1Numbers of the less common tick species collected by dragging at the Skukuza and Nhlowa Road sites in the Kruger National Park (August 1988–March 2002). http://ojvr.org/index.php/ojvr/article/downloadSuppFile/41/111
Haemaphysalis elliptica Haemaphysalis elliptica is an old taxon – originally described by Koch around the Cape of Good Hope in the nineteenth century – and has recently been reinstated as a valid species (Apanaskevich et al. 2007). All reports of Ha. leachi in South Africa from before 2007 are, in fact, incorrect and should actually refer to Ha. elliptica, as Ha. leachi does not occur in this country (Apanaskevich et al. 2007). Adult ticks were the most commonly collected stage of Ha. elliptica. In the KNP adult ticks have most often been collected from the larger felids, such as lions, leopards (Panthera pardus), cheetahs (Acinomyx jubatus) and African civets (Civettictis civetta). They have also been recovered from African wild cats (Felis silvestris) and feral cats (Felis cattus), black-backed jackals (Canis mesomelas), wild dogs (Lycaon pictus) and spotted hyaenas (Crocuta crocuta) (Horak et al. 1987; Horak et al. 2000a). The immature stages are usually found on rodents (Braack et al. 1996; Horak, Fourie & Braack 2005), but small numbers may also infest carnivores, scrub hares and helmeted guineafowls (Horak et al. 1987; Horak et al. 1991; Horak et al. 1993; Horak et al. 1995; Horak et al. 2000a). Very few larvae or nymphs were collected from the vegetation (Table 1). However, as their preferred hosts are rodents, they probably quest for these from the soil surface and do not attach to flannel strips dragged over the vegetation. Haemaphysalis elliptica adults were more commonly collected at Nhlowa Road than at Skukuza (p = 0.001). Landscape Zone 17 is at the centre of lion activity in the KNP (Gertenbach 1983), which may account for the greater number of adult ticks in this area. There was a significant difference between the numbers of adults collected over years (p < 0.001). Some were collected from 1988 to 1990, but few were collected from 1991 to 1993. The numbers then increased, with a marked peak in 2000 (Figure 3a). The patterns were similar at both sites, but there was a significant year-by-site interaction (p < 0.001), because more were collected at Skukuza in 1988 and 1989 while more were collected at Nhlowa Road in the other years. The collections of adult ticks were correlated with annual rainfall of the preceding year at both sites (r > 0.67; p < 0.01). A significant correlation with rainfall 2 years before was also observed at Skukuza (p = 0.64; p < 0.05), and a positive but non-significant correlation with rainfall observed at Nhlowa road (p = 0.48; p < 0.2). The dramatic increase in numbers in 1999 and 2000 followed 2 years of above-average rainfall in 1998 and 1999. Following a rodent explosion in 1993 (Horak, Spickett & Braack 2000b), after above-average annual rainfall in 1992, numbers peaked slightly at Nhlowa Road in 1994 and 1995. The increase in numbers of Ha. elliptica adults around the turn of the century was probably also associated with an increase in rodent populations during a period of above-average rainfall. According to the time series assessment, the seasonality of Ha. elliptica adults was not statistically significant, probably because of the small numbers collected in most years. However, an ANOVA showed a significant difference between months (p < 0.001), with the largest numbers collected in late summer and autumn (February–June) and the smallest numbers in spring (September–November) (Figure 3b). A similar pattern was observed at both sites. There are no data regarding the seasonality of adult Ha. elliptica on carnivores in the KNP, but in north-eastern KwaZulu-Natal, south-east of the KNP, adult ticks on dogs in rural communities were found mostly from January to March or April (Horak, Emslie & Spickett 2001). Haemaphysalis elliptica larvae were more commonly collected at Skukuza than at Nhlowa Road. Most larvae were collected in 1989 and 1990, and only sporadically thereafter. The largest numbers were collected in September and November, and only two of the 60 were collected between January and April. Nymphs were collected sporadically in the early 1990s and again towards the turn of the century. Eight of the 10 nymphs were collected between July and October. The September–November and July–October peaks for collections of Ha. elliptica larvae and nymphs, respectively, correspond to the seasonal peaks in Ha. elliptica/spinulosa larval and nymphal infestations on red veld rats in the southern KNP (Braack et al. 1996). As shown in Table 2, the largest numbers of Ha. elliptica adults were collected in the gullies, while fewest were collected in woodland (p < 0.01). This pattern was consistent over months and at both sites. However, there was a significant difference between years (p = 0.02), with the largest numbers collected in the gullies until the late 1990s (Figure 3c) followed by more frequent collections in grassland and woodland. Eight of the ten nymphs were collected in the gullies.
Tall grasslands appear to support a higher diversity of small mammal populations (Monadjem 1997), but many of the rodent hosts of the immature stages of Ha. elliptica prefer sheltered, rocky areas (Skinner & Smithers 1990). During periods of below-average rainfall, when grass swards were shorter and ground cover was reduced, gullies were probably the preferred habitat of many of the rodent hosts. Around the turn of the century the majority of Ha. elliptica adults were collected in grassland and woodland. Denser ground cover and taller grass swards following a period of higher rainfall would have provided a more suitable habitat for many rodent species, and an increase in rodent populations would have led to an expansion of habitat use. Thus, the population dynamics and habitat distribution of questing Ha. elliptica are probably determined by the effects of rainfall on the populations of rodent hosts of the immature stages, rather than the carnivore hosts of the adults. Hyalomma truncatum Although only 24 larvae and five adult Hy. truncatum were collected from the vegetation (Table 1), these low numbers should not be regarded as a reflection of actual abundance of this tick in the KNP. During the first 6 years of this survey, five scrub hares were examined monthly around Skukuza, and the 360 examinations during this time yielded a total of 36 647 larvae and 9896 nymphs of this two-host tick (Horak et al. 1993; Horak et al. 1995). Adult Hy. truncatum have been collected from the large browsers and grazers in the KNP, including giraffes (Giraffa camelopardalis), Burchell’s zebras (Equus burchellii), elands, (Taurotragus oryx), white rhinoceroses and kudus, as well as warthogs (Phacochoerus africanus) (Horak, De Vos & De Klerk 1984; Horak et al. 1988; Horak et al. 1992; Horak, Golezardy & Uys 2007; Knapp et al. 1997). The discrepancy between the numbers collected by dragging and the numbers on scrub hares strongly suggests that Hy. truncatum larvae quest for hosts from the soil surface. The adults definitely quest for hosts from the soil surface and can readily be seen scuttling along the ground towards any large potential host. Rhipicephalus evertsi evertsi Rhipicephalus evertsi evertsi is a two-host tick that infests a wide range of host species (Walker et al. 2000). In the KNP, Burchell’s zebras and giraffes appear to be preferred hosts for all stages (Horak et al. 1984; Horak et al. 2007), while impalas and scrub hares are important hosts for the immature stages (Horak et al. 1993; Horak et al. 1995; Horak et al. 2003). Larvae were most commonly collected during dragging (Table 1) and, theoretically, only larvae and adults should quest for hosts. The single nymph that was collected had probably become dislodged just before or after moulting and was questing for a host. Very few adults were collected, probably because they quest for hosts from the soil surface or, like the adults of many species, they do not attach to flannel strips. In previous drag-sampling studies in Landscape Zones 4 and 17 there was no evidence of seasonality in the numbers of questing R. evertsi evertsi larvae collected (Spickett et al. 1992; Horak et al. 2006b). The present study, however, showed significant periodicity at both sites (p < 0.001). At Nhlowa Road there were two annual peaks (November–February and June–July), whereas at Skukuza, there was only a single peak (November–December) with a nadir between May and June (Figure 4a). Based on the development times seen in the laboratory, R. evertsi evertsi can complete more than one life cycle annually at the prevailing temperatures in the KNP (Horak et al. 2003). At Nhlowa Road the summer and winter peaks correspond to those observed on Burchell’s zebras (Horak et al. 1984), suggesting that the seasonal pattern was related to the pattern of zebra migration. At Skukuza, the late spring peak and late autumn nadir differed not only from the pattern observed in other drag-sampling studies but also from that observed on impalas and scrub hares in this landscape zone (Horak et al. 1993; Horak et al. 2003). The reasons for the differences between the seasonal patterns observed in the present study and previous studies are unknown. They may be related to seasonal differences in habitat use by ungulates within Landscape Zone 4, or they may be because of the relatively short duration of the sampling periods (1–4 years) in the earlier studies. In the present study there was considerable variability among years and the general seasonal pattern was seen only over the longer time period. The numbers of R. evertsi evertsi larvae collected differed significantly among years (p < 0.001) and there was a significant year-by-site interaction (p = 0.028), with proportionally greater changes at Skukuza than at Nhlowa Road. However, the trends were similar at both sites, with peaks in the early 1990s, a decline through the mid-1990s, and subsequent increases in the late 1990s. Numbers declined in 2000 (Figure 4b). The numbers were not significantly correlated with seasonal rainfall at either site. The apparent differences in the annual trends at the two sites may be related to differences in the host communities. The populations of the larger ungulates at Nhlowa Road, such as zebras and giraffes, appear to be less sensitive to changes in rainfall (Ogutu & Owen-Smith 2005) than the populations of smaller ungulates, such as impalas, at Skukuza. Larvae were more commonly collected at Nhlowa Road than at Skukuza (p < 0.001) and there was a significant habitat-by-site interaction (p = 0.002). At Nhlowa Road, larvae were least frequently collected in the gullies and most commonly in the grassland (Table 2), probably because of the large numbers of zebras and other grazers at this locality. At Skukuza, R. evertsi evertsi larvae were most commonly collected in the woodland, probably because of the presence of large numbers of impalas and other browsers, but the difference among habitats was not statistically significant (p > 0.1). The differences among habitats were not significant among months or years (p > 0.4). Rhipicephalus simus Adults were the most commonly collected stage of R. simus. The preferred hosts of adult R. simus are large ruminants, such as African buffaloes, and monogastric animals, such as large carnivores, warthogs, zebras and rhinoceroses (Walker et al. 2000). Large numbers of R. simus adults have been collected from lions, leopards, warthogs, Burchell’s zebras and white rhinoceroses in the KNP (Horak et al. 1984; Horak et al. 1988; Horak et al. 2000a; Knapp et al. 1997). The collections of R. simus were seasonal, with a peak between February and March and a nadir between August and September (Figure 5a). The numbers did not differ significantly between the two sites (p = 0.2) and the seasonal patterns were similar. The peak in adult numbers corresponds with that on Burchell’s zebras and warthogs in the KNP (Horak et al. 1984; Horak et al. 1988) and on warthogs in Swaziland in a Sclerocarya caffra – Acacia nigrescens savanna (Gallivan & Surgeoner 1995). There was a significant difference between the numbers of R. simus adults collected over the years (p < 0.001). Numbers declined from 1988 to 1991, then increased again in 1994, followed by a peak in 2000 (Figure 5b). The trends differed significantly between the two sites (p < 0.001). At Skukuza, numbers tended to be higher between 1988 and 1989 than from 1997 to 2000. However, at Nhlowa Road the numbers of R. simus adults were higher from 1993 to 1995, with a marked peak in 1994. The numbers of adult R. simus collected at Skukuza were significantly correlated with annual rainfall during the 2 previous years (p < 0.05). At Nhlowa Road, the numbers were significantly correlated with rainfall 2 years before (p = 0.05), but not with that of the preceding year. The decline in numbers in the early 1990s corresponded to a period of decreasing annual rainfall and to a marked decline in the warthog population in the KNP (Ogutu & Owen-Smith 2005). The decline in annual rainfall probably also caused a decline in the populations of rodents, which are the preferred hosts of the immature stages of this tick (Braack et al. 1996; Horak et al. 2005; Norval & Mason 1981; Petney et al. 2004). Following a period of above-average rainfall in 1992, there was an eruption of rodent populations in 1993 (Horak et al. 2000b) that may have accounted for the large number of adult R. simus collected at Nhlowa Road during 1994. As with the adults of Ha. elliptica, the increase in the numbers of R. simus adults around the turn of the century was probably associated with an increase in rodent populations during a period of above-average rainfall. As shown in Table 2, adult R. simus were most commonly collected in the gullies and least frequently in the grassland (p < 0.001). There was a significant difference in the habitat distribution between the two sites (p = 0.03). At Skukuza, 48.3% of the ticks were collected in the gullies and 16.4% in grassland, whereas at Nhlowa Road, 69.2% were collected in the gullies and only 7.6% in grassland. Habitat distribution differed significantly among months (p = 0.025), with the most pronounced difference during February and March, the period of peak activity. There was also a marginally significant difference in habitat distribution among years (p = 0.1), with highest numbers in the gullies; however, in 2000 the numbers were marginally higher in woodland. As in the case of Ha. elliptica, the habitat distribution probably corresponds to the pattern of habitat use by the hosts of the immature stages. Rhipicephalus simus larvae were more frequently collected at Skukuza than at Nhlowa Road. Almost half (45.8%) were collected in 1989, while the second largest collection (14.6%) was made in 2001. Other collections were sporadic. At Skukuza, most R. simus larvae were collected from January to June, but at Nhlowa Road most were collected from June to November. At Skukuza, more larvae were collected in the gullies than in grassland, whereas at Nhlowa Road, most larvae were collected in woodland. Rhipicephalus turanicus Adult R. turanicus have been collected from lions, leopards, cheetahs, African wild dogs, feral cats and scrub hares in the KNP, but none of the animals were heavily infested (Horak et al. 1993; Horak et al. 1995; Horak et al. 2000a). No immature stages have been collected from animal hosts within the KNP or adjacent nature reserves. Scrub hares examined on farms around Hluhluwe in north-eastern KwaZulu-Natal were infested with all stages of R. turanicus (Horak et al. 1995) and crested francolins (Francolinus sephaena) on a farm in Limpopo were infested with larvae (Uys & Horak 2005). Adult ticks were also common on dogs in Maputo Province, Mozambique, adjacent to the KNP (Neves, Afonso & Horak 2004). Rhipicephalus turanicus was most commonly collected at Nhlowa Road (97.8%) and adults were the most commonly collected stage (Table 1). As mentioned before, Landscape Zone 17 is at the centre of lion distribution within the KNP (Gertenbach 1983) and the herds of large grazers would support populations of other carnivores. Collections were seasonal (p < 0.001), with a peak between February and March (Figure 6a). There were significant differences between the numbers collected among years (p = 0.002), with peaks in 1991, 1994, 1995, 1999, 2001 and 2002 (Figure 6b). The numbers of R. turanicus adults were not correlated with rainfall and, as shown in Table 2, ticks of this stage were collected in the gullies more often than in woodland (p < 0.001). This pattern was consistent among years and months. There was a strong correlation (r = 0.7; p = 0.009) between the numbers of adult R. simus and adult R. turanicus collected annually at Nhlowa Road. The year-to-year patterns of the two species were similar and both species were most commonly collected in the gullies. However, woodland yielded the fewest R. turanicus adults, whereas the grassland yielded the fewest R. simus adults. The distribution of adult R. turanicus among habitats and year-to-year collection patterns were also similar to those of adult Ha. elliptica at the Nhlowa Road site. Conclusion In order to determine the population dynamics of free-living ixodid ticks, questing ticks were collected monthly for 164 months from the vegetation at two localities in the KNP. Of the collected species, 14 could be identified to specific level. Larvae of A. marmoreum and R. evertsi evertsi, and adults of Ha. elliptica, R. simus and R. turanicus were collected in sufficient numbers to conclude that they quest for hosts from the vegetation. The host-seeking strategies of their remaining developmental stages and those of the tick species collected only in small numbers still need to be investigated. The value of long term sampling at more than one locality and within various habitats at each locality yielded several answers and posed a number of questions. Should more samples be taken within the predominant habitat at a locality, for example in the thickets and woodlands of a thicket locality and in the grasslands of a savanna locality, to obtain more accurate results pertaining to an entire locality? What are the reasons for markedly more numerous questing ticks in a treed savanna locality compared with a locality composed largely of thickets? What value can be added by simultaneously sampling the major host species within a study site for ticks and determining host densities and daily and seasonal movements? Finally, logistical challenges to what can be achieved in the field in a large nature reserve need to be considered, for example (1) the dangers posed to field workers by large predators, African buffaloes, rhinoceroses and elephants, (2) the number of drag samples that can be accomplished in a day to ensure reasonable homogeneity, as the total length of the drags placed end to end covered a distance of 2250 m at each locality, and (3) the number of people, besides an armed ranger, needed to collect, within a reasonable time frame, the thousands of ticks sometimes collected in a single drag. Acknowledgements We are indebted to the South African National Parks (SANParks) for placing their staff and facilities in the KNP at our disposal. We gratefully acknowledge the assistance of Dr Leo Braack and Mr André Potgieter with arranging the logistics for the collections. A number of nature conservation and veterinary students assisted with many of the field collections. 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