, were at times incomplete.

Blood slides were made from ear blood and fixed with methyl-alcohol within three hours. From July 1978, capillary haematocrit tubes were used for blood sampling and the haematocrit recorded. The tubes were also scanned for trypanosomes.

Meterological data were initially derived from instruments set up at the Centre. However, it was found that the records being kept between visits were not reliable and so the meteorological data quoted were derived from the National Meteorological Service at Umbeluzi, 16 km away.

Results of the work

Tick populations. The number of ticks collected from sheep and goats is shown by species in Figures 1 and 2 together with rainfall. In each case, the figures represent the mean number present per animal.

• Rhipicephalus evertsi-evertsi: Neumann, 1897 (see Fig. 1)

Adults were found throughout the year, infesting sheep and goats in approximately equal numbers. There was a suggestion of a seasonal rise in numbers during the wet months of 1978–79 but this did not occur in 1977–78. Goats carried a heavier burden of immature stages than sheep and there were marked variations, apparently without pattern, in the numbers collected. Adults were found mostly on the trunk (around the anus and on the thin skin of the belly and groin) with immature forms found deep in the ears. This tick is the vector of Theileria ovis and T. separata both of which were observed in blood smears from the animals.

• Rhipicephalus appendiculatus: Neumann, 1901 (see Fig. 1)

This species showed a marked seasonal incidence in the wet months, the number of adults increasing rapidly in both sheep and goats during January-February and persisting in diminishing numbers until May-July. Sheep were preferred to goats as hosts for both adults and immature forms, the latter exhibiting a strong seasonal prevalence during May-September. This species was usually found on the head and ears.

• Other Rhipicephalus species

These included R. simus: Koch, 1844; R. neavei: Warburton, 1912; R. pravus: Donitz, 1910; R. sanguineus: Latreille, 1806; R. maculatus: Neumann, 1901 and R. lunulatus: Neumann, 1907, in order of prevalence. Numbers of each species were too few to enable conclusions to be drawn regarding their seasonal incidence.

• Amblyomma hebraeum: Koch, 1844 (see Fig. 2)

Figure 2. Mean tick numbers collected from sheep and goats by months and species with meteorological data

This was prevalent throughout the year, increasing slightly in the rainy months (September-November 1978, February-April and October-November 1979). Sheep were more attractive as hosts than goats. Immature forms were most numerous in May-August. The feet, body and genitalia were the common sites of attachment (especially larvae and nymphae), the head rarely being parasitized. It was shown that hoof abscesses due to Amblyomma bites could be effectively eliminated by twice-weekly foot baths using an organophosphorous acaricide.

• Boophilus decoloratus: Koch, 1844 (see Fig. 2)

This species was less prevalent than had been expected and showed a strong seasonal incidence of both immature and adult forms during the heavy and prolonged rainy season of October-December 1978. Both sheep and goats appeared equally attractive hosts. B. microplus: Canestrini, 1887, was identified on only two occasions but the actual number may have been greater, owing to the small total numbers of Boophilus found and the difficulty of distinguishing between the females of B. microplus and B. decoloratus when the mouth parts are damaged. B. microplus was the predominant boophilid tick found on cattle grazing the same area and the observation may indicate a real lack of suitability of sheep and goats as hosts for B. microplus.

• Hyalomma rufipes: Koch, 1844

This was the only other species of tick encountered, one adult female being collected from a sheep in February 1978.

Blood parasites identified

The results of the blood slide examinations for protozoa and rickettsia are given in Tables 1 (sheep) and 2 (goats). Mean numbers of up to ten infected cells per 10 000 are recorded as + and heavier parasitaemias as ++.

• Theileria ovis: Rhodain, 1916.

This was found in both sheep and goats throughout the year. Sheep were more often infected and had larger parasitaemias than goats. On one occasion, a particular sheep had 19 percent erythrocytes infected with T. ovis but no symptoms were noted at the time of sampling. T. separata: Uilenberg and Andersen, 1966, was detected in sheep during October-November and December 1978. It was again found in smears taken in October 1979-January 1980 although systematic counting had then been discontinued. Its presence in some cases appeared to be associated with fever. It was never seen in blood smears from goats.

• Anaplasma species

An anaplasma-like organism (probably A. ovis) was seen in blood smears from both sheep and goats in small numbers throughout the year.

No relationship could be seen between the presence of erythrocytes parasitized by either of these parasites and the environmental factors studied, including parasite burdens as expressed by worm egg counts (Specht, 1981).

• Trypanosomes

Trypanosomes were seen in blood smears from both sheep and goats throughout the trial period but there appeared to be no marked seasonal incidence. Both T. vivax: Ziemann, 1905, and T. congolense: Broden, 1904, were found, the latter predominating during 1979.

Significance of results

Amblyomma hebraeum stands out as being the tick species of greatest practical significance for sheep and goats in southern Mozambique. Its prevalence throughout the year means that control measures should be continuous.

The species is significant in two respects: as a vector of Cowdria ruminantium infection (heartwater) and as a cause of tick bites, which often become infected and result in abscesses. Unfortunately, no detailed statistics were kept of the incidence of abscesses but it is estimated that approximately one animal in five was affected during the winter of 1977, the proportion in young animals being even greater. Bites in the feet were most troublesome, causing lameness, loss of condition and, when infection spread, septicaemia, pneumonia and death. Secondary infection of bites caused abscesses on the ventral abdomen, axillae, groin or genitalia, sometimes leading to orchitis or to severe local inflammation and, especially in young animals, to generalized infections.

Landim and Boer goats on the savannah

Landim and Blackhead Persian sheep on the savannah

After a few months, following the demonstration of the importance of the feet as sites of attachment, the animals which were not being observed for ticks were walked through a shallow (15 cm) foot bath of acaricide twice a week. This resulted in good control of ticks on the feet and, to a lesser extent on the body. Complete eradication of Amblyomma was neither practicable nor desirable on the farm (unless widespread vaccination against heartwater were to be introduced), since the use of foot baths was sufficient to reduce the level of infestation and maintain a flock immunity against heartwater. This practice needs to be adopted for other sheep and goat flocks, unless dipping on a rigid schedule or vaccination can be guaranteed.

The other ticks, especially Rhipicephalus adults during January-March and immature forms in April-July, were only seasonally important in causing tick worry. Since these ticks constitute a real source of irritation and loss of condition, control by spraying or complete body immersion is necessary during these months. A practical recommendation would be to spray the head and neck of all sheep and goats every two weeks during April-July or whenever infestation was observed to be heavy.

The seasonal incidence of Boophilus spp. is of interest and justifies further studies of these species in the case of cattle. The observation that B. microplus, although more common than B. decoloratus on cattle on the same grazings does not freely parasitize small ruminants, also requires confirmation and further study. This apparent inability of B. microplus to attach or mature on sheep and goats might be exploited in areas of Mozam bique and elsewhere in the world where it is the dominant species. Grazings could then be selectively cleared of the tick.

Trypanosomiasis was common and by the end of the period all the animals had, at one time or another, shown parasites in blood smears. Since Trypanosoma congolense was the dominant species, this suggested cyclical transmission through tsetse flies but, in spite of three surveys in areas of the farm thought likely to provide habitats for Glossina austeni or G. brevipalpis, no adults or pupae of these files were found, but pupae of the latter and adult flies of the former were collected in the year following the conclusion of these studies.

Apart from the practical considerations above, it is of interest to consider the present seasonal incidence in relation to those described for Africa by other authors. Most of the field studies have concerned R. appendiculatus. Although Hoogstraal (1956) considered relative humidity to be the most important factor determining the distribution of Rhipicephalus species, Yeoman (1966) failed to find any correlation between infections of adult R. appendiculatus and either current or previous rainfall. It is probable, however, that as suggested by more recent investigations in Australia, Argentina and Kenya (Newsom, 1975), the micro-climate in which the eggs are deposited for the larvae to emerge determines the survival rate of most tick species. Although there is a big variation in tolerance of different tick species to desiccation, it is the period spent waiting for the first host which is the most critical in the life cycle of the tick.

The eggs and larvae of R. appenliculatus, for example, are more resistant than those of Boophilus microplus (a one-host tick of relatively humid environment). They are, however, considerably less resistant to adverse climatic conditions than their nymphal or adult stages, which have the capacity to remain in protected areas in soil or herbage until, with the rains, they emerge, ascend vegetation and await a host. In this way, Newsom (1975) explains the seasonal prevalence of adult R. appendiculatus and the far more even distribution of the larval forms throughout the year in Kenya.

Given this characteristic of R. appendiculatus, one could expect a tendency for “waves” of ticks to be triggered off by the rains and for a second generation of adults to result three to four months later, when the crop of eggs laid by these ticks came to maturity. There are some indications that this did occur in both years since a second rise in numbers of adult R. appendiculatus was observed in May of each year following the initial rise in January. A third wave which might theoretically have been expected in September was not observed.

In southern Mozambique, the numbers and seasonal variation in prevalence of R. evertsi-evertsi, both adult and immature forms, were far greater than those recorded in Kenya by Newsom (1975).

No great differences were observed in the present study between the numbers of R. appendiculatus found on sheep and goats, although both Yeoman (1966) in Tanganyika and Barnett and Bailey (1955) in Kenya found sheep to be less popular hosts of R. appendiculatus than cattle on the same grazings. This was especially true of the larval and nymphal forms. Goats were poor hosts of the adults of this species but carried twice as many larvae and nymphae as sheep in the same area.

References

Barnett, S.F. & Bailey, K.P. 1951. E. Africa Vet. Res. Organization Annual Report, p. 13.

Hoogstraal, H. 1956. African Ixodoidea I, ticks of the Sudan. US Dept of the Navy, Bureau of Medicine and Surgery. Research Report No. NM 005.29.07.

McCulloch, B., Kalaye, W.J., Tungaraza, R., Suda, B.Q.J. & Mbasha, E.M.S. 1968. A study of the life history of the tick R. appendiculatus -- the main vector of East Coast fever with reference to its behavior under field conditions with regard to its control in Sukamaland, Tanzania. Bull. epiz. Dis. Afr., 16: 477– 500.

Newsom, R.M. 1975. Life cycle studies of R. appendiculatus and associated species in the field. FAO Technical Report No. 4 for the Government of Kenya, AG/DP/KEN/70,522.

Specht, E.J.K. 1981. Incidencia de helmintos nos ovinos e caprinos no Sul de Moçambique. FAO/INIV Internal Report.

Travassos Dias, J.A. 1952. List of Moçambique ticks and their known hosts. Direcçao dos Serviços de Veterinária de Moçambique, S. 1950. p. 227–252.

Travassos Dias, J.A. 1954. Lista das carraças de Moçambique e respectivos hospedeiros. Direcçao dos Serviços de Veterinária de Moçambique, 4 (1951): 121–166.

Travassos Dias, J.A. 1960. Lista das carraças de Moçambique e respectivos hospedeiros. Direcçao dos Serviços de Veterinária de Moçambique, 6 (1953– 1954): 213–287.

Yeoman, G.H. 1966. Field vector studies of epizootic East Coast fever, II. Seasonal studies of R. appendiculatus on bovine and non-bovine hosts in East Coast fever enzootic, epizootic and free areas. Bull. epiz. Dis. Afr., 14: 113–140.

Yeoman, G.H. 1967. Field vector studies of epizootic East Coast Fever, III. Pasture ecology in relation to R. appendiculatus infestation rates on cattle. Bull. epiz. Dis. Afr., 15: 89–114.

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