1Sampling areas in three regions of the North West province, South Africa. http://ojvr.org/index.php/ojvr/article/downloadSuppFile/305/233
During each collection phase, nominated animal health technicians from each region received in-house training in basic tick identification, collection and specimen handling before collection commenced at their specified sites. The fourth phase (performed at the Onderstepoort Veterinary Institute [OVI]) involved species identification, database acquisition, distribution mapping using ArcGIS (ESRI) software and reporting. Ticks were collected off one side of livestock hosts – mainly cattle, goats and sheep – using forceps. Each collection was placed in 70% alcohol in a specimen bottle for dispatch to the OVI for identification and recording. Only one collector, in the Bray area, consistently sampled chicken coops. Owing to prior training collectors were able to perform basic tick species identification in situ, so that as wide a range of species present on the animal could be collected. To gain data on species seasonality, monthly collections from most sites were attempted. Tick collections were, however, disrupted to some extent during the second phase (central region) because of a swine fever outbreak in the Eastern Cape, which required secondment of personnel to assist with containment operations. In some areas of the north-eastern region, a high incidence of both Rhipicephalus (Boophilus) decoloratus and Rhipicephalus (Boophilus) microplus, the vectors of bovine babesiosis, was evident. A standard immunofluorescent antibody test (Joyner et al. 1972) and a competitive inhibition enzyme-linked immunosorbent assay (Ndung’u et al. 1995; Visser et al. 1992) were used to test blood samples for antibodies to Babesia bovis and Babesia bigemina, and Anaplasma marginale, respectively. Sera collected from 13 properties in the affected areas (from at least 30 cattle per herd, 9–12 months of age) were tested to determine the antibody status of these herds to African and Asiatic babesiosis and anaplasmosis. Results and discussion Number of ticks, species composition and collections A total of 42 566 ticks (from 1190 collections across 265 collection sites) were received for identification. The breakdown of collections is as follows: (1) north-eastern region: 21 045 specimens from 429 collections (2) central region: 10 391 specimens from 398 collections (3) western region: 11 130 from 363 collections. Owing to the collection method employed almost all the ticks received were adults (97.9%), with roughly equal numbers of males and females. The immatures (nymphs = 1.8%; larvae = 0.3%), mostly Rhipicephalus evertsi evertsi and four nymphs of Otobius megnini, were collected more by chance than intention from the ears of cattle. Altogether 22 tick species were identified (18 from six Ixodidae genera; four from three Argasidae genera). The main tick species were all hard ticks (Ixodidae) and included R. evertsi evertsi (31.5%), Hyalomma rufipes (22.4%), Amblyomma hebraeum (17.3%), R. (B.) decoloratus (12.5%), Rhipicephalus appendiculatus (11.2%), Hyalomma truncatum (2.3%), R. (B.) microplus (1.6%), Rhipicephalus evertsi mimeticus (0.5%) and Rhipicephalus simus (0.21%). Other ticks of lesser importance or those collected in low numbers or during only a few collections, as well as the Argasidae collections, are as shown in Table 2.
2Ixodid ticks of lesser importance and argasid ticks identified from each of the three collection regions. http://ojvr.org/index.php/ojvr/article/downloadSuppFile/305/234
Monthly collections over a period of 10–12 months were received from 70 collection sites, which allowed the seasonal occurrence of the major tick vectors to be determined. Monthly collections from a further 175 collection sites were received over a period varying from 1 to 9 months. Tick species distribution and seasonality The distribution patterns and seasonality of the major tick species collected are described below. Amblyomma hebraeum According to Norval and Horak (2004), Amblyomma hebraeum is present in grassed bushveld and wooded savanna regions. In the present survey, A. hebraeum accounted for 17.3% of the collected ticks and appears well established in the Mixed and Sourish-mixed Bushveld areas of the North West province (Figure 3). It is present mainly in the north-eastern and northern portion (Mixed Bushveld) of the central region, with singular intrusions into the Kalahari Thornveld south-east of Vryburg and west of Mafikeng. The latter distribution appears to be established populations because they were consistently collected during the summer months at these sites. Adult ticks prefer large hosts such as cattle and large wild ruminants, but also infest sheep and goats (Horak et al. 1987; Walker et al. 2003). In this survey 90.8% of A. hebraeum specimens were recovered from cattle, 4.9% from goats and 3.3% from sheep (1.0% were not stipulated). The adults of this species were present throughout the year, with a high incidence in both the north-eastern and central regions during November and December (summer), similar to observations by Rechav (1982) for the Eastern Cape. Higher numbers of adults were found in the central region between March and May (autumn) than in the north-eastern region during these months. Hyalomma rufipes H. rufipes (previously the subspecies Hyalomma marginatum rufipes [Apanaskevich & Horak 2008]) is a vector of the Crimean–Congo haemorrhagic fever virus. It is the most widely distributed species of this tick genus in South Africa, occurring in the greater part of the country (Norval & Horak 2004). It was found distributed widely over the whole of the North West province, with it being absent from only eight of the collection sites (Figure 4). The life cycle may be completed in one year and peak numbers of adults were evident in the summer months (November–February). H. rufipes accounted for 22.4% of the total number of specimens collected in this survey. Of these, 97.2% were from cattle, 1.5% from sheep and 0.5% were found on goats (0.8% were not assigned a host). Hyalomma truncatum H. truncatum is widely distributed over the whole of the North West province (Figure 5) and was present in all the ecological zones sampled. Of the adult H. truncatum specimens collected, 89.9% were from cattle, 0.8% from sheep and 8.5% from goats; 0.8% were not assigned a host. H. truncatum accounted for only 2.3% of the total number of specimens collected. Some strains of this species transmit a toxin that causes an epitheliotrophic condition called sweating sickness, which affects young calves in particular (Neitz 1959). The tendency for adults to attach preferentially in the tail switch of cattle (where it is easily overlooked during sampling) may explain why this tick was not collected at more of the collection sites. Its seasonal occurrence in the North West province confirms its annual life cycle, with adults reaching peak numbers between January and March. Rhipicephalus appendiculatus R. appendiculatus is restricted to the higher-rainfall, eastern regions of South Africa (Walker et al. 2000) and according to Theiler (1962) does not occur in open grassland without bush; it prefers tall grass interspersed with trees. Accordingly, this species was found well established in the north-eastern region of the province and in the bushveld areas of the northern reaches of the central region around Mafikeng (Figure 6). The remainder of the province, especially the western region, appears to be ecologically unsuited to the establishment of this tick species. This species accounted for 11.2% of the specimens collected. Of the total number of adults collected, 86.9% were from cattle, 7.4% from goats and 5.0% from sheep; the remaining 0.7% were not assigned a host. Adult activity commenced only during the summer months (between December and March), as reported for the Eastern Cape by Rechav (1982). Rhipicephalus (Boophilus) decoloratus The ticks we have chosen to name R. (B.) decoloratus and R. (B.) microplus were originally known as Boophilus decoloratus and Boophilus microplus, respectively. However, based on molecular evidence (Beati & Keirans 2001; Murrell, Campbell & Barker 2000), they were included in a 2002 world list of valid tick names as R. (B.) decoloratus and R. (B.) microplus (Horak, Camicas & Keirans 2002). Guglielmone et al. (2010) have subsequently omitted the subgenus and these ticks appear in their list of valid tick names as R. decoloratus and R. microplus. We chose to include the subgenus in our nomenclature.R. (B.) decoloratus represented 12.5% of the collections in this survey, with 98.1% of specimens being collected from cattle, only 0.5% from sheep and 0.3% from goats. The remaining 1.1% were not assigned hosts. This distribution confirms its host preference for large ungulates (Mason & Norval 1980). The species normally occurs in temperate savanna regions, typically in grass- and woodland areas used by cattle, and tends to be absent in drier areas (Walker et al. 2003). It is well established in the grassed Bushveld biomes (especially the Sourish-mixed Bushveld) of the north-eastern region and northern reaches of the central region of the North West province, around Rustenburg, Zeerust, Mafikeng and Potchefstroom (Figure 7). The tick also inhabits seemingly suitable habitats (probably created by irrigated land use) in the Cymbopogon–Themeda veld near Bloemhof and the Kalahari Thornveld near Kudumane and Vryburg in the western region. Apparently, suitably high temperatures – well above the developmental threshold of 10 ºC (Spickett & Heyne 1990) – and host availability yielded high numbers of this one-host species, even during the winter months. Peak numbers were evident in December and January and again from March to July. Since R. (B.) decoloratus is a vector of B. bigemina, African babesiosis may therefore be a threat throughout the year. Rhipicephalus (Boophilus) microplus R. (B.) microplus, as R. (B.) decoloratus, inhabits savanna climatic regions in wooded grasslands used as cattle pasture (Walker et al. 2003). R. (B.) microplus (Figure 8) was found to have a more limited distribution compared to that of R. (B.) decoloratus, being confined to the Sourish-mixed Bushveld of the north-eastern region (around Rustenburg, north-east of Potchefstroom and north of Zeerust). The species was also found in an isolated pocket near Bloemhof, probably introduced by cattle and finding suitable habitats here. Cattle are considered the only effective hosts of R. (B.) microplus (Mason & Norval 1980), to the extent that this species is absent in game parks, where no cattle occur (Horak et al. 1986). Recently, goats have been implicated as alternate hosts for this species, but in the presence of cattle in order to maintain populations (Nyangiwe & Horak 2007). In the present survey 81.8% of R. (B.) microplus specimens were collected from cattle and, significantly, a relatively high 7.7% were found on goats. None were found on sheep. The remaining 10.5% of the collected R. (B.) microplus specimens were not assigned a host by the collectors, but were most probably collected off cattle. The seasonality of R. (B.) microplus was similar to that of R. (B.) decoloratus, with peak numbers occurring during the autumn months of April and May.Rhipicephalus evertsi evertsi R. evertsi evertsi is widely distributed and common on livestock throughout much of Africa, occurring in desert, steppe, savanna and temperate climatic regions (Walker et al. 2003). It has the most widespread distribution of species in the genus Rhipicephalus in Africa and has an extensive host range (Walker et al. 2000). It was the most commonly collected species in the North West province (31.5% of all specimens), being distributed over the whole province and absent at only two collection sites (Figure 9). In this survey, the adults that were collected came from cattle (79.1%), goats (15.9%) and sheep (3.9%), whilst the remaining 1.1% were unaccounted for as to host. Peak activity was recorded early in autumn (May), although high numbers were also recorded during the summer months. Rhipicephalus evertsi mimeticus Although of minimal economic importance, this species is interesting in that it is recorded as occurring in the arid regions of Angola, Namibia and Botswana (Theiler 1962). With regard to morphology and biology it is very similar to its subspecies R. evertsi evertsi and can also cause paralysis in sheep, mainly lambs, owing to secreting a toxin in the saliva whilst feeding (Gothe 1999). This species has infiltrated the North West province, with suitable habitat conditions enabling it to establish populations in the western region (Figure 10), possibly by means of sheep introduced from Botswana or Namibia, and thus likely displacing R. evertsi evertsi at these localities. Recurring monthly collections of relatively high numbers off sheep from these sites confirmed the establishment of viable R. evertsi mimeticus populations. Being subspecies, R. evertsi mimeticus and R. evertsi evertsi should interbreed, yet both were found to be morphologically distinct and could easily be distinguished taxonomically at the same localities, which may indicate some degree of speciation. This observation needs further investigation. Rhipicephalus simus This species establishes in regions with a savanna climate and is never encountered in high numbers (Norval & Mason 1981; Walker et al. 2000). It is well established in the bushveld areas of the north-eastern region of the province to which its distribution is confined (Figure 11). Of the R. simus collected, 71.9% were from cattle, 4.0% from sheep and 18.5% from goats. This species was also recovered from dogs (4.0%), whilst 1.6% were not assigned a host by collectors. Tick-borne disease serology As shown in Figures 7 and 8, R. (B.) decoloratus and R. (B.) microplus occurred sympatrically at some localities in the north-eastern region of the province. Both species are associated with the transmission of the causative organism of anaplasmosis (Ana. marginale) as well as the organisms causing bovine babesiosis (Babesia bigemina and Babesia bovis) (De Vos & Potgieter 1994). The antibody status of cattle herds to these tick-borne pathogens in the areas of sympatric distribution of these two tick vector species, as well as the presence (or absence) of the two tick vector species is shown in Table 3.
3Serology results from livestock at various localities and associated presence or absence of vectors. http://ojvr.org/index.php/ojvr/article/downloadSuppFile/305/235
The results indicate that only one property (Commiesiedrift) is in a state of endemic stability (Norval et al. 1983) to B. bigemina (100%), whereby sufficient infected vector ticks (R. [B.] decoloratus) are present to transmit the pathogen such that all the animals show an antibody response indicative of disease immunity. All other properties appear to experience endemic instability to both B. bigemina and B. bovis, strongly suggesting that intensive chemical control is practiced on these properties, thereby reducing vector challenge and, subsequently, pathogen transmission. On the endemically unstable properties, more than 40% of the cattle show no antibodies to the causative organisms and are thus fully susceptible and at risk to babesiosis should they be challenged by infected ticks. None of the animals on six properties showed antibodies to B. bigemina despite the presence of the tick vector, possibly owing to uninfected ticks (unlikely) or extremely stringent tick control practices. These animals could be completely susceptible to bovine babesiosis should they be challenged by infected ticks. R. (B.) microplus was absent on five of these properties and, as expected, none of the animals tested positive for B. bovis antibodies. However, on one of the properties (Leeukraal) on which no animals tested positive for B. bigemina in the presence of the tick vector, 50% of the animals tested positive for B. bovis in the presence of the vector tick. The latter case is difficult to explain: it is possibile that R. (B.) microplus, as a vector, presented a much higher challenge than did R. (B.) decoloratus and that antibody manifestation to B. bigemina was subsequently lost. On two properties, respectively 28% and 40% of the animals showed antibody titres to B. bovis, indicative of R. (B.) microplus infestation, although this vector tick was not collected at the time of the survey. Conclusion This study was conducted to survey the occurrence and distribution of ticks infesting livestock in the North West province of South Africa. The survey entailed the monthly collection of tick specimens from livestock hosts at specified sites in the north-eastern, central and western regions of the province. Tick specimens were subsequently identified and the distributions of the major species plotted. According to this survey, livestock in this province harbour 22 tick species (18 ixodids; 4 argasids). The major tick-borne diseases were prevalent mainly in the north-eastern region, which also displayed the highest tick species diversity. The vectors of Corridor disease (buffalo-associated Theileria parva), namely R. appendiculatus and Rhipicephalus zambeziensis were present in the north-eastern region of the province, which indicates that care should be exercised in the introduction of Corridor-infected buffalo in these regions. The central region appears transitory to the major vectors A. hebraeum and R. (B.) decoloratus, whilst the two Hyalomma vectors of Crimean–Congo haemorrhagic fever virus are widespread over the whole province. The north-western area (Bray) of the western region has been infiltrated with R. evertsi mimeticus, a species considered to be non-endemic to South Africa. Most herds sampled for serology in areas endemic for babesiosis and anaplasmosis in the north-eastern region are endemically unstable and at risk to these tick-borne diseases should vector control measures become ineffective. 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