Comments on controversial tick (Acari: Ixodida) species names and species described or resurrected from 2003 to 2008

There are numerous discrepancies in recent published lists of the ticks of the world. Here we review the controversial names, presenting evidence for or against their validity and excluding some altogether. We also address spelling errors and present a list of 17 species described or resurrected during the years 2003–2008. We consider the following 35 tick species names to be invalid: Argas fischeri Audouin, 1826, Ornithodoros boliviensis Kohls and Clifford, 1964, Ornithodoros steini (Schulze, 1935), Amblyomma acutangulatum Neumann, 1899, Amblyomma arianae Keirans and Garris, 1986, Amblyomma bibroni (Gervais, 1842), Amblyomma colasbelcouri (Santos Dias, 1958), Amblyomma concolor Neumann, 1899, Amblyomma cooperi Nuttall and Warburton, 1908, Amblyomma curruca Schulze, 1936, Amblyomma cyprium Neumann, 1899, Amblyomma decorosum (Koch, 1867), Amblyomma nocens Robinson, 1912, Amblyomma perpunctatum (Packard, 1869), Amblyomma striatum Koch, 1844, Amblyomma superbum Santos Dias, 1953, Amblyomma testudinis (Conil, 1877), Amblyomma trinitatis Turk, 1948, Dermacentor confractus (Schulze 1933), Dermacentor daghestanicus Olenev, 1928, Haemaphysalis himalaya Hoogstraal, 1966, Haemaphysalis vietnamensis Hoogstraal and Wilson, 1966, Hyalomma detritum Schulze, 1919, Ixodes apteridis Maskell, 1897, Ixodes donarthuri Santos Dias, 1980, Ixodes kempi Nuttall, 1913, Ixodes neotomae Cooley, 1944, Ixodes rangtangensis Teng, 1973, Ixodes robertsi Camicas, Hervy, Adam and Morel, 1998, Ixodes serrafreirei Amorim, Gazetta, Bossi and Linhares, 2003, Ixodes tertiarius Scudder, 1885, Ixodes uruguayensis Kohls and Clifford, 1967, Ixodes zealandicus Dumbleton, 1961, Ixodes zumpti Arthur, 1960 and Rhipicephalus camelopardalis Walker and Wiley, 1959. We consider the following 40 names valid: Argas delicatus Neumann, 1910, Argas vulgaris Filippova, 1961, Ornithodoros aragaoi Fonseca, 1960, Ornithodoros dugesi Mazzoti, 1943, Ornithodoros knoxjonesi Jones and Clifford, 1972, Ornithodoros marocanus Velu, 1919, Ornithodoros nattereri Warburton, 1927, Amblyomma beaurepairei Vogelsang and Santos Dias, 1953, Amblyomma crassipes (Neumann, 1901), Amblyomma echidnae Roberts, 1953, Amblyomma fuscum Neumann, 1907, Amblyomma orlovi (Kolonin, 1995), Amblyomma parkeri Fonseca and Arag?o, 1952, Amblyomma pseudoconcolor Arag?o, 1908, Bothriocroton oudemansi (Neumann, 1910), Bothriocroton tachyglossi (Roberts, 1953), Dermacentor abaensis Teng, 1963, Dermacentor confragus (Schulze 1933), Dermacentor ushakovae Filippova and Panova, 1987, Haemaphysalis anomaloceraea Teng, 1984, Haemaphysalis filippovae Bolotin, 1979, Haemaphysalis pavlovskyi Pospelova-Shtrom, 1935, Hyalomma excavatum Koch, 1844, Hyalomma isaaci Sharif, 1928, Hyalomma rufipes Koch, 1844, Hyalomma turanicum Pomerantzev, 1946, Ixodes arabukiensis Arthur, 1959, Ixodes boliviensis Neumann, 1904, Ixodes columnae Takada and Fujita, 1992, Ixodes maslovi Emel′yanova and Kozlovskaya, 1967, Ixodes sachalinensis Filippova, 1971, Ixodes siamensis Kitaoka and Suzuki, 1983, Ixodes sigelos Keirans, Clifford and Corwin, 1976, Ixodes succineus Weidner, 1964, Rhipicephalus aurantiacus Neumann, 1907, Rhipicephalus cliffordi Morel, 1965, Rhipicephalus pilans Schulze, 1935, Rhipicephalus pseudolongus Santos Dias, 1953, Rhipicephalus serranoi Santos Dias, 1950 and Rhipicephalus tetracornus Kitaoka and Suzuki, 1983.     

Photoperiodic Control of Developmental Diapause in Nymphs of Prostriate Ixodid Ticks (Acari: Ixodidae)

Extrinsic control of developmental diapause in nymphs of prostriate ticks of the subgenus Ixodes sensu stricto (Ixodes ricinus and Ixodes persulcatus from Eurasia and Ixodes scapularis from North America) appears to be based on a complex two-step photoperiodic reaction of a short-day/long-day type. Diapause control in the subgenus Afrixodes (the South African tick Ixodes rubicundus) appears to be based on a simple long-day reaction. The option between non-diapause development and diapausing arrest in engorged nymphs is determined by both pre- and post-feeding photoperiodic regimes. Consequently diapausing arrest in engorged nymphs of Ixodes sensu stricto can be induced either by a short-day (after their engorgement) or by a long-day regime (in unfed nymphs), while active, non-diapause development is possible only when the short-day pre-feeding regime is followed by a long-day post-feeding regime. The photoperiodic response in I. (Afrixodes) rubicundus nymphs seems to be of the long-day type both before and after feeding. Consequently this non-diapause development is enabled by a long-day regime, while diapause is induced by a short-day regime of exposure. Nevertheless, there are some indications that the control of nymphal diapause in the latter species is also of a complex nature. This revised version was published online in July 2006 with corrections to the Cover Date.     

Borrelia burgdorferi sensu lato in ticks (Acari: Ixodidae) from two different foci in Spain

The prevalence of Borrelia burgdorferi sensu lato in several tick species was studied over a 2 year period in two ecologically different areas in Spain. One area was an endemic area for Lyme disease, with a number of autochthonous human cases and supported large populations of Ixodes ricinus on cattle and birds; the second area was characterized by the absence of I. ricinus together with the presence of foxes and their associated tick species. While I. ricinus was the main vector of B. burgdoreri in the endemic area (with a mean prevalence of 14% in adults and 51% in nymphs), adults of both Ixodes canisuga and Ixodes hexagonus had high rates of B. burgdorferi prevalence (30 and 28%, respectively) in the zone where I. ricinus was absent. Immatures of Ixodes frontalis were found to be carriers of the spirochete only in those zones where I. ricinus is present, suggesting evidence for reservoir competence in a tick-bird cycle.     

Description of three new species of Ixodes Latreille, 1795 (Acari: Ixodidae), parasites of tenrecs (Afrotheria: Tenrecidae) on Madagascar

Ixodes soarimalalae n. sp., Ixodes uilenbergi n. sp. and Ixodes uncus n. sp. (Acari: Ixodidae), are described based on females ex various species of tenrecs (Afrosoricida: Tenrecidae) from Madagascar. Females of all of these new species are similar to those of other species of the subgenus Afrixodes Morel, 1966 known from Madagascar, from which they can be distinguished and from one other by the size of scutum, size of scutal setae, shape of alloscutal setae, shape of genital aperture, development of genital apron, size of auriculae, size of anterior angle of basis capituli, size of palpi, dental formula on hypostome and size and development of spurs on coxa I.

     

Ticks (Acari: Ixodidae) parasitizing migrating and local breeding birds in Finland

Ticks are globally renowned vectors for numerous zoonoses, and birds have been identified as important hosts for several species of hard ticks (Acari: Ixodidae) and tick-borne pathogens. Many European bird species overwinter in Africa and Western Asia, consequently migrating back to breeding grounds in Europe in the spring. During these spring migrations, birds may transport exotic tick species (and associated pathogens) to areas outside their typical distribution ranges. In Finland, very few studies have been conducted regarding ticks parasitizing migrating or local birds, and existing data are outdated, likely not reflecting the current situation. Consequently, in 2018, we asked volunteer bird ringers to collect ticks from migrating and local birds, to update current knowledge on ticks found parasitizing birds in Finland. In total 430 ticks were collected from 193 birds belonging to 32 species, caught for ringing between 2018 and 2020. Furthermore, four Ixodes uriae were collected from two roosting islets of sea birds in 2016 and 2020. Ticks collected on birds consisted of: Ixodes ricinus (n?=?421), Ixodes arboricola (4), Ixodes lividus (2) and Hyalomma marginatum (3). Ixodes ricinus loads (nymphs and larvae) were highest on thrushes (Passeriformes: Turdidae) and European robins (Erithacus rubecula). The only clearly imported exotic tick species was H. marginatum. This study forms the second report of both I. uriae and I. arboricola from Finland, and possibly the northernmost observation of I. arboricola from Europe. The importation of exotic tick species by migrating birds seems a rare occurrence, as over 97% of all ticks collected from birds arriving in Finland during their spring migrations were I. ricinus, a species native to and abundant in Finland.

     

Ixodid ticks in Bosnia and Herzegovina

Ticks of the Ixodidae family represent an enormous threat to human and animal health. From January to December 2004, a total of 10,050 ixodid ticks were collected from 26 areas in Bosnia and Herzegovina and determined to the species level. Ticks were collected from dogs, sheep, cows, goats, rodents, humans and plants. Ixodes ricinus was the most prevalent species, followed by Dermacentor marginatus marginatus, Rhipicephalus bursa, Hyalomma marginatum marginatum, Rhipicephalus sanguineus, Haemaphysalis punctata, Dermacentor reticulatus and Ixodes hexagonus.     

Infestation of urban populations of the Northern white‐breasted hedgehog,Erinaceus roumanicus,by Ixodes spp. ticks in Poland

Infestation by the nest‐dwelling Ixodes hexagonus Leach and the exophilic Ixodes ricinus (Linnaeus) (Ixodida: Ixodidae) on the Northern white‐breasted hedgehog, Erinaceus roumanicus (Erinaceomorpha: Erinaceidae), was investigated during a 4‐year study in residential areas of the city of Poznań, west‐central Poland. Of 341 hedgehogs, 303 (88.9%) hosted 10 061 Ixodes spp. ticks encompassing all parasitic life stages (larvae, nymphs, females). Ixodes hexagonus accounted for 73% and I. ricinus for 27% of the collected ticks. Male hedgehogs carried significantly higher tick burdens than females. Analyses of seasonal prevalence and abundance of I. hexagonus revealed relatively stable levels of infestation of all parasitic stages, with a modest summer peak in tick abundance noted only on male hosts. By contrast, I. ricinus females and nymphs peaked in spring and declined steadily thereafter in summer and autumn, whereas the less abundant larvae peaked in summer. This is the first longterm study to evaluate the seasonal dynamics of both tick species on populations of wild hedgehogs inhabiting urban residential areas.     

Preliminary studies on virus and spirochete accumulation in the cement plug of ixodid ticks

We provide evidence that tick-borne encephalitis virus and Borrelia burgdorferi s.l. are accumulated in the cement plug in the host skin within the first few hours after tick attachment. Extirpation of the tick without the cement plug, even very soon after the attachment, did not prevent the transmission by Ixodes ricinus, Ixodes persulcatus or Dermacentor reticulatus to mice. This was within 1 hour in the case of the TBE virus and after 20–22 h of attachment, in the case of Borrelia and I. persulcatus. The epidemiological significance of these findings is discussed.     

Maps of ticks (Acari: Argasidae,Ixodidae) for Austria and South Tyrol,Italy

A first compilation of georeferenced tick locations in Austria and South Tyrol, Italy, is presented here. This allows the tick fauna to be examined in the various climatic regions of the European Alps. The dataset comprises 424 tick locations of Austria and 48 tick locations of South Tyrol, which were digitized from literature and visualized in the form of geographical maps. The tick fauna of Austria includes two species of Argasidae in the genera Argas and Carios and 15 species of Ixodidae in the genera Dermacentor, Haemaphysalis, and Ixodes, altogether 17 tick species. In addition, two species of Ixodidae in the genera Hyalomma (each spring imported by migratory birds) and Rhipicephalus (occasionally imported by dogs returning from abroad with their owners) are included in the tick atlas. Of these, the georeferenced locations of 18 tick species are depicted in maps. The occurrence of the one remaining tick species, Ixodes inopinatus, is given at the level of the federal states. The first Austrian distribution map of the long-legged bat tick Ixodes vespertilionis, which was reported from 21 caves, deserves special mention. The most common and widespread tick species is Ixodes ricinus, with records in all nine federal states of Austria, followed by Ixodes canisuga, Ixodes hexagonus, and I. vespertilionis in six federal states each. Haemaphysalis concinna and Dermacentor reticulatus are only endemic in the eastern plains, while Dermacentor marginatus only occurs in the west, in the Tyrolean Alpine valleys. Eight tick species were reported from South Tyrol, Italy. There, the most frequently flagged tick from the vegetation is also I. ricinus, while D. marginatus and Haemaphysalis punctata are often collected from sheep. The locations are shown together with those from North and East Tyrol on a separate Tyrol map. The tick atlas in Austria and South Tyrol as well as the underlying digital dataset in the supplement contribute to the closing of data gaps in global distribution maps of ticks and improve the data basis for new species distribution models.

     

Borrelia tanukii Sp. Nov. and Borrelia turdae Sp. Nov. Found from Ixodid Ticks in Japan: Rapid Species Identification by 16S rRNA Gene-Targeted PCR Analysis

Based on the results of RFLP-ribotyping, whole DNA/DNA hybridization and phylogenetic analysis of the 16S rRNA gene, we previously defined two genomic groups of spirochetes closely related to Borrelia burgdorferi sensu lato: group Hk501 for strains isolated from Ixodes tanuki ticks and group Ya501 for strains isolated from Ixodes turdus ticks. In this report, we propose that group Hk501 should be classified as Borrelia tanukii sp. nov. and group Ya501 as Borrelia turdae sp. nov. The alignment of previously published Borrelia 16S rRNA gene sequences led us to design species-specific PCR primer sets. The primers allowed the rapid identification of B. tanukii and B. turdae.     

Detection of tick‐borne pathogens in ticks from migratory birds in the Baltic region of Russia

We report the finding of tick‐borne encephalitis (TBE)‐virus in indigenous Ixodes ricinus (L.), ‘Candidatus Neoehrlichia mikurensis’ in exotic Ixodes frontalis (Panzer) and Rickettsia aeshlimannii in exotic Hyalomma marginatum Koch subadult ticks detached from 18.5% (107/577) infested migratory birds in the Baltic region of Russia. This is the first record of human pathogenic ‘Candidatus N. mikurensis’ in I. frontalis ticks. Moreover, seven other pathogens were identified in I. ricinus ticks. Spotted Fever Group rickettsiae were the predominant pathogen group and were detected only in nymphs. Future investigations are warranted to further characterize the role of birds in the epizootiology of tick‐borne pathogens in this region.     

Variability in cuticular hydrocarbons and phenotypic discrimination of Ixodes ricinus populations (Acarina: Ixodidae) from Europe

The cuticular hydrocarbon composition and a stepwise discriminant analysis are used to elucidate the phenotypic relationships of 66 populations of Ixodes ricinus in Europe. The method correctly allocates Ixodes persulcatus (outgroup) populations away from the main cluster of I. ricinus samples and separates the samples into ten relatively defined clusters of specimens. Populations from Poland are inseparable from samples collected in Germany, Switzerland and the Italian Alps, while individuals from Slovakia and the Czech Republic come into separate groups of phenotypic similarity. Irish and British specimens are separated but highly related and Spanish populations show an unexpectedly high distance from the remaining clusters.     

Recent discovery of widespread Ixodes affinis (Acari: Ixodidae) distribution in North Carolina with implications for Lyme disease studies

Ixodes affinis, which is similar morphologically to Ixodes scapularis, is widely distributed in North Carolina. Collections have documented this species in 32 of 41 coastal plain counties, but no piedmont or mountain counties. This coastal plain distribution is similar to its distribution in Georgia and South Carolina, where it is considered an enzootic vector of Borrelia burgdorferi sensu stricto. An updated list of hosts for I. affinis in the U.S.A. is included, increasing the number to 15 mammal and one bird species. The presence of questing adults of I. affinis from April to November reinforces the need for confirmed identifications of suspected tick vectors of Borrelia spirochetes collected during warm months.     

Transmission of Lyme disease spirochetes (Borrelia burgdorferi)

The field and laboratory evidence incriminating nymphalIxodes dammini as the main vectors ofBorrelia burgdorferi is substantial. Furthermore, other members of theIxodes (Ixodes) ricinus complex, includingI. ricinus, I. persulcatus, I. pacificus, andI. scapularis, are competent vectors of the Lyme disease spirochete. Although ticks in other genera are also naturally infected withB. burgdorferi, experimental evidence suggests thatAmblyomma andDermacentor ticks are inefficient vectors of these spirochetes. Current research on the kinetics ofB. burgdorferi growth within ticks demonstrates that Lyme disease spirochetes are dramatically influenced by physiological events during the tick's life-cycle.     

First survey on hard ticks (Ixodidae) collected from humans in Romania: possible risks for tick-borne diseases

The importance of studies on the diversity of ticks attacking humans resides mostly in the relatively highly-specific tick-pathogen associations. Human tick bites are commonly reported worldwide but removal of ticks from patients is rarely followed by specific identification of the ticks, leaving to some degree of hazard the preventive treatment of possible associated diseases. A total number of 308 ticks were collected between April and June 2010 from 275 human patients who voluntarily presented to a hospital from Cluj-Napoca, Romania. The mean intensity of infection was 1.12 ± 0.46. Four species of ticks were identified Ixodes ricinus, Dermacentor marginatus, Haemaphysalis concinna and H. punctata. Ixodes ricinus was the most abundant species feeding on humans in the study area. A brief review of possible associated pathogen is provided.     

Molecular detection and identification of piroplasms (Babesia spp. and Theileria spp.) and Anaplasma phagocytophilum in questing ticks from northwest Spain

Anaplasma phagocytophilum and some piroplasm species are pathogens mainly transmitted by Ixodes ricinus. Considering that this tick species is predominant in north‐western Spain, individual specimens (652 nymphs, 202 females and 202 males) and 23 larval pools were processed to determine the prevalence of these pathogens in questing I. ricinus from that region. Additionally, Dermacentor marginatus, Dermacentor reticulatus, Ixodes frontalis and Ixodes acuminatus were individually analysed. The groESL operon as well as the 16S rRNA and msp2 genes of Anaplasma were analysed. Similarly, piroplasms were identified at the 18S rRNA gene and the ITS1 of Babesia spp. and Theileria spp. Babesia venatorum (1.5%), A. phagocytophilum (0.7%), Babesia microti (0.3%) and Theileria sp. OT3 (0.2%) were detected in I. ricinus. A single I. frontalis (8.3%) tested positive to A. phagocytophilum. Although a low percentage of I. ricinus were infected with A. phagocytophilum and piroplasms, a potentially human pathogenic variant of A. phagocytophilum was detected, and both Babesia species found were zoonotic. Since the vector of Theileria sp. OT3 remains unknown, further investigations are needed to unravel the role of I. ricinus in the transmission of this piroplasm.     

Seasonal incidence of Ixodes ricinus ticks (Acari: ixodidae) on rodents in western France

Data collected from a longitudinal survey carried out over 2 years on four farms in western France were used to assess the incidence and infestation of Ixodes ricinus on rodents. Once a month, on each farm, 25 Sherman live traps were set in hedges bordering selected pastures. A total of 799 micromammals were examined, including Apodemus sylvaticus, Clethrionomys glareolus, Microtus agrestis, Microtus arvalis, and Crocidura spp. Larvae and nymphs of I. ricinus were found. Small numbers of Ixodes (Exopalpiger) trianguliceps were also recovered from each farm. The mean infestation rate of the I. ricinus larvae (1.6–5.9) among all animals examined varied between farms Most animals were infested by only a single tick, but one M. agrestis harboured 43 I. ricinus larvae. Larvae or nymphs were found throughout the year, with peaks from March to October.     

Detection of Lyme disease spirochete,Borrelia burgdorferi sensu lato,including three novel genotypes in ticks (Acari: Ixodidae) collected from songbirds (Passeriformes) across Canada

Lyme disease is reported across Canada, but pinpointing the source of infection has been problematic. In this three‐year, bird‐tick‐pathogen study (2004–2006), 366 ticks representing 12 species were collected from 151 songbirds (31 passerine species/subspecies) at 16 locations Canada‐wide. Of the 167 ticks/pools tested, 19 (11.4%) were infected with Borrelia burgdorferi sensu lato (s.l.). Sequencing of the rrf‐rrl intergenic spacer gene revealed four Borrelia genotypes: B. burgdorferi sensu stricto (s.s.) and three novel genotypes (BC genotype 1, BC genotype 2, BC genotype 3). All four genotypes were detected in spirochete‐infected Ixodes auritulus (females, nymphs, larvae) suggesting this tick species is a vector for B. burgdorferi s.l. We provide first‐time records for: ticks in the Yukon (north of 60° latitude), northernmost collection of Amblyomma americanum in North America, and Amblyomma imitator in Canada. First reports of bird‐derived ticks infected with B. burgdorferi s.l. include: live culture of spirochetes from Ixodes pacificus (nymph) plus detection in I. auritulus nymphs, Ixodes scapularis in New Brunswick, and an I. scapularis larva in Canada. We provide the first account of B. burgdorferi s. l. in an Ixodes muris tick collected from a songbird anywhere. Congruent with previous data for the American Robin, we suggest that the Common Yellowthroat, Golden‐crowned Sparrow, Song Sparrow, and Swainson's Thrush are reservoir‐competent hosts. Song Sparrows, the predominant hosts, were parasitized by I. auritulus harboring all four Borrelia genotypes. Our results show that songbirds import B. burgdorferi s.l.‐infected ticks into Canada. Bird‐feeding I. scapularis subadults were infected with Lyme spirochetes during both spring and fall migration in eastern Canada. Because songbirds disperse millions of infected ticks across Canada, people and domestic animals contract Lyme disease outside of the known and expected range.     

Ticks (Acari: Ixodoidea: Argasidae, Ixodidae) of Chile

The tick species recorded from Chile can be listed under the following headings: (1) endemic or established: Argas keiransi Estrada-Peña, Venzal and Gonzalez-Acuña, A. neghmei Kohls and Hoogstraal; Ornithodoros amblus Chamberlin; Otobius megnini (Dugès); Amblyomma parvitarsum Neumann; A. tigrinum Koch; Ixodes auritulus Neumann; I. chilensis Kohls; I. cornuae Arthur, I. sigelos Keirans, Clifford and Corwin; I. stilesi Neumann; I. uriae White; Rhipicephalus sanguineus Koch. (2) Probably established or endemic: Argas miniatus Koch; Ornithodoros spheniscus Hoogstraal, Wassef, Hays and Keirans; Ixodes abrocomae Lahille; I. neuquenensis Ringuelet; I. pararicinus Keirans and Clifford. (3) Doubtfully established: Argas reflexus Fabricius; Ornithodoros talaje (Guérin-Méneville). (4) Exotic: Amblyomma argentinae Neumann; A. latum Koch, Rhipicephalus (=Boophilus) microplus (Canestrini). (5) Erroneously identified as present in Chile: Amblyomma americanum (Linnaeus); A. maculatum Koch; A. varium Koch; Ixodes conepati Cooley and Kohls; I. frontalis (Panzer); I. ricinus (Linnaeus); Margaropus winthemi Karsch. (6) Nomina nuda: Argas reticulatus Gervais; Amblyomma inflatum Neumann; Ixodes lagotis Gervais. Hosts and localities (including new records) are presented. Argas neghmei, O. amblus, O. megnini, I. uriae and R. sanguineus may cause severe injury to their hosts, including humans. The Chilean Ixodes fauna is unique to the Neotropical Zoogeographic Region, and additional research is needed in order to understand the biological importance of these species.This revised version was published online in May 2005 with a corrected cover date.