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New data regarding distribution of cattle ticks in the south-western Indian Ocean islands
© Stachurski et al.; licensee BioMed Central Ltd. 2013
Received: 8 October 2012
Accepted: 1 August 2013
Published: 9 September 2013
Recent studies have produced new insight into the origin and distribution of some cattle ticks in the south-western Indian Ocean islands. Rhipicephalus appendiculatus, introduced from Tanzania in 2002, is now well established on Grande Comore but has not yet reached the other islands of the archipelago (Mohéli, Anjouan and Mayotte). Only one of the two clades identified in Africa has settled so far. Amblyomma variegatum, which was not supposed to be able to persist in the Antananarivo region (1300 m) nor in other Malagasy regions of high altitude without regular introductions of ticks by infested cattle, is now endemic as a general rule up to 1600 m although other regions of lower altitude (1400 m) are still free of the tick. This species remains confined in a small area of the west coast on La Reunion Island. On the contrary, Hyalomma dromedarii could not settle on Madagascar where it was introduced in 2008 and Rhipicephalus evertsi evertsi is not yet present in Grande Comore despite regular introductions by infested cattle from Tanzania. A phylogeographic approach has been carried out at an intra-specific level for A. variegatum. This study has led to the identification of two main lineages, one covering all species distribution and one restricted to East Africa and the Indian Ocean area. These two lineages are in sympatry in Madagascar where a high genetic diversity has been described, whereas a lower genetic diversity is observed on other islands. These results seem to agree with the historical data concerning the introduction of the tick in the Indian Ocean area.
Table of contents
Successful ancient introductions
Failed recent tick introductions
Successful recent tick introductions
Alteration of tick distribution
Islands of the south-western Indian Ocean (SWIO) did not host ruminants (cattle, sheep and goats, deer) before human settlement regardless whether they split from Gondwana about 150 million years ago (Madagascar) or emerged de novo as volcanoes during the last 10 million years (Mauritius, Comoros, La Reunion). Cattle introduction occurred between the Ist and Vth centuries on Madagascar, in the VIIth century on Comoros, and in the XVIIth century on the Mascarene archipelago (Mauritius, Rodrigues and La Reunion). Archaeological research carried out on Madagascar led to the discovery of cattle bones dated from the V-VIIth centuries, the shape of the investigated skulls suggesting that Bos taurus was present at that period . Zebus (Bos indicus) might have been bred on this island since at least the Xth century; it is, however, not clear whether these introductions were of Indonesian, Indian or African origin . On Mauritius, cattle were introduced at least from the middle of the XVIIIth century for the needs of the sugarcane industry, the introduction of zebus from Madagascar being documented in the early XIXth. Malagasy zebus were also introduced in La Reunion during the XVIIth and XVIIIth centuries and later crossbred with Bos taurus of European origin. Altogether, the available data suggest that the introduction of cattle on the islands of the region occurred first in Madagascar (Bos taurus followed by Bos indicus) and Comoros, and then in the Mascarene archipelago from Madagascar (Bos indicus) and from Europe (Bos Taurus).
Consequently, all cattle ticks present on these islands were introduced with their hosts after human settlement. As a result, some of the tick species have probably been present for centuries while others were introduced more recently. Tick species distribution may subsequently vary and evolve in response to cattle breeding characteristics, cattle movements or climate change. The latest data regarding the presence and distribution of cattle ticks in SWIO islands are presented below.
2. Successful past introductions
Despite the probable repeated introduction of ticks associated with centuries of regular cattle importation in Madagascar, cattle ticks were not described on the island before 1899. At that time, the presence of A. variegatum was reported both in Madagascar  and Mauritius  while it was not reported on La Reunion until 1949 . Boophilus microplus, first described under other names [4, 6] at the beginning of the XXth century on Madagascar and other SWIO islands, is presently prevalent on all islands and in all environments. Regional cattle movements between East and Southern Africa and Madagascar lasted at least until the 1960s, causing a risk of introduction of new tick species (see below) and probably maintaining some level of gene flow between African and Malagasy tick populations. Cattle importation is still common in Grande Comore (see below) whereas no cattle have been introduced on La Reunion and Mauritius for decades, limiting the risk of tick species introduction. It is unclear whether these historical differences in cattle introduction resulted in the establishment of tick populations with different genetic and physiological characteristics. This has been recently studied for A. variegatum from different countries of SWIO in comparison with populations from Africa, where this species originates, and from the Caribbean islands, where it was introduced more than two centuries ago.
At the local level, the two lineages are found in sympatry on Madagascar whereas the “worldwide” lineage is found quite exclusively on the other SWIO Islands (La Reunion, Mayotte and the Comoros Islands) (Jacquet, personal communication). A higher genetic variability (a high nucleotidic and haplotypic diversity and a positive Tajima D value) is observed on Madagascar, indicating large, stable population sizes. Whereas cattle ticks were not described on Madagascar before 1899, the introduction of A. variegatum is probably much older and concomitant with the cattle introduction on this island (see above). This ancient introduction followed by several successive re-introductions could have led to this high genetic diversity. A similar situation has been shown for the Aedes aegypti mosquito in Madagascar . Conversely, a reduced genetic variability is observed on the other islands. This can be caused by a more recent introduction of the cattle tick to these islands and by repeated genetic bottlenecks (low number of ticks introduced, less re-introductions or repeated acaricide treatments), leading to smaller population sizes more susceptible to genetic drift. On Madagascar, it has been observed that the “worldwide” lineage was present throughout the island whereas the “East African” lineage was only detected in the center and the eastern part of the island which are the areas of Madagascar with the highest rainfall (Jacquet, personal communication). It has been hypothesized that the “worldwide” lineage could have a greater ecological plasticity allowing it to thrive in more variable conditions. This could explain the predominance of ticks belonging to this lineage on other islands of the Indian Ocean.
3. Failed recent tick introductions
Uilenberg mentioned repeated episodes of tick introduction on Madagascar without successful colonisation . The ticks were generally discovered during cattle inspection at the quarantine in Toamasina harbour (east coast) on animals imported from South Africa: Rhipicephalus appendiculatus as well as other Rhipicephalus species, Amblyomma hebraeum, Hyalomma marginatum rufipes and Hyalomma truncatum were thus observed in these circumstances. Uilenberg also reported that goats were moved in 1963 from the harbour to a locality in the south of Madagascar where they were found infested by H. truncatum and Rhipicephalus evertsi evertsi. It seemed, however, that these species could not settle in spite of an apparently suitable climate.
Recently, five dromedaries were offered to Madagascar by the head of state of Libya. They arrived at Antananarivo airport in January 2008 with certificates guarantying an acaricide treatment before exportation and were immediately moved to a governmental residence in the south of the capital. One month later, the veterinarian in charge of the dromedaries brought ticks to the Veterinary Research Department (DRZV) of the National Centre of Applied Research for Rural Development (FOFIFA) where they were identified as Hyalomma dromedarii males. Two weeks later, the dromedaries were examined again by acarologists and found to be still infested by 40 male ticks. It is likely that, soon after their arrival in Madagascar, the female ticks had all engorged and dropped off in the pasture and premises where the animals were kept, in the vicinity of a dairy farm. However, four years later, no H. dromedarii had been reported either on the cows or on the dromedaries, which were in the meantime moved to the Antananarivo zoological gardens. It can thus be assumed that the local humid climate (more than 1200 mm of annual rainfall) and/or some other factors make the local environment unsuitable for this Sahelian tick.
In 2010, R. e. evertsi was found on cattle imported from Tanzania to Comoros, while it was absent on local cattle . This suggests that this species either could not adapt to the local environmental conditions or that it was on its way to colonise Grande Comore. A proper tick survey on Comoros is necessary to check whether this species will succeed in colonising the archipelago.
4. Successful recent tick introductions
Rhipicephalus appendiculatus, a species of high veterinary importance in East Africa, was observed for the first time in Mauritius in 1980 although probably introduced from South Africa some 20 years earlier . More recently, this species was introduced on Grande Comore through cattle importation from Tanzania in 2002, leading to numerous mortalities due to East Coast Fever (ECF) during the following months . Interestingly, the origin of cattle importation to Comoros has switched from Madagascar to Tanzania following a free trade bill signed in 2000. This switch was associated with the emergence of several epidemics (ECF, Chikungunya, Rift Valley Fever - RVF - and Dengue), some of which spread to other islands of the region (Chikungunya and RVF). This is a documented episode emphasizing the importance of trade-associated cattle movements in the emergence of zoonosis [11–15].
As stated above, R. appendiculatus is present on Mauritius but not Theileria parva, the pathogen responsible for ECF. In 1980, the tick was observed only on two farms located on the south of the island. In 2009, a R. appendiculatus male was collected in a cattle farm in the north of the country (Grande Daube), highlighting the need for a proper survey of tick distribution on the island. Since the vector seems to have been established on that island, introduction of animals coming from Comoros should be as restricted and controlled as that from the African mainland. Madagascar used to export cattle to Comoros until 2000 but the reverse seemingly never occurs, at least officially. Whatever the case, this recent settlement and the consecutive mortalities, which are going on 10 years later, should prompt the veterinary authorities of all the islands of the region to strictly control animal movements and use adequate quarantine containment facilities when cattle introductions are required or decided .
5. Alteration of tick distribution
On La Reunion, A. variegatum seems to becoming scarce. Barré and Morel found it from Saint-Denis (north) to l’Etang Salé (south-west) up to 300 m altitude . In 2001, a survey confirmed its presence on the island but with a distribution restricted to the western portion of the previous distribution area. However, some specimens were collected at 900 m altitude. In 2009–2010, cattle and goats on 22 farms of the west coast were examined and A. variegatum were observed at only 2 sites, La Saline and Saint-Leu, where only 59 ticks were collected on the 70 examined cattle, all being “Moka”, i.e. Malagasy zebus or crossbred with that breed (Grimaud, personal communication). On Mauritius, similar changes did not occur. The tick is still present throughout the island, although mainly on lowland pastures, parasitizing cattle and deer as previously observed .
The distribution area has extended to the Ambatolampy and Antsirabe areas (central high plateau) where A. variegatum is now present in villages below 1600 m, and perhaps up to 1700 m in some isolated places like Faratsiho (Figure 4). There are, however, still some tick-free pockets, in the highest and therefore coldest areas. As the Antsirabe area is the dairy production zone of Madagascar, where exotic cattle (pure or crossbred of Friesian or red and white Norwegian) are reared, important losses due to cowdriosis are a clear threat. Some field veterinarians have already reported cowdriosis although this was never confirmed in the laboratory.
The presence of A. variegatum up to 1600 m on Madagascar and on the Adamawa highland of Cameroon  is an indication that the absence of the tick in high pastures of La Reunion is probably not due to the inability of the species to survive in such conditions. Very regular tick control, good monitoring of cattle movements between farms, lack of trade between the “Moka” herds and the other livestock (Friesian, Limousin) may be sufficient to limit the distribution of this tick on that island.
Data analysis demonstrates that the degree of success of tick colonisation of new areas depends on a range of factors (e.g. environmental, climatic, anthropic and genetic). Recent observations regarding cattle tick distribution in SWIO show that, despite the fact that some tick species have been established on islands for centuries, alterations in their distribution continue to occur mainly associated with host movements and/or climate change. A new vector species (R. appendiculatus) was recently introduced to Grande Comore and may potentially settle on the neighbouring islands, where it could lead to significant losses. As far as A. variegatum is concerned, the recent extension of its distribution in Madagascar could also lead to major losses due to cowdriose or dermatophilosis in areas where dairy cattle of European breeds are reared. Several apparent failures in establishment of new tick populations were also reported: only one of the two A. variegatum lineages has a wide distribution in the region; only one of the two R. appendiculatus clades settled at present on Grande Comore; R. e. evertsi has not succeeded to settle on Madagascar or Comoros despite several introductions. Yet, this apparent inability of certain tick species or subspecies to colonise additional islands or particular environments should not cause postponement in the establishment and strict enforcement of safety measures against introduction of new tick species and their associated tick-borne pathogens to the SWIO islands.
This work was supported by GIS-CRVOI (projet DIGEERAV-OI), by INRA AIP Bio-Ressources 2008, by CIRAD-INRA, by the Fonds Européen de Développement Régional, Programme Opérationnel de Coopération Territoriale Réunion, Pathogènes Associés à la Faune Sauvage Océan Indien #31189, and by the Service de Coopération et d’Action Culturelle of the French Embassy in Madagascar. For A. variegatum collections, we are indebted to H. Adakal, R. Pegram, M. Frebling, M. Asnaoui, M. Saimo, A. Boulanger, N. Cangi, S. Girard, Y. Grimaud, and M.R. Jaumally. For technical help to M. Dupraz, R. Aprelon and R. Rivallan. And to T. De Meeus for help regarding phylogeographic analyses.
- Andrianaivoarivony R: L’alimentation carnée chez les anciens malgaches. Nouv Centre Art Archéo. 1987, 5–6: 22-26. (in French)Google Scholar
- Meyer C: Dictionnaire des Sciences Animales. [http://dico-sciences-animales.cirad.fr]
- Robequain C: Destin d’une île à sucre : l’économie et le peuplement de Maurice. Ann geogr. 1954, 63: 255-273. 10.3406/geo.1954.15509. (in French)View ArticleGoogle Scholar
- Uilenberg G, Hoogstraal H, Klein JM: Les tiques (Ixodoidea) de Madagascar et leur rôle vecteur. Arch Inst Pasteur Madagascar. 1979, NS: 1-153. (in French)Google Scholar
- Barré N, Morel PC: Ticks (Acarina, Ixodoidea) of the Mascarene Islands (Indian Ocean) and diseases transmitted by them. Rev Elev Med Vet Pays Trop. 1983, 36: 371-377. (in French)PubMedGoogle Scholar
- Barré N, Uilenberg G: Propagation de parasites transportés avec leurs hôtes : cas exemplaires de deux espèces de tiques du bétail. Rev Sci Tech Off Int Epiz. 2010, 29: 135-147. (in French)Google Scholar
- Beati L, Patel J, Lucas-Williams H, Adakal H, Kanduma EG, Tembo-Mwase E, Krecek R, Mertins JW, Alfred JT, Kelly S, Kelly P: Phylogeography and demographic history of Amblyomma variegatum (Fabricius) (Acari: Ixodidae), the tropical bont tick. Vector Borne Zoonotic Dis. 2012, 12: 514-525. 10.1089/vbz.2011.0859.PubMed CentralView ArticlePubMedGoogle Scholar
- Walker AR, Bouattour A, Camicas J, Estrada-Peña A, Horak IG, Latif AA, Pegram RG, Preston PM: Ticks of domestic animals in Africa: a guide to identification of species. 2003, Edinburgh: BioScience ReportsGoogle Scholar
- Delatte H, Bagny L, Brengue C, Bouetard A, Paupy C, Fontenille D: The invaders: phylogeography of dengue and chikungunya viruses Aedes vectors, on the South West islands of the Indian Ocean. Infect Genet Evol. 2011, 11: 1769-1781. 10.1016/j.meegid.2011.07.016.View ArticlePubMedGoogle Scholar
- Uilenberg G: Notes sur les hématozoaires et tiques des animaux domestiques à Madagascar. Rev Elev Med Vet Pays Trop. 1964, 17: 337-359. (in French)Google Scholar
- Yssouf A, Lagadec E, Bakari A, Foray C, Stachurski F, Cardinale E, Plantard O, Tortosa P: Colonization of Grande Comore Island by a lineage of Rhipicephalus appendiculatus ticks. Parasit Vectors. 2011, 4: 38-10.1186/1756-3305-4-38.PubMed CentralView ArticlePubMedGoogle Scholar
- De Deken R, Martin V, Saido A, Madder M, Brandt JRA, Geysen DM: An outbreak of East Coast Fever on the Comoros: a consequence of the import of immunised cattle from Tanzania?. Vet Parasitol. 2007, 143: 245-253. 10.1016/j.vetpar.2006.08.018.View ArticlePubMedGoogle Scholar
- Andriamandimby SF, Randrianarivo-Solofoniaina AE, Jeanmaire EM, Ravololomanana L, Razafimanantsoa LT, Rakotojoelinandrasana T, Razainirina J, Hoffmann J, Ravalohery JP, Rafisandratantsoa JT, Rollin PE, Reynes JM: Rift Valley fever during rainy seasons, Madagascar, 2008 and 2009. Emerg Infect Dis. 2010, 16: 963-970. 10.3201/eid1606.091266.PubMed CentralView ArticlePubMedGoogle Scholar
- Carroll SA, Reynes JM, Khristova ML, Andriamandimby SF, Rollin PE, Nichol ST: Genetic evidence for Rift Valley fever outbreaks in Madagascar resulting from virus introductions from the East African mainland rather than enzootic maintenance. J Virol. 2011, 85: 6162-6167. 10.1128/JVI.00335-11.PubMed CentralView ArticlePubMedGoogle Scholar
- Tortosa P, Pascalis H, Guernier V, Cardinale E, Le Corre M, Goodman SM, Dellagi K: Deciphering arboviral emergence within insular ecosystems. Infect Genet Evol. 2012, 12: 1333-1339. 10.1016/j.meegid.2012.03.024.View ArticlePubMedGoogle Scholar
- Stachurski F, Musonge EN, Achu-Kwi MD, Saliki JT: Impact of natural infestation of Amblyomma variegatum on the liveweight gain of male Gudali cattle in Adamawa (Cameroon). Vet Parasitol. 1993, 49: 299-311. 10.1016/0304-4017(93)90128-A.View ArticlePubMedGoogle Scholar
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