Diversity and Distribution of Mites (Acari: Ixodida, Mesostigmata, Trombidiformes, Sarcoptiformes) in the Svalbard Archipelago

Svalbard is a singular region to study biodiversity. Located at a high latitude and geographically isolated, the archipelago possesses widely varying environmental conditions and unique flora and fauna communities. It is also here where particularly rapid environmental changes are occurring, having amongst the fastest increases in mean air temperature in the Arctic. One of the most common and species-rich invertebrate groups in Svalbard is the mites (Acari). We here describe the characteristics of the Svalbard acarofauna, and, as a baseline, an updated inventory of 178 species (one Ixodida, 36 Mesostigmata, 43 Trombidiformes, and 98 Sarcoptiformes) along with their occurrences. In contrast to the Trombidiformes and Sarcoptiformes, which are dominated in Svalbard by species with wide geographical distributions, the Mesostigmata include many Arctic species (39%); it would thus be an interesting future study to determine if mesostigmatid communities are more affected by global warming then other mite groups. A large number of new species (42 spp.) have been described from Svalbard, including 15 that have so far been found exclusively there. It is yet uncertain if any of these latter species are endemic: six are recent findings, the others are old records and, in most cases, impossible to verify. That the Arctic is still insufficiently sampled also limits conclusions concerning endemicity.

Full names of species are provided in Table 1, while in other tables and figures abbreviations are used. The species within families are organized alphabetically. The names of localities follow in alphabetical order (Table 1).

Ixodida
Only one species, the seabird tick (Ixodes uriae), is known from Svalbard. This species has a wide geographical distribution (Table 1) but in Svalbard has been found only recently on Bjørnøya and Spitsbergen [76][77][78].

Mesostigmata
Thus far, 36 species of Mesostigmata from 13 families have been found in Svalbard (Table 1). Amongst these families, the richest in species is the Ascidae (12 spp.), followed by the Zerconidae (6 spp.); these two families contribute almost 50% of mesostigmatic alpha diversity in Svalbard ( Figure 2).
The peculiarity of the mesostigmatic mite communities of Svalbard compared to other mite groups is manifested by the description of one new genus (Arctoseius) and seven species [Halolaelaps coulsoni Gwiazdowicz & Teodorowicz, 2017; H. gerlachi Hirschmann, 1966; Antennoseius (Vitzthumia) oudemansi (Thor, 1930); Arctoseius laterincisus Thor, 1930; Proctolaelaps parvanalis (Thor, 1930); Neoseiulus grumantensis Kolodochka & Gwiazdowicz, 2014; and N. magnanalis (Thor, 1930)], all first described from the largest island of the archipelago-Spitsbergen. Moreover, based on recently collected samples from this island, redescriptions of several species have been published: Zercon solenites Haarløv, 1942; Antennoseius (Vitzthumia) oudemansi; Arctoseius haarlovi Lindquist, 1963; Proctolaelaps parvanalis; Neoseiulus ellesmerei (Chant & Hansell, 1971); and N. magnanalis [27][28][29]79,80]. Note: *-new to science; **-redescription on the base of material from Svalbard; †-so far found only on Svalbard. 1 [150] proposed the genus Neoprotereunetes for those species of "Protereunetes" that remained in the Eupodidae after the type specimen of Protereunetes (P. agilis Berlese, 1923) was transferred to Ereynetes [66]. It is implied that this new genus includes Protereunetes borneri Thor, 1934, but the combination was not published. 2 Identity and generic affiliation of this species is questionable [46]; possible record from Greenland with inconclusive identification [48]. 3 Species not included in [50], species inquierenda? 4 Inadequately described, not included in key to species [61]. 5 Although specimens from Svalbard were apparently examined, this species was not confirmed from Svalbard [65]. More than a half of the Mesostigmata species known from Svalbard have been recorded there only once ( Table 2). The majority of these are recent findings, but four were reported only in the first half of the last century, including Arctoseius laterincisus, which has an Arctic distribution. Four other records come from the second half of the last century, including another species with an Arctic distribution-Halolaelaps gerlachi. More than a half of the Mesostigmata species known from Svalbard have been recorded there only once ( Table 2). The majority of these are recent findings, but four were reported only in the first half of the last century, including Arctoseius laterincisus, which has an Arctic distribution. Four other records come from the second half of the last century, including another species with an Arctic distribution-Halolaelaps gerlachi.  Most of the Mesostigmata species known from Svalbard have a Palaearctic distribution (Figure 3). Arctic species are also abundant and comprise nearly 40% of Svalbards total mesostigmatic diversity, while Holarctic species are less numerous. Five species have so far been found only in Svalbard (Table 1), including recent records (Halolaelaps coulsoni and Neoseiulus grumantensis) and historic records (Halolaelaps gerlachi, Arctoseius laterincisus and Neoseiulus magnanalis). Mesostigmata have been recorded from five islands in the Svalbard archipelago (Figure 1). Although most of the species are known from Spitsbergen, Saprosecans baloghi Karg, 1964, is known only from Edgeøya and Zerconopsis muestairi (Schweizer, 1949) has been found exclusively on Bjørnøya (Table 1). (C) Sarcoptiformes. No figure was made for the Ixodida, which are represented in Svalbard by one species with a distribution in "at least two regions" (see Table 1 for details).

Trombidiformes
The order Trombidiformes is represented in Svalbard only by the suborder Prostigmata with 17 families and 43 species recorded. The most diverse are the marine Halacaridae (12 spp.), followed by the terrestrial Bdellidae (7 spp.); these two families together comprise 44% of all the Trombidiformes known from Svalbard (Figure 1).

Trombidiformes
The order Trombidiformes is represented in Svalbard only by the suborder Prostigmata with 17 families and 43 species recorded. The most diverse are the marine Halacaridae (12 spp.), followed by the terrestrial Bdellidae (7 spp.); these two families together comprise 44% of all the Trombidiformes known from Svalbard (Figure 1).
Species with wide geographical distributions predominate; cosmopolitan and Holarctic species, and those present in at least two zoogeographic regions (except that the Holarctic is treated as one unit) together comprise 66% of all the Trombidformes (Figure 2). Arctic species are also abundant representing 27% of the recorded species, while the fewest number of species have Palaearctic distributions. There are seven species which have only been recorded from Svalbard (Table 1), but these are mostly single old records of Sig Thor, including Tydeus langei, T. svalbardensis, Podothrombium svalbardense, Eustigmaeus oudemansi, E. pulchellus, and Kerdabania arctica. The one exception is the recently described Chenophila nanseni.
Trombidiformes have been found on five islands/island groups, predominantly on Spitsbergen (40 species), with others collected from Bjørnøya (11), Prins Karls Forland (6), Hopen (4), and a single species on the small islands of the Hinlopenstretet. A large number of species (27) have been found exclusively on Spitsbergen, one species [Sperchon brevirostris (Koenike, 1895)] only on Bjørnøya and two others (Thalassarachna coeca and T. princeps) only on Hopen (Table 1).

Sarcoptiformes
In Svalbard, 98 species of Sarcoptiformes from two suborders (Endeostigmata with 5 species and Oribatida with 93 species) have been recorded (Table 1). They represent 33 families; the richest in species is the Brachychthoniidae (14 spp.), followed by the Crotoniidae (12 spp.), Ceratozetidae (10 spp.), Oppiidae (9 spp.), and Punctoribatidae (5 spp.). Together, these five families comprise 51% of the species diversity of Sarcoptiformes in Svalbard (Figure 1). Some families are represented by only 1-4 species, yet this constitutes a significant share of their known global diversity. For example, 22% of the species belonging to the endeostigmatid family Alicorhagiidae occur in Svalbard. The oribatid families Eniochthoniidae, Peloppiidae and Tectocepheidae are also represented by large proportions of their total known species diversity, with 17%, 27%, and 24%, respectively.
Species with wide geographic ranges together form 58% (cosmopolitan, 5%; Holarctic, 42%; and those found in at least two regions, 11%) of the sarcoptiform species (Figure 2). Species with a Palaearctic distribution also make up a substantial proportion (33%), with the remaining species having an Arctic distribution. Two of these Arctic species have only been found in the north of Spitsbergen: Autogneta kaisilai in Biskayerhuken and Scutozetes clavatosensillus Ermilov, Martens & Tolstikov, 2013, in Mosselbukta; and Fuscozetes coulsoni exclusively on Edgeøya (Table 1, Figure 3). Three species have been recorded only from Svalbard and these are all recently described new species (Table 1).
Approximately one third of the sarcoptiform species have been recorded in Svalbard only once ( Table 2). Seven of them were found in the first half of the last century and, 12 others, in the second half of the last century, including the descriptions of four new species.

Discussion
The acarofauna of the Svalbard archipelago is diverse with 178 recorded species comprising one Ixodida, 36 Mesostigmata, 43 Trombidiformes, and 98 Sarcoptiformes. However, compared with other regions of the Arctic (Alaska, Greenland, Iceland, and Taimyr), the species diversity is lower [151]. This paucity is likely to be explained by a combination of the small area of Svalbard (60% covered by permanent snow or glaciers) [4], the greater geographic isolation, and in some cases, the more northerly locality and harsher climate. As an example, from Iceland there are 428 species of mites known, with eight Ixodida, 131 Mesostigmata, 101 Trombidiformes, and 188 Sarcoptiformes [151][152][153]. Although Iceland has an area only 1.5 times greater than Svalbard, the island lies at a lower latitude (between 63 • and 66 • north latitude), glaciers cover only 11% of its area, and it lies in the path of the North Atlantic Current, which results in a more ameliorated climate. The diversity of mites in Svalbard is also much poorer in comparison to mainland Norway: Ixodida comprise 8% here with Mesostigmata-15%, Trombidiformes-13%, and Sarcoptiformes-30% [154][155][156][157]. However, these differences are not unexpected considering that the Svalbard archipelago is situated 900 km from the northern border of mainland Norway and has an area of only one fifth of that of mainland Norway [158].
The geographical isolation of islands, as a rule, results in reduced biodiversity [159], but, on the other hand, nurtures unique endemic species [160]. Svalbard has a unique flora and fauna, including endemic invertebrates: three rotifers, four tardigrades, and two aphids [86]. Fifteen mite species have been found exclusively in Svalbard, six of them being recent observations. The remaining are single historic records (i.e., from the first half of the last century) and it is consequently uncertain if any of these are endemic to Svalbard or the result of taxonomic confusion. Finding and studying the types or neotypes in Svalbard, along with more extensive sampling in the Arctic and including molecular studies, could help resolve this question.
Nevertheless, the Svalbard acarofauna is unique due to its specific Arctic elements. Amongst the Svalbard Mesostigmata in particular there are many species with an Arctic distribution (which make up nearly 40% of this group) and are similar to that observed on Greenland [151]. By contrast, the Sarcoptiformes in Svalbard are predominated by species with wide geographical ranges extending beyond the Arctic, as also seen with the Sarcoptiformes species known from Greenland [151] and northern Russia [161]. This difference between the two orders may be explained by the younger geological age of the Mesostigmata and their faster evolution rate [162]. Similarly, the Trombidiformes, which are also an ancient group [163], are dominated in Svalbard by species with wide geographic distributions. Nonetheless, Arctic species seem to be abundant among the Trombidiformes of Svalbard, comprising 27% of the species recorded, but these data should be treated with caution because they are mostly based on historic records that need to be confirmed.
Another characteristic feature of the Svalbard acarofauna is the large number of species new to science described from this region-they form approximately 25% of all mite species known from Svalbard. Seven of these species belong to the Mesostigmata, 19 to Trombidiformes, and 16 to Sarcoptiformes. However, many of these new species were found only once and early in the study of the mite fauna of Svalbard. These species include one mesostigmatid species, 18 Trombidiformes species (i.e., 90% of all new species from this group), and two Sarcoptiformes species. Confirming these identifications is complicated by outmoded descriptions, incomplete, or too general drawings, and by the unavailability of most type material. These species require special attention in future studies. They are possibly rare or have been wrongly identified but the possibility cannot be excluded that they have disappeared from Svalbard due to environmental changes or that they were introduced and their populations have not established in Svalbard.
Out of 36 mite species found in Svalbard only once by early workers, the majority of species (24) were collected by Sig Thor, including one new species of Mesostigmata, eight new species of Trombidiformes, and two new species of Sarcoptiformes (Table 2). Despite the widespread belief that the collection of Thor along with all his valuable type material was destroyed in accordance with Thor's wishes (see, e.g., remark 2 on page 1308 in [148]), this collection exists and is kept at the Natural History Museum in Oslo, Norway [164]. However, it is in a very poor condition and it is not certain whether the Svalbard material is in a suitable condition for re-examination.
Recently, the first species of Ixodida, the seabird tick (Ixodes uriae), was discovered in Svalbard [76][77][78]. This tick is a major parasite of seabirds breeding at high latitudes and has the most extensive geographical distribution of all tick species [23], being also common throughout mainland Norway [165]. Its increasing occurence in Svalbard may be related to warming winters (the tick overwinters at the breeding sites of the seabirds) [78] as was similarly observed in Iceland with another tick species, I. ricinus Linnaeus, 1758, and which has become more common in recent years [153].
Studies conducted during the past 20 years have also added 16 species of Mesostigmata [8,18,20,27,28,30,85,92,93,95,98,166] and 36 species of Sarcoptiformes to the Svalbard fauna [8][9][10]67,71,72,74,146,167]. This indicates that despite the relatively long history of mite studies for a region in the Arctic, our knowledge remains surprisingly poor. It is striking, however, that the Trombidiformes have been much less studied in Svalbard than other mite groups ( Table 1). The reference list presented here includes only 18 papers referring to the Trombidiformes (vs. 72 papers on Sarcoptiformes and 34 on Mesostigmata), most of which were published at the end of the 19th and first half of the 20th centuries. Only three come from the present century. Therefore, it is clear that in future studies this group in particular should receive more attention.
There are also some species in Svalbard that have extraordinary disjunct distribution patterns: they occupy mainly the Arctic and parts of the subarctic regions, but are also found in some distant localities, in harsh conditions. One example is an oribatid species, Ceratozetes spitsbergensis, which has been assumed to be an Arctic species, present in Svalbard, Alaska [148], northern Canada [168,169] and the Nordic Arctic of the Russian Far East [148,170], but was found also in the Altai Mountains in Mongolia, at an altitude of 2800-3200 m a.s.l. [171] and in the Alps in Austria, at an altitude of 3300 m a.s.l. [172]. Since it was not found at lower elevations and/or lower latitudes, its presence in the Alps was explained by one of these theories: relict distribution [a cold-adapted species that was widely distributed in Europe during the Last Glacial Maximum (LGM), but when conditions became warmer it retreated to very restricted areas at high altitudes], or the nunatak hypothesis (survival of species on ice-free refuges) [172]. Some studies suggest that parts of Svalbard, e.g., Amsterdamøya (north-west of Svalbard), remained ice-free during the LGM [173]. It is thus possible that some invertebrates survived the LGM in situ in these glacial refugia, although, due to the harsh conditions prevailing over an extended period of time, it seems likely that most biota could probably not survive on nunataks [86]. Another oribatid mite with an interesting distribution is Scutozetes clavatosensillus, which has been found only in Svalbard and in Nepal (Dhaulagiri massif, 3200-3600 m a.s.l.); its distribution may also be related to glacial history. Similarly to S. clavatosensillus, the mesostigmatic species, Paragamasus (Aclerogamasus) insertus, may also be a glacial relict since it is known only from the Gory Stolowe Mtns., Poland [174,175], where it occurred in rock crevices in very extreme conditions with long-lasting snow cover, and recently collected in Svalbard [18].
The composition of the present acarofauna of Svalbard likely results mostly from postglacial immigration [86]. The mites, being wingless, have rather low dispersal abilities. However, phoresy with migrating birds [13][14][15][16][17] or insects [18,95], and transport on driftwood or even direct dispersal in or on seawater with ocean currents [11], are possible dispersal pathways from the mainland to, or between, remote islands such as the Svalbard archipelago. Humans may also play a role in the dispersal of mites; as with the import of fertile agricultural soils transported from southern Russia and contemporary Ukraine to the Russian settlements on Spitsbergen (Barentsburg and Pyramiden) to enrich the soils of the greenhouses and grass lawns [18,19]. Mite communities in such transformed microhabitats differ noticeably from those of the adjacent Arctic tundra. Moreover, manure from abandoned cow sheds provided specific ameliorated environmental conditions enabling the survival of terrestrial invertebrate species not yet recorded elsewhere in Svalbard [18][19][20]. Introduction of new species to islands can be deleterious since the island communities may be disrupted, often resulting in the extinction of their endemic species [176][177][178].
Reconstructing the colonization of Svalbard after the LGM may be attempted by observing primary succession before retreating glaciers. For example, at the Midtre Lovén glacier foreland, two oribatid species, Camisia foveolata and Tectocepheus velatus, were the first colonizers. Mesostigmata appeared later, Proctolaelaps parvanalis being the first species recorded at this glacier foreland [10]. All these species are widely distributed in different parts of the archipelago (see Table 1). Tectocepheus velatus was also the earliest colonizer on a glacier foreland in southern Norway [179], while Camisia foveolata was one of the first colonizers on geothermally active lava fields in Iceland [180]. Oribatida are mainly saprophagous but species that are fungivores, bacteriovores, algivores, or omnivores, such as T. velatus, can find the appropriate food on seemingly baren ground [181]. In turn, the development of the first animal communities provides prey to the predatory Mesostigmata.
As shown in the present review, acarological studies of Svalbard are heavily geographically biased since most sampling has been carried out on the largest island-Spitsbergen; 90% of papers refer to this island and 90% of species have been found there (see Table 1). Almost 20% of papers refer to Bjørnøya and 25% of the species total for the archipelago have been found there, while 7% of papers refer to Edgeøya and 17% of the species are known from there. Nine other islands and island groups have been studied to a much lesser extent, with single records from other locations. It needs to be emphasized that some mites have been found exclusively on one island, other than Spitsbergen: five species on Edgeøya (Saprosecans baloghi, Liochthonius clavatus, L. strenzkei, Neoliochthonius piluliferus, and Fuscozetes coulsoni), four on Bjørnøya (Zerconopsis muestairi, Sperchon brevirostris, Subbelba montana, and Ameronothrus nigrofemoratus), and two on Hopen (Thalassarachna coeca and T. princeps), including three species new to science. It is unclear why these species have not been collected from Spitsbergen despite the more comprehensive sampling efforts on this island. The importance of further studies in different parts of the Svalbard archipelago is highlighted, in particular since the archipelago is extremely diverse geographically and climatically.
In natural conditions, the species composition and abundance of mites depends mainly on the vegetation [89], which, in turn, depends largely on the climate. For example, a relatively high mesostigmatid diversity is present along the western coast of Spitsbergen (about 30 species) [86], which experiences a comparatively mild climate for the latitude, in contrast to the polar deserts, where only five species were recorded [30]. Within the same climatic conditions, the densities of the mites also vary greatly according to the vegetation types [22,30,88,89,136].
Since mites are connected in different ways with other parts of the ecosystem, it would be particularly interesting to apply a multi-disciplinary approach to trace the effect of climate change in Svalbard. For example, one of the understudied mite groups is the family Eriophyidae. This family includes phytophagous species of great economic importance and with high invasive potential, and could be very useful for ecological studies on the effects of a changing climate at Svalbard [67]. Another poorly known group is the hyperorder Astigmata, parasitizing birds [74]. It is well-documented that climatic changes are affecting the diversity of seabirds by changing their foraging and breeding ecology, as well as increasing the abundance of temperate species [6], which could in turn affect bird-associated Astigmata.
Attention should also be paid to the least known mite order in Svalbard, the Trombidiformes, which is extremely diverse with respect to their feeding preferences (this taxon includes algivores, bacterivores, fungivores, predators, and parasites), and occupies terrestrial, freshwater, and marine habitats [182], but has not been studied at all from an ecological perspective in Svalbard.
Acarological research in the Arctic has developed rapidly in the last 20 years, markedly contributing to the knowledge of the mite communities and increasing somewhat our understanding of the factors determining these communities. Nonetheless, little is understood about the physical and morphological adaptations of mites, their adaptations to the extreme Arctic environment, or the genetic biodiversity of these isolated populations. Moreover, research has focused on the larger and more easily accessible regions of the archipelago to the detriment of the more environmentally extreme eastern and northern regions. There has also been a focus on the Sarcoptiformes and Mesostigmata while the Trombidiformes have been neglected. These areas will remain the subject of our research in the forthcoming years.