
==== Front
Curr Res Parasitol Vector Borne Dis
Curr Res Parasitol Vector Borne Dis
Current Research in Parasitology & Vector-borne Diseases
2667-114X
Elsevier

S2667-114X(24)00036-0
10.1016/j.crpvbd.2024.100205
100205
Review Article
A systematic review of ticks and tick-borne pathogens of cattle reared by smallholder farmers in South Africa
Monakale Katleho Sechaba a
Ledwaba Maphuthi Betty a
Smith Rae Marvin b
Gaorekwe Realeboga Masego a
Malatji Dikeledi Petunia malatdp@unisa.ac.za
a⁎
a Department of Agriculture and Animal Health, College of Agriculture and Environmental Science, University of South Africa, South Africa
b Department of Life and Consumer Science, College of Agriculture and Environmental Science, University of South Africa, South Africa
⁎ Corresponding author. malatdp@unisa.ac.za
27 7 2024
2024
27 7 2024
6 10020512 4 2024
24 7 2024
26 7 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Ticks are important ectoparasites of domestic animals, wild animals and humans. They spread a variety of infective agents such as protozoans, viruses, and bacteria. Cattle reared by smallholder farmers are susceptible to ticks and tick-borne pathogens due to the type of production system practiced by the farmers. Hence, this review was focused on the occurrence of ticks and tick-borne pathogens in cattle reared by smallholder farmers in South Africa. The systematic search produced a total of 13,408 articles from four databases, and after screening processes, the review utilized 23 articles published between 1983 and 2023. A total of 26 tick species belonging to seven genera were identified in the reviewed articles, with Rhipicephalus (Boophilus) decoloratus and Rhipicephalus evertsi evertsi being the most frequently reported tick species in South Africa followed by Amblyomma hebreum, Rhipicephalus appendiculatus, Hyalomma marginatum rufipes, Rhipicephalus microplus, Rhipicephalus follis, Rhipicephalus gertrudae and Hyalomma truncatum. The most frequently reported tick-borne pathogens across the provinces included Babesia bigemina, Babesia bovis, and Anaplasma marginale, with Eastern Cape Province accounting for most of the records followed by KwaZulu-Natal and Mpumalanga Provinces. The findings of this review confirm that cattle reared by smallholder farmers harbour various ticks and tick-borne pathogens of veterinary, public health and economic importance, and regular monitoring of tick infestations in South Africa is recommended to avoid disease outbreaks.

Graphical abstract

Image 1

Highlights

• A systematic review of ticks and tick-borne pathogens of cattle reared by smallholder farmers in South Africa.

• A total of 26 tick species belonging to 7 genera were reported in the reviewed articles.

• The most frequently reported tick species were Rhipicephalus (Boophilus) decoloratus and Rh. evertsi evertsi.

• The most frequently reported tick-borne pathogens were Babesia bigemina, B. bovis and Anaplasma marginale.

• Eastern Cape Province accounted for most of the tick-borne pathogen reports.

Keywords

Cattle
Smallholder farmers
Ticks
Tick-borne pathogens
==== Body
pmc1 Introduction

Tick infestation and tick-borne pathogens cause major challenges for farmers in the villages. They account for a huge global economic loss that is estimated at US$30 billion, US$160 million in Africa and US$29 million in South Africa annually (Dold and Cocks, 2001; Mapholi et al., 2014; Nyangiwe et al., 2018). Ticks are of primary importance in animal and human health because of the role they play in transmitting various disease-causing pathogens (Abubakar et al., 2018). They are obligate blood-feeders and vectors of pathogens that affect 80% of the world’s cattle population and rank first as disease transmitters in animal production (Solomon and Tanga, 2020). At present, there are approximately 970 tick species that have been identified globally, of which ∼750 are hard ticks (Ixodidae) and ∼218 are soft ticks (Argasidae), with only one species belonging to the Nuttalliellidae (Dantas-Torres, 2018; Dantas-Torres and Otranto, 2022). A total of 83 ixodid tick species have been reported in Southern Africa of which 22 are endemic to the region (Horak et al., 2018).

As of August 2023, there were approximately 12.2 million head of cattle in South Africa (DALRRD, 2023). Previous indicators show that 60% of the cattle in South Africa are owned by commercial farmers while 40% are owned by communal and emerging farmers (DAFF, 2019). The poorly resourced and communal farmers keep indigenous beef cattle mainly on natural pastures to meet a range of needs, such as the production of milk, meat, manure, and income generation (Bester et al., 2003; Mkwanazi et al., 2020). Animals in these communal farming systems are exposed to ticks, which has economic implications, affecting production by causing conditions which include, allergy, irritation, paralysis and destruction to genitalia, hides and teats (Jongejan and Uilenberg, 2004). Additionally, ticks cause major losses in cattle production by reducing productivity and fertility, and result in mortality (Kaufman et al., 2011). Bell-Sakyi et al. (2004) reported that the most economically important genera of tick-borne pathogens responsible for infecting cattle in communal areas are Anaplasma spp., rickettsiae, Ehrlichia spp., and the protozoan parasites Theileria spp. and Babesia spp.

Communal farmers have limited access to veterinary services and information about prevention and treatment of tick-borne pathogens, but they can identify diseases in their indigenous language (Chakale et al., 2022). They mainly rely on traditional medicine to combat the constraints of ticks and tick-borne pathogens because of the costs of and reach to veterinary drugs and services, respectively (Hlatshwayo and Mbati, 2005; Hesterberga et al., 2007). In South Africa, there are government initiatives where acaricides are sourced for communal farmers and cattle dip tanks are provided to the community. However, in most African countries this initiative still puts emerging farmers from rural communities at risk due to ticks acquiring resistance to these acaricides (Bell-Sakyi et al., 2004; Githaka et al., 2022).

Studies conducted in South Africa indicated that rickettsiae, Anaplasma spp., Ehrlichia spp. (formerly Cowdria), Babesia spp. and Theileria spp. are pathogens prevalent in cattle from Limpopo, North-West, Gauteng, Free State, Mpumalanga and coastal regions of KwaZulu-Natal and the west of Eastern Cape provinces (Marufu, 2008; Horak et al., 2018). According to our knowledge, there is a need to investigate and summarise the findings reported on ticks and tick-borne pathogens of cattle reared by smallholder farmers in South Africa. Thus, the objective of this systematic review was to provide information on the documented ticks and tick-borne pathogens identified in South Africa from 1983 to 2023 focusing on smallholder farming systems.

2 Materials and methods

2.1 Literature search

A systematic search of literature from January 1983 to March 2023 was conducted from various databases by three authors (KSM, MBL, DPM) independently as per the PRISMA guidelines (Page et al., 2021). Various research databases and internet search engines, such as Google Scholar, Science Direct, University of South Africa LibSearch and NETD were identified and selected for sourcing of information. Keywords such as “Tick identification”, “Morphology”, “Molecular”, “Tick characterization”, “Tick-borne pathogens”, “Communal cattle production”, and “Village cattle production in South Africa” were used for information search, and they were used individually or in combination using Boolean operators “AND”, “OR” and “NOT”.

2.2 Inclusion and exclusion criteria

The eligibility of every article was assessed based on the pre-set criteria, which included targeting research articles, systematic review articles, and academic resources (MSc and PhD theses), that included ethical considerations in their studies. The records were screened based on the questions: (i) Is the article written in English, peer-reviewed and published between January 1983 and March 2023? (ii) Did the study report ticks and tick-borne pathogens in rural areas? (iii) Is the sample population well-defined in the study? (iv) Did the study report on samples collected from cattle? The review excluded all articles not written in English, not peer-reviewed, with unclear sample information, and published before 1983. The disagreements among the authors were managed by re-checking and re-validation of articles. All eligible studies that screened for ticks and tick-borne pathogens using morphology-based and molecular approaches were included. The search results were narrowed to 23 articles. The generated data were compiled and analysed using Microsoft Excel 2016.

3 Results

3.1 Outcomes of the literature search

The systematic search produced a total of 11,200 articles from Google Scholar, followed by 1944 (Science Direct), 152 (UNISA Libsearch) and 112 (NEDT) which resulted in a total of 13,408 articles, including duplicate articles, peer-reviewed articles, theses, books, and reports. The articles were screened against eligibility criteria and a total of 13,242 records were excluded, comprising duplicates, papers not written in English, studies published before 1983 and studies not conducted in South Africa. Mendeley was used as a reference manager and a tool to filter the duplicates. A total of 166 articles were scanned using title and abstract to determine possible eligibility and 9 articles were excluded, leaving 157 articles considered for full-text review; of these, 95 articles were later excluded. Only relevant articles (n = 62) were chosen and downloaded for full evaluation. Of these, 39 were removed because they did not focus on ticks and tick-borne pathogens of village cattle and/or the samples used in the studies were not collected in South Africa. Thus, a total of 23 eligible articles were subjected to qualitative synthesis and thus included in the review (Fig. 1).Fig. 1 PRISMA flow diagram for the article selection process.

Fig. 1

The results of this study summarized in Table 1 show that the reviewed studies covered all nine South African provinces. However, in 23 studies ticks were identified in seven of the nine South African provinces except for two (Western Cape and Northern Cape). Moreover, 19 tick-borne pathogens were identified in all provinces.Table 1 Characteristics of the articles included in the review.

Table 1Province	Sample type	Method of tick identification/tick-borne pathogen detection	Tick species	Pathogen species	Reference	
Free state	Blood	Molecular	None	A. bovis, A. marginale, B. bigemina, B. bovis, Ehrlichia sp. (Omatjenne), Th. taurotragi	Mtshali et al. (2013)	
Eastern Cape, Free State, Kwa-Zulu Natal	Ticks	Molecular	Am. hebraeum, Rh. appendiculatus, Rh. decoloratus, Rh. evertsi evertsi	A. marginale, Babesia sp., C. burnetii, E. ruminantium, Rickettsia sp., Theileria sp.	Guo et al. (2019)	
Mpumalanga, North-West	Ticks	Morphology	Hy. marginatum rufipes, Hy. truncatum, Rh. appendiculatus, Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. microplus, Rh. simus, Rh. tricuspis, Rh. zambeziensis	None	Bryson et al. (2002)	
Free State, Eastern Cape, Kwa-Zulu Natal, Mpumalanga	Ticks	Morphology & molecular	Am. hebraeum, Hy. marginatum rufipes, Rh. appendiculatus, Rhipicephalus sp., Rh. evertsi evertsi, Rh. (Bo) decoloratus	A. phagocytophilum, C. burnetii, E. ruminantium, Rickettsia sp.	Mtshali et al. (2016)	
North-West	Ticks	Morphology	Am. hebraeum, Ha. elliptica, Hy. rufipes, Hy. truncatum, I. pilosus group, I. rubicundus, Ma. winthemi, Rh. appendiculatus, Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. follis, Rh. gertrudae, Rh. (Bo.) microplus, Rh. cf. pravus, Rh. sulcatus, Rh. zambeziensis, Rh. simus	None	Spickett et al. (2011)	
Mpumalanga	Blood, ticks	Serology & Morphology	Am. hebraeum, Hy. marginatum rufipes, Rh. appendiculatus, Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. (Bo.) microplus, Rhipicephalus sp.	Anaplasma sp., B. bigemina, B. bovis	Rikhotso et al. (2005)	
Free State	Blood, ticks	Giemsa-stained blood smears & Serology	Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. follis, Rh. gertrudae, Rh. warburtoni	A. marginale, B. bigemina	Mbati et al. (2003)	
Limpopo	Ticks	Morphology & molecular	Am. hebraeum, Rh. (Bo.) decoloratus	R. africae	Halajian et al. (2016)	
Free State	Ticks	Morphology	Hy. marginatum rufipes, Hy. truncatum, I. rubicundus, Ma. winthemi, O. megnini, Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. follis, Rh. gertrudae, Rhipicephalus sp.	None	Dreyer et al. (1998a)	
Eastern Cape	Ticks	Morphology	Hyalomma sp., Rh. appendiculatus, Rh. (Bo.) decoloratus, Rh. evertsi evertsi	None	Marufu et al. (2011)	
Eastern Cape	Ticks	Morphology & molecular	Am. hebraeum, Hy. marginatum rufipes, Rh. appendiculatus, Rh. evertsi evertsi, Rh. sanguineus (s.l.)	Ehrlichia sp.	Iweriebor et al. (2017)	
Mpumalanga	Ticks	Morphology & molecular	Am. hebraeum	R. africae	Mazhetese et al. (2022)	
Eastern Cape	Blood, ticks	Serology & Morphology	Hyalomma sp., Rh. appendiculatus, Rh. (Bo.) decoloratus, Rh. evertsi evertsi	A. marginale, B. bigemina, B. bovis	Marufu (2008)	
Eastern Cape	Blood, ticks	Serology & Morphology	Am. hebraeum, Hy. rufipes, Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. microplus	A. marginale, B. bigemina, B. bovis, E. ruminantium	Yawa et al. (2021)	
Free State	Ticks	Morphology	Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. follis, Rh. gertrudae, Rh. warburtoni	None	Mtshali et al. (2013)	
Free State, Eastern Cape, Gauteng, Limpopo, Kwa-Zulu Natal, Mpumalanga, North-West, Northern Cape, Western Cape	Blood	Molecular	None	B. bigemina, B. bovis	Mtshali and Mtshali (2013)	
Free state	Blood	Serology	None	A. marginale, B. bigemina, B. bovis	Dreyer et al. (1998b)	
Kwa-Zulu Natal	Blood	Molecular	None	B. bigemina, B. bovis, B. rossi, Th. mutans, Th. parva, Th. taurotragi, Th. velifera, Theileria sp. (sable), T. theileri, T. vivax	Yusufmia et al. (2010)	
Limpopo, Gauteng	Ticks	Morphology & molecular	Amblyomma sp.	R. africae	Mhlambo et al. (2023)	
North-West	Ticks	Morphology & molecular	Am. hebraeum	R. africae	Thekisoe et al. (2023)	
Eastern Cape	Ticks	Morphology & molecular	Am. hebraeum, Rh. (Bo.) microplus, Rhipicephalus sp.	R. africae	Pillay and Mukaratirwa (2020)	
Kwa-Zulu Natal, Eastern Cape, Gauteng, Limpopo, Northern Cape, Mpumalanga, Western Cape North-West	Blood	Molecular	None	A. marginale	Mutshembele et al. (2014)	
Free State, Eastern Cape, Gauteng, Limpopo, Kwa-Zulu Natal, North-West, Mpumalanga, Northern Cape	Blood	Serology	None	B. bigemina, B. bovis	Terkawi et al. (2011)	
Abbreviations: Am, Amblyomma; A, Anaplasma; B, Babesia; Bo, Boophilus; C, Coxiella; E, Ehrlichia; Ha, Haemaphysalis; Hy, Hyalomma; I, Ixodes; Ma, Margaropus; O, Otobius; Rh, Rhipicephalus; R, Rickettsia; Th, Theileria; T, Trypanosoma.

3.2 Sample types collected to identify ticks and detect tick-borne pathogens

The present review indicates that studies on ticks and tick-borne pathogens have been conducted in all the provinces of South Africa (Western Cape, Free State, Eastern Cape, Gauteng, Kwa-Zulu Natal, Limpopo, Northern Cape, North-West and Mpumalanga). These studies used different sample types to detect tick-borne pathogens and identify ticks obtained from cattle reared by smallholder farmers. As indicated in Fig. 2, out of 23 articles, in 13 (56.5%) of the studies ticks were collected to identify tick species and tick-borne pathogens, whereas in 6 (26.1%) and 4 (17.4%) of the studies, respectively, blood and/or a combination of both blood and tick samples were collected for tick-borne pathogen detection.Fig. 2 Distribution of included articles per sample types used.

Fig. 2

Fig. 3 Distribution of included articles per methods used to detect tick-borne pathogens.

Fig. 3

3.3 Methods of tick identification and tick-borne pathogen detection used

The results of the present review indicate that 17 studies used both molecular and morphological methods to identify ticks whereas some of the studies used either of the two methods. As illustrated in Figs. 3, 66.7%, 27.8% and 5.6% of the studies used molecular, serology or a combination of serology and Giemsa-stained blood smears methods to detect tick-borne pathogens, respectively.

3.4 Ticks in smallholder farming systems

The included articles report a total of 26 tick species, with the most frequently identified ticks in South Africa being Rhipicephalus (Boophilus) decoloratus (n = 12) and Rhipicephalus evertsi evertsi (n = 12). These were followed by Amblyomma hebraeum (n = 10), Rhipicephalus appendiculatus (n = 8), Hyalomma marginatum rufipes (n = 7), Rhipicephalus microplus (n = 5), Rhipicephalus follis, Rhipicephalus gertrudae and Rhipicephalus sp. (n = 4 each), and Hyalomma trancatum (n = 3) (Fig. 4). The rest of the ticks were identified in either one or two studies. The study that reported the greatest number of tick species is that by Spickett et al. (2011) (n = 19), followed by Dreyer et al. (1998a) (n = 10), Bryson et al. (2002) (n = 9) and Rikhotso et al. (2005) (n = 7). Additionally, as indicated in Table 1, special cases of uncommon ticks in South Africa were reported in some provinces. Thus, Otobius megnini and Rhipicephalus warburtoni were found in the Free State Province, and Ixodes pilosus group, Haemaphysalis elliptica and Rhipicephalus sulcatus were identified in the North-West Province. Furthermore, North-West and Free State provinces shared cases of Margaropus winthemi and Ixodes rubicundus.Fig. 4 Tick species identified in the studies included in the review.

Fig. 4

3.5 Tick distribution on host body

Nine studies provided information about tick location on host body. These reports showed that ticks mainly attach to four regions: inside the ears, on abdomen and perineum, and under the tail (Fig. 5). One study found ticks on the vegetation (Rikhotso et al., 2005, Fig. 5).Fig. 5 Tick distribution per location on host in the studies included in the review.

Fig. 5

3.6 Tick-borne pathogens

Out of the nine South African provinces, the Free State Province had the most diverse list of tick-borne pathogens at 24.75%, followed by Eastern Cape (22.77%), KwaZulu-Natal (18.81%) and Mpumalanga provinces (7.92%). Western Cape Province had the least diverse list of tick-borne pathogens at 2.97%. As shown in Fig. 6, the most frequently reported tick-borne pathogens across the provinces include Babesia bigemina (n = 23), Babesia bovis (n = 21), and Anaplasma marginale (n = 15). The study by Yusufmia et al. (2010) detected the largest number of tick-borne pathogens (n = 10), followed by Guo et al. (2019) (n = 6), Mtshali et al. (2013) (n = 5), Mtshali et al. (2016) and Yawa et al. (2021) (n = 4 each). The rest of the reviewed studies detected less than 16% of the pathogens per study. In the Free State Province, the most dominant pathogens were A. marginale, B. bigemina and B. bovis followed by separate cases of Anaplasma sp. (Omatjenne) (formerly Erhlichia) and Theileria taurotragi (Dreyer et al., 1998b; Mbati et al., 2003; Mtshali et al., 2013). The most dominant pathogens in Eastern Cape Province were also B. bigemina, A. marginale and B. bovis with isolated cases of Rickettsia africae and Ehrlichia spp. (Pillay and Mukaratirwa, 2020; Iweriebor et al., 2017; Marufu, 2008). Limpopo, North-West and Mpumalanga provinces were mainly dominated by R. africae (Halajian et al., 2016; Mazhetese et al., 2022; Thekisoe et al., 2023).Fig. 6 Distribution of tick-borne pathogens per province.

Fig. 6

4 Discussion

This systematic review succeeded in identifying research papers that detected and identified ticks and their associated pathogens affecting smallholder farms in South Africa. A total of 26 tick species belonging to seven genera were reported in the included articles based on samples collected from cattle in communal farms. The findings of this review are consistent with distributions reported in the literature as reviewed by Makwarela et al. (2023).

Most studies included in this review targeted either tick or blood samples, while a few studies employed both sample types. The choice of sample type to use in a study depends on many factors including the assay procedure, ease of sample collection, type of study, etc. (Vaught and Henderson, 2011). In most cases, the choice of sample type is based on the aim of the study, tests to be used in the investigation, and whether the sample type will help to achieve the objectives of the study. The use and/or collection of several sample types, e.g. ticks, blood, etc. where feasible, makes it possible to investigate further if there is any inconclusive or interesting hypothesis. As signified by the sample type used in the included articles, morphological and/or molecular assays were the most frequently used in the studies. Typically, microscopy/morphological methods as well as culture-based and serology are used to identify ticks and detect tick-borne pathogens (Clay and Fuqua, 2010). While morphological evaluation of ticks can help in identifying ticks to a given taxonomic level (species, genus, family), they have some limitations and are insufficient in identifying immature and/or engorged ticks, physically damaged specimens, as well as differentiating between closely related species (Ledwaba et al., 2022; Paguem et al., 2023).

The use of molecular assays has contributed greatly to the studies investigating ticks and tick-borne pathogens since their efficacy allows characterization of species to the genus and/or species level targeting varying conserved regions (Clay et al., 2008), although they also have some setbacks. Recent studies (Viljoen et al., 2021; Mazhetese et al., 2022; Intirach et al., 2023) used morphological assays in combination with molecular tests, and this has proven to be beneficial as the results from both assays were shown to complement each other for definitive identification. Most of the reviewed studies utilized molecular approach to detect tick-borne pathogens, as compared to other methods. Molecular methods based on polymerase chain reaction have improved diagnostic and analytical specificity and sensitivity ensuring that most of the pathogens are detected. The studies that have employed the molecular methods succeeded in detecting tick-borne pathogens (Thekisoe et al., 2020; Mapholi et al., 2022; Heylen et al., 2023).

The tick prevalence determined in this review shows that species of Rhipicephalus, especially Rh. (Bo) decoloratus and Rh. evertsi evertsi were the most frequently identified species in the included studies. Rhipicephalus evertsi evertsi occurs throughout South Africa and is recorded in all the seasons, therefore, its high prevalence was expected due to its distribution and seasonal activities (Fivaz and De Waal, 1993; Yawa et al., 2019). Rhipicephalus (Bo.) decoloratus has been reported to attach to every part of the cattle host body (Baker and Ducasse, 1967). This might be one of the reasons why this tick was the most frequently recorded species as it stands a high chance of being collected and detected.

Tick-borne pathogens were detected in all of the South African provinces; however, Free State Province showed the highest prevalence compared to other provinces. This might be due to the fact that the majority of the articles analysed here were conducted using samples collected from the Free State Province. Generally, the occurrence of tick-borne pathogens in cattle depends mainly on the presence and distribution of tick vectors (de Vos, 1979). In South Africa, B. bigemina is transmitted by Rh. (Bo.) microplus, Rh. evertsi evertsi and Rh. (Bo.) decoloratus (de Vos and Potgieter, 1994). As one of the most frequently identified tick species in this review, Rh. evertsi evertsi might have contributed to the occurrence of B. bigemina. Similar findings were observed in a study by Thekisoe et al. (2020) who reported B. bigemina as one of the most prevalent protozoan parasites in cattle. Anaplasma marginale is transmitted by Rh. evertsi evertsi, Rh. (Bo.) decoloratus, R. (Bo.) microplus, and Hy. marginatum rufipes (De Waal, 2000); these are among the five most frequently reported tick species recorded in this review. Due to the number of ticks involved in the transmission of A. marginale, it is not surprising that this pathogen was among the most detected in this review.

Rhipicephalus (Bo.) decoloratus and Rh. evertsi evertsi together with Rh. (Bo.) microplus and Rh. appendiculatus are of veterinary importance as they are members of the genus Rhipicephalus known to transmit tick-borne pathogens in Southern Africa as well as in the Southern Africa Development Community (SADC) region (Horak et al., 2017; Jongejan and Uilenberg, 2004). Horak et al. (2009), reported that the invasive Asian tick Rh. (Bo.) microplus has displaced Rh. (Bo.) decoloratus in most regions of the Eastern Cape Province. This displacement was further reported in subsequent studies that collected samples from cattle in communal farms (Spickett et al., 2011; Nyangiwe et al., 2013). Both species are one-host ticks and known vectors of pathogens such as B. bigemina and/or B. bovis as well as A. marginale, which cause severe infections in cattle (Madder et al., 2007). In addition, the pathogens were reported to result in high mortality in infected cattle (de la Fuente et al., 2023). Moreover, Rh. appendiculatus is a known vector of Th. parva, the pathogenic and most economically significant organism causing theileriosis in cattle in the central, eastern and southern regions of Africa (Perry et al., 1991; Norval et al., 1992). Additionally, most Rhipicephalus spp. are known vectors of species of Babesia, Ehrlichia, Rickettsia, and Theileria, causing diseases to humans, livestock and companion animals (Mucheka et al., 2023).

Aspects such as the host body site preference, morphological features, geographical locality, season, and ecological requirements are important in the identification and differentiation of tick species (Madder et al., 2013). The host body sites on which ticks are collected tend to stipulate the type of ticks that may be found and may also play a role in influencing the number of reported tick species in South Africa. Ticks such as Rh. (Bo.) decoloratus attach to the whole body of the host (Baker and Ducasse, 1967). On the contrary, some tick species target particular locations on cattle, for instance, the brown ear tick (Rh. appendiculatus) prefers to feed around and inside the ear of the host. This tick was also amongst the most frequently reported tick species identified in this review, and this might be associated with the high number of ticks collected from the ears in the included articles. Thus, the tick collection strategy used in cattle, i.e. the targeted host’s body parts, can lead to biases if not employed correctly.

Ticks are known to have a parasitic relationship with vertebrate animals, and they spend much of their time in their habitats waiting for susceptible hosts. The life-cycles and longevity of ticks are determined by factors such as landscape, temperature, rainfall and humidity (Grigoryeva and Shatrov, 2022). This is in agreement with a study conducted in the Eastern Cape Province by Marufu (2008), which reported that the tick prevalence varied due to seasons, with more ticks being more prevalent in the wet season (from November to March) than in months that are cool/dry (May to July). Moreover, these authors also indicated that ticks were prevalent due to the availability of hosts, warm season and type of vegetation in the area. Yawa et al. (2018) found that the more abundant vegetation and hot weather, the greater the number of ticks will be found in the area. Another study observed higher tick counts in September–February, representing the hot-dry and hot-wet seasons (Mapholi et al., 2022). The majority of the reviewed articles did not indicate the season during which sampling took place, which is a limitation in many studies as the prevalence of ticks varies per season. Limpopo Province is one of the hottest provinces in South Africa (Phophi et al., 2020); however, some regions experience a cold winter season which can result in a lower prevalence of tick infestation. One would expect the prevalence of ticks in this province in the reviewed studies to be high compared to provinces such as Eastern Cape Province. However, this was not the case, and several factors might have played a role including, among others, the number of studies considered in this review, the sampling season, etc. Therefore, without information on the season at the time of sample collection, it becomes difficult to conclude whether the prevalence shown in the reviewed papers was high or low when comparing the provinces.

Ticks are known vectors of viral, bacterial and protozoan pathogens causing diseases in various hosts. They rank second to mosquitoes as pathogen vectors and are known to greatly impact human and animal health in farms and communal areas (Guo et al., 2019). This review reported seven genera of pathogens such as Anaplasma, Babesia, Coxiella, Ehrhlichia, Rickettsia, Theileria, and Trypanosoma. Piroplasm parasites of the genera Babesia and Theileria can affect various domestic and wild hosts, causing emerging and already established diseases such as babesiosis and theileriosis, respectively. Ricketssia africae, a causative agent of endemic tick-borne rickettsiosis, was reported in most studies in the review. This bacterium is transmitted by Am. hebraeum and causes African tick-bite fever in humans (Ledger et al., 2022). A review conducted by Lilak et al. (2024) also reported R. africae as the most frequently reported bacterium in studies carried out in six countries in sub-Saharan Africa (Chad, Djibouti, Ethiopia, Kenya, Tanzania, and Uganda).

5 Conclusions and recommendations

In conclusion, accurate identification of ticks is at the centre of understanding the epidemiology of tick-borne pathogens and developing more effective control strategies. Morphological identification of ticks is the traditional method which is based on the phenotypic traits of ticks followed by a combination of microscopic and molecular methods (Wanjira, 2015). This review showed that cattle in rural areas of South Africa are parasitized by a diverse range of tick species. Moreover, it showed that Rh. (Bo.) decoloratus, Rh. evertsi evertsi, Rh. appendiculatus and Am. hebraeum are the tick species prevalent in domestic cattle in South Africa. These ticks are associated with several pathogens such as R. africae, E. ruminantium, B. bigemina, B. bovis, A. marginale and Th. parva which were also detected in the reviewed papers and cause challenges to already strained farmers in the smallholder farming systems.

The present systematic review explored the data on ticks and tick-borne pathogens of cattle kept by smallholder farmers of all the nine provinces of South Africa and the findings suggest that ticks and tick-borne pathogens are a problem in smallholder farming system. Therefore, there is a need for this information to reach the affected farmers in sampled areas and education should be provided regarding ticks and tick-borne pathogens affecting their farming production. The South African Government needs to provide more intervention and enough extension officers to facilitate and train the village farmers on ticks and tick-borne pathogens and their effects. This education will help them understand the relationship between ticks and their cattle which will improve their production.

Funding

This study was financially supported by the 10.13039/501100008227 University of South Africa , Johannesburg, South Africa.

Ethical approval

Not applicable.

CRediT authorship contribution statement

Katleho Sechaba Monakale: Investigation, Methodology, Formal analysis, Writing – original draft, Funding acquisition. Maphuthi Betty Ledwaba: Investigation, Methodology, Formal analysis, Writing – review & editing. Rae Marvin Smith: Writing – review & editing, Supervision. Realeboga Masego Gaorekwe: Writing – review & editing, Supervision. Dikeledi Petunia Malatji: Conceptualization, Investigation, Methodology, Formal analysis, Writing – review & editing, Supervision.

Declaration of competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data availability

The data supporting the conclusions of this article are included within the article.

Acknowledgements

The authors acknowledge the financial support by the 10.13039/501100008227 University of South Africa .
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