DOI 10.1007/s10493-010-9390-8 Rhipicephalus (Boophilus) microplus: a most successful invasive tick species in West-Africa M. Madder E. Thys L. Achi A. Touré R. De Deken Received: 20 April 2010 / Accepted: 15 July 2010 Ó Springer Science+Business Media B.V. 2010 Abstract The cattle tick Rhipicephalus (Boophilus) microplus is known to be a highly reproductive and efficient vector of Babesia bovis, two characters which make this tick a threat to livestock keeping in many continents. The authors identified this tick in Ivory Coast, West Africa, in 2007, and hypothesized the spread to be minimal, as this tick was not observed in previous years. To determine the extent of its distribution and to a lesser extent the possible impact of the tick on the livelihoods of Ivorian smallholders, a crosssectional survey was carried out in the Abidjan and Agboville Departments of Ivory Coast, in April 2008. The results of the study reveal that the newly introduced tick has almost completely displaced all indigenous Rhipicephalus (Boophilus) species in the study area and gave rise to unsuccessful tick control, inappropriate pesticide use, loss of milk production and even increased mortality in dairy cattle. Keywords Rhipicephalus (Boophilus) microplus Displacement Babesia bovis Acaricides Importation Introduction Rhipicephalus (Boophilus) microplus, the pantropical blue tick, is without any doubt one of the most important disease vectors of livestock in the world, mainly because of its large geographical distribution, and its ability to transmit redwater or babesiosis, caused by Babesia bovis and B. bigemina (Coetzer and Tustin 2004), as well as anaplasmosis. This tick species originates from Asia but during the latter half of the nineteenth century it, and the diseases it transmits, were spread by cattle transport to Australia, Madagascar, M. Madder (&) E. Thys R. De Deken Department of Animal Health, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium e-mail: mmadder@itg.be L. Achi A. Touré Laboratoire National d Appui au Développement Agricole (LANADA), 4 Bp 612, Abidjan 4, Ivory Coast
South Africa, Latin America, Mexico and the United States (Hoogstraal 1956; Temeyer et al. 2004). Rhipicephalus (Boophilus) microplus was eradicated from the US in 1943 through the costly Cattle Fever Tick Eradication Program, which started in 1906. The most resistant strain studied to date has been shown to survive the dipping procedure used at the US Mexico border as part of an import barrier to prevent the reentry of B. microplus into the United States (Temeyer et al. 2004). Until recently B. microplus was not present in West Africa, but the tick has unfortunately been introduced into Ivory Coast (Madder et al. 2007). This paper describes a survey conducted in April 2008, around Azaguié, about 50 km north of Abidjan, Ivory Coast, to determine the impact of this introduction in and around a dairy cattle project, previously funded by the Belgian Technical Cooperation, and with the aim of looking at possible control measures. Materials and methods Study area The sampling took place between 8 and 17 April 2008, about 1 year after the first discovery of R. (B.) microplus in Ivory Coast (Madder et al. 2007). Samples were taken from livestock hosts in a radius of 50 km around Azaguié, the village from which R. (B.) microplus ticks were first recorded on four different dairy farms early 2007. These farms are all linked to the Projet d appui au développement de la production laitière dans le sud de la Côte d Ivoire (Lait sud), an Ivorian Belgian project to support dairy farms in the Azaguié area. In total 10 farms supported by the project were sampled (farms 1 to 6, farm 8, farm 10 and farms 12 to 13 see Table 1 and Fig. 1) as well as 4 commercial livestock breeding farms (farms 7, 11, 14 and 16), 6 traditional agropastoral farms (9, 17, 18, 19, 20 and 23), 1 quarantine farm (15) and 3 farms of sedentary pastoralists (farm 21, 22 and 24) with Zebu and/or Ndama cattle. Tick collection In each of the farms, as indicated in Table 1, between two and five bovines were sampled and between one and three small ruminants if present. The whole body was sampled, taking care to collect also the small R. (Boophilus) males as they contribute significantly to an accurate identification. On animals with a very high tick burden (mainly R. (Boophilus) and Amblyomma spp.), only a fraction of all ticks was collected due to time constraints. The ticks were removed with forceps and stored in vials containing 70% alcohol until identification. For each animal sampled an individual vial was used and a label containing date, farm, species, sex and age of the host was included in the vial. A short questionnaire was filled out during the visit. The main questions related to acaricide use, tick problems including resistance, disease occurrence, and origin of the animals. The geographic coordinates of each farm were registered using a hand-held GPS-receiver. Tick identification All adult ticks were identified up to species level using a stereo-microscope (Zeiss Stemi 2000). For the identification of the different R. (Boophilus) species, a microscope (Zeiss
Table 1 Collection sites, dates and animals sampled Nr. Geo-reference Date of collection Number of animals Longitude Latitude Bovines Small ruminants Number sampled Bovines Small ruminants 1-4.07059 5.66115 4/8/08 12 0 2 0 2-4.06948 5.65819 4/8/08 18 0 2 0 3-4.06971 5.66033 4/8/08 10 0 2 0 4-4.05999 5.64911 4/8/08 9 0 2 0 5-4.15701 5.62195 4/8/08 9 0 2 0 6-4.05621 5.61340 4/9/08 15 0 2 0 7-4.03064 5.67206 4/9/08 10 0 2 0 8-4.03360 5.64139 4/9/08 13 0 2 0 9-4.17985 5.34811 4/9/08 13 11 2 3 10-4.00285 5.65568 4/10/08 15 0 2 0 11-4.00718 5.61610 4/10/08 197 10 2 3 12-4.09432 5.65505 4/10/08 34 4 2 2 13-4.11760 5.61404 4/10/08 12 0 2 0 14-4.08593 5.58592 4/10/08 91 0 3 0 15-3.87363 5.36231 4/11/08 8 10 3 0 16-3.87269 5.36581 4/11/08 86 0 5 0 17-4.08081 5.54809 4/14/08 20 10 3 0 18-4.04017 5.56421 4/14/08 10 0 0 0 19-3.78291 5.58999 4/15/08 31 0 3 0 20-3.73063 5.51736 4/15/08 35 0 4 0 21-4.30203 6.06591 4/16/08 21 0 4 0 22-4.22637 5.93609 4/16/08 21 0 5 0 23-4.35392 5.31774 4/17/08 44 3 3 1 24-4.36192 5.33073 4/17/08 70 0 2 0 Axioscope) at magnification 1009 was used especially for the visualization of the hypostome dentition and presence or absence of the ventro-internal protuberance bearing setae. Immature stages of this genus were only identified up to genus level. Results Tick collection In total 4,544 ticks were collected from 3 sheep and 81 cattle. Eighteen percent of the ticks were found to be Amblyomma variegatum, 54% Rhipicephalus (Boophilus) microplus, 1% Rhipicephalus (Boophilus) decoloratus, 1% Rhipicephalus (Boophilus) geigyi, 22% Rhipicephalus (Boophilus) spp. (ticks that could not be identified because of damaged mouthparts or being immature), 2% Rhipicephalus lunulatus, 1% Rhipicephalus senegalensis, while only a few specimens of Rhipicephalus muhsamae, Rhipicephalus ziemanni and Haemaphysalis parmata were found.
Fig. 1 Distribution of Rhipicephalus (Boophilus) spp. around Azaguié, Ivory Coast. Collection sites are only shown on the first map Rhipicephalus (Boophilus) microplus was present on 19 out of 23 farms (Fig. 1). All of the dairy farms, situated around Azaguié, were infested. Only the agropastoral farms south of Azaguié and eastwards towards Alepe did not harbour any R. (B.) microplus. On about half of the R. (Boophilus)-infested farms (10 out of 19) R. (B.) geigyi was found but in extremely low numbers (2.6% of the total number of identified R. (Boophilus) spp.). Only on one of the farms (23), the three R. (Boophilus) spp. were present, but R. (B.) microplus was always predominant. On two farms (14 and 19), only a few specimens of either R. (B.) geigyi or R. (B.) decoloratus were collected and no R. (B.) microplus. Only 1.5% of the total number of identified R. (Boophilus) spp. belonged to R. (B.) decoloratus. Rhipicephalus (B.) annulatus was not found in the collections. Acaricide use Most farmers in the region around Azaguié intensively use acaricides, especially during the rainy season in heavily infested areas, where cattle are treated once and sometimes twice a week. During the rest of the year acaricides are applied on the cattle once to thrice a month.
Traditional farmers most frequently use spray-formulations of alpha-cypermethrin (Dominex), amitraz (Antitique, Vestos, Abotik) and deltamethrin (Vectocid). More professional breeders (farm 14 and 16) often use pour-on formulations of flumethrin (Bayticol) or cypermethrin. A worrying phenomenon in the region is the irresponsible use of agrochemical insecticides on livestock. It appears that fenitrothion (Fenical 500 EC) alone or as a mixture with deltamethrin (Decis) and even pirimiphos-methyl (Actellic) is regularly used to control ticks on dairy cattle. These aberrations are in response to the massive challenge by R. (B.) microplus, the apparent acaricide resistance of these ticks and livestock losses due to tick-borne diseases. Many farmers were not aware of withdrawal times for milk after application of insecticides on dairy cattle. Discussion The introduction of R. (B.) microplus in Ivory Coast as reported by Madder et al. (2007) appears to be more widespread as expected. It had been hypothesized that the spread of these ticks would be limited and localized around the farms of the project Lait sud, allowing eradication. Earlier surveys undertaken in 2005 and 2006 on the project and surrounding farms, as part of a PhD thesis, did not reveal any single R. (B.) microplus tick (Betschart, personal communication). The present study indicates that the majority of the R. (Boophilus) spp. collected and identified in this study consists of R. (B.) microplus (96%); R. (B.) decoloratus (1.5%) and R. (B.) geigyi (2.5%) seem to be displaced almost completely. The fast and almost complete displacement of local R. (Boophilus) spp. by R. (B.) microplus was also observed in Eastern and Southern Africa and could be the result of different factors. A higher reproductive output combined with a shorter generation length, especially in this humid and tropical forest habitat, certainly enables R. (B.) microplus to outcompete other R. (Boophilus) species. Especially in the recently established farms of the project Lait Sud, the grazing land was still unmodified vegetation with trees, shrubs and bushes creating an ideal habitat for the survival of the eggs and larvae. Also the acaricide resistance acquired by this species to most of the acaricides available on the market could have favoured the displacement (Baffi et al. 2008). Frequent but irregular acaricide use (recommendations of the National Agricultural Development Support Agency (ANADER) stipulate weekly treatment during the rainy season and twice weekly during the dry season), as a result of unsuccessful control of R. (B.) microplus population in the area, could certainly have facilitated acaricide resistance development or intensification. As a result, the more susceptible local species could simply have been eradicated chemically and not displaced biologically. The route of introduction of R. (B.) microplus into West Africa has not been identified but very likely occurred during the importation of cattle from Brazil or South Africa. Several exotic cattle breeds have been imported in many West African countries to improve livestock production during the last decades. Especially Gir and Girolando breeds from Brazil seem to be among the most popular breeds in this region. From 1980 onwards, several importations from Brazil have been organized to the centre of the country, more recently, between 2002 and 2004. Rhipicephalus (B.) microplus from both countries have been shown to possess significant acaricide resistance (Ntondini et al. 2008; Baffi et al. 2008). Because of this severe acaricide resistance, ticks may have survived acaricide treatment before exportation, if applied, in Brazil or South Africa and/or after arrival in Ivory Coast. During the collection of ticks in Ivory Coast, it was noticed that recently and frequently
treated animals still carried high loads of live ticks; severe acaricide resistance, underdosage of acaricide treatment or inappropriate application or a combination could cause the observed phenomenon. The speed, with which the replacement occurs in Ivory Coast, is alarming. If the ticks were really introduced only 3 4 years ago, the displacement has been extremely efficient. A similar displacement of R. (B.) decoloratus by R. (B.) microplus was observed in Limpopo Province South Africa (Tønnesen et al. 2004; Nyangiwe and Horak 2007) and Zambia (Berkvens et al. 1998). When historical data of Wedderburn et al. (1991) in Swaziland are compared to a study performed by Dlamini in 1995 (Dlamini 2004), a significant increase in occurrence of R. (B.) microplus is demonstrated. Furthermore, more recent studies carried out between 1998 and 2001 (Lynen et al. 2008) show the extended distribution range of this tick in all the northern regions of Tanzania. Considering the equatorial climate in Azaguié, Ivory Coast, R. (B.) microplus should be able to cycle continuously throughout the year with a minimum of 4 generations. According to Tønnesen et al. (2004), displacement would only take between 4 and 10 generations. Thus replacement in the Azaguié region might easily be completed within 2 years. The further spread of the tick, known to feed preferentially on cattle, will be highly dependent on cattle movement and is difficult to determine. In a radius of 50 km, a high degree of displacement has been observed in all types of farms. These results highlight the importance of further research. One of the priorities is the estimation of the impact of R. (B.) microplus in Ivory Coast, both due to direct effect of parasitism but secondly also to disease transmission. In addition, the observed acaricide resistance will need to be determined to formulate recommendations for effective tick control. No need to emphasize the importance of a functional well managed importation and exportation service and quarantine facilities. Acknowledgments The authors would like to thank the International Consortium of Ticks and Tick-borne Diseases (ICCTD3) for its financial support of the tick survey in Ivory Coast. We also want to acknowledge the Laboratoire National d Appui au Développement Agricole (LANADA), Abidjan, Ivory Coast, for the reception of the scientific team, and for making available the help of the laboratory technicians and all other support to facilitate the tick survey in the region. Also the willingness of the farmers to exchange information and allow for the collection of the ticks from their animals is highly appreciated. References Baffi MA, de Souza GR, de Sousa CS, Ceron CR, Bonetti AM (2008) Esterase enzymes involved in pyrethroid and organophosphate resistance in a Brazilian population of Riphicephalus (Boophilus) microplus (Acari, Ixodidae). Mol Biochem Parasitol 160:70 73 Berkvens DL, Geysen DM, Chaka G, Madder M, Brandt JR (1998) A survey of the ixodid ticks parasitising cattle in the Eastern province of Zambia. Med Vet Entomol 12:234 240 Coetzer JAW, Tustin RC (2004) Infectious diseases of Livestock, 2nd edn. Oxford University Press, Southern Africa Dlamini P (2004) Seasonal occurence and distribution of ticks in Swaziland. Institute of Tropical Medicine- MSTAH Thesis, n 5 Hoogstraal H (1956) African ixodoidea. Vol. 1.Ticks of the Sudan. (With special reference to Equatoria Province and with preliminary reviews of the genera Boophilus, Margaropus and Hyalomma). Research report NM 005 050. 29.07. Department of the Navy, Bureau of Medicine and Surgery, Washington Lynen G, Zeman P, Bakuname C, Di Giulio G, Mtui P, Sanka P, Jongejan F (2008) Shifts in the distributional ranges of Boophilus ticks in Tanzania: evidence that a parapatric boundary between Boophilus microplus and B. decoloratus follows climate gradients. Exp Appl Acarol 44:147 164
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