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.     

Molecular Detection and Identification of Spotted Fever Group Rickettsiae in Ticks Collected from the West Bank,Palestinian Territories

Background

Tick-borne rickettsioses are caused by obligate intracellular bacteria belonging to the spotted fever group (SFG) rickettsiae. Although Spotted Fever is prevalent in the Middle East, no reports for the presence of tick-borne pathogens are available or any studies on the epidemiology of this disease in the West Bank. We aimed to identify the circulating hard tick vectors and genetically characterize SFG Rickettsia species in ixodid ticks from the West Bank-Palestinian territories.

Methodology/Principal Findings

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 Rh. turanicus, Rh. 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 Rh. bursa and H. aegyptium, were infected. Four SFG rickettsiae were identified: Rickettsia massiliae, Rickettsia africae, Candidatus Rickettsia barbariae and Candidatus Rickettsia goldwasserii.

Significance

The results of this study demonstrate the geographic distribution of SFG rickettsiae and clearly indicate the presence of at least four of them in collected ticks. Palestinian clinicians should be aware of emerging tick-borne diseases in the West Bank, particularly infections due to R. massiliae and R. africae.     

The genus Hyalomma. XI. Redescription of all parasitic stages of H. (Euhyalomma) asiaticum (Acari: Ixodidae) and notes on its biology

The tick Hyalomma (Euhyalomma) asiaticum Schulze & Schlottke is provisionally considered to belong to the H. (E.) asiaticum group of closely related species. Males of H. asiaticum can be distinguished from those of other species of the group by their long and very deep cervical grooves, long, narrow, straight adanal plates, long dorsal prolongation of the spiracular plates, dorsal posterior margin of the basis capituli deeply concave and angular, and unbroken ivory-coloured strip on the dorsal aspect of the leg segments. Females of H. asiaticum can be distinguished from those of other species of the H. asiaticum group by their very deep cervical grooves, narrowly U-shaped genital aperture, with bulging preatrial fold. Larger domestic and wild ungulates are the principal hosts of the adults, while nymphs and larvae parasitize mainly rodents, leporids and hedgehogs. Hyalomma asiaticum is widely distributed in Asia, from Syria in the West to eastern China in the East. Here all the parasitic stages of H. asiaticum are illustrated and redescribed. Data on its disease relationships are also provided.     

The genus Hyalomma. VI. Systematics of H. (Euhyalomma) truncatum and the closely related species, H. (E.) albiparmatum and H. (E.) nitidum (Acari: Ixodidae)

The geographic distribution of three closely related Hyalomma species, namely Hyalomma (Euhyalomma) truncatum Koch, 1844, Hyalomma (Euhyalomma) albiparmatum Schulze, 1919 and Hyalomma (Euhyalomma) nitidum Schulze, 1919 is confined to Africa. A detailed comparison of all stages of development of the three taxa reveals that they possess many more shared than distinguishing characters. In fact differentiation between these species is based on single or dual qualitative characters on their adults. These are a conspicuous, ivory-coloured parma on H. (E.) albiparmatum males, and the absence or reduction in clarity of ivory-coloured bands on the leg segments of H. (E.) nitidum adults, as well as the shape of the external cuticular preatrial fold of the genital operculum of females of the latter species. The adults of all three species and the larva of H. (E.) truncatum are redescribed. The nymph of H. truncatum and the larva and nymph of H. (E.) albiparmatum and H. (E.) nitidum are described for the first time. Data on their geographic distributions and hosts are provided.     

Description of a new species of <Emphasis Type="Italic">Amblyomma</Emphasis> Koch, 1844 (Acari: Ixodidae), parasite of deer (Artiodactyla: Cervidae) and wild pigs (Artiodactyla: Suidae) in the Philippines

Amblyomma anicornuta n. sp. (Acari: Ixodidae) is described based on adults and nymphs ex deer (Artiodactyla: Cervidae) and wild pigs (Artiodactyla: Suidae) from Luzon, Philippines. Adults of A. anicornuta n. sp. are similar to those of several Asian and Australasian species of Amblyomma Koch, 1844 with a 4/4 dental formula on the hypostome but can be distinguished by the colouration and pattern of punctations on the conscutum in the male and scutum in the female, the absence of a marginal groove on the conscutum in the male, the possession of long, thick, prominent setae on the alloscutum in the female, projections on anal valves and sclerotised ring around them in the male, a large median sclerite ventrally in the male, as well by the shape of the genital aperture in the female and the size and shape of spurs on coxae I–IV in both sexes. The nymph of A. anicornuta n. sp. is somewhat similar to that of A. babirussae Schulze, 1933 and A. geoemydae (Cantor, 1847) but can be distinguished by the colouration pattern on the scutum, the presence of dorsal cornua and the size of the spurs on coxae I–IV.     

The genus Hyalomma Koch, 1844. IX. Redescription of all parasitic stages of H. (Euhyalomma) impeltatum Schulze & Schlottke, 1930 and H. (E.) somalicum Tonelli Rondelli, 1935 (Acari: Ixodidae)

The ticks Hyalomma (Euhyalomma) impeltatum Schulze &; Schlottke, 1930 and H. (E.) somalicum Tonelli Rondelli, 1935 [a species resurrected for “Hyalomma ? species” of Hoogstraal (1956) and H. erythraeum of Kaiser &; Hoogstraal (1968)] are tentatively considered to belong to the H. (E.) asiaticum group of closely related species. Amongst other features that are fairly similar, males of H. impeltatum can be distinguished from those of H. somalicum by the oval posterior margin of the conscutum, a narrow, subtriangular parma, the lack of ventral sclerotised plaques on median, paramedian and 4th festoons, and an incomplete to complete ivory-coloured stripe on the dorsal aspect of the leg segments; whereas males of H. somalicum have a broad but only slightly convex posterior conscutal margin, in most cases no parma, well-developed sclerotised ventral plaques on all festoons, and only a small ivory-coloured spot on the dorsal aspect of the leg segments. Females of H. impeltatum can be distinguished from those of H. somalicum by the bulging rather than flat preatrial fold of the genital aperture. All parasitic stages of both ticks are illustrated and redescribed, and the characteristics that distinguish the adults from those of other closely related species are detailed. Larger domestic and wild ungulates are the principal hosts of the adults of both ticks. Nymphs and larvae of H. impeltatum parasitise rodents, leporids, birds and lizards, whereas the hosts of the immature stages of H. somalicum are unknown. H. impeltatum is widely distributed in Africa north of the equator, Arabia, the Near East and south-western part of Central Asia; in contrast, H. somalicum has a more limited distribution in East Africa and possibly the Arabian Peninsular. Data on their possible disease relationships are also provided.     

Potential tick vectors for Theileria equi in Israel

Theileria equi Mehlhorn and Schein, 1998 (Piroplasmida: Babesiidae) 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 Ha. parva and R. annulatus as potential novel vectors of T. equi, and suggest that parasite genotype selection occurs within the tick vector.     

Description of four new species of Haemaphysalis Koch, 1844 (Acari: Ixodidae) from the H. (Rhipistoma) spinulosa subgroup,parasites of carnivores and rodents in Africa

Systematic Parasitology - Haemaphysalis (Rhipistoma) bochkovi n. sp., H. (R.) burkinae n. sp., H. (R.) horaki n. sp. and H. (R.) walkerae n. sp. (Acari: Ixodidae), are described based on males and...     

Larval identification of species and subspecies of the genus Hyalomma (Acari: Ixodidae) from Russia and neighbouring territories

The following species and subspecies of Hyalomma Koch, 1844 are recorded from Russia and neighbouring territories, including those involved in natural foci of tick-borne diseases: H. (Hyalomma) aegyptium (Linnaeus, 1758), H. (Euhyalomma) dromedarii Koch, 1844, H. (Euh.) asiaticum asiaticum Schulze et Schlottke, 1930, H. (Euh.) asiaticum caucasicum Pomerantzev, 1940, H. (Euh.) asiaticum kozlovi Olenev, 1931, H. (Euh.) anatolicum Koch, 1844, H. (Euh.) excavatum Koch, 1844, H. scupense Schulze, 1918, H. (Euh.) marginatum marginatum Koch, 1844, H. (Euh.) marginatum turanicum Pomerantzev, 1946, and H. (Euh.) marginatum rufipes Koch, 1844. The geographic distribution and host-parasite relationships of each taxon are discussed. Species characters of the larval stage, that can be distinguished using light microscopy, are found to be very few. These characters include shape of scutum, shape and rate of hypostome denticulation, shape and rate of the development of spurs on coxae I to III. Measurements of some morphological structure and their rations show statistically significant differences between some closely related species, even if qualitative discriminating characters are unknown. Only measurements and their ratios can be used for the discrimination of larval H. anatolicum from larval H. excavatum, because qualitative discriminating features have not been found for these species. The complex structure of the subspecific morhological differentiation of all parasitic stages in the polymorphic species H. asiaticum and H. marginatum is revealed. This structure probably reflects some peculiarities of the microevolutionary processes. Identification key for the larval stage of seven Hyalomma species is provided.     

The Influence of Interspecific Competition and Host Preference on the Phylogeography of Two African Ixodid Tick Species

A comparative phylogeographic study on two economically important African tick species, Amblyomma hebraeum and Hyalomma rufipes was performed to test the influence of host specificity and host movement on dispersion. Pairwise AMOVA analyses of 277 mtDNA COI sequences supported significant population differentiation among the majority of sampling sites. The geographic mitochondrial structure was not supported by nuclear ITS-2 sequencing, probably attributed to a recent divergence. The three-host generalist, A. hebraeum, showed less mtDNA geographic structure, and a lower level of genetic diversity, while the more host-specific H. rufipes displayed higher levels of population differentiation and two distinct mtDNA assemblages (one predominantly confined to South Africa/Namibia and the other to Mozambique and East Africa). A zone of overlap is present in southern Mozambique. A mechanistic climate model suggests that climate alone cannot be responsible for the disruption in female gene flow. Our findings furthermore suggest that female gene dispersal of ticks is more dependent on the presence of juvenile hosts in the environment than on the ability of adult hosts to disperse across the landscape. Documented interspecific competition between the juvenile stages of H. rufipes and H. truncatum is implicated as a contributing factor towards disrupting gene flow between the two southern African H. rufipes genetic assemblages.