Mediterranean Spotted Fever (MSF) is a tick-borne diseases caused by Rickettsia conorii. The disease is widely distributed in India, Africa, Europe and the Middle East bordering the Mediterranean, sub-Saharan Africa and around the Black and Caspian Sea. The main vector of MSF in the Mediterranean area is the brown dog tick Rhipicephalus sanguineus (Mumcuoglu et al. 2002).
An outbreak of MSF was investigated by studying questing and parasitic stages of ticks in two settlements of equal size and population located 20 km apart in the Negev Desert. Although high morbidity from SFGR was found in one of the settlements (Kibbutz Ze'elim), no clinical cases were observed in the second (Kibbutz Re'im). Using flagging and CO2-trapping, approximately 9 times more ticks were collected in Ze'elim than in Re'im. Rhipicephalus sanguineus was the dominant species in Ze'elim, whereas in Re'im Rh. turanicus was the most abundant species. The seasonality of the different tick species and stages, the infestation rate of the domestic and wild animals inside and outside the settlements, the climatic and soil differences prevailing in these sites and the percentage of host animals seropositive to SFGR were examined and significant differences between the two settlements were found. It was also shown that in Ze'elim, 7.1% of dog owners acquired MSF during the period 1984-1989 compared with only 1.4% of people without dogs (Mumcuoglu et al. 1990, 1993a).
Domestic dogs in Ze'elim were studied for infestation with Rh. sanguineus over a period of one year. The mean number of ticks per dog per month was 16.4. The majority of ticks were adults. Male ticks were more abundant on the ears, whereas female ticks were more abundant on the ears and abdomen of the dogs. A strong correlation between the tick numbers and the ambient temperatures was found (Mumcuoglu et al. 1993b). Of 549 Rh. sanguineus specimens examined in 1989/90 from Ze'elim, 7.3% were positive for SFGR when tested by the immunofluorescence technique. In Re'im, 2.2% of 156 Rh. turanicus were positive. In 1994, 27.4% of the ticks in Ze'elim and 2.6% in Re'im were positive for SFGR. To our knowledge, this is the first report of the infection of Rh. turanicus with SFGR (Guberman et al. 1996).
The life-cycle of two closely related tick species of Rh. sanguineus and Rh. turanicus was studied under laboratory conditions. Female Rh. turanicus produced twice as many eggs as Rh. sanguineus due to greater amount of blood engorged by females and the smaller weight of Rh. turanicus eggs. In all developmental stages, the weight increase after engorgement, which provides the interstage growth, was greater in R. turanicus. The higher density and the greater height of the dorsal epicuticular folds, as well as the special indentations inside the folds in nymphal Rh. turanicus, allow this tick to stretch its body during blood engorgement to a greater extent than Rh. sanguineus. The rate of blood ingestion, egg maturation and metamorphosis of Rh. turanicus was greater than those of Rh. sanguineus (Ioffe-Uspensky et al. 1997).
Absolute and relative weight characteristics of 25 species of three-host exophilic ticks from 5 genera have been compared. Ixodes and Haemaphysalis species differ from Hyalomma species by having lighter unfed females, heavier eggs and, hence, considerably smaller interstage compensatory growth. In Hyalomma, Dermacentor and Rhipicephalus species, the compensatory growth is mainly realized through a large weight increase during nymphal feeding (Uspensky et al. 1999).
Sequences from the Anaplasma phagocytophilum 16S rRNA gene were detected in 5 ticks representing 3 species (Hyalomma marginatum, Rhipicephalus turanicus, and Rhipicephalus (Boophilus) kohlsi) collected from roe deer (Capreolus capreolus) in Mount Carmel, Israel. The sequences were all identical to those of Ap-variant 1 strain (Keysary et al. 2007).
The ectoparasite fauna of reintroduced roe deer (Capreolus capreolus) was surveyed in a Mediterranean forest in Israel. Ectoparasites were collected from four female hand-reared deer during 2004 and 2005. Seasonality, predilection sites of infestation, and the apparent effect of the parasites are presented. This is the first study of roe deer parasites in the East Mediterranean. The ectoparasite fauna included three hippoboscid fly (Lipoptena capreoli, Hippobosca equina, and Hippobosca longipennis), four tick (Rhipicephalus sanguineus, Rhipicephalus turanicus, Rhipicephalus kohlsi, and Hyalomma marginatum), and one unidentified trombiculid mite species. For most of these ectoparasites, this is the first record on roe deer. All ectoparasite species were documented in Israel prior to the reintroduction program; exotic ectoparasites were not detected (Wallach et al. 2008).
In the Mediterranean region, the brown dog tick, Rhipicephalus sanguineus, is the recognized vector of Rickettsia conorii. To study tick-pathogen relationships and pathogenesis of infection caused in model animals by the bite of an infected tick, we attempted to establish a laboratory colony of Rh. sanguineus persistently infected with R. conorii. Rh. sanguineus ticks of North American and Mediterranean origin were exposed to R. conorii isolates of African (R. conorii conorii strain Malish) and Mediterranean (R. conorii israelensis strain ISTT) origin. Feeding of ticks upon infected mice and dogs, intra-hemocoel inoculation, and submersion in suspensions of purified rickettsiae were used to introduce the pathogen into uninfected ticks. Feeding success, molting success and the longevity of molted ticks were measured to assess the effects of R. conorii on the survival of Rh. sanguineus. In concordance with previously published results, Rh. sanguineus larvae and nymphs from both North American and Mediterranean colonies exposed to R. conorii conorii Malish experienced high mortality during feeding and molting or immediately after. The prevalence of infection in surviving ticks did not exceed 5%. On the other hand, exposure to ISTT strain had lesser effect on tick survival and resulted in 35–66% prevalence of infection. Rh. sanguineus of Mediterranean origin were more susceptible to infection with either strain of R. conorii than those from North America. Previous experimental studies had demonstrated transovarial and transstadial transmission of R. conorii in Rh. sanguineus; however, our data suggest that different strains of R. conorii may employ different means of maintenance in nature. The vertebrate host may be a more important reservoir than previously thought, or co-feeding transmission between different generations of ticks may obviate or lessen the requirement for transovarial maintenance of R. conorii (Levin et al. 2009).
A survey of the vectors of spotted fever group Rickettsiae and of murine typhus was carried out in Rahat, a Bedouin town in the Negev Desert, where the diseases are endemic. Houses with known cases of spotted fever group Rickettsiae or murine typhus were compared with those without reported clinical cases. A neighboring Jewish community, Lehavim, where no cases of spotted fever group Rickettsiae and murine typhus were reported in recent years, was used as a control. In the houses of patients with spotted fever group Rickettsiae in Rahat, an average of 7.4 times more ticks were found than in control houses. Out of 190 ticks isolated from sheep and goats or caught by ßagging in Rahat, 90% were Rhipicephalus sanguineus (Latreille), 7.9% Rhipicephalus turanicus Pomerantzev, and 2.1% were Hyalomma sp. In the houses of patients with murine typhus, three times more rats were caught and, on the average, each rat was infested with 2.2 times more fleas than rats in the control houses. Out of 323 ßeas collected from 35 Norwegian rats (Rattus norvegicus), 191 were Xenopsylla cheopis and 132 Echidnophaga murina. Thus, there was a six to seven times higher probability of encountering a tick or flea vector where infections had occurred than in control houses in Rahat. The percentage of rats seropositive to Rickettsia typhi was similar in study and control households (78.3 and 76.2, respectively). In the control settlement, Lehavim, only three Mus musculus were caught, which were not infested with ectoparasites and their sera were negative for murine typhus. Out of 10 dogs examined in this settlement, 15 Rh. sanguineus and eight specimens of the cat flea (Ctenocephalides felis felis) were isolated. No rats were caught in this settlement. These data indicate that there is a correlation among the density of domestic animals, their ectoparasites, and the incidence of spotted fever group Rickettsiae and murine typhus in Rahat (Mumcuoglu et al. 2001).
The aim of this study was to characterize the diversity of rickettsiae in ticks collected from vegetation and the ground, from different parts of Israel. Non-engorged questing adult ticks were collected from 13 localities. A total of 131 tick pools, 83 of Rhipicephalus turanicus and 48 of Rhipicephalus sanguineus (each with 2–10 ticks per pool), were included in this study. In addition, 13 Hyalomma sp. ticks were collected. The ticks were molecularly screened for rickettsiae, targeting the citrate synthase (gltA) and the outer membrane protein A (ompA) gene loci. Rickettsia massiliae ompA DNA (100% sequence similarity; 180 bp) was detected in 32 Rh. turanicus and 12 Rh. sanguineus tick pools. R. conorii israelensis was detected in three Rh. sanguineus pools. Rickettsia sibirica mongolitimonae ompA DNA (100% sequence similarity; 182 bp) was found in one Hyalomma tick. This study reports the first detection of R. massiliae and R. sibirica mongolitimonae in ticks from 2 Israel. This is the first report describing the presence of these human pathogens in the Middle East (Harrus et al. 2010a).
In this study, the efficiency of R. conorii israelensis transmission between co-feeding Rh. sanguineus ticks was assessed. Infected Rh. sanguineus adults and uninfected nymphs were fed simultaneously upon either naive dogs or a dog previously exposed to this agent. When ticks were placed upon naive dogs, 92–100% of nymphs acquired the infection and 80–88% of infected engorged nymphs transmitted it transstadially. When ticks were placed upon a seropositive dog, only 8–28.5% of recipient nymphs became infected. Our results establish the first evidence for efficient natural transmission of R. conorii israelensis between co-feeding ticks upon both naive and seropositive dogs. This route of transmission can ensure continuous circulation of R. conorii israelensis in tick vectors even in the absence of naive reservoir hosts (Zemtsova et al. 2010).
The aim of this study was to characterize the diversity of domestic animal pathogens in ticks collected from vegetation and the ground, from different parts of Israel. Non- engorged questing adult ticks were collected from 13 localities. A total of 1196 ticks in 131 pools—83 pools of Rhipicephalus turanicus and 48 of Rhipicephalus sanguineus (with two to ten ticks per pool)—were included in this study. In addition, 13 single freeroaming Hyalomma spp. ticks were collected. Screening by molecular techniques revealed the presence of Ehrlichia canis, Anaplasma platys, Anaplasma bovis and Babesia canis vogeli DNA in Rh. turanicus ticks. E. canis, A. bovis, B. canis vogeli and Candidatus Midichloria mitochondrii DNA sequences were detected in Rh. sanguineus ticks. Candidatus Midichloria mitochondrii DNA was also detected in Hyalomma spp. ticks. Neither Hepatozoon spp. nor Bartonella spp. DNA was detected in any of the ticks examined. This study describes the first detection of E. canis in the tick Rh. turanicus, which may serve as a vector of this canine pathogen; E. canis was the most common pathogen detected in the collected questing ticks. It also describes the first detection of A. bovis and Candidatus Midichloria mitochondrii in Israel. To the best of the author’s knowledge, this is the first report describing the detection of DNA of the latter two pathogens in Rh. sanguineus, and of A. bovis in Rh. turanicus (Harrus et al. 2010b).
The molecular evidence for the presence of spotted fever group rickettsiae (SFGR) in ticks collected from roe deer, addax, red foxes, and wild boars in Israel was reported. Rickettsia aeschlimannii was detected in Hyalomma marginatum and Hyalomma detritum while Rickettsia massiliae was present in Rhipicephalus turanicus ticks. Furthermore, a novel uncultured SFGR was detected in Haemaphysalis adleri and Haemaphysalis parva ticks from golden jackals. The pathogenicity of the novel SFGR for humans is unknown; however, the presence of multiple SFGR agents should be considered when serological surveillance data from Israel are interpreted because of significant antigenic crossreactivity among Rickettsia. The epidemiology and ecology of SFGR in Israel appear to be more complicated than was previously believed (Keysary et al. 2011).
The present study evaluates the reproductive compatibility between Rhipicephalus sanguineus ticks from North America, Israel, and Africa. Female ticks of the parent generation were mated with males from the same and alternate colonies. Every pure and hybrid cohort was maintained separately into the F2 generation with F1 females being allowed to mate only with males from the same cohort. The following survival parameters were measured and recorded for every developmental stage: feeding duration and success; engorgement weight, fertility, and fecundity of females; molting and hatching success. Ticks from North American and Mediterranean populations hybridized successfully. The survival parameters of all their hybrid lines were similar to those in pure lines throughout the F1 generation, and F1 adults were fully fertile. Parent adult ticks from the African population hybridized with either North American or Mediterranean ticks and produced viable progenies whose survival parameters were also similar to those in pure lines throughout the F1 generation. However, F1 adults in the four hybrid lines that included African ancestry were infertile. No parthenogenesis was observed in any pure or hybrid lines as proportion of males in F1 generation ranged from 40 to 60 %. Phylogenetic analysis of the 12S rDNA gene sequences placed African ticks into a separate clade from those of the North American or Mediterranean origins. Our results demonstrate that Rh. sanguineus ticks from North America and Israel represent the same species, whereas the African population used in this study is significantly distant and probably represents a different taxon (Levin et al. 2012).
A 16S rRNA gene approach, including 454 pyrosequencing and quantitative PCR (qPCR), was used to describe the bacterial community in Rhipicephalus turanicus and to evaluate the dynamics of key bacterial tenants of adult ticks during the active questing season. The bacterial community structure of Rh. turanicus was characterized by high dominance of Coxiella and Rickettsia and extremely low taxonomic diversity. Parallel diagnostic PCR further revealed a novel Coxiella species which was present and numerically dominant in all individual ticks tested (n_187). Coxiella sp. densities were significantly higher in female versus male ticks and were overall stable throughout the questing season. In addition, we revealed the presence of the novel Coxiella sp. in Rh. sanguineus adult ticks, eggs, and hatched larvae, indicating its vertical transmission. The presence of both spotted fever group Rickettsia spp. (SFGR) and non-SFGR was verified in the various individual ticks. The prevalence and density of Rickettsia spp. were very low compared to those of Coxiella sp. Furthermore, Rickettsia sp. densities were similar in males and females and significantly declined toward the end of the questing season. No correlation was found between Coxiella sp. and Rickettsia sp. densities. These results suggest different control mechanisms in the tick over its different bacterial populations and point to an obligatory and facultative association between the two tick species and Coxiella sp. and Rickettsia spp., respectively (Lalzar et al. 2012).
Out of 340 stray cats in Jerusalem, 186 (54.7%) were infested with the cat flea, Ctenocephalides felis, 49 (14.4%) with the cat louse, Felicola subrostratus, 41 (12.0%) with the ear mite, Otodectes cynotis, three (0.9%) with the fur mite, Cheyletiella blakei, two (0.6%) with the itch mite Notoedres cati, and 25 (7.3%) with ticks of the species Rhipicephalus sanguineus sl, Rhipicephalus turanicus or Haemaphysalis adleri. A higher number of flea infestations was observed in apparently sick cats (P <0.05) and in cats aged <6 months (P <0.05). The proportion of flea-infested cats (P <0.01), as well as the number of fleas per infested cat (P <0.01), was higher in autumn than in other seasons. By contrast with findings in cats with flea infestations, rates of infestation with ticks were higher amongst cats with clinical signs (P <0.01) and cats aged ≥6 months (P <0.05) (Salant et al. 2013).
One of the most common explanations of the alternative nest-building behavior in raptors’ population is the “Ectoparasite-avoidance’’ hypothesis, which claims that switching to alternative nests each year reduces nests’ parasites that could decrease their breeding success. Our aim was to investigate this hypothesis concerning the Judean Long-legged Buzzard (Buteo rufinus) and Short-toed Eagle (Circaetus gallicus) population, in Israel. Furthermore, we also investigated whether any specific parasites for each of these raptors’ species actually exist. Thirty-one nests of Long-legged Buzzards (LLB) and 61 nests of Shorttoed Eagles (STE) were located and systematically examined during the period of February-September 2011, in an area of 450 km2 in the Judean Foothills, Israel. Nest material samples were collected from the center of the nest of 26 LLB and 45 STE nests. Four specimens of the Mallophaga Laemobothrion maximum were isolated from three nests of LLB and one male of Degeeriella leucopleura from a nest of STE. In addition, a hard tick larva (Rhipicephalus sp.), an argasid nymph (Argas sp.) and six specimens of dermanyssid mites were isolated from nests of STE. In 82.1% of the LLB nests, Coleoptera larvae and/or adults were found, most of them belonging to the families Scarabaeidae, Buprestidae, Elateridae and Dermestidae. Although nest parasites were actually found, in significant small numbers, we cannot support the “ectoparasite-avoidance” hypothesis in our study system (Friedemann et al. 2013).
The DNA of Rickettsia africae was detected in a Hyalomma detritum tick from a wild boar and DNA of Candidatus Rickettsia barbariae was detected in Rhipicephalus turanicus and Rhipicephalus sanguineus collected from vegetation. The DNA of Rickettsia massiliae was found in Rh. sanguineus and Haemaphysalis erinacei, whereas DNA of Rickettsia sibirica mongolitimonae was detected in a Rhipicephalus (Boophilus) annulatus. Clinicians should be aware that diseases caused by a variety of rickettsiae previously thought to be present only in other countries outside of the Middle East may infect residents of Israel who have not necessarily traveled overseas. Furthermore, this study reveals again that the epidemiology of the spotted fever group rickettsiae may not only involve Rickettsia conorii but may include other rickettsiae (Waner et al. 2014). In this study, we aimed to identify and genetically characterize spotted fever group (SFG) rickettsiae in ticks, domestic one-humped camels, and horses from farms and Bedouin communities in southern Israel. A total of 618 ixodid ticks (Hyalomma dromedarii, Hyalomma turanicum, Hyalomma excavatum, and Hyalomma impeltatum) collected from camels and horses, as well as 152 blood samples from 148 camels and four horses were included in the study. Initial screening for rickettsiae was carried out by targeting the gltA gene. Positive samples were further analyzed for rickettsial ompA, 17kDa, ompB, and 16S rRNA genes. Rickettsia aeschlimannii DNA was detected in the blood of three camels and 14 ticks (H. dromedarii, H. turanicum, and H. excavatum). Rickettsia africae was found in six ticks (H. turanicum, H. impeltatum, H. dromedarii, and H. excavatum). In addition, Rickettsia sibirica mongolitimonae was detected in one H. turanicum tick. These findings represent the first autochthonous detection of R. africae in Israel. Furthermore, we report for the first time the finding of R. aeschlimannii in H. turanicum and H. excavatum ticks, as well as the first identification of R. sibirica mongolitimonae in H. turanicum ticks (Kleinerman et al. 2013).
The aim of the current study was to investigate the presence of Bartonella spp. in commensal rodents and their ectoparasites in Nigeria. We report, for the first time, the molecular detection of Bartonella in 26% (46/177) of commensal rodents (Rattus rattus, R. norvegicus and Cricetomys gambianus) and 28% (9/32) of ectoparasite pools (Xenopsylla cheopis, Haemolaelaps spp., Ctenophthalmus spp., Hemimerus talpoides, and Rhipicephalus sanguineus) from Nigeria. Sequence analysis of the citrate synthase gene (gltA) revealed diversity of Bartonella spp. and genotypes in Nigerian rodents and their ectoparasites. Bartonella spp. identical or closely related to Bartonella elizabethae, Bartonella tribocorum and Bartonella grahamii were detected. High prevalence of infection with Bartonella spp. was detected in commensal rodents and ectoparasites from Nigeria. The Bartonella spp. identified, were previously associated with human diseases highlighting their importance to public health (Kamani et al. 2013a).
Blood samples and ticks (Rhipicephalus sanguineus, Rhipicephalus turanicus and Heamaphysalis leachi) collected from 181 dogs from Nigeria were molecularly screened for human and animal vector-borne pathogens by PCR and sequencing. DNA of Hepatozoon canis (41.4%), Ehrlichia canis (12.7%), Rickettsia spp. (8.8%), Babesia rossi (6.6%), Anaplasma platys (6.6%), Babesia vogeli (0.6%) and Theileria sp. (0.6%) was detected in the blood samples. DNA of E. canis (23.7%), H. canis (21.1%), Rickettsia spp. (10.5%), Candidatus Neoehrlichia mikurensis (5.3%) and A. platys (1.9%) was detected in 258 ticks collected from 42 of the 181 dogs. Co- infections with two pathogens were present in 37% of the dogs examined and one dog was co-infected with 3 pathogens. DNA of Rickettsia conorii israelensis was detected in one dog and Rhipicephalus sanguineus tick. DNA of another human pathogen, Candidatus N. mikurensis was detected in Rh. sanguineus and H. leachi ticks, and is the first description of Candidatus N. mikurensis in Africa. The Theileria sp. DNA detected in a local dog in this study had 98% sequence identity to Theileria ovis from sheep (Kamani et al. 2013b).
In this study, 197 Hyalomma ticks (Ixodida: Ixodidae) collected from 51 camels (Camelus dromedarius) in Kano, northern Nigeria, were screened by amplification and sequencing of the citrate synthase (gltA), outer membrane protein A (ompA) and 17-kDa antigen gene fragments. Rickettsia sp. gltA fragments were detected in 43.3% (42/97) of the tick pools tested. Rickettsial ompA gene fragments (189 bp and 630 bp) were detected in 64.3% (n = 27) and 23.8% (n = 10) of the gltA-positive tick pools by realtime and conventional polymerase chain reaction (PCR), respectively. The amplicons were 99-100% identical to Rickettsia aeschlimannii TR/Orkun-H and R. aeschlimannii strain EgyRickHimp-El-Arish in GenBank. Furthermore, 17-kDa antigen gene fragments of 214 bp and 265 bp were detected in 59.5% (n = 25) and 38.1% (n = 16), respectively, of tick pools, and sequences were identical to one another and 99-100% identical to those of the R. aeschlimannii strain Ibadan A1 in GenBank. None of the Hyalomma impressum ticks collected was positive for Rickettsia sp. DNA. Rickettsia sp. gltA fragments (133 bp) were detected in 18.8% of camel blood samples, but all samples were negative for the other genes targeted. This is the first report to describe the molecular detection of R. aeschlimannii in Hyalomma spp. ticks from camels in Nigeria (Kamani et al. 2015).
We aimed to identify the circulating hard tick vectors and genetically characterize SFG Rickettsia species in ixodid ticks from the West Bank-Palestinian territories. A total of 1,123 ixodid ticks belonging to eight species (Haemaphysalis parva, Haemaphysalis adleri, Rhipicephalus turanicus, Rhipicephalus sanguineus, Rhipicephalus bursa, Hyalomma dromedarii, Hyalomma aegyptium and Hyalomma impeltatum) were collected from goats, sheep, camels, dogs, a wolf, a horse and a tortoise in different localities throughout the West Bank during the period of January-April, 2014. A total of 867 ticks were screened for the presence of rickettsiae by PCR targeting a partial sequence of the ompA gene followed by sequence analysis. Two additional genes, 17 kDa and 16SrRNA were also targeted for further characterization of the detected Rickettsia species. Rickettsial DNA was detected in 148 out of the 867 (17%) tested ticks. The infection rates in R. turanicus, R. sanguineus, H. adleri, H. parva, H. dromedarii, and H. impeltatum ticks were 41.7, 11.6, 16.7, 16.2, 11.8 and 20%, respectively. None of the ticks, belonging to the species R. bursa and H. aegyptium, were infected. Four SFG rickettsiae were identified: Rickettsia massiliae, Rickettsia africae, Candidatus Rickettsia barbariae and Candidatus Rickettsia goldwasserii (Ereqat et al. 2016).
This study aimed to genetically characterize spotted fever group rickettsiae (SFGR) in questing ixodid ticks from Israel and to identify risk factors associated with SFGR- positive ticks using molecular techniques and geographic information systems (GIS) analysis. Overall, 1,039 ticks from the genus Rhipicephalus were collected during 2014. 109/1039 (10·49%) carried SFGR-DNA of either Rickettsia massiliae (95), 'Candidatus Rickettsia barbariae' (8) or Rickettsia conorii (6). Higher prevalence of SFGR was found in Rhipicephalus turanicus (18·00%) compared with Rhipicephalus sanguineus sensu lato (3·22%). Rickettsia massiliae was the most commonly detected species and the most widely disseminated throughout Israel (87·15% of all Rickettsia-positive ticks). GIS analysis revealed that Central and Northern coastal regions are at high risk for SFGR. The presence of ticks was significantly associated with normalized difference vegetation index and temperature variation over the course of the year. The presence of rickettsiae was significantly associated with brown type soils, higher land surface temperature and higher precipitation. The latter parameters may contribute to infection of the tick with SFGR (Rose et al. 2017).
Hyalomma Koch, 1844 are ixodid ticks that infest mammals, birds and reptiles, to which 27 recognized species occur across the Afrotropical, Palearctic and Oriental regions. Despite their medical and veterinary importance, the evolutionary history of the group is enigmatic. To investigate various taxonomic hypotheses based on morphology, and also some of the mechanisms involved in the diversification of the genus, we sequenced and analyzed data derived from two mtDNA fragments, three nuclear DNA genes and 47 morphological characters. Bayesian and Parsimony analyses based on the combined data (2242 characters for 84 taxa) provided maximum resolution and strongly supported the monophyly of Hyalomma and the subgenus Euhyalomma Filippova, 1984 (including H. punt Hoogstraal, Kaiser and Pedersen, 1969). A predicted close evolutionary association was found between morphologically similar H. dromedarii Koch, 1844, H. somalicum Tonelli Rondelli, 1935, H. impeltatum Schulze and Schlottke, 1929 and H. punt, and together they form a sister lineage to H. asiaticum Schulze and Schlottke, 1929, H. schulzei Olenev, 1931 and H. scupense Schulze, 1919. Congruent with morphological suggestions, H. anatolicum Koch, 1844, H. excavatum Koch, 1844 and H. lusitanicum Koch, 1844 form a clade and so also H. glabrum Delpy, 1949, H. marginatum Koch, 1844, H. turanicum Pomerantzev, 1946 and H. rufipes Koch, 1844. Wide scale continental sampling revealed cryptic divergences within African H. truncatum Koch, 1844 and H. rufipes and suggested that the taxonomy of these lineages is in need of a revision. The most basal lineages in Hyalomma represent taxa currently confined to Eurasia and molecular clock estimates suggest that members of the genus started to diverge approximately 36.25 million years ago (Mya). The early diversification event coincides well with the collision of the Indian and Eurasian Plates, an event that was also characterized by large scale faunal turnover in the region. Using S-Diva, we also propose that the closure of the Tethyan seaway allowed for the genus to first enter Africa approximately 17.73Mya. In concert, our data supports the notion that tectonic events and large scale global changes in the environment contributed significantly to produce the rich species diversity currently found in the genus Hyalomma (Sands et al. 2017).
Hyalomma ticks (Acari: Ixodidae) are hosts for Francisella-like endosymbionts (FLE) and may serve as vectors of zoonotic disease agents. This study aimed to provide an initial characterization of the interaction between Hyalomma and FLE and to determine the prevalence of pathogenic Rickettsia in these ticks. Hyalomma marginatum, Hyalomma rufipes, Hyalomma dromedarii, Hyalomma aegyptium, and Hyalomma excavatum ticks, identified morphologically and molecularly, were collected from different hosts and locations representing the distribution of the genus Hyalomma in Israel, as well as from migratory birds. A high prevalence of FLE was found in all Hyalomma species (90.6%), as well as efficient maternal transmission of FLE (91.8%), and the localization of FLE in Malpighian tubules, ovaries, and salivary glands in H. marginatum. Furthermore, we demonstrated strong co-phylogeny between FLE and their host species. Contrary to FLE, the prevalence of Rickettsia ranged from 2.4% to 81.3% and was significantly different between Hyalomma species, with a higher prevalence in ticks collected from migratory birds. Using ompA gene sequences, most of the Rickettsia spp. were similar to Rickettsia aeschlimannii, while a few were similar to Rickettsia africae of the spotted fever group (SFG). Given their zoonotic importance, 249 ticks were tested for Crimean Congo hemorrhagic fever virus infection, and all were negative. The results imply that Hyalomma and FLE have obligatory symbiotic interactions, indicating a potential SFG Rickettsia zoonosis risk. A further understanding of the possible influence of FLE on Hyalomma development, as well as on its infection with Rickettsia pathogens, may lead to novel ways to control tick-borne zoonoses. This study shows that Francisella-like endosymbionts were ubiquitous in Hyalomma, were maternally transmitted, and co-speciated with their hosts. These findings imply that the interaction between FLE and Hyalomma is of an obligatory nature. It provides an example of an integrative taxonomy approach to simply differentiate among species infesting the same host and to identify nymphal and larval stages to be used in further studies. In addition, it shows the potential of imported Hyalomma ticks to serve as a vector for spotted fever group rickettsiae. The information gathered in this study can be further implemented in the development of symbiont-based disease control strategies for the benefit of human health (Azagi et al. 2017).
Molecular assays were used to detect and characterize two agents of zoonotic importance, Coxiella burnetii and Rickettsia spp. in 194 peridomestic rodents captured in a peri-urban setting in Nigeria, and 32 pools of ectoparasites removed from them, to determine their possible role in the epidemiology of these diseases in this country. Targeting and characterizing the insertion sequence IS1111, C. burnetii DNA was detected in 4 out of 194 (2.1%) rodents comprising 3 out of 121 (2.5%) Rattus norvegicus and 1 out of 48 (2.1%) Rattus rattus screened in this study. Rickettsia spp. DNA was detected in two Rhipicephalus sanguineus sensu lato pools (i.e. RT1 and RT4) using the citrate synthase (gltA) gene and further characterized by amplification and sequence analysis of six genes to determine their identity. The RT1 sample consistently gave 98-100% identity to Rickettsia conorii str. Malish 7 for the various genes and loci studied (Kamani et al. 2018a).
Using polymerase chain reaction targeting the 18S rRNA gene and DNA sequencing the prevalence and diversity of Apicomplexa and Piroplasmida infections in rodents from Nigeria was studied. Overall, 13 of 194 (7.7%) rodent blood samples tested were positive for Hepatozoon spp. while 2 (1.0%) were positive for Sarcocystis dispersa. Hepatozoon spp. DNA was detected in all the rodent species tested except Neotoma spp., and was most prevalent (50%) in the African giant rat (Cricetomys gambianus), followed by Mus musculus (18.2%), Rattus rattus (6.3%) and Rattus norvegicus (4.1%). The Hepatozoon spp. DNA sequences from the rodents were 98-100% identical to each other and to Hepatozoon spp. DNA sequence from small mammals deposited in GenBank. Five of the sequences from R. rattus (n = 2) and R. norvegicus (n = 3) were 98-99% identical to Hepatozoon felis (KY649442.1). Sarcocystis dispersa DNA was detected in one R. rattus (2.1%) and one R. norvegicus (0.8%). The pools of Rhipicephalus sanguineus and Haemaphysalis leachi were negative (Kamani et al. 2018b).
The aim of this study was to determine the bacterial and protozoan vector-borne pathogens in ticks infesting humans in the Corum province of Turkey. From March to November 2014 a total of 322 ticks were collected from patients who attended the local hospitals with tick bites. Ticks were screened by real time-PCR and PCR, and obtained amplicons were sequenced. The detected tick was belonging to the genus Hyalomma, Haemaphysalis, Rhipicephalus, Dermacentor and Ixodes. A total of 17 microorganism species were identified in ticks. The most prevalent Rickettsia spp. were: R. aeschlimannii (19.5%), R. slovaca (4.5%), R. raoultii (2.2%), R. hoogstraalii (1.9%), R. sibirica subsp. mongolitimonae (1.2%), R. monacensis (0.31%), and Rickettsia spp. (1.2%). In addition, the following pathogens were identified: Borrelia afzelii (0.31%), Anaplasma spp. (0.31%), Ehrlichia spp. (0.93%), Babesia microti (0.93%), Babesia ovis (0.31%), Babesia occultans (3.4%), Theileria spp. (1.6%), Hepatozoon felis (0.31%), Hepatozoon canis (0.31%), and Hemolivia mauritanica (2.1%). All samples were negative for Francisella tularensis, Coxiella burnetii, Bartonella spp., Toxoplasma gondii and Leishmania spp. (Karasartova et al. 2018).
In order to investigate the species distribution, epidemiology and seasonal dynamics of ticks infesting horses in Israel, 3267 ticks were collected from 396 horses in 24 farms across the country from July 2014 to June 2015. Ticks were found on 50% of the farms and on 25% of the horses, with Hyalomma being the most prevalent genus (70% of ticks). Pasture was the most prominent risk factor for tick infestation (99% of ticks, P < 0.001), and is represented here by two areas with a Mediterranean climate that differ in their environmental characteristics: the Golan Heights (GH, 74% of ticks); and the Carmel mountain ridge (CMR, 24%). Although these two sites are less than 100 km apart, the composition of the tick populations infesting horses differed significantly between them. In GH the most abundant tick species was Hyalomma excavatum (P < 0.001), while in CMR it was Hyalomma marginatum (P < 0.001). The GH also hosted a more diverse tick fauna than the CMR, including Haemaphysalis parva (peaking in the autumn, P < 0.001) and Rhipicephalus turanicus (peaking in the spring, P < 0.001), which were not found at the other sites. A few Rhipicephalus bursa, Hyalomma rufipes and Hyalomma turanicum were also found on horses (Tirosh-Levy et al. 2018).
Babesia microti is an important tick-borne zoonotic parasite with rodents serving as reservoir hosts. In the present study, 536 rodents were captured from Burdur, Bartin, Giresun, and Yozgat provinces of Turkey between the years 2010 and 2012, and blood samples were examined for the presence of Babesia spp. using conventional PCR which targeted the 18S rRNA gene. The sequence analysis of PCR amplicons was tested for B. microti as well as for Hepatozoon spp., and Sarcocystis spp. Overall, 5.8% of the rodents were positive for B. microti: 41% in Myodes glareolus, 7.7% in Chionomys roberti, and 2% in Apodemus spp., whereas no Babesia DNA was detected in Mus macedonicus and Microtus spp. Six rodents were positive for Hepatozoon spp. and one rodent was positive for Sarcocystis spp. Overall, 14.9 and 4.5% of rodents captured from Bartin and Giresun provinces, respectively, were PCR positive for B. microti, whereas none of rodents captured in Burdur and Yozgat were positive for Babesia spp. The sequence data of B. microti from rodents revealed that all sequences belonged to the zoonotic genotype. Sequences of B. microti obtained from rodents of the Bartin province were genotypically closer to European isolates, whereas those obtained from rodents of the Giresun province were closer to Russian and Mongolian isolates (Usluca et al. 2019).
Theileria equi is an important tick-borne pathogen of horses that is highly endemic in many parts of the world, including Israel. The present study evaluated the potential roles of five hard tick species [Hyalomma excavatum Koch, 1844; Hyalomma marginatum Koch, 1844; Rhipicephalus turanicus Pomerantsev 1936; Rhipicephalus annulatus Say, 1821; Haemaphysalis parva (Neumann, 1897) (all: Ixodida: Ixodidae)], previously found to infest horses in Israel, in acting as vectors for piroplasmosis. For this, DNA was extracted from whole ticks and, when possible, from the salivary glands in each species (n = 10-59). Polymerase chain reaction amplification and sequencing of the 18S rRNA gene were used to detect T. equi in 48 of the 127 ticks (37.8%) and in 21 of the 90 extracted salivary glands (23.3%) in all five species. All but two sequences were classified as T. equi genotype A; the remaining two were classified as genotype D. The findings of this study point to H. parva and R. annulatus as potential novel vectors of T. equi, and suggest that parasite genotype selection occurs within the tick vector (TiroshLevy et al. 2020).
Azagi T, Klement E, Perlman G, Lustig Y, Mumcuoglu KY, Apanaskevich DA, Gottlieb Y. 2017. Francisella-like endosymbionts and Rickettsia species in local and imported Hyalomma ticks. Appl Environ Microbiol. 2017 Aug 31; 83(18). pii: e01302-17. doi: 10.1128/AEM.01302-17.
Ereqat S, Nasereddin A, Al-Jawabreh A, Azmi K, Harrus S, Mumcuoglu K, Apanaskevich D, Abdeen Z. 2016. Molecular detection and identification of Spotted Fever Group Rickettsiae in ticks collected from the West Bank, Palestinian Territories.PLoS Negl Trop Dis 10(1): e0004348. doi:10.1371/journal.pntd.0004348.
Friedemann, G., Izhaki, I., Leshem, L. & K.Y. Mumcuoglu. 2013. Alternative nestbuilding behavior of the Long-legged Buzzard (Buteo rufinus) and the Short-toed Eagle (Circaetus gallicus) in the Judean Foothills, and the parasitic and non-parasitic arthropod fauna in their nests. Isr. J. Entomol. 43: 11-19.
Guberman, D., K.Y. Mumcuoglu, A. Keysari, I. Ioffe-Uspensky, J. Miller & R. Galun. 1996. Prevalence of spotted fever group rickettsiae in ticks from Southern Israel. J. Med. Entomol. 33:979-982.
Harrus S, Perlman-Avrahami A, Mumcuoglu KY, Morick D, Baneth G. 2010a. Molecular detection of Rickettsia massiliae, Rickettsia sibirica mongolitimonae and Rickettsia conorii israelensis in ticks from Israel. Clin Microbiol Infect. DOI. 10.1111/j.1469-0691.2010.03224.x
Harrus S, Perlman-Avrahami A, Mumcuoglu KY, Morick D, Baneth G. 2010b. Molecular detection of Ehrlichia canis, Anaplasma bovis, Anaplasma platys, Candidatus Midichloria mitochondrii and Babesia canis vogeli in ticks from Israel. Eur. Soc. Clin. Microbiol. Infect. Dis. 10.1111/j.1469-0691.2010.03316.x
Ioffe-Uspensky, I., K.Y. Mumcuoglu, I. Uspensky & R.Galun. 1997. Rhipicephalus sanguineus and Rhipicephalus turanicus (Acari:Ixodidae): Closely related species with different biological characteristics. J. Med. Entomol. 34: 74-81.
Kamani J, G. Baneth, KY Mumcuoglu, NE Waziri, O Eyal, Y Guthmann, S Harrus. 2013b. Molecular detection and characterization of tick-borne pathogens in dogs and ticks from Nigeria. PLoS NTDs Link
Kamani, J, Morick D, Mumcuoglu KY, Harrus S. 2013a. Prevalence and diversity of Bartonella species in commensal rodents and ectoparasites from Nigeria, West Africa. PLoS Neg Trop Dis 7 (5): e2246. doi:10.1371/journal.pntd.0002246.
Kamani J, Baneth G, Apanaskevich DA, Mumcuoglu KY, Harrus S. 2015. Molecular detection of Rickettsia aeschlimannii in Hyalomma spp. ticks from camels (Camelus dromedarius) in Nigeria, West Africa. Med. Vet. Entomol. doi: 10.1111/mve.12094.
Kamani J, Baneth G, Gutiérrez R, Nachum-Biala Y, Mumcuoglu KY, Harrus S. 2018a. Coxiella burnetii and Rickettsia conorii: Two zoonotic pathogens in peridomestic rodents and their ectoparasites in Nigeria. Ticks Tick Borne Dis. 2018;9(1):86–92. doi:10.1016/j.ttbdis.2017.10.004.
Kamani J, Harrus S, Nachum-Biala Y, Gutiérrez R, Mumcuoglu KY, Baneth G. 2018b. Prevalence of Hepatozoon and Sarcocystis spp. in rodents and their ectoparasites in Nigeria. Acta Tropica 187: 124-128.
Karasartova D, Gureser AS, Gokce T, Celebi B, Yapar D, Keskin A, et al. 2018. Bacterial and protozoal pathogens found in ticks collected from humans in Corum province of Turkey. PLoS Negl Trop Dis 12(4): e0006395.
Keysary, A., R. Massung, M. Inbar, A. Wallach, U. Shanas, K.Y. Mumcuoglu & T. Waner. 2007. First direct evidence of the prevalence of Anaplasma phagocytophilum in Israel. EID 13: 1411-1412.
Keysary, A.; Eremeeva, M.; Leitner, M.; Beth Din, A.; Wikswo, M.; Mumcuoglu, K.Y.; Inbar, M.; Wallach, A.; Shanas, U.; King, R.; Waner, T. 2011. Spotted fever group rickettsiae in ticks collected from wild animals in Israel. Amer. J. Trop. Med. Hyg. 85: 919-923.
Kleinerman G, Baneth G,. Mumcuoglu KY, van Straten M, Berlin D, Apanaskevich DA, Abdeen Z, Nasereddin A, Harrus S. 2013. Molecular detection of Rickettsia africae, Rickettsia aeschlimannii and Rickettsia sibirica mongolitimonae in camels and Hyalomma spp. ticks from Israel. Vector-borne Zoonotic Dis. 13: 1-6. DOI: 10.1089/vbz.2013.1330
Salant, H., Mumcuoglu, K.Y., Baneth, G. 2013. Ectoparasites in urban stray cats in Jerusalem, Israel: differences in infestation patterns of fleas, ticks and permanent ectoparasites. Med. Vet. Entomol. 28: 314-318, doi: 10.1111/mve.12032.
Lalzar, I., S. Harrus, K.Y. Mumcuoglu, & Y. Gottlieb. 2012. Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl. Environm. Microbiol. 78:4110-4116.
Levin, M.L., L. Killmaster, G. Zemtsova, D. Grant, K.Y. Mumcuoglu, M.E. Eremeeva & G.A. Dasch. 2009. Incongruent effects of two isolates of Rickettsia conorii on the survival of Rhipicephalus sanguineus ticks. Exp. Appl. Acarol. DOI:10.1007/s10493- 009-9268-9.
Levin ML, Studer E, Killmaster L, Zemtsova G, Mumcuoglu KY. 2012. Crossbreeding between different geographical populations of the brown dog tick, Rhipicephalus sanguineus (Acari: Ixodidae). Exp Appl Acarol. 2012 Apr 21.
Mumcuoglu, K.Y., K. Frish, R. Galun, B. Sarov, E. Manor & E. Gross. 1990. Ecological and epidemiological studies on Mediterranean Spotted Fever in the Negev Desert of Israel. Virginia J. Sci. 41:159-160.
Mumcuoglu, K.Y., K. Frish, B. Sarov, E. Manor, E. Gross, Z. Gat & R. Galun. 1993a. Ecological studies on the brown dog tick Rhipicephalus sanguineus in Southern Israel and its relationship to spotted fever group rickettsiae. J. Med. Entomol. 30:114-121.
Mumcuoglu, K.Y., I. Burgan, I. Ioffe-Uspensky & O. Manor. 1993b. Rhipicephalus sanguineus: Observations on the parasitic stage on dogs in the Negev Desert of Israel. Appl. Exp. Acarol. 17:793-798.
Mumcuoglu, K.Y., I. Ioffe-Uspensky, S. Alkrinawi, B. Sarov, E. Manor & R. Galun. 2001. Prevalence of vectors of the spotted fever group rickettsiae and murine typhus in a Bedouin town in Israel. J. Med. Entomol. 38: 458-461.
Mumcuoglu, K.Y., A. Keysary & L. Gilead. 2002. Mediterranean spotted fever in Israel: a tick borne disease. Isr. Med. Ass. J. 4: 44-49.
Rose J, Nachum-Biala Y, Mumcuoglu KY, Alkhamis MA, Ben-Nun A, Lensky I, Klement E, Nasereddin A, Abdeen ZA, Harrus S. 2017. Genetic characterization of spotted fever group rickettsiae in questing ixodid ticks collected in Israel and environmental risk factors for their infection. Parasitology 23: 1-14. doi: 10.1017/S0031182017000336.
Sands F, Apanaskevich D, Matthee S, Horak I, Harrison A, Karim S, Mohammad M, Mumcuoglu KY, Rajakaruna R, Santos-Silva M, Kamani J. 2017. Effects of tectonics and large scale climatic changes on the evolutionary history of Hyalomma ticks. Mol. Phylogenet. Evol. 114: 153-165. doi: 10.1016/j.ympev.2017.06.002.
Tirosh-Levy S, Gottlieb Y, Apanaskevich DA, Mumcuoglu KY, Steinman A. 2018. Species distribution and seasonal dynamics of equine tick infestation in two Mediterranean climate niches in Israel. Parasites and Vectors 11:546. Link
Tirosh-Levy S, Steinman A, Einhorn A, Apanaskevich DA, Mumcuoglu KY, Gottlieb Y. 2020. Potential tick vectors for Theileria equi in Israel. Med. Vet. Entomol. doi: 10.1111/mve.12435.
Usluca S, Celebi B, Karasartova D, Gureser AM, Matur F, Oktem MA, Sozen M, Karatas A, Babur C, Mumcuoglu KY, Taylan Ozkan A. 2019. Molecular survey of Babesia microti (Aconoidasida: Piroplasmida) in wild rodents in Turkey. J. Med. Entomol. X X(X), 2019, 1–5, doi: 10.1093/jme/tjz084.
Uspensky, I., I. Ioffe-Uspensky, K.Y. Mumcuoglu & R. Galun. 1999. Body weight characteristics of some ixodid ticks: Reflecting adaptations to conditions of their habitats. In: Ecology and Evolution of the Acari. J. Bruin, L.P.S. van der Geest & M.W. Sabelis (eds.), pp. 657-665, Kluwer, the Netherlands.
Wallach, A.D., U. Shanas, K.Y. Mumcuoglu & M. Inbar. 2008. Ectoparasites on reintroduced roe deer Capreolus capreolus in Israel. J. Wildl. Dis. 44: 693-696.
Waner, T., Keysary, A., Eremeeva, M.A., Beth Din, A., Mumcuoglu, K.Y., King, R. & Y. Atiya-Nasagi. 2014. Rickettsia africae and Candidatus Rickettsia barbariae in ticks in Israel. Am. J. Trop. Med. Hyg., 90: 920–922. doi:10.4269/ajtmh.13-0697.
Zemtsova, G., L. F. Killmaster, K. Y. Mumcuoglu & M. L. Levin. 2010. Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks. Exp. Appl. Acarol. 52: 383-392. DOI 10.1007/s10493-010-9375-7.
Additional publications on this subject
Ioffe-Uspensky, I., I. Uspensky, K.Y. Mumcuoglu & R. Galun. 2005. Rhipicephalus sanguineus and R. turanicus (Acari: Ixodidae): Numerical indices for distinguishing between adults of closely related species in Israel. Proceedings of the 5th International Conferences on Ticks and Tick-Borne Pathogens, University of Neuchatel, Switzerland, August 29-September 2, 2005, p. 171-175.
Kassis, I., I. Ioffe-Uspensky, I. Uspensky & K.Y. Mumcuoglu. 1997. Human toxicosis caused by the tick Ixodes redikorzevi in Israel: A case report. Isr. J. Med. Sci. 33: 760-61.
Podvinec, M., J. Ulrich, T. Rufli & K.Y. Mumcuoglu. 1984. Facialis palsies of infectious origin. Proc. Intern. Symp. Facial Nerve, Bordeaux, Sept. 3.-6., pp. 283-286.
Ramot, Y. A. Zlotogorski & K.Y. Mumcuoglu. 2012. Brown dog tick (Rhipicephalus sanguineus) infestation of the penis detected by dermoscopy. Intnl. J. Dermatol. DOI: 10.1111/j.1365-4632.2010.04756.x
Rufli, T. & K.Y. Mumcuoglu. 1981. Dermatological Entomology. 18./19. Ixodidae/Hard ticks and Argasidae/Soft ticks (in German). Schweiz. Rundschau Med. 70:362-385.