A comparison between tick species collected in a controlled and control free area on a game ranch in South Africa

Copyright: © 2013. The Authors. Licensee: AOSIS OpenJournals. This work is licensed under the Creative Commons Attribution License. Despite the large number of collection records, there are no recent collections of ixodid ticks of this magnitude in the Waterberg area, Limpopo Province, South Africa. Free-living ticks on a commercial game farm were obtained by a total of 432 drag-samples in eight sample sites from September 2003 to August 2008. The ticks were collected to establish the difference between tick species and densities associated with acaricide-controlled (semi-intensive) and controlfree areas on a game farm in the Thabazimbi District, Limpopo Province, South Africa. A total of eight tick species were collected, namely Amblyomma hebraeum, Rhipicephalus (Boophilus) decoloratus, Haemaphysalis elliptica, Hyalomma rufipes, Rhipicephalus appendiculatus, Rhipicephalus evertsi evertsi, Rhipicephalus zambeziensis and Rhipicephalus spp. The most abundant tick species collected was Rhipicephalus (Boophilus) decoloratus. The difference in species and numbers reflects the effectiveness of acaricide treatment against ticks and its relevance to tick numbers on a game farm.


Introduction
Ticks are blood-feeding external parasites of mammals, birds, and reptiles throughout the world (Vredevoe 2006).Ticks thus affect wildlife and domestic animal management worldwide, with approximately 896 species of ticks in three families having been described (Guglielmone et al. 2010).Research on South African ticks commenced nearly 200 years ago and since then over 80 tick species have been identified and documented (Walker 1991).
Ticks of all types are important vectors of animal and human pathogens.It was established that ticks were being controlled for a lack of a better method to control tick-borne diseases (TBD).Certain tick-borne diseases are of major importance throughout the world.In the United States of America, there are many diseases caused by tick-borne pathogens that include Lyme disease, ehrlichiosis, babesiosis, Rocky Mountain spotted fever, tularaemia and tick-borne relapsing fever (Vredevoe 2006).In Tanzania, diseases are listed as a major farming constraint, especially tick-borne diseases such as East Coast Fever (Theileria parva), anaplasmosis and cowdriosis (Swai et al. 2005).
In Zambia, tick-borne diseases, particularly Theileriosis, pose a serious threat to the development of the cattle industry.Tick infestation is considered to be one of the main constraints to successful game ranching in southern Africa (Horak 1980;Lightfoot & Norval 1981;Norval & Lightfoot 1982).
Approximately 80% of the world's cattle population of 1281 million are at risk from ticks and tickborne diseases (Stafford 2004).McCosker (1979) estimated global costs of control and productivity losses to be some $7000 million annually.In Africa, with 186 million head of cattle, ticks and tickborne diseases are the most serious constraints to increased production (Stafford 2004).
This study was undertaken on a commercial game ranch in the Waterberg District of the Limpopo Province, South Africa.In this specific undertaking, rare and threatened ungulates such as roan antelope (Hippotragus equinus equinus) are being semi-intensively bred in breeding camps ranging  in size from 20 ha to 50 ha for commercial and biodiversity purposes.Furthermore, high value disease-limited species such as buffalo (Syncerus caffer) are also ranched intensively.The roans are being bred until the population reaches a predetermined stocking ratio, after which, the animals are sold with the ultimate objective of increasing the size of the metapopulation.The roan antelope are kept separate from other species due to their low tolerance for competition.All predators have been excluded from the breeding camps to limit mortalities.Despite satisfactory breeding results of roan antelope throughout South Africa, theileriosis specifically is seen as one of the main causes for the abnormally high mortality rate in calves and one of the reasons for the population decline (Van der Vegt 2007, unpublished data).
The main tick-related problems affecting the semi-intensive commercial game ranching operation are corridor disease (T.parva lawrencei) in the buffaloes and acute Theileriosis in juvenile roan antelopes (A.C. Uys 2003, personal communication).
Although wild animals native to a specific area are seldom affected by the endemic tick-borne blood parasites, translocation of hosts and/or ticks into non-endemic areas can cause severe losses amongst naïve animals (Lightfoot & Norval 1981).In addition to tick-borne diseases, other direct effects of ticks on their hosts include tick toxicosis, metabolic disturbances, anaemia and tick worry, which can result in production losses and/or deaths (O'Kelly & Seifert 1969).Tick-bite wounds can also become secondarily infected with bacteria and maggots, potentially leading to death (Lightfoot & Norval 1981).
A larval tick survey was undertaken in order to determine the species composition in the controlled (semi-intensive) and control-free areas on the game ranch.These results will ultimately be used to establish whether the use of acaricides has an effect on tick numbers by comparing the tick numbers in the controlled area with those in the control free area.

Study area
The wildlife breeding farm 'Hoopdal' KQ96 is 2210 ha in area and is located in the Thabazimbi district, Limpopo Province, South Africa.It is bounded by longitudes 24º16'16.07"Sand 24º20'43.56"S,latitudes 27°29'42.89"Eand 27°26'57.85"E,with altitudes ranging from 993 m to 1035 m above sea level.The farm consists mainly of plains (Van Staden 2002) and is located in the Waterberg region in the north-western corner of the mixed Bushveld (Acocks 1988).The vegetation comprises Mixed Bushveld and Sourish Mixed Bushveld of the Savanna Biome (Low & Rebelo 1996).Mucina and Rutherford (2006) classified the area as Western Sandy Bushveld, comprising tall open woodland to low woodland in which broad-leaved as well as microphyllous tree species are prominent.Rainfall during the study period amounted to a mean annual rainfall of 826.64 mm.The mean minimum monthly temperature during the study period was 12.81 °C, ranging from 0.5 °C to 19 °C.The mean maximum annual temperature during the same period was 30.13 °C, ranging from 22.0 °C to 40.5 °C (Figure 1).

Drag-sampling
Drag-sampling with flannel strips was chosen as a means of recovering immature ticks questing on vegetation (Zimmerman & Garris 1985), using a technique described by Petney and Horak (1987).Drag-sampling was performed on a monthly basis at the same time each month (20th -26th) for a period of 5years from September 2003 to August 2008.A grassland and a woodland zone were selected for dragging in each of the controlled and control-free areas.Ten flannel strips (1000 mm x 100 mm) were attached with Velcro tape to a 1200 mm-long wooden spar.Each collection was made by dragging the spar by means of a loop of rope attached at either end for a distance of 300 m over the vegetation.Each month, four drag samples were performed in the woodland areas and four drag samples in the grassland areas for both the controlled and control-free areas.After each drag, all the ticks were removed from the flannel strips using fine-point tweezers and placed in 70% alcohol.The ticks were identified at the Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria.

Statistical methods
Because of their over-dispersed nature, the tick drag-results were sampled and logarithmically transformed (log [x + 1]) (Petney, Van Ark & Spickett 1990).The transformation to standard logarithms and not natural logarithms was chosen because the mean to variance ratio approaches one.
The Wilcoxon test for matched pairs is a simple nonparametric test for comparing the medians of two matched samples.It calls for the calculation of a test statistic T whose probability distribution is known.In the test, one observation in a matched pair is subtracted from the other.Observations must therefore be measured on an interval scale (Fowler et al. 2003).
The null hypothesis H 0 is that there is no difference in median tick numbers between the two sets of data.The alternative hypothesis, Hα, is that there is a difference, but with no prediction for which way the difference will lie (i.e. a twotailed test) (Fowler et al. 2003) (Table 2).
Of the 6836 ticks collected, the most abundant tick species recorded was R. (Boophilus) decoloratus, and this species was mainly collected in the controlled areas of the game farm.
Table 1 shows the species collected with the percentage collected in the controlled and control-free areas of the game farm.The higher numbers of R. (Boophilus) decoloratus collected in the controlled area as compared to the lower numbers in the control-free area, a differences of 9.8%, is attributed to the fact that acaricide treatment has an effect on tick numbers.The acaricide used in the controlled area was 'Drastic Deadline'® (Bayer Animal Health Division, Isando).The acaricide was applied using two application methods simultaneously: feed bins with an extended outer rim holding the acaricide (this was undertaken with every feed) and the tick-off pressure plate system at the entrance to the waterhole (this was refilled monthly).
The difference in tick numbers collected between the two areas was recorded as 9.8%.This is explained by the number of R. (Boophilus) decoloratus collected in the controlled area.This shows a high probability that this tick species had become resistant to the acaricide treatment being applied in the study area.
Significant differences were found between the tick numbers collected in the controlled and control-free areas for the study period for each individual species (Table 2).

Discussion
The mean number of ticks recovered per drag-sample per month over the 5-year study period was 15.82.This is lower than the 168 ticks collected by monthly dragging in the Kruger National Park by Horak (1998) and the 138 ticks collected per drag in Zambia by Zieger, Horak and Cauldwell (1998) and the 80 ticks collected per drag in 'Hoopdal' KQ96 by Schroder, Uys & Reilly (2006).Ticks removed by drag samples depend on many factors such as microclimatic conditions in specific sites at specific times, host numbers on the site, host species and favourability and host utilisation of the habitat.Thus, variations are expected between sites and even between the same sites over the years.
The presumed reason for R. (Boophilus) decoloratus numbers being so high in the controlled area as opposed to the other seven tick species found during the study period is bad management of acaricide treatment, resulting in this tick species becoming impervious to the acaricide treatment.This is known as tick resistance and has been confirmed especially in this species by Baker (1982), Du Toit, Graf andBekker (1941), Solomon (1983) and Walker (1991).
Tick resistance has been detected in R. (Boophilus) decoloratus after controlled field trials and laboratory tests that confirm their resistance (Mekonnen 2005).Figure 2 shows the individual tick numbers collected for each tick species in the controlled and control-free areas.

Conclusions
In conclusion, it is evident that of the eight tick species collected on the farm 'Hoopdal' KQ96 in the Thabazimbi District, Limpopo Province, South Africa, six of the tick species were more prevalent in the control-free area, one species was found equally in both areas and only one species, R. (Boophilus) decoloratus, was found predominantly in the controlled area during the study period, September 2003 until August 2008.
Thus it is evident that acaricide treatment is an important management tool to control ticks and tick-borne diseases.It is therefore essential that tick loads and presence should be monitored ensure that acaricide treatments are used during peak tick load periods and not on a permanent basis; this will result in more effective use of the acaricide in terms of the number of tick deaths and ensure that the ticks will not become resistant to the acaricide treatment.This will ultimately lead to less acaricide being used, which will be more cost effective.A study by Mekonnen (2002) confirmed that the use of acaricides at high frequencies and high concentrations was one of the main causes of tick resistance and financial loss.

FIGURE 1 :
FIGURE 1: Temperatures and rainfall in the study area from September 2003 to August 2008, (a) mean minimum and maximum temperatures and (b) rainfall.

FIGURE 2 :
FIGURE 2: Tick numbers per species collected in the controlled (semi-intensive) and uncontrolled areas of the study area.

TABLE 1 :
Ticks collected on the farm 'Hoopdal' KQ96 from September 2003 to August 2008.

TABLE 2 :
The eight tick species collected according to their significance.Source:The table is adapted fromFowler et al., 2003, publishedwork entitled 'Practical statistics for field biology' T, Wilcoxon test statistic.