Zoologia Caboverdiana 4 (2): 31-42 Available at www.scvz.org © 2013 Sociedade Caboverdiana de Zoologia

The haematophagous (Animalia: Arthropoda) of the Cape Verde Islands: a review

Elves Heleno Duarte1

Keywords: Arthropods, -borne diseases, bloodsucking, hematophagy, Cape Verde Islands

ABSTRACT

Arthropoda is the most diverse phylum of the kingdom. The majority of bloodsucking arthropods of public health concern are found in two classes, Arachnida and Insecta. Mosquitoes, ticks, cattle , horseflies and biting midges are the main hematophagous groups occurring in the Cape Verde Islands and whose role in infectious disease transmission has been established. In this literature review, the main morphological and biological characters and their role in the cycle of disease transmission are summarized.

RESUMO

Os artrópodes constituem o mais diverso entre todos os filos do reino animal. É na classe Arachnida e na classe Insecta que encontramos a maioria dos artrópodes com importância na saúde pública. Os mosquitos, os carrapatos, as moscas do gado, os tabanídeos e os mosquitos pólvora são os principais grupos hematófagos que ocorrem em Cabo Verde e possuem clara associação com a transmissão de agentes infecciosos. Nesta revisão da literatura apresentamos os principais caracteres morfológicos e biologicos e o seu papel no ciclo de transmissão de doenças.

1 Direcção Nacional da Saúde, Ministério da Saúde, Avenida Cidade de Lisboa, C.P. 47, Praia, Republic of Cape Verde; [email protected]

Duarte 32 Haematophagous arthropods

INTRODUCTION With over a million described species, which ca. 500 are strongly associated with the Arthropoda is the most diverse and species rich transmission of infectious agents (Grimaldi & clade of the animal kingdom. Five main Engel 2005, Lehane 2005). It has been estimated taxonomic groups are usually recognized: the that of infectious diseases worldwide, about 17% extinct Trilobitomorpha and the extant are vector-borne. Unfortunately, vaccines for Chelicerata, Miriapoda, Hexapoda and Crustacea most of these diseases are not available. (Ruppert & Barnes 1994). Because they Therefore, increased emphasis on vector control represent an important source of food, transmit strategies is required, based upon the selection of numerous infectious agents and include an array proven intervention methods tailored to of agricultural pest species, arthropods are biological characters and ecological circum- widely studied (Chown & Nicolson 2004). stances of local vectors (WHO 2004). Haematophagous arthropods occur in two major The terrestrial arthropod fauna of the Cape groups, i.e. Arachnida (Chelicerata) and Insecta Verde Islands was reviewed by van Harten (Hexapoda) (Fig. 1), and are vectors of (1993), while a summary update was recently pathogens worldwide. So far, more than 16,000 provided by Arechavaleta et al. (2005). In Cape haematophagous species have been identified, of Verde, several vector-borne diseases occur.

Fig. 1. Main groups of haematophagous arthropods occurring in the Cape Verde Islands. Modified after Lehane (2005) and Estrada-Peña et al. (2010).

Duarte 33 Haematophagous arthropods

Many of these are emerging and/or re-emerging to the importance of bloodsucking arthropods in as a result of ecological and environmental the Cape Verde archipelago and to better changes that favour increased vector densities understand their role in the most common (Gratz 1999). In order to reduce the chance of infectious agent transmissions. The result will (re)emergence of arthropod-transmitted diseases, hopefully be useful in making policy decisions knowledge of local vector populations is crucial and in formulating new strategies in the fight in tracking any changes in their biology. This against vector-borne diseases in the Cape Verde review was conducted in order to draw attention Islands.

METHODS

The literature was scanned using the PubMed, Archive) were also scrutinized. Relevant Google Scholar and SCIELO databases from references were organized in a spreadsheet, but January 2013 to December 2013. Combinations only those references actually mentioning of the following key words were used: bloodsucking arthropods were maintained. Using arthropods, arthropod-borne disease, blood- the same databases, the medical and/or sucking, haematophagy and Cape Verde Islands. veterinary importance of the references was Three different languages (English, French, assessed. Medical and/or veterinary importance Portuguese) were used to obtain results. was allotted when at least one infectious agent Unpublished reports in national institutions (e.g. was isolated in the wild or when experimental Ministry of Health, Ministry of Rural Develop- infection was successfully realized in the ment, National Library, National Historical laboratory.

RESULTS

The database search resulted in 22 publications ticks), with over 700 species, including the most (articles, books, reports) mentioning the presence important vectors; ii) Argasidae (soft ticks), of haematophagous arthropods in the Cape Verde comprising ca. 200 species; iii) Nuttalliellidae, Islands. Of extant bloodsucking arthropods, only with a single species (Nuttalliella namaqua), Lepidoptera (represented by a single exclusively found in southern Africa (Parola & haematophagous species in Southeast Asia) do Raoult 2001, Basu et al. 2012). not occur in the archipelago. Only one study (on Being arachnids, ticks can be easily mosquitoes) was conducted exclusively by distinguished from by having three pairs national researchers (Duarte et al. 2012). Also of appendices during the immature stage and focusing on mosquitoes, six publications were four pairs as adults, by having the mouthpart published by a combined team of national and transformed into chelicerae and by the absence foreign workers (Appendix 1). The remaining of wings (Randolph 1998). Only few studies on studies were conducted solely by foreign ticks have been conducted in the Cape Verde workers and dealt with ticks, cattle flies, Islands (Tendeiro 1954, Meira et al. 1957, horseflies, biting midges, blackflies, mites, fleas Kirchner et al. 2008, Götsch et al. 2009, Gómez- and lice. Publications appeared in 19 journals Díaz et al. 2012). All except the study by and other sources (Appendix 1). Up until now, a Gómez-Díaz et al. (2012) were conducted fully role in the disease transmission cycle has been or partially in Santiago Island. Recent studies confirmed for three taxonomic groups in the showed domestic to be highly Cape Verde archipelago (see group descriptions parasitized and it was recommended to prevent below). transportation of animals (especially dogs) from Cape Verde to Europe (Kirchner et al. 2008, TICKS (ARACHNIDA: ACARI: IXODIDA) Götsch et al. 2009). Ripicephalus sanguineus Ticks are mandatory ectoparasites that parasitize was the only species found in recent studies, a variety of vertebrates and cause direct and although other species such as Amblyomma indirect financial loss (Parola & Raoult 2001, variegatum, Margaropus decoloratus and Estrada-Peña et al. 2010). This large group is Hyalomma sp. had previously been reported subdivided into three families: i) Ixodidae (hard (Tendeiro 1954, Meira et al. 1957), all of them Duarte 34 Haematophagous arthropods

Ixodidae. The most recent study of ticks forewings, while the hindwings are reduced to conducted in the archipelago (Gómez-Díaz et al. dumbbell-shaped knobs called halteres. They 2012) dealt with diversity and genetic structure have long legs and antennae, chipper-shaped of Ornithodoros capensis, a parasite of seabirds. mouthparts adapted to suction and generally show marked sexual dimorphism (Consoli & LIFE CYCLE Lourenço de Oliveira 1994, Harbach 2007). In Ticks have a complex life cycle, which – the Cape Verde archipelago, 11 species of depending on family, species and environmental mosquitoes occur, representing two subfamilies, parameters – may take 2-3 years (Parola & i.e. Anophelinae (two species in one ) and Raoult 2001). Their feeding behaviour is also Culicinae (nine species in three genera) (Ribeiro complex. Hard ticks need a long time to feed (2- et al. 1980, Alves et al. 2010, in press). Of these, 15 days) and feeding only takes place once about half is involved in the transmission of during each stage (larva, nymph and adult). Soft infectious agents, particularly Anopheles ticks consume several meals per stage but, unlike arabiensis, Aedes aegypti and two members of hard ticks, these may take from a few minutes to the Culex pipiens complex (C. p. pipiens and C. a few hours (Vial 2009). Approximately 75% of p. quinquefasciatus) (Alves et al. 2010). a hard tick’s life cycle is spent while being attached to an animal (Parola & Raoult 2001), LIFE CYCLE whereas soft ticks only attach to animals to feed During their life cycle, mosquitoes pass through (Vial 2009). four stages: eggs, larvae, pupae and adults, of which the first three are aquatic (Consoli & MEDICAL AND VETERINARY IMPORTANCE Lourenço de Oliveira 1994, Lehane 2005). The African swine fever (ASF) is a highly contagious larvae feed mostly on organic particles in water, and extremely deadly disease in domestic pigs while pupae only use the energy stored during (FAO 2000) and is one of the most important the larval stage. Adult mosquitoes are terrestrial, tick-borne ailments in Cape Verde. Ticks of the this being the stage of reproduction and genus Ornithodoros play an important role as dispersion. Males feed exclusively on plant vector of the disease (Basto et al. 2006). fluids, while females need animal (including Although there is no consensual view on their human) blood for the maturation of their eggs precise role in ASF transmission, the persistence (Consoli & Lourenço de Oliveira 1994). of the disease after several veterinary interventions and absence of transmission during MEDICAL AND VETERINARY IMPORTANCE various months (Penrith 1998) suggests that In Cape Verde, mosquitoes have been identified vectors or pigs (or both) act as reservoirs. as vector of several infectious agents that cause No human diseases transmitted by ticks are malaria, yellow fever, lymphatic filariasis and, known to occur in the archipelago. Lyme disease more recently, dengue (Franco & Menezes 1955, is an illness caused by the spirochete Borrelia Ribeiro et al. 1980; Alves 2004, WHO 2009). burgdorferi s.l. and is transmitted by hard ticks A. arabiensis is the only member of the A. of the genus Ixodes (Karami 2012), but has not gambiae complex occurring in Cape Verde been found in Cape Verde so far. Beyond their (Cambournac et al. 1982, Diallo 2003, Alves et implication in disease transmission, ticks al. 2010, Dia et al. 2011). In addition to being themselves pose problems to both man and the only vector of malaria, it was also the vector animals because they cause various harmful side- of Wulchereria brancrofti, the infectious agent effects to the host, ranging from anaemia caused causing lymphatic filariasis (Franco & Menezes by massive infestation to allergy due to the 1955). Since the 1950s, no new cases of inoculation of saliva during blood meals (Lehane lymphatic filariasis have become known in Cape 2005). Verde and the decease has seemingly been eradicated in the islands. In a recent study MOSQUITOES (INSECTA: NEMATOCERA: conducted in all inhabited islands, no cases were CULICIDAE) diagnosed (Benzerroug 2005). Before the 1950s, Mosquitoes are dipteran insects belonging to the the annual incidence of malaria was more than family Culicidae, in which three subfamilies are 100 cases/1000 inhabitants (Rodriguez et al. recognized: Anophelinae, Culicinae and 2012), but currently only limited and localized Toxirhichitinae (Consoli & Lourenço de Oliveira transmission occurs in two (Santiago and Boa 1994). Diptera have only one pair of wings, the Vista) of the 10 islands (WHO 2012). Duarte 35 Haematophagous arthropods

Epidemic dengue fever occurred in Cape LIFE CYCLE Verde in 2009 when ca. 21,000 cases were During their life cycle, cattle flies go through reported (WHO 2009, Monteiro 2010), mainly in four stages: egg, larvae, pupae and adult (Lehane Santiago and Fogo Islands. A. aegypti, the only 2005). The eggs are laid in groups of 40 to 80. vector of dengue described in the archipelago Hatching occurs approximately 24 hours after (Alves et al. 2010), was also the only vector of laying, while larval development time depends yellow fever, being resistant to DDT 4% and also on temperature and other environmental suspected to be resistant to propoxur (Dia et al. conditions. After the last instar, larvae move to 2012). During the dry season, it takes advantage dry areas for pupation. Adults live for about 30 of household water containers for its days, with males on average living slightly reproduction, thus maintaining high densities longer than females (Zumpt 1973, Lehane 2005). over the reproductive period (Duarte et al. 2012, 2013). Using experimental infection techniques, MEDICAL AND VETERINARY IMPORTANCE it has been shown that A. aegypti (ssp. formosus) Cattle flies are characterized by having from Santiago Island has a moderate ability to interrupted blood meals and they can bite several transmit dengue virus serotype 3, but a high hosts during the course of the same feeding susceptibility of becoming infected with and to round. This has important epidemiological transmit chikungynya (CHIKV) and yellow fever consequences (Zumpt 1973). Therefore, their virus (Vazeille et al. 2013). economic damage is categorized as either direct Despite their role in the transmission of or indirect. Direct damage is inflicted by blood several infectious agents in other countries, the spoliation, decrease in immune defense (inducing two members of the C. pipiens complex that latent diseases), production loss, diminished occur in Cape Verde have as yet not been weight, etc. Indirect damage is caused by the associated with infectious agent transmission. transmission of viruses, bacteria and other Elsewhere, these taxa are instrumental in the infectious agents (Zumpt 1973, Lehane 2005). transmission of West Nile virus, Wulchereria S. calcitrans is a pest species with a brancrofti, Rift Valley fever viruses, encephalitis worldwide distribution, known for disturbing viruses and others (Turell 2012). In Cape Verde, cattle and causing considerable losses (Lehane C. p. quinquefasciatus was first documented in 2005). The species can also transmit 1950 (although the presence of C. pipiens s.l. had trypanosomes, mainly Trypanosoma equinum in already been reported in 1947), while the Neotropical countries and T. evansi (which occurrence of C. p. pipiens was established in causes severe disease in horses and dogs and less 1977 (Ribeiro et al. 1980). Based on severe illness in cattle) and it has a secondary morphological studies of the male genitals, role in the transmission of the infectious agent Ribeiro et al. (1980) identified hybrids C. p. causing African trypanosomiasis or sleeping pipiens x C. p. quinquefasciatus. This was sickness (Lehane 2005). The only reported link subsequently confirmed by molecular analysis between S. calcitrans and disease in Cape Verde (Alves et al. 2010, Gomes et al. 2012). These occurred in the past, when its larvae caused hybirds have been shown to have the ability to myiasis among humans (Azevedo & Moreira enhance arbovirus transmission in areas where 1946). they occur (Gomes et al. 2012). HORSEFLIES (INSECTA: BRACHYCERA: CATTLE FLIES (INSECTA: BRACHYCERA: TABANIDAE) MUSCIDAE) Horseflies are robust insects (adults: 5-25 mm) Cattle flies are bloodsucking ectoparasites of with a cosmopolitan distribution. The males feed mammals (especially cattle) in the genus on plants, while the hematophagous females also Stomoxys. They are similar to houseflies Musca feed on nectar (Middlekauff & Lane 1980, domestica, but the distinguishing character is the Lehane 2005). Their head is larger than the cattle flies’ mouthparts, which are adapted to thorax, the mouthparts are of the chipper/sucking bloodsucking (Zumpt 1973). Both males and type and they have long antennae. The Tabanidae females feed on blood. Three species occur in comprise more than 4,300 described species in Cape Verde, i.e. Stomoxys calcitrans, S. niger more than 130 genera and three subfamilies and S. sitiens (Arechavaleta et al. 2005), of (, Chrysopsinae, Pangoninae) of which which only S. calcitrans has anthropophagic the first two are the epidemiologically more preferences. important (Lehane 2005). Atylotus agrestis is Duarte 36 Haematophagous arthropods

probably the only species that occurs in the Cape African horse sickness virus (AHSV) and Verde Islands (Arechavaleta et al. 2005). Bluetongue virus (BTV) in Africa – C. schultzei and C. nivosus occur in the Cape Verde LIFE CYCLE archipelago (Boorman & van Harten 1992). The life cycle of horseflies includes eggs, larvae (with 6-13 stages), pupae and adults. Egg laying LIFE CYCLE occurs in aquatic environments and eggs hatch 2- The Culicoides life cycle includes eggs, four 3 days after laying. Larvae also need humid larval stages, pupae and adults. The immature environments to survive; they are carnivorous stages require humid places to survive (Kettle and feed on small invertebrates. Horseflies can 1977, Mellor et al. 2000). Breeding sites are remain at the larval stage for up to two years similar to those of mosquitoes. Eggs are laid at before transforming into pupae. After 1-3 weeks, the substrate surface and, depending on species adults emerge and live for about two months. and environmental conditions, hatching occurs 2- Mating occurs soon after emergence and females 7 days after laying (Mellor et al. 2000). Larvae lay their eggs only after having consumed blood feed on vegetal debris, but some species are meals (Middlekauff & Lane 1980, Lehane 2005). predators. Pupae can be found moving free in the water or fixed on the substrate. Depending on the MEDICAL AND VETERINARY IMPORTANCE species, adults are active during daylight or Horseflies possess some characteristics that twilight, possess only limited capacity for flight favour the transmission of infectious agents: only and dispersal and are generally passive (Kettle few species are autogenous (most require a blood 1962, 1977, Mellor et al. 2000). meal for egg maturation), they are telmophagous (skin deceleration during blood meal), they MEDICAL AND VETERINARY IMPORTANCE require a fair amount of blood (and thus have a Worldwide, more than 50 arboviruses have been long engorgement time) and they interrupt their isolated from Culicoides, sometimes playing a meal due to being chased off because of their secondary role in the transmission cycle (Mellor painful bite, thus seeking another host et al. 2000). Many species transmit infectious (Middlekauff & Lane 1980, Lehane 2005). They agents causing diseases in animals, but only few may transmit a large variety of infectious agents, of them in humans. Among infectious agents including bacteria, viruses, protozoa, filariae and transmitted, Rift Valley fever (RVF) virus, others. Anthrax, anaplasmoses, Q fever, African horse sickness (AHS) virus, bluetongue trypanosomiasis, filariasis, encephalitis and virus (BTV), equine encephalitis viruses and African swine fever are some of the diseases epizootic hemorrhagic disease (EHD) virus are transmitted (Lehane 2005). Because some of some examples (Mellor et al. 2000, MacLachlan these diseases occur in Cape Verde and due to & Guthrie 2010). Two of these agents, AHSV the fact that Atylotus agrestis is associated with and BTV (Orvivirus, Reoviridae), cause diseases the transmission of some infectious agents of significant international impact and have been (Desquesnes & Dia 2003a, 2003b), further reported in the Cape Verde Islands (Sellers et al. studies are needed to clarify the role of this 1977, Boorman & van Harten 1992). AHSV is a species as a vector in the archipelago. non-contagious disease that causes 90% mortality in infected horses and has been BITING MIDGES (INSECTA: NEMATOCERA: introduced in Cape Verde from Senegal (Sellers CERATOPOGONIDAE) et al. 1977, MacLachlan & Guthrie 2010). Nine Biting midges are small (1-4 mm) flies of the serotypes of AHSV that occur in Africa are family Ceratopogonidae, having composed eyes, transmitted by C. imicola and C. bolitinos chipper-shaped mouthparts, short legs and the (MacLachlan & Guthrie 2010). abdomen divided into 10 segments (Mellor et al. 2000). With the exception of New Zealand, OTHER TAXA Patagonia, the Hawaiian Islands and the polar A single species of black (Nematocera: regions, they have a worldwide distribution. The Simuliidae), Simulium ruficorne, occurs in the genus Culicoides includes ca. 1,400 species of Cape Verde archipelago (Arechavaleta et al. which 96% engage in bloodsucking (females 2005). Worldwide, there are about 1,800 species only). They parasitize mammals (including of black flies in 25 genera, of which four are of humans) and (Mellor et al. 2000, Zimmer public health concern: Austrosimulium, Cnephia, et al. 2008). C. imicola – the main vector of Prosimulium and Simulium (Lehane 2005). Duarte 37 Haematophagous arthropods

These black flies transmit Onchocerca volvulus, Erythraeus capeverdensis) may have some which causes onchocerciasis in Africa, but in degree of hematophagous habits. Although few Cape Verde S. ruficorne has as yet not been data are available for these species, it has been shown to be a vector of infectious agents. shown elsewhere that Balaustium mites Not surprisingly, Cimex hemipterus (Eryrthraeidae) have very generalized feeding (Heteroptera: Cimicidae), the common bedbug, habits, including references to attacks on humans also occurs in Cape Verde (van Harten 1993, causing dermatitis (Newell 1963, Ido et al. Arechavaleta et al. 2005). Both sexes are 2003). hematophagous and preferably bite at night It appears that all taxa of lice (Anoplura) that (Lehane 2005). Although they are suspected of affect humans occur in the Cape Verde transmitting infectious agents, the role of archipelago, i.e. Pediculus humanus bedbugs in spreading them is not clear and there (Pediculidae) and Pthirus pubis (Pthiridae) (van is no clear evidence for their involvement in the Harten 1993, Arechavaleta et al. 2005). Louse- transmission of disease agents (Delaunay et al. borne diseases affect all levels of society, but 2011). they are most common under poor hygienic Both (louse flies) and circumstances and extreme poverty. Of the two, Oestridae () occur in the Cape Verde only P. pubis is associated with sexual activity archipelago (van Harten 1993, Arechavaleta et (Brouqui 2011). al. 2005). Van Harten (1993) cited three species Among the 2,000 species of fleas for the archipelago: Hippobosca rufipes, H. (Siphonaptera) that have been described equine and Olfersia aenescens. Worldwide, more (Krasnov 2008), at least four occur in the Cape than 200 species have been described and several Verde archipelago, i.e. Ctenocephalides felis, of them have been implied in the transmission of Pulex irritans and Echidnophaga gallinacea infectious agents (e.g. Rahola et al. 2011). (Pulicidae) and Tunga penetrans (Tungidae) is the only species of (Gomes 1969, Arechavaleta et al. 2005). P. occurring in Cape Verde and it has been irritans and T. penetrans have a preference for implicated in causing myiasis in several species human blood (Lehane 2005, Krasnov 2008). elsewhere in the world (Denion et al. 2004). They are potential vectors of numerous Although many species of mites infectious agents, among them viruses and (Siphonaptera) have been confirmed to occur in bacteria, and especially Yersinia pestis, the the Cape Verde Islands (Mahunka 1991, causal agent of Black Death (Lehane 2005, Arechavaleta et al. 2005, Haitlinger 2009), only Krasnov 2008). Eryrthraeidae (Leptus salicus, L. korneli,

CONCLUSIONS

Although many bloodsucking arthropods, foreign researchers, illustrating the need to including known vectors, occur in the Cape encourage local research teams to study the Verde Islands, only few studies have been biology of these species, which include several carried out on their biology and role in disease taxa imposing serious threats to public health, transmission in the archipelago. Most studies and obtain a better understanding of their have largely or exclusively been carried out by environmental requirements in Cape Verde.

ACKNOWLEDGEMENTS

I would like to express my thanks to Dr Joana encouragement while I was writing this review. Alves (Ministry of Health, Praia, Cape Verde) Helpful comments on the manuscript were for providing valuable information and for her received from two anonymous referees.

Duarte 38 Haematophagous arthropods

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APPENDIX 1. Haematophagous arthropods of the Cape Verde Islands and sources used in this review. Researchers Taxonomic (Cape Verde Authors Source Taxa group and/or Foreign) Ribeiro et al. Journal Anopheles gambiae s.l. Foreign (1979) Aedes aegypti, Ae. caspius meirais, Anopheles gambiae s.l., An. pretoriensis, Culex Ribeiro et al. Book bitaeniorynchus (Syn. Cx. Foreign (1980) ethiopicus), Cx. p. pipiens, Cx. p. quinquefasciatus, Culiseta longiareolata Cambournac et Journal Anopheles arabiensis Foreign al. (1982) Cambournac et Journal Culex tigripes Foreign/CV al. (1984) Anopheles arabiensis, An. Diallo (2003) Report pretoriensis, Aedes aegypti, Foreign Culex pipiens s.l. Aedes aegypti, Ae. caspius, Anopheles arabiensis, An. pretoriensis, Culex Mosquitoes bitaeniorynchus (Syn. Cx. (Insecta: Alves et al. ethiopicus), Cx. perexiguus, Journal CV/Foreign Nematocera: (2010) Cx. p. pipiens, Cx. p. Culicidae) quinquefasciatus, Cx. pipiens s.l. hybrids, Cx. tigripes, Culiseta longiareolata Anopheles arabiensis, An. pretoriensis, Aedes aegypti, Ae. caspius, Culex Dia et al. (2011) Report Foreign/CV bitaeniorynchus (Syn. Cx. ethiopicus), Cx. pipiens s.l., Culex sp. Dia et al. (2012) Journal Aedes aegypti Foreign Duarte et al. Aedes aegypti, Anopheles Journal CV (2012) gambiae s.l., Culex sp. Vazeille et al. Journal Aedes aegypti ssp. formosus Foreign/CV (2012) Duarte et al. Journal Aedes aegypti CV/Foreign (2013) Alves et al. in Journal Culex tritaeniorhynchus CV/Foreign press

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APPENDIX 1 continued. Tendeiro et al. Journal Amblyomma variegatum Foreign (1954) Amblyomma variegatum, Meira et al. Hylomma sp., Margaropus Journal Foreign (1957) decoloratus, Rhipicephalus Ticks sanguineos (Arachnida: Kirchner et al. Ixodida) Journal Rhipicephalus sanguineos Foreign (2008) Götsch et al. Journal Rhipicephalus sanguineos Foreign (2009) Gómez-Díaz et Journal Ornthodoros capensis Foreign al. (2012) Cattle flies (Insecta: Arechavaleta et Stomoxys calcitrans, S. Book Foreign Brachycera: al. (2005)* sitiens, S. niger Muscidae) Horse flies (Insecta: Arechavaleta et Book Atylotus agrestis Foreign Brachycera: al. (2005) Tabanidae) Biting midges (Insecta: Boorman & van Culicoides imicola, C. Journal Foreign Nematocera: Harten (1992) schultzei, C. nivosus Ceratopogonida) Simulium rificorne, Ctenocephalides felis, Echidnophaga galinácea, Pulex irritans, Tunga van Harten penetrans, Pediculus Journal Foreign (1993) humanus, Pthirus pubis, Other taxa Cimex hemipterus, Hippobosca rufipes, H. equina, Olfersia aenescens, Oestrus ovis Haitlinger Leptus salicus, L. korneli, Journal Foreign (2009) Erythraeus capeverdensis

Received 14 August 2013 Revision received 4 March 2014 Accepted 25 April 2014