Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia.

BACKGROUND: Trombiculid mites are globally distributed, highly diverse arachnids that largely lack molecular resources such as whole mitogenomes for the elucidation of taxonomic relationships. Trombiculid larvae (chiggers) parasitise vertebrates and can transmit bacteria (Orientia spp.) responsible for scrub typhus, a zoonotic febrile illness. Orientia tsutsugamushi causes most cases of scrub typhus and is endemic to the Asia-Pacific Region, where it is transmitted by Leptotrombidium spp. chiggers. However, in Dubai, Candidatus Orientia chuto was isolated from a case of scrub typhus and is also known to circulate among rodents in Saudi Arabia and Kenya, although its vectors remain poorly defined. In addition to Orientia, chiggers are often infected with other potential pathogens or arthropod-specific endosymbionts, but their significance for trombiculid biology and public health is unclear. RESULTS: Ten chigger species were collected from rodents in southwestern Saudi Arabia. Chiggers were pooled according to species and screened for Orientia DNA by PCR. Two species (Microtrombicula muhaylensis and Pentidionis agamae) produced positive results for the htrA gene, although Ca. Orientia chuto DNA was confirmed by Sanger sequencing only in P. agamae. Metagenomic sequencing of three pools of P. agamae provided evidence for two other bacterial associates: a spirochaete and a Wolbachia symbiont. Phylogenetic analysis of 16S rRNA and multi-locus sequence typing genes placed the spirochaete in a clade of micromammal-associated Borrelia spp. that are widely-distributed globally with no known vector. For the Wolbachia symbiont, a genome assembly was obtained that allowed phylogenetic localisation in a novel, divergent clade. Cytochrome c oxidase I (COI) barcodes for Saudi Arabian chiggers enabled comparisons with global chigger diversity, revealing several cases of discordance with classical taxonomy. Complete mitogenome assemblies were obtained for the three P. agamae pools and almost 50 SNPs were identified, despite a common geographic origin. CONCLUSIONS: P. agamae was identified as a potential vector of Ca. Orientia chuto on the Arabian Peninsula. The detection of an unusual Borrelia sp. and a divergent Wolbachia symbiont in P. agamae indicated links with chigger microbiomes in other parts of the world, while COI barcoding and mitogenomic analyses greatly extended our understanding of inter- and intraspecific relationships in trombiculid mites.

New species and new records of chigger mites (Acariformes, Trombiculidae) from Cambodia.

Two new chigger species, Leptotrombidium mondulkiri sp. nov. and Walchia keoseima sp. nov., and one new subspecies, Leptotrombidium pilosum cambodiensis subsp. nov., are described from Cambodia. Three species, Walchia lupella (Traub and Evans, 1957), W. micropelta (Traub and Evans, 1957), and W. kritochaeta (Traub and Evans, 1957), are for the first time reported from the country. A redescription of W. lupella is given based on new materials from Cambodia and Thailand.

A revision of the chigger genus Afrotrombicula (Acariformes: Trombiculidae).

The chigger genus Afrotrombicula Kolebinova and Vercammen-Grandjean, 1978 has been revised based on examination of museum specimens and reference data. Six species have been transferred to this genus from Neotrombicula Hirst, 1925 with the following new combinations: Afrotrombicula (Afrotrombicula) centrafricana (Goff, 1995), comb. nov., A. (A.) claviglia (Radford, 1948), comb. nov., A. (A.) kenyaensis (Goff, 1995), comb. nov., A. (A.) nicolei (Taufflieb, 1958), comb. nov., A. (A.) rickenbachi (Taufflieb, 1965), comb. nov., and A. (A.) zairiensis (Taufflieb, 1966), comb. nov. Re-descriptions of two incompletely described species have been provided. Four new synonyms have been established for two species: A. (A.) rickenbachi (Taufflieb, 1965), comb. nov. (= Neotrombicula cercopitheci cercopitheci Vercammen-Grandjean, 1965 (nomen nudum), syn. nov.; = N. chicapa Vercammen-Grandjean, 1965 (nomen nudum), syn. nov.; = N. kinduensis Vercammen-Grandjean, 1965 (nomen nudum), syn. nov.), and A. (Tauffliebicula) machadoi (Taufflieb, 1962) (= A. lophuromyia Kolebinova and Vercammen-Grandjean, 1978, syn. nov.). Afrotrombicula rickenbachi has been for the first time recorded in the Democratic Republic of the Congo and found on six new host species. A key to the 14 species referred to the genus Afrotrombicula has been compiled. According to the results of revision, the genus Afrotrombicula is an endemic of the Tropical Africa, and its distribution is probably restricted to subequatorial territories.

New species and records of chiggers (Acariformes: Trombiculidae) from birds of the Neotropics.

The study focuses on chigger mites parasitizing bird hosts in three countries of Latin America, Costa Rica, Paraguay, and Peru. In total, 785 chiggers collected from 145 birds of 67 species have been identified. Three new species have been described: Eutrombicula talamancensis sp. nov., from ten bird species in Costa Rica, Eutrombicula cathari sp. nov., from two species of the genus Catharus Bonaparte, 1850 in Costa Rica, and Eutrombicula gonzalezi sp. nov., from three bird species in Paraguay. Eutrombicula helleri (Oudemans, 1911), considered as a synonym of Eutrombicula goeldii (Oudemans, 1910) since 1949, has been restored as a separate species. Re-descriptions of E. helleri, E. goeldii, and Eutrombicula pacae (Floch and Fauran, 1957) have been provided based on new materials. Five species have been for the first time recorded in Paraguay, four in Peru, and two in Costa Rica. Five species have been for the first time recorded on bird hosts. Data on a geographic morphometric variability of E. helleri and Blankaartia sinnamaryi (Floch and Fauran, 1956) have been provided. Co-occurrence of two (three, in one case) chigger species on one host individual has been recorded in 17% of birds.

Novel Vector of Scrub Typhus in Sub-Antarctic Chile: Evidence From Human Exposure.

The exposure of a research team to chigger mites in southern Chile allowed the first identification of a trombiculid species as vector and reservoir of scrub typhus outside the tsutsugamushi triangle, providing unique insights into the ecology and transmission of this recently discovered rickettsial infection in South America.

Distribution of chigger mites (Acari: Trombiculidae) over hosts, parasitopes, collection localities, and seasons in northern Iran.

We studied the distribution of chigger mite species over mammal hosts, attachment sites on the host body, habitats, and seasons in Iran. The study was based on 2155 specimens of 36 chigger species collected from 10 species of Muridae, Cricetidae, and Soricidae across six provinces of northern Iran. A high level of mixed infestation by chiggers was recorded-76% of hosts parasitized by chiggers were infested by more than one (2-8) species. Statistically significant differences in the preference for anterior and posterior parts of the host body were found. Three species-Neotrombicula lubrica, N. delijani, and Cheladonta firdousii-preferred the posterior part of the host body; 12 species were characterized by the occurrence in the anterior part and differed from one another by the frequency of presence in the posterior part. One species, Hirsutiella alpina, was found only in the anterior part of the host body (inside the ears of rodents). The most diverse chigger fauna was on the fringe of Golestan National Park (species richness = 21, Shannon-Wiener index = 2.823). The chigger fauna of the high-mountain localities on the Alborz Range was the least diverse (species richness = 16, Shannon-Wiener index = 2.439). The seasonal aspect of activity was evident for Neotrombicula elegans, which exposed the autumn-winter period of the occurrence on hosts, and N. vernalis, with the winter-spring peak of abundance.

Re-descriptions of eight chigger mite species (Acariformes: Trombiculidae) of the Leptotrombidium generic complex from Vietnam.

Six mite species of the genus Leptotrombidium Nagayo, Miyagawa, Mitamura and Imamura, 1916 and one species from each of the genera Lorillatum Nadchatram, 1963 and Trombiculindus Radford, 1948, incompletely described by Schluger et al. (1960b, 1963) from rodents and tree shrews in North Vietnam, are re-described based on type series. Lectotypes and paralectotypes have been designated for all redescribed species. Two new synonyms have been established: Leptotrombidium magnum (Schluger, 1960) (= Leptotrombidium dooleyi Nadchatram, 1970, syn. nov.; = Leptotrombidium submagnum Wang, Li and Shi, 1988, syn. nov.).

Redescriptions of ten chigger mite species (Acariformes: Trombiculidae) from Vietnam.

Ten species of chigger mites from the genera Gahrliepia Oudemans, 1912, Walchia Ewing, 1931, Cheladonta Lipovsky, Crossley and Loomis, 1955, Doloisia Oudemans, 1910, Schoutedenichia Jadin and Vercammen-Grandjean, 1954, and Microtrombicula Ewing, 1950, incompletely described by Schluger et al. (1960a, c, 1961, 1963) from rodents in North Vietnam, are redescribed based on type series. Lectotypes and paralectotypes have been designated for all species. A new synonymy has been established: Walchia delicatula (Schluger, Grochovskaja, Ngu, Hoe and Tung, 1960) (= Walchia tianguangshanensis Zhao, 1981 syn. nov.).

A checklist of chigger mites (Acariformes: Trombiculidae) of Southeast Asia.

Chigger mites (Acariformes: Trombiculidae) of Southeast Asia, including Myanmar, Malaysia, Brunei, Singapore, Indonesia, Thailand, Cambodia, Vietnam, and the Philippines have been revised based on reference data and examination of type materials in European collections of chiggers. For 450 species of 49 genera synonymy, collection data on types, lists of known host species and lists of countries are given. The lists of hosts include in total 649 valid species and subspecies of mammals, birds, reptiles, amphibians, and arthropods. Two new synonyms were established: Doloisia (Doloisia) Oudemans, 1910 (= Doloisia (Trisetoisia) Vercammen-Grandjean, 1968, syn. nov.) and Gahrliepia lui Chen and Hsu, 1955 (= Gahrliepia (Gateria) octosetosa Chen, Hsu and Wang, 1956, syn. nov.). Twenty-seven new combinations were proposed: Walchia (Ripiaspichia) biliranensis (Brown, 1997), comb. nov., Walchia (Ripiaspichia) huberti (Upham and Nadchatram, 1968), comb. nov., Walchia (Ripiaspichia) parmulaseta (Brown, 1997), comb. nov., and Walchia (Ripiaspichia) serrata (Brown and Goff, 1988), comb. nov., transferred from Gahrliepia Oudemans, 1912; Farrellioides consuetum (Womersley, 1952), comb. nov. (originally in Trombicula Berlese, 1905), Farrellioides nakatae (Nadchatram and Traub, 1964), comb. nov. (originally in Leptotrombidium Nagayo, Miyagawa, Mitamura and Imamura, 1916), and Farrellioides striatum (Nadchatram and Traub, 1964), comb. nov. (originally in Leptotrombidium), transferred from Euschoengastia Ewing, 1938; Guntheria (Phyllacarus) bushlandi (Philip, 1947), comb. nov. (originally in Ascoschoengastia Ewing, 1946), transferred from Guntherana Womersley and Heaslip, 1943 (syn. of Guntheria Womersley, 1939); Kayella masta (Traub and Sundermeyer, 1950), comb. nov. (originally in Ascoschoengastia), transferred from Cordiseta Hoffmann, 1954; Neoschoengastia stekolnikovi (Kalúz, 2016), comb. nov., transferred from Hypogastia Vercammen-Grandjean, 1967; Susa chiropteraphilus (Brown, 1997), comb. nov., Susa masawanensis (Brown, 1998), comb. nov., and Susa palawanensis (Brown and Goff, 1988), comb. nov., transferred from Cheladonta Lipovsky, Crossley and Loomis, 1955; Ericotrombidium cosmetopode (Vercammen-Grandjean and Langston, 1971), comb. nov., transferred from Leptotrombidium; Eutrombicula gigarara (Brown, 1997), comb. nov., transferred from Siseca Audy, 1956; Microtrombicula eltoni (Audy, 1956), comb. nov., transferred from Eltonella Audy, 1956; Trombiculindus alethrix (Traub and Nadchatram, 1967), comb. nov., Trombiculindus cuteanum (Vercammen-Grandjean and Langston, 1976), comb. nov., Trombiculindus frondosum (Traub and Nadchatram, 1967), comb. nov., Trombiculindus hastatum (Gater, 1932), comb. nov., Trombiculindus lepismatum (Traub and Nadchatram, 1967), comb. nov., Trombiculindus limi (Traub and Nadchatram, 1967), comb. nov., Trombiculindus maxwelli (Traub and Nadchatram, 1967), comb. nov., Trombiculindus roseannleilaniae (Brown, 1992), comb. nov., Trombiculindus sarisatum (Traub and Nadchatram, 1967), comb. nov., Trombiculindus vanpeeneni (Hadi and Carney, 1977), comb. nov., and Trombiculindus yooni (Traub and Nadchatram, 1967), comb. nov., transferred from Leptotrombidium.

Host Associations of Ectoparasites of the Gray Mouse Lemur, Microcebus murinus, in Northwestern Madagascar.

Eight species of ectoparasites were collected during 225 gray mouse lemur, Microcebus murinus (J. F. Miller), captures, in Ankarafantsika National Park, Madagascar, in 2010-2011. The ixodid tick, Haemaphysalis lemuris Hoogstraal, was the most common ectoparasite and was mostly represented by nymphs. Other ectoparasites recorded include the polyplacid sucking louse, Lemurpediculus madagascariensis Durden, Kessler, Radespiel, Zimmermann, Hasiniaina, and Zohdy; the ixodid tick, Haemaphysalis simplex Neumann; an undescribed laelapid mite in the genus Aetholaelaps; another laelapid belonging to the genus Androlaelaps; the chigger mite Schoutedenichia microcebi Stekolnikov; an undescribed species of atopomelid mite in the genus Listrophoroides; and an undescribed species of psoroptid mite in the genus Cheirogalalges. Except for the 2 species of ticks and 1 species of chigger, these ectoparasites may be host-specific to M. murinus. Total tick (H. lemuris and H. simplex) infestation was significantly greater in August than October, whereas louse (L. madagascariensis) infestation was significantly greater in October. There was no significant difference in tick infestations between male and female lemurs, but male lemurs had significantly more lice than female lemurs. Reproductive status was not a significant predictor of tick infestation in males and females.

Chigger Mites (Acariformes: Trombiculidae) of Chiloé Island, Chile, With Descriptions of Two New Species and New Data on the Genus Herpetacarus.

Three species of chigger mites are recorded in our collections from four species of cricetid rodents on Chiloé Island (southern Chile, Los Lagos Region), an area endemic to scrub typhus (Orientia sp.). Two species are described as new-Herpetacarus (Abonnencia) eloisae sp. nov. and Quadraseta chiloensis sp. nov. One species, Paratrombicula goffiStekolnikov and González-Acuña 2012, is for the first time recorded on a mammal host (one species of cricetid rodent), and its distribution is extended to the Los Lagos Region of Chile. The genus ProschoengastiaVercammen-Grandjean, 1967 is synonymized with the subgenus Herpetacarus (Abonnencia)Vercammen-Grandjean, 1960, and four new combinations are established: Herpetacarus (Abonnencia) herniosa (Brennan and Jones, 1961), comb. nov., Herpetacarus (Abonnencia) insolita (Brennan and Jones, 1961), comb. nov., Herpetacarus (Abonnencia) macrochaeta (Brennan and Jones, 1961), comb. nov., and Herpetacarus (Abonnencia) antarctica (Stekolnikov and Gonzalez-Acuña, 2015), comb. nov.

First report of Ericotrombidium ibericense in domestic dogs.

PURPOSE: Larval stages of trombiculid mites infest a wide variety of wild and domestic animals. The most common clinical signs related with the presence of these parasites are alopecia, crusts, erythema, excoriation, erosion, papules, pustules and vesicles. Most of trombiculid infestations may not be perceived by the clinician due to their small size. Although Ericotrombidium ibericense has been recorded on cats, it has not been found on dogs. METHODS: In August 2019, three domestic dogs presenting pruritic dermatological lesions in the ventral area of the body and interdigital spaces were presented at a veterinary clinic in Santarém, central Portugal. Trombiculid mites were extracted from the skin and preserved in 70% ethanol. Specimens were prepared in slides with Hoyer's medium and observed with optical microscopy. RESULTS: After morphological examination of the specimens, mites were identified as E. ibericense (Acariformes: Trombiculidae). CONCLUSIONS: Most of the trombiculids recorded in European clinical practice are generally identified as Neotrombicula autumnalis by default, since, in most cases, mites are not examined morphologically. This is the first record of E. ibericense in domestic dogs. More studies are needed to evaluate the distribution of these mites in Portugal. Veterinary clinicians must be aware of this parasitosis, as trombiculids can cause exuberant clinical signs, but are often misdiagnosed.

Pathology of Trombiculosis caused by Neoschoengastia simonovichi in Wild Red-Legged Partridges (Alectoris rufa).

Lesions caused by trombiculid mite larvae ('chiggers') in birds have been inadequately described. A juvenile red-legged partridge (Alectoris rufa) presented with multifocal, crater-like lesions of necrotizing dermatitis, which often contained multiple orange mites. Microscopically, there was a nodular necrotizing and pyogranulomatous dermatitis with occasional intralesional arthropods. Histologically, the mites were readily identified by the presence of stylostomes within the necrotic areas. Morphological and morphometrical studies on isolated mites identified them as Neoschoengastia (Hypogastia) simonovichi. This is the first report of N. simonovichi as an aetiological agent of severe trombiculosis in wild birds in Western Europe. Infestation with this parasite requires further study to understand its role in animal and human trombiculosis and its potential role as a vector of infectious, including zoonotic, agents.

Contributions to the fauna of chigger mites (Acariformes: Trombiculidae) of Iran.

Chigger mites of northern Iran were studied on the basis of field collections from rodent hosts. Thirty-five species were recorded. Two new species, Cheladonta afshari Stekolnikov and Shamsi sp. nov., collected on Apodemus sp. in Guilan and Mazandaran Provinces, and Neotrombicula tehranensis Stekolnikov and Shamsi sp. nov., collected on Cricetulus migratorius and Chionomys sp. in Tehran Province, are described. One new synonym is established: Neotrombicula vernalis (Willmann, 1942) (= Neotrombicula kermani Kudryashova, 1977 syn. nov.). Seventeen species were recorded in Iran for the first time; thus, the number of known Iranian chiggers constitutes 104. The record of Neotrombicula autumnalis (Shaw, 1790) in Iran is important from the veterinarian and medical points of view, as this species attacks humans and domestic animals.

The diversity and distribution of chigger mites associated with rodents in the South African savanna.

Chigger mites (Trombiculidae) are temporary habitat-specific ectoparasites that often occur on rodents. Little ecological data are available on chiggers associated with rodents in South Africa. The study aims were to (1) record the chigger species associated with rodents in the savanna, (2) assess if chigger species display parasitope preference on the rodent body and (3) compare the distribution of chigger species in natural, agricultural and urban habitats. Rodents (n = 314) belonging to eight genera were trapped in the savanna biome during 2014 and 2015. Twelve chigger species, of which five are recently described species, were recorded from 161 rodent hosts. The data include three new country locality records. Microtrombicula mastomyia was the most prevalent species across sampling seasons and habitat types. Significant parasitope preference was recorded for two species, with the ear, face and tail base some of the preferred attachment sites. Sampling season and habitat type had a significant effect on chigger communities with summer and agricultural habitats recording the highest species richness, while the highest species diversity was recorded in natural habitats. The study contributes to our current knowledge regarding rodent-associated chigger diversity and distribution in South Africa and further highlights the importance of environmental characteristics in shaping chigger communities.

A catalogue of the holotypes of chigger mites (Acariformes: Trombiculidae) at the Natural History Museum of Geneva.

The personal collection of P.H. Vercammen-Grandjean, which is deposited in the Natural History Museum of Geneva (Switzerland), is revised and a catalogue of holotypes is compiled. The inventory includes data on the holotypes of 92 valid trombiculid species, 18 specimens erroneously labeled as holotypes and 84 specimens designated as holotypes of unpublilshed species (nomina nuda).

Bat-infesting chiggers (Acariformes: Trombiculidae) of the Balearic Islands and new data on the genus Trisetica Traub et Evans, 1950.

A sample of chigger mites from bat hosts collected in the Balearic Islands (Western Mediterranean Sea) is found to include two species. These are the first records of bat-infesting chiggers identified to species in Spain. Chiggers collected from Pipistrellus kuhlii (Kuhl) in Menorca are identified as Oudemansidium komareki (Daniel et Dusbábek, 1959); this species, which was known from Austria, Bulgaria, Romania, Slovakia, Moldova, Crimea, and Azerbaijan, is recorded for the first time in Spain. Chiggers collected from Plecotus austriacus (Fischer) in Formentera are identified as Trombicula knighti Radford, 1954, which was insufficiently described from a bat in Yemen and known only from its type locality. We transfer this species to the genus Trisetica Traub et Evans, 1950 and provide its re-description based on paratypes and the material from the Balearic Islands. The species Sasatrombicula (Rudnicula) balcanica Kolebinova, 1966 is synonymised with T. knighti. One species closely related to T. knighti, Trisetica aethiopica (Hirst, 1926), which was recorded in Ghana, Uganda, South Sudan, and Madagascar, is re-described on the basis of its syntype deposited in the Natural History Museum, London, UK. This specimen is designated as lectotype.

A new species of Schoutedenichia Jadin & Vercammen-Grandjean, 1954 from Madagascar and a re-description of S. dutoiti (Radford, 1948) from South Africa (Acariformes: Trombiculidae).

A new chigger mite species, Schoutedenichia microcebi n. sp. is described from the grey mouse lemur Microcebus murinus (J.F. Miller) from Madagascar. The new species is closely related to S. dutoiti (Radford, 1948), a species described from a single specimen collected on a rodent in South Africa. Examination of the holotype and new material on S. dutoiti from South Africa enabled us to re-describe this species and provide new data on its hosts and geographical distribution.

Chigger mites (Acariformes: Trombiculidae) of Iran.

Chigger mites of Iran have been revised based on examination of type materials in the collection of Zoological Museum of Moscow University and reference data. Hitherto, 85 species of trombiculids were recorded in Iran; synonymy, diagnoses, data on depositories of type specimens, lists of hosts and collection localities are given for each species. Original measurements of holotypes or paratypes are provided for 46 species. Four new combinations are proposed: Ornithogastia merops (Vercammen-Grandjean, Rohde and Mesghali, 1970) comb. nov., transferred from Guntherana; O. oenanthe (Vercammen-Grandjean, Rohde and Mesghali, 1970) comb. nov., transferred from Guntherana; Microtrombicula galerida (Vercammen-Grandjean, Rohde and Mesghali, 1970), comb. nov., transferred from Eltonella; and M. meriones (Vercammen-Grandjean, Rohde and Mesghali, 1970), comb. nov., transferred from Eltonella. Comparison of our measurements of holotypes with those given in the original species descriptions published by Kudryashova was carried out using statistical methods to establish probable systematic bias between metric data obtained by different researchers. A key to species of Iranian trombiculid larvae is compiled. With the use of public geoinformation online resources, actual names and coordinates were established for all 48 sites of Iran where chigger mites were collected.

Ecological and microbiological diversity of chigger mites, including vectors of scrub typhus, on small mammals across stratified habitats in Thailand.

BACKGROUND: Scrub typhus, caused by a bacterial pathogen (Orientia spp.), is a potentially life-threatening febrile illness widely distributed in the Asia-Pacific region and is emerging elsewhere. The infection is transmitted by the larval stage of trombiculid mites ("chiggers") that often exhibit low host specificity. Here, we present an analysis of chigger ecology for 38 species sampled from 11 provinces of Thailand and microbiomes for eight widespread species. RESULTS: In total, > 16,000 individual chiggers were collected from 1574 small mammal specimens belonging to 18 species across four horizontally-stratified habitat types. Chigger species richness was positively associated with higher latitudes, dry seasonal conditions, and host maturity; but negatively associated with increased human land use. Human scrub typhus incidence was found to be positively correlated with chigger species richness. The bacterial microbiome of chiggers was highly diverse, with Sphingobium, Mycobacterium, Neisseriaceae and various Bacillales representing the most abundant taxa. Only Leptotrombidium deliense was found to be infected with Orientia and another potential pathogen, Borrelia spp., was frequently detected in pools of this species. ß-diversity, but not α-diversity, was significantly different between chigger species and geographic regions, although not between habitat types. CONCLUSION: Our study identified several key environmental and host-derived correlates of chigger species richness across Thailand, which in turn impacted on human scrub typhus incidence. Moreover, this first extensive field survey of the chigger microbiome revealed species- and province-level variation in microbial ß-diversity across the country, providing a framework for future studies on interactions between pathogens and other symbionts in these understudied vectors.