1✉ Laboratory of Parasitic Arthropods, Zoological Institute of the Russian Academy of Sciences, Saint Petersburg, Russia.
2Natural Sciences Section, Institut Menorquí d’Estudis Menorca, Balearic Islands, Spain.
3Department of Evolutionary Ecology, Estación Biológica de Doñana (CSIC), Sevilla, Spain.
4Department of Evolutionary Ecology, Estación Biológica de Doñana (CSIC), Sevilla, Spain.
2022 - Volume: 62 Issue: 4 pages: 1201-1209
https://doi.org/10.24349/qojp-y0owChigger mites (parasitic larvae of Trombiculidae) expose different levels of hosts preferences. Many of them were recorded on many host species belonging to different classes, while some genera and species are specific parasites of amphibians, birds, reptiles or bats (Traub & Wisseman 1968; Goff 1979; Kudryashova 1998). Zajkowska et al. (2018) summarized all records of chigger mite species from bat hosts. Shortly thereafter, Stekolnikov & Quetglas (2019) recorded bat chiggers from Spain for the first time, reporting Oudemansidium komareki (Daniel & Dusbábek, 1959) from Pipistrellus kuhlii (Kuhl) in Menorca and Trisetica knighti (Radford, 1954) from Plecotus austriacus (Fischer) in Formentera (Balearic Islands). The checklist published by Zajkowska et al. (2018) erroneously recorded the American species Speleocola secunda Brennan & Jones, 1960 from Spain.
Our collections added four Chiroptera parasitizing chiggers to the Spanish fauna.
Material was collected in three localities
● 1 — Sierra de Las Nieves National Park, Ronda, Málaga province, 36.6925°N, 5.0439°W. In June 2019, 31 bats belonging to 9 species were mist-netted there and examined for chiggers: family Vespertilionidae: Eptesicus isabellinus (Temminck) – 2 specimens, Hypsugo savii (Bonaparte) – 2, Myotis myotis (Borkhausen) – 3, Myotis escalerai Cabrera – 10, Nyctalus lasiopterus (Schreber) – 3, Nyctalus leisleri (Kuhl) – 2, Pipistrellus pipistrellus (Schreber) – 1, Plecotus austriacus (J. Fischer) – 7; family Miniopteridae: Miniopterus schreibersii (Kuhl) – 1. One of the two adult males of E. isabellinus carried ca. 10 very small chiggers in plagiopatagium and uropatagium on both sides. One of the two adult males of H. savii was heavily infested with conspicuous reddish chiggers all over the patagium, whereas second male carried only a few chiggers in plagiopatagium and uropatagium.
● 2 — Vicinity of Palacio de Doñana, Doñana National Park, Almonte, Huelva province, 36.9907°N, 6.4435°W. In July 2019, we examined an entire maternity colony of N. lasiopterus (40 adult females, 10 adult males and 19 juveniles) occupying five bat boxes. Whitish chiggers were recorded on the face, eyelids and ears of only one adult female. All bats of the colony were tagged with rings and transponders; the infested female, ringed that day as K03283, could be identified as new in the colony.
● 3 — Parque Natural Sierra de Cebollera, La Rioja province, 42.0663°N, 2.6860°W. The sampling sites were La Blanca and El Achichuelo situated south to Villoslada de Cameros, by the Iregua river. In August 2020, we caught 66 bats representing 8 species (Vespertilionidae) at their drinking ponds and visually examined them for chiggers: Barbastella barbastellus (Schreber) – 1, Eptesicus serotinus (Schreber) – 6, H. savii – 1, Myotis daubentonii (Kuhl) – 4, N. lasiopterus – 37, N. leisleri – 12, P. pipistrellus – 3, and Plecotus auritus (L.) – 2. All specimens were males, except for one E. serotinus, B. barbastellus, and H. savii. We recorded chiggers on the ears and patagium of two E. serotinus males (Fig. 1).
In August 2021, we examined 26 bats at the same sites: E. serotinus – 1 male, M. daubentonii – 1 male, N. lasiopterus – 21 males, P. pipistrellus – 1 female, and P. auritus – 1 male and 1 female. Whitish chiggers attached on the head were recorded on three N. lasiopterus males.
Thus, we collected trombiculids in summer months of 2019–2021 from four species of bats belonging to the family Vespertilionidae, E. isabellinus, E. serotinus, H. savii, and N. lasiopterus. Chiggers were attached to head and wing membrane of the bats. The mites were removed using O'TOM tick twisters (H3D, Lavancia, France) or spraying TABERNIL [Tetrametine + Piperony butoxide] (Divasa-Farmavic, S.A., Barcelona, Spain) on a swab and applying it to the chiggers, and after some time removing them by pushing gently with the forceps, without need for grabbing, avoiding the possibility of damaging the mites. Samples were stored in Eppendorf tubes with 70% ethanol at room temperature. Chiggers from different bat individuals of the same species from La Rioja were combined.
Mites were mounted on microscope slides using Berlese's medium. Specimens were examined and photographed under a Leica DM2500B microscope (Leica Microsystems GmbH, Wetzlar, Germany) with a Leica DMC 4500 digital camera using differential interference contrast. Measurements necessary for identification were made using a microscope MBI-3 (LOMO plc, St. Petersburg, Russia) with phase contrast optics and ocular micrometer. We used monographs of Kudryashova (1998) and Vercammen-Grandjean & Langston (1976), a revision of the genus Willmannium Vercammen-Grandjean & Langston, 1976 (Kudryashova 1992), and other referenced sources for identification of chiggers.
All chigger specimens are deposited in the collection of the Zoological Institute of the Russian Academy of Sciences (ZIN).
Willmannium cavus moldaviensis Kudryashova (1992) (original designation); Kudryashova (1998, 2004); Benda et al. (2019)
Material examined — Eleven larvae (ZIN 16794, 16795, 16800 – 16808) ex two males of H. savii Nos 190629-1 and 190629-6, SPAIN, Málaga province, Ronda, Sierra de las Nieves, fire pond Los Quejigales, 29 Jun. 2019, collected by Juan Quetglas, Sonia Sánchez-Navarro, and Carlos Ibáñez; four larvae (ZIN 16796 – 16799) ex male of E. isabellinus No. 190629-2, other data same; four larvae (ZIN 16920 – 16922, 16927) ex E. serotinus, SPAIN, La Rioja province, Villoslada de Cameros, 26 Aug. 2020, collected by Carlos Ibáñez.
Remarks — This subspecies was described from Moldova, ex N. noctula and E. serotinus. Later it was recorded from Albania, on Vespertilio murinus L., Hypsugo savii, Pipistrellus pipistrellus, Pipistrellus pygmaeus (Leach) and Tadarida teniotis (Rafinesque) (Benda et al. 2019). Eptesicus isabellinus is a new host species for this chigger.
Our specimens depart from the original description in having a concave (vs. almost straight) posterior margin of scutum and by shorter legs – Ip = 815 – 887 vs. 952 in the holotype (Table 1). However, the length of leg III tarsus in our material is almost the same as in the holotype – TaIIIL = 76 – 86 (mean 81) vs. 83. In general, we do not support the practice of subspecies descriptions in the chigger taxonomy. Revision of the genus, with the possibility of raising some subspecies to the species level and synonymizing of others, is needed.
According to Kudryashova (1992), species of the genus Willmannium are known from Asia, Africa, and America. In Europe, three taxa belonging to this genus were recorded – Willmannium bulgaricum (Dusbabek, 1964) from Bulgaria, W. cavus moldaviensis from Moldova and Albania (Kudryashova 1992, 1998, 2004; Benda et al. 2019), and Willmannium cavus cavus Kudryashova, 1992 from Albania (Benda et al. 2019). Here, we record a representative of this genus in the Western Europe for the first time.
Neoschoengastia latyshevi Schluger (1955) (original designation)
Ascoschoengastia (Paralaurentella) latyshevi: Kepka (1964)
Laurentella latyshevi: Muljarskaja (1968)
Ascoschoengastia (Ascoschoengastia) latyshevi: Daniel & Heneberg (1972)
Ascoschoengastia latyshevi: Sun & Wen (1984); Li et al. (1997); Kudryashova (1998); Literak et al. (2007); Stekolnikov & Daniel (2012); Moniuszko & Mąkol (2014)
Material examined — Three larvae (ZIN 17496 – 17498) ex three males of N. lasiopterus (No. 210811-1), SPAIN, La Rioja province, Villoslada de Cameros, El Achichuelo, 11 Aug. 2021, collected by Carlos Ibáñez.
Remarks — This species was known from Corsica (France), Austria, Czech Republic, Slovakia, Montenegro, Bulgaria, Moldova, Poland, Ukraine, Belarus, Russia, Azerbaijan, Turkey, Kazakhstan, Kyrgyzstan, Tajikistan, Mongolia, and China (Moniuszko & Mąkol 2014). Kudryashova (1998) refuted the record of A. latyshevi from Mongolia and reported on the presence of two closely related species from this country— Ascoschoengastia kitajimai (Fukuzumi & Obata, 1953) and Ascoschoengastia mongolica Kudryashova, 1998. Ascoschoengastia latyshevi was recorded on many species of rodents, the soricomorph Crocidura suaveolens (Pallas) (Kudryashova 1998), and six species of birds (Literak et al. 2007). This species is recorded from bats collected in Spain for the first time. The fact of its parasitizing on N. lasiopterus agrees with the conclusion of Sixl (1969) on A. latyshevi as an inhabitant of hollow trees during the whole life cycle, since tree cavities are the typical habitat of N. lasiopterus (Ibáñez et al. 2004).
Trombicula (Leptotrombidium) intermedia europaea Daniel & Brelih (1959) (original designation)
Leptotrombidium (Leptotrombidium) europaeum europaeum: Vercammen-Grandjean & Langston (1976); Kolebinova (1992)
Leptotrombidium europaeum: Kudryashova (1998); Stekolnikov (2004, 2013); Stekolnikov & Daniel (2012); Moniuszko & Mąkol (2014)
Material examined — Four larvae (ZIN 16923 – 16926) ex E. serotinus, SPAIN, La Rioja province, Villoslada de Cameros, 26 Aug. 2020, collected by Carlos Ibáñez.
Remarks — This species was known from Spain, France, Austria, Czech Republic, Slovakia, Slovenia, Serbia (Kosovo), Macedonia, Montenegro, Albania, Bulgaria, Romania, Moldova, Poland, Lithuania, Latvia, Estonia, Ukraine, Belarus, Russia, Azerbaijan, and Turkey (Moniuszko & Mąkol 2014), from a wide range of rodents and insectivores, and also from the hare, Lepus europaeus (Pallas), and the great tit, Parus major L. (Kudryashova 1998). Here, it is recorded from a bat for the first time.
Thrombidium russicum Oudemans (1902) (original designation); Oudemans (1909)
Trombicula russicum: Fuller (1952)
Leptotrombidium (Leptotrombidium) russicum russicum: Vercammen-Grandjean & Langston (1976)
Leptotrombidium russicum: Kudryashova (1998); Mąkol et al. (2010); Stekolnikov (2013); Benda et al. (2019)
Leptotrombidium (Leptotrombidium) russicum: Kolebinova (1970, 1992); Fernandes & Kulkarni (2003)
Material examined — 12 larvae (ZIN 17499 – 17510) ex N. lasiopterus (No. 210811-1), SPAIN, La Rioja province, Villoslada de Cameros, El Achichuelo, 11 Aug. 2021, collected by Carlos Ibáñez; six larvae (ZIN 16809 – 16814) from face of adult female of N. lasiopterus (No. 190716-2, Ring k03283), SPAIN, Huelva province, Almonte, Palacio de Doñana, 16 Jul. 2019, collected by Juan Quetglas and Carlos Ibáñez.
Remarks — For the complete synonymy and full bibliography on this species before 1976 see Vercammen-Grandjean & Langston (1976). This species was known from Ireland, France, Belgium, The Netherlands, Austria, Switzerland, Germany, Czech Republic, Slovakia, Albania, former Yugoslavia, Hungary, Bulgaria, Romania, Moldova, Poland, Ukraine, Russia, Azerbaijan, Kazakhstan, Kyrgyzstan, Tajikistan, and India, on many species of bats and, occasionally, on yellow-necked mouse, Apodemus flavicollis (Melchior) (Kudryashova 1998; Moniuszko & Mąkol 2014; Fernandes & Kulkarni 2003; Benda et al. 2019). Here, it is recorded from Spain and on N. lasiopterus for the first time.
The metric characters of specimens collected from Villoslada de Cameros are very close to the typical L. russicum. However, the specimens collected in Almonte are significantly larger (Table 2). Seven of the nine specimens examined had the arrangement of dorsal idiosomal setae characteristic for L. russicum (fD = 2H-8-6-6-4-2); one specimen from Villoslada de Cameros had 2H-8-7-6-4-2 and one specimen from Almonte had 2H-10-6-7-4-3. Only one specimen from Villoslada de Cameros and one from Almonte had the numbers of all idiosomal setae characteristic for L. russicum according to Vercammen-Grandjean & Langston (1976) and Kudryashova (1998) (DS = 28, V = 22, and NDV = 50). Other specimens have V = 23 – 28 and NDV = 51 – 57.
Contrary to Kudryashova (1998) and Stekolnikov (2013), sensillary bases in our specimens were slightly posterior to the PLs (P-PL – PSB = 0 – 6 µm). The ratio PW/AP = 2.77 – 3.64 in our material and 3.35 according to Vercammen-Grandjean & Langston (1976).
Leptotrombidium russicum was described by a single specimen collected from an unidentified bat near Kiew (currently Kyiv, Ukraine) (Kudryashova 1998). The holotype is deposited in Rijksmuseum van Natuurlijke Historie (RMNH; currently, Naturalis Biodiversity Center, Leiden, Netherlands). Fuller (1952) noted that this specimen is nearly fully engorged, its scutum is tipped forward, and the posterior scutal margin is hidden under a fold of the cuticle. Vercammen-Grandjean & Langston (1976) provided a complete re-description of L. russicum on the base of the holotype, one specimen from Maastricht (Netherlands) deposited in the Oudemans collection (RMNH), and literature data. Kudryashova (1998) re-described this species on the base of new materials from Moldova, Kyrgyzstan, and European Russia (Moscow, Tver, and Tula Oblast); her measurements and morphological drawings were in good agreement with those of Vercammen-Grandjean & Langston (1976). Fernandes & Kulkarni (2003) also gave full morphological and morphometric data for an Indian sample of L. russicum; these data are consistent with previous descriptions, except for the barbs of scutal setae, which look fairly long on their drawing of the scutum.
Many records of this species from hosts other than bats were misidentifications (Vercammen-Grandjean & Langston 1976; Kudryashova 1998). In part, the species Leptotrombidium subrussicum Kolebinova, 1970 is morphometrically similar to L. russicum (Stekolnikov 2013) and could be misidentified. This species was described from rodents on Corsica (Kolebinova 1970) and later recorded from rodents, soricomorphs, and one bird in Bulgaria (Vercammen-Grandjean & Langston 1976; Kolebinova 1992). We also found a series of specimens belonging to L. subrussicum in the collection of ZIN collected from rodents in North and Western Caucasus (Russia) and in Transcaucasia (Armenia) and originally identified as L. russicum or L. fulleri (Ewing, 1945).
There are several species of Leptotrombidium that may be specific to bats, including four described from Romania and one from the UK (Stekolnikov 2013). Leptotrombidium russicum differs from all of them in having fewer idiosomal setae and fD = 2H-8-6-6-4-2 vs. 2H-10-8-8-... or 2H-8-6-6-6-.... One larva from France (Ariège) identified by Kolebinova (1970) as L. russicum, with fD = 2H-9-8-8-8-6-4-2, probably belongs to another species. However, our finding of L. europaeum on E. serotinus from La Rioja demonstrates that some European species of Leptotrombidium, usually parasitizing rodents and soricomorphs, can also infest bats. Therefore, we may expect the joint occurrence of morphologically similar species, such as L. subrussicum and L. russicum, which can be represented by different intraspecific forms, on same individuals of bats in Europe. Two size forms of L. russicum were described in the present work; L. subrussicum also shows a wide range of size variations, probably depending on altitude (Vercammen-Grandjean & Langston 1976).
A recent work on bat-infesting chiggers in Poland reported the presence of four different Leptotrombidium identified by mitochondrial cytochrome c oxidase subunit I gene (COI) sequences. One was identified morphologically as L. russicum, whereas the identity of other three forms remain unclear (Zajkowska & Mąkol 2022). Interestingly the genetic distance between the form designated as Leptotrombidium sp. 2 and L. russicum was only 5.6 – 5.9%. This distance is rather close to the threshold of the intraspecific variation in Trombiculidae, which attained 4.6% by the COI sequence (Zajkowska & Mąkol 2022). Further morphological examination of these samples is required to establish the nature of the observed molecular forms more definitely.
Noteworthy is that our material on L. russicum was collected from N. lasiopterus, a bat usually inhabiting tree cavities (Ibáñez et al. 2004). This allows us to conclude that hollow trees can be at least one of possible habitats where the life cycle of L. russicum takes place.
Stekolnikov et al. (2014) presented the list of 19 chigger mite species known from Spain at that time, but omitted Ericotrombidium ibericense (Vercammen-Grandjean & Langston, 1976) from this list. However, we suppose that the previous record of E. hasei (Feider, 1958) could have been E. ibericense. Later, Stekolnikov & Quetglas (2019) added two more species to the chigger fauna of Spain. Currently, 25 chigger species are recorded from Spain, including the results of the present study. Six species were collected from bats and three – L. russicum, O. komareki, and T. knighti – only parasitize bats.
This research was supported by the Ministry of Science and Higher Education of the Russian Federation (122031100263-1, to AAS). We thanks Reserva Biológica de Doñana–ICTS for field and laboratory facilities and Joxerra Aihartza for the photographs of parasitizing chiggers taken in La Rioja. We are grateful to Martin Ševčík (Charles University in Prague, Praha, Czech Republic) and one anonymous reviewer for their important notes and suggestions.