Ticks (Acari: Ixodida) of the genus Haemaphysalis Koch, 1844 in Senegal: a review of host associations, chorology, and identification

The Haemaphysalis genus (Acari, Ixodidae) in Senegal is reviewed. This embodies a summary of specimens collected from vertebrate hosts over three decades. 454 collections were performed over this period (408 frommammals and 46 from birds), representing a total of 5752 ticks in different developmental stages. SevenHaemaphysalis spp. were collected, identified, and inventoried including: H. (Kaiseriana) rugosa, H. (Ornithophysalis) hoodi, H. (Rhipistoma) houyi, as well as four other species belonging to the leachi group, namely H. (Rhipistoma) leachi, H. (Rh.) moreli, H. (Rh.) muhsamae and H. (Rh.) spinulosa. Vertebrate hosts ofHaemaphysalis species were identified and listed in different ecological zones of Senegal. An identification key of the haemaphysalids of Senegal is proposed, which is also applicable to the haemaphysalid fauna of the Occidental sub-region of the Afrotropical zoogeographical region. The role of these species as potential vectors of zoonotic diseases in Senegal is also discussed.


Introduction
The genus Haemaphysalis Koch, 1844 belongs to the Ixodidae family (Hyalomminae subfamily). Haemaphysalid ticks are characterized by a scutum without ornamentation, a distinctive feature among ixodid ticks of the Metastriata group. These eyeless and inornate ticks lack adanal and subanal plates in males, while females have two short spurs of unequal length on coxa 1. Some other notable characteristics include: short palpi, usually conical with a large palpal segment 2 extending laterally beyond the basis capituli, at least two times longer than segment 1; short mouthparts; a large rear-facing spur on trochanter I; festoons are also present on the posterior margin. Haemaphysalis spp. have a three-host life cycle, are mostly associated with wild animals, but sometimes infest livestock (Morel, 2003). Few studies have been carried out on the Haemaphysalis genus so far, and those performed mostly focused on their economic importance to livestock in Eurasia, Africa, Australia, and New Zealand (Levin, 2016), with less emphasis on their diversity and role as potential vectors and reservoirs of human and animal pathogens. Indeed, some adaptive changes in haemaphysaline behavior such as a shift from wild deer and antelope to domestic cattle, sheep and goats have been noticed (Levin, 2016), implying a potential for the emergence of pathogens associated with wild populations into the peridomestic environment within livestock.
Research was performed on hard ticks (i.e. Ixodids) infesting domestic livestock and wild animals in Senegal in order to establish a list of all ixodid ticks found in Senegal (Sylla et al., 2007;. The knowledge previously acquired on the Haemaphysalis genus includes: the description of immature stages of Haemaphysalis rugosa (Camicas, 1978); revisiting the taxonomy of the H. leachi group, with the description of H. moreli ; the delineation of the aciculifer group from the rugosa group Camicas, 1978). More recently, Apanaskevich et al. (2007) screened many collections of Haemaphysalis, previously identified as Haemaphysalis (Rhipistoma) leachi, and compared them with typed H. (Rh.) leachi specimens from North Africa and the holotype specimen of Haemaphysalis (Rhipistoma) elliptica, concluding that many of the Southern and East African ticks previously identified as H. (Rh.) leachi were misdiagnosed and are actually H. (Rh.) elliptica.
The present study reviews Haemaphysalis species known to occur in different geographic areas of Senegal and describes features of their specific diagnosis, their host associations and their chorology.

Materials and methods
Most of the data presented here originate from a collection currently held at the laboratory of Medical Zoology, Research Institute for Development (IRD, Mbour Centre, Senegal). This collection has been continuously enriched by different research projects including: research conducted on birds, wild and domestic mammals during the Crimean-Congo Hemorrhagic Fever (CCHF) program (1987)(1988)(1989)(1990)(1991)(1992)(1993)  ; a project on climatic change and health (Action Thematique Interdisciplinaire, 2003-2004 focusing on tick inventories and the impact of climatic change on their geographical distribution and associated risk of CCHF emergence . For these studies, rodents were caught in different geographical areas of Senegal, and ticks were removed from the hosts and preserved in a 70% ethanol solution for further study. More recently, the EDEN project (European Commission Project on "Emerging Diseases in a Changing European Environment: http://www. eden-fp6project.net, 2004-2007) included an investigation of West Nile virus ecology leading to bird trapping and tick collection in the Djoudj National Park of Birds (16°25'N, 16°18'W, Saint Louis Department, Saint Louis Region) and Barkedji (15°17'N,14°52'W,Linguere Department,Louga Region).
Study sites and tick collections have been presented in detail elsewhere (Sylla et al., 2004;. Tick collections were mapped at the scale of the squared degree including the locality where each tick sample was collected. Maps were generated using SavGIS software (IRD, www.savgis.org). Geographical position of each locality was given by the gazetteer of Senegal (Board on Geographic Names, 1965, Dpt. of the Interior, Washington, D.C., 20240, 1965, IV + 194 pp.) or by using a GPSMAP ® 62S (Garmin Inc. Wichita KS).
Haemaphysalis species diagnosis followed an in-house identification key adapted to the ixodid fauna of the Occidental sub-region of the Afrotropical Region (Matthysse and Colbo, 1987A;Elbl and Anastos, 1966) that follows the systematic terminology of Camicas and Morel (Camicas and Morel, 1977;Camicas et al., 1998;Morel, 2003). Features pointed out by Apanaskevich et al. (2007) for the diagnosis of the H. (Rh.) leachi group are considered in this study. Vertebrate host terminologies follow Walker (1999a and b) and Wilson and Reeder (1992) for mammals and Cabot et al. (1992A and B) for birds.

Discussion
Haemaphysalis rugosa infests antelopes and buffalo as principal hosts for adults, but the species can also be found on carnivores and livestock. In Senegal, immature stages were collected on Carnivores of the Herpestidae and Viverridae families, adult stages were recorded from wild Bovidae including bushbuck, reedbuck and oribi (Table 2). Immature ticks are known to feed on civets, genets, rodents, and hares (Camicas, 1978;Hoogstraal and Kim, 1985;Yeoman andWalker, 1967, Hoogstraal and. It is a typical species of wet savannas. H. rugosa has been recorded from Senegal in the south and the West Coast of Dakar. It is known in Burkina Faso, Ivory Coast, Ghana, Benin, Uganda, Sudan, Central African Republic (north-eastern), and Democratic Republic of Congo (north-eastern). Haemaphysalis hoodi preferentially parasitizes ground feeding birds at all stages. All stages were collected from different bird orders including: Cuculiforma, Galliforma and Passeriforma, in the sudanian and sudano-guinean domains of Senegal (Table 3). Hoogstraal (1958) also recorded it from domestic chicken, Gallus domesticus. Haemaphysalis hoodi is known from sub-Saharan Africa and Morocco (Walker, 1991).
Haemaphysalis houyi is characterized by strict host-parasite specificity, only known to infest the African Ground Squirrel, X. erythropus. It is recorded in all geographic domains of Senegal, due to the wide distribution of its hosts. This species is also reported to occur in Mali, Burkina Faso, Ivory Coast, Ghana, Chad, Central African Republic, Cameroon, Sudan, Ethiopia, Uganda, and Kenya (Hoogstraal and Kim, 1985;Ntiamoa-Baidu et al., 2004).
Haemaphysalis spinulosa adults appear to feed on various small and medium-sized carnivores, as well as hedgehogs. In Senegal, immature stages are found on Carnivora of the families Herpestidae and Viverridae; they can also feed on small mammals as rodents (Table 7). This species has been recorded in sub-Saharan Africa and Yemen (Hussein and Mustafa, 1983;Hoogstraal and Kim, 1985;Walker, 1991).
Haemaphysalis parmata was not recorded in Senegal, but is known from Ivory Coast, in the same biogeographic Occidental subarea, and is considered in the proposed key.
Haemaphysalis (Rhipistoma) leachi group (subgroup leachi) includes five species of which three are described from the Occidental subarea of the Afrotropical region: 1) H. (Rh.) leachi (Audouin, 1826) was originally described in Egypt from grass-rats, Arvicanthis niloticus (Desmarest, 1822), and the Long-eared hedgehog, Hemiechinus auritus aegyptius E. Geoffroy, 1803 and their resting habitats (Hoogstraal, 1958). Adults can also feed on jungle cat, Felis chaus nilotica de Winton, 1898; the common fox, Vulpes vulpes aegyptica (Sonnini, 1816) and the wolf jackal, Canis aureus lupaster Hemprich and Ehrenberg, 1833; 2) H. (Rh.) moreli yellow or African dog tick, is found in tropical and southern Africa and can transmit canine and feline babesiosis, Mediterranean spotted fever, Q-fever, and Boutonneuse fever (Sonenshine, 1992b;Khoo et al., 2016). With respect to climate change, migration and commercial trade, understanding the health risks associated with tick-borne pathogens appears of public health importance in the geographic domains where haemaphysalid tick circulate. Indeed, their relative abundance, their seasonality, their geographical extension need to be assessed; the involvement of the Haemaphysalis genus in pathogen transmission may be underestimated.