Ixodid Ticks Infesting Domestic Goats in Communal Land Areas of Zimbabwe

INTRODUCTION The topography of Zimbabwe can be described as a series of plateaus 1. The high central plateau, known as the 'highveld' (1200–1675 m above sea level), stretches from the southwest of the country to the northeast, culminating in the east in Mount Inyangani at an altitude of 2592 m. The low altitude areas (below 610 m) in the valleys of the Zambezi River in the northwest and the Limpopo and Sabi Rivers in the south and southeast constitute the 'lowveld'. Between the high-and the lowveld lies the middleveld plateau ranging from 600 to 1200 m in altitude 1. Temperature and relative humidity on the high central plateau are moderate, whereas the climate in the lowveld tends to be very hot and dry. The country has been divided into 5 agro-ecological zones according to climate, land-use and vegetation , and these are known as Natural


INTRODUCTION
The topography of Zimbabwe can be described as a series of plateaus 1 .The high central plateau, known as the 'highveld' (1200-1675 m above sea level), stretches from the southwest of the country to the northeast, culminating in the east in Mount Inyangani at an altitude of 2592 m.The low altitude areas (below 610 m) in the valleys of the Zambezi River in the northwest and the Limpopo and Sabi Rivers in the south and southeast constitute the 'lowveld'.Between the high-and the lowveld lies the middleveld plateau ranging from 600 to 1200 m in altitude 1 .Temperature and relative humidity on the high central plateau are moderate, whereas the climate in the lowveld tends to be very hot and dry.The country has been divided into 5 agro-ecological zones according to climate, land-use and vegetation, and these are known as Natural Regions (NR) I, II, III, IV and V 27 .Aridity increases from Region I to V.
The state-owned communal lands of Zimbabwe are predominantly located in areas of low agricultural potential in the middle and lowveld of regions IV and V, and are characterised by marginal rainfall, high temperatures and poor, acidic sandy soils 27 .In addition, irrespective of the agro-ecological zone in which they are located, decades of tree felling for fuel, clearing of land for crops, the construction of houses for an increasing human population, and high livestock densities, have contributed to sparse vegetation and poor quality pastures in many of the communal lands.Because of their adaptability to the conditions described above, goats are the predominant livestock kept by resource-poor farmers on the stateowned communal lands.Most of the goats owned by these farmers belong to the indigenous Matabele and Mashona breeds 6 and their crosses, and are grazed on the communal pastures together with cattle and other livestock.
Norval and his co-workers, in a series of papers published between 1980 and 1985, have recorded the tick species that occur in Zimbabwe and described their ecology [14][15][16][18][19][20][21][22][23] . In thee publications they list a total of 14 tick species that have been collected from domestic goats in Zimbabwe.Despite the prevalence of ticks on goats, their control, as well as that of the pathogens that they transmit, by the state-run veterinary service is minimal, and tick control mostly targets cattle.The objective of the present study was to address this shortcoming by at least identifying those tick species that infest goats kept by resource-poor farmers on communal lands.

Survey localities
Ticks were collected from goats in the communal lands of Chihota in Mashonaland East province (NR II; 18°19'S, 31°12'E; altitude 1481 m), Sanyati in Mashonaland West province (NR III; 18°07'S, 29°16'E; altitude 1064 m), Chirumhanzu in Midlands province (NR III; 19°34'S, 30°45'E; altitude 1370 m), and at Filabusi (NR IV; 20°31'S, 29°14'E; altitude 1076 m) and Beitbridge (NR V; 22°13'S, 30°00'E; altitude 467 m) in the Matabeleland South province (Fig. 1).Because Chihota lies within a moist region, most of the available land is under cultivation.The uncultivated areas have very sparse vegetation and are used for livestock farming.Although Filabusi is located in region IV, which is generally dry, it is situated at a slightly higher altitude and receives occasional showers during the dry season, while Beitbridge lies in the hot and dry Limpopo River valley.

Tick collections
The 1st collections, which were made between February and April 2001, were part of a larger study on the causes of kid mortality in Chihota and Filabusi.Visible adult ticks were picked off their predilection attachment sites on adult goats, without ensuring that all ticks were collected, or recording the number of goats that were examined.
The 2nd set of collections was more thorough and was made from goats at Chirumhanzu, Sanyati and Beitbridge during 2005 and 2006.During the preliminary visits made to Chirumhanzu and Beitbridge in July 2005, 10 goats were randomly selected from homesteads in each study area.During the December 2005 and March 2006 visits, which coincided with the rainy season and peak adult tick activity, at least 50 goats were sampled per area, randomly choosing 3-5 goats per homestead from easily accessible homesteads.The goats had to be at least 3 months old, free-grazing and resident in the area for a minimum of 1 month.The animals were physically restrained and all visible adult ticks and a sample of immature ticks were collected by means of forceps.The ticks from each goat were placed separately in stoppered vials containing 70 % methanol.At the same time lesions attributable to the attachment of ticks were recorded.The ticks were transported to the laboratory where they were identified and counted using a stereomicroscope.Because of a shortage of funds sampling was not done at Beitbridge during March 2006.

RESULTS
No tick control was applied to any of the goats.The tick species and numbers collected from goats at the various study sites are summarised in Tables 1-4.
A total of 14 ixodid tick species was recovered and the 2 most abundant species collected were Rhipicephalus evertsi evertsi and a Rhipicephalus sp.(near R. punctatus).Four species were present on goats at every sampling locality, namely Amblyomma hebraeum, Hyalomma truncatum, R. evertsi evertsi and Rhipicephalus simus.Rhipicephalus appendiculatus was collected from goats in regions II and III, while Rhipicephalus zambeziensis was present on the edge of region III and in region V.Other ticks recovered in lesser numbers were Amblyomma marmoreum, Amblyomma variegatum, Hyalomma rufipes, Rhipicephalus (Boophilus) decoloratus, Rhipicephalus lunulatus, Rhipicephalus tricuspis and Rhipicephalus turanicus.A total of 324 goats was examined during 2005 and 2006 and of these 230 (71 %) were tickinfested.The proportion of infested goats was higher at Chirumhanzu (97.3%) than at Sanyati (52.1%) and Beitbridge (68.1%).Very few ticks were collected from goats during the cool, dry season (July 2005), and tick-infested goats were sometimes only encountered after visiting a number of households (Tables 3, 4).
Amblyomma hebraeum was most prevalent in Chirumhanzu, and its presence in the inter-digital space was associated with purulent ulcers and abscesses accompanied by lameness in 15 goats.Similarly, the attachment of H. truncatum in the inter-digital space in March 2006 was associated with lameness in 3 goats at Sanyati and 7 at Chirumhanzu, suppurative lesions on teats and udders on 5 goats at Chirumhanzu, and abscesses on other parts of the body of 1 goat at Sanyati and 4 at Chirumhanzu.Adult R. e. evertsi were mostly attached in and around the anal region and the immature stages in the outer ear canals.Some of its peri-anal attachment sites were characterised by non-purulent to purulent ulcerations, which were present on 12 goats at Sanyati, 6 at Chirumhanzu and 5 at Beitbridge.Occasionally, lesions associated with the various tick species were concurrently present on a single goat.

DISCUSSION
The collections of ticks from goats in Chihota and Filabusi in 2001 were made rather haphazardly, and hence are not comparable with those made during 2005 and 2006, in which all adult ticks were collected.
Because of their role in the transmission of Ehrlichia ruminantium, the causative organism of heartwater in cattle, sheep, goats and wild ruminants 17,22 , the distributions of A. hebraeum and A. variegatum in Zimbabwe have been well studied 25,26 .Historically Zimbabwe had successfully managed to control heartwater and its vectors, and by 1975 had virtually confined the disease to 3 relatively small areas in the south 12   northwest and to limited pockets in the northeast 22 .A. variegatum remained confined mostly to the northwest, where in comparison with A. hebraeum it was the dominant species.It was also present at a single locality on the eastern border 22 .At that time the highveld was appar-ently free of both these ticks.By 1997 A. hebraeum had spread towards the east and west as well as northwards onto the highveld, while A. variegatum had spread eastwards from the northwest to highveld areas such as Zvimba and Mhondoro 26    Larvae of the South African tortoise tick, A. marmoreum, were present on goats during the March collection at Sanyati, where coincidentally its distribution overlapped that of A. hebraeum and A. variegatum. A. marmoreum has previously been reported in all eco-climatic zones of Zimbabwe, and tortoises, which are the preferred hosts of its adults 10 , seem to be a major factor in determining its distribution 22 .In addition to tortoises, the immature stages infest a variety of wild and domestic mammals, as well as ground-frequenting birds 10 .The ability of A. marmoreum to transmit E. ruminantium has been demonstrated experimentally 3 , suggesting that it could play some role in the maintenance and transmission of this rickettsia.
Even though A. hebraeum was not encountered in large numbers, its attachment sites were occasionally associated with lesions on the posterior lower abdomen, including the udder, and the inter-digital space.Studies in the valley bushveld regions of the Eastern Cape Province, South Africa, have implicated A. hebraeum as a contributory cause of foot abscess and hence lameness in goats 13 .The small numbers of A. variegatum on goats in the present survey were not associated with any direct lesions, but the occurrence of large numbers on cattle at Sanyati and Mhondoro has been accompanied by dermatophilosis 5 .
Although H. truncatum was present at all localities sampled, it was never very numerous.By contrast, only a single specimen of H. rufipes was collected.This is in agreement with earlier observations in Zimbabwe in which adults of H. truncatum were recorded on a much wider range of hosts, including sheep and goats, than those of H. rufipes, which prefer larger ungulates as hosts 18 .The immature stages of both these ticks feed on hares 9 .Similar observations have been made in Somalia, where H. truncatum was more commonly found on sheep and goats, while other Hyalomma spp., including H. rufipes, were most numerous on camels and cattle 24 .Despite the small numbers of adult H. truncatum collected, their attachment sites were sometimes associated with lesions on the posterior lower abdomen, including the udder.Attachment in the inter-digital space was occasionally associated with lameness, a condition that has previously been recorded in sheep 11 .
Small numbers of R. (B.) decoloratus were collected from goats at Sanyati, Chirumhanzu and Beitbridge, and their occurrence coincided with the rainy season.Cattle are the domestic host most frequently parasitised by this tick in Zimbabwe 14 , but it has also been collected from goats in South Africa 2,4 .
The ecology of R. appendiculatus and R. zambeziensis has been thoroughly studied in Zimbabwe, where R. appendiculatus is widely distributed in the cooler moister areas in the east and the south and R. zambeziensis is largely restricted to the hotter, drier areas of the northern, north western and southern parts of the country 19 .A similar distribution pattern has been reported elsewhere in southern, central and East Africa, where R. zambeziensis replaces R. appendiculatus in several of the hotter and more arid regions 19,28 .In the present study, R. appendiculatus parasitised goats in Natural Regions II and III, which are moist.The 3 adult R. zambeziensis that were collected came from goats in the middleveld area of Chirumhanzu, in region III close to its border with region IV, where there is a gradual transition from cool, high plateau to hot, low altitude and very dry conditions, and from region V. R. appendiculatus was also present at Chirumhanzu, but not at Beitbridge.Cattle and some of the large wild ruminants such as African buffalo, eland and greater kudu are the major hosts of both ticks 19,28 , while sheep and goats are usually not parasitised to the same extent 28 .
Rhipicephalus e. evertsi was the most prevalent tick on goats in all agro-ecological zones sampled, and was present throughout the year.It tolerates a wide range of climatic conditions 28 , and occurs on domestic and wild ungulates throughout Zimbabwe 16 .Skin damage was only noticed when adult ticks formed clusters in the peri-anal region.Female R. e. evertsi produce a paralysis-inducing toxin when they reach an engorgement weight between 15 and 21 mg 7 .However, it is only under certain climatic and management conditions that sufficient numbers of female ticks in this stage of engorgement are present to cause paralysis 8 , particularly in young lambs and kids.Although adult R. e. evertsi were sometimes present in large numbers on some goats, no paralysis was observed in the current study.
The tick herein referred to as Rhipicephalus sp.(near R. punctatus) has been recorded as widespread in Zimbabwe 23 , and is possibly an undescribed species of the Rhipicephalus pravus group 28 .It has been collected from cattle, sheep and goats, but seems to be particularly prevalent on greater kudus, duikers, steenbok and grysbok 23 .In the present study it was most abundant on goats at Sanyati and Chirumhanzu during the peak rainy season in March.It has not been associated with any disease condition in domestic livestock in Zimbabwe.
The glossy brown tick, R. simus, was collected in all 5 areas sampled.The adults have a preference for domestic and wild equids, suids and canids, but domestic and wild ruminants are also infested 15,28 .Although the tick is widespread, it is seldom collected in large numbers from a single host.The immature stages infest rodents 15,28 .It has been associated with paralysis in calves and lambs in some parts of southern Africa 15 .
A species morphologically indistinguishable from R. turanicus has previously been reported in Zimbabwe, where it was most prevalent during the warm wet season from November to April 21 .It was common on sheep and goats, particularly in the north of the country, and especially severe infestations of the ears of sheep grazing communal lands at Urungwe were recorded.It also fed on other domestic and wild hosts 21 .At the time the authors were reluctant to refer to it as R. turanicus, as it was believed that the distribution of this species was confined to the Mediterranean countries of southern Europe and North Africa and to the Near and Middle East where it is common on cattle, sheep, goats and domestic dogs 28 .It has subsequently been confirmed that R. turanicus is widespread in sub-Saharan Africa, where it has been collected mostly from cattle, sheep, domestic and wild carnivores and hares 28 .In the present survey it was present on goats at Chihota, Filabusi and Sanyati.
Rhipicephalus lunulatus and R. tricuspis belong to the Rhipicephalus follis species group, and are morphologically very similar to each other 28 .The few adult ticks of both species recovered in the present study were restricted to the December collection from the Chirumhanzu district.R. lunulatus has previously been recorded as widespread, particularly in the north of Zimbabwe 20 , while R. tricuspis has been found in Hwange, the most northern district in western Zimbabwe 20 , and in the southeast of the country 28 .Although neither of these ticks is considered to be economically important, R. lunulatus (previously misidentified as R. tricuspis) has been mentioned as a possible cause of paralysis in calves and lambs 12 .