Here we report S. brevipennis from the two new localities including several sites in the Franz-Josef Land and a single site on Vize Isalnd, Western Russian Arctic, thus filling the gap between Svalbard (Boheman, 1856; Stur, Ekrem, 2020) and previously known Siberian sites (Sæther, 2004). Besides, our findings are the northernmost localities for the entire species range.
Specimens of S. brevipennis from the Franz-Josef Land were previously incorrectly attributed to females of Metriocnemus sibiricus (Krasheninnikov, Gavrilo, 2013, 2014), which are also brachypterous, occur in similar habitats and have a reduced antenna consisting of 5 flagellomeres (Sæther, 1995). In the case of S. brevipennis, we deal with a flightless parthenogenetic species with reduced wings, which, in turn, affects many other characters and accounts for their high variability (Sæther, 2004).
Parthenogenesis is a widespread form of asexual reproduction in which an organism develops from an unfertilized egg (virgin reproduction). Parthenogenesis occurred independently in various phylogenetic lineages of animals but most common in rotifers, flatworms, gastropods, crustaceans, spiders, insects and some groups of vertebrates, such as amphibians, crocodiles, squamata, fishes and birds (Lynch, 1984, Ross et al., 1997, Korenko et al., 2009, Schut et al., 2009, Booth et al., 2023, etc.). Among insects three main types can be distinguished: arrhenotoky (the birth of only haploid males from unfertilized eggs and diploid females from fertilized eggs), thelytoky (birth of only diploid females from unfertilized eggs) and deuterotoky (birth of males and females from unfertilized eggs) (Lynch, 1984, Amiri Bandaniet, 2021). Thelytoky is most common type of Parthenogenesis among the lower and higher Diptera, including Sciaridae, Psychodidae, Chironomidae, Simuliidae, Cecidomyiidae, Ceratopogonidae, Tipulidae, Hybotidae, Lonchopteridae, Agromyzidae, Ctenostylidae, Chamaemyiidae Cnemospathididae and other (Sperling, Glover, 2023). Among chironomids, parthenogenesis is a relatively rare phenomenon which has been found to date in 21 species of Chironominae, 36 Ortocladiinae and 4 of Telmatogetoninae (Lindeberg, 1971; Armitage et al., 1995; Gokhman and Kuznetsova 2017, Lackmann et al., 2020, Sperling, Glover, 2023).
Parthenogenesis is an adaptation of chironomids to survive in harsh environments (Lackmann et al., 2020). Separate parthenogenetic populations within of bisexual species, in the Northern Hemisphere are more often found at high latitudes and altitudes (for example, in the tundra, on islands with arctic desert), with unstable conditions. Asexual populations at the edge of a species range can lead to geographic separation of bisexual and unisexual populations («geographic parthenogenesis»; Vandel, 1928). Chironomids of extreme high latitudes that survive in harsh conditions usually have sexual populations in the warmer edge of their range, e.g. Paratanytarsus laccophilus species group (Lackmann et al., 2020) Paratanytarsus grimmii (Carew et al., 2013) Tanytarsus heliomesonyctios (Orel and Semenchenko, 2019; Stur and Ekrem, 2020). Parthenogenetic populations usually have low sizes, in which the female is theoretically capable of producing offspring herself, reducing the risk associated with finding a mate and allowing for rapid population and productivity growth (Lackmann et al., 2020).
The most peculiar is the discovery of S. brevipennis on the Vize Island. This isolated offshore island is located at the northern border of the Kara Sea shelf, 575 km from the mainland and some 300 km from the nearest large archipelagos of Severnaya Zemlya, Novaya Zemlya, and Franz-Josef Land. This small (288 km2) ice-free and hilly lowland island (the highest elevation is 22 m a.s.l.) has extremely uniform landscapes with many rivers, streams, and wet habitats. The mean air temperatures are positive only in July and August (0.5°C and 0.1°C, respectively). The vegetation is dominated by forb and cryptogam high-Arctic tundra. The first and the only terrestrial invertebrate ever reported from Vize Island is vagrant larch tortrix Zeiraphera griseana (Hübner, 1799) (Insecta, Lepidoptera, Tortricidae) (Gavrilo et al., 2021), however, according to visual observations Collembola are common in different habitats (M.V.Gavrilo, 2020, unpublished data).
Different wet localities in the southern coastal area were examined in search of adult chironomids during warm season of 2020 under favourable weather conditions (M.V.Gavrilo, 2020 unpublished data). No imago could be found anywhere. In four freshwater habitats, including streams, pond and moss turf overflown with water, which were sampled in 2022 only enchytraeids (Annelida, Oligochaeta, Enchytraeidae) were recorded in zoobenthos. Worth to mention, this is the first report of freshwater benthos from the Vize Island. Unfortunately, the degree of preservation of the material was unsatisfactory due to fixation with table salt, therefore it was neither possible to identify collected enchytraeids to the lower taxa nor to estimate their numbers and biomass. The only sample with S. brevipennis larvae was taken under the small colony of kittiwakes (Fig. 5).
Finding S. brevipennis larvae only in association with seabird colony suggests the gulls to be involved in insects’ transport into this habitat. The possibility of transfer of non-parasitic microarthropods by the birds is discussed in details by N.V. Lebedeva and D.A. Krivolutsky (2003). They showed that birds can carry various groups of free-living mites, collembols, dipterian larvae, and staphylinids in their feathers. N.V. Lebedeva (2012) assumes seabird colonies, most likely, are the center of formation of soil biota diversity in the high-Arctic. Therefore, our first hypothesis is a phoresy of S. brevipennis larvae in the kittiwake plumage. Subsequently, the larvae could fall out from the nest along with the nesting material. The weak side of such hypothesis is a pelagic life style of the kittiwakes (Hatch et al., 2020): the gulls are connected to the land only while breeding, they build nests on the cliffs or occasionally on buildings (like on Vize Island), make use of freshwater reservoirs to freshen their plumage, rest or collect nesting materials on tundra. All terrestrial activities they perform nearby their nesting colonies during breeding season, then they migrate out to the sea and stay there until the next summer, thus long-distance transfer of larvae from the area of known range of S. brevipennis to the remote offshore island is unlikely.
Another hypothesis related to phoresy by kittiwake is the transport with nesting materials. The gulls use plenty of wet mosses, other plants, mud, as well as seaweed to build their nests. Given the Vize Island is a remote island isolated from other landforms with at least some 300 km, finding of S. brevipennis larvae under their nests suggests its local transfer with nesting materials from a suitable habitat nearby their colony, for example, from marine coastal beach. In Svalbard S. brevipennis larvae were reported from a beach area, affected by the sea in a community dominated by bear sedge Carex ursina (Dewey, 1835), the littoral species forming characteristic tussocks (Sendstad et al., 1976). This suggests the semi-aquatic larvae of S. brevipennis is tolerant to salinity. Our finding of larvae in ornithogenic soils immediately beneath the kittiwakes’ nests where no vegetation was observed except a thin film of algae suggests larvae tolerance to guanophication accompanying excessive feces deposits in seabird colonies (Grant et al., 2022 and references therein).
To test this hypothesis, further sampling of beached debris and littoral community on the Vize Island is needed.
Further, this hypothesis is followed by the reasonable question of how the flightless midges happened to get to the Vize Island beach? We then hypothesize that the sea ice-rafted debris could assist such a journey.
While analyzing sea ice habitats of foraging ivory gulls Pagophila eburnea (Phipps,1774) using high-resolution satellite images (M.V.Gavrilo and D.V.Dobrynin, unpublished data), a considerable amount of dirty ice was observed in the area surrounding the Vize Island. These ice floes are believed to contain mineral contamination by sand and/or silt (Fig. 6). Sea ice is one of the most important agents of sediment transport in the Arctic, while shallow Siberian shelves of the Kara and Laptev seas are the major source of ice formation and sediment entrainment and further export of sediment-laden sea ice to the Arctic Basin (Stein, 2008). General currents system of the Kara Sea with prevailing catabatic currents from the Ob-Enisey estuary system northwards ensure transport of ice-rafted debris from the mainland coastal area into the Arctic Basin and the northeastern Barents Sea bypassing the Vize Island (McClimans et al., 2000). Dominance of freshwater diatoms (up to 70% of all species observed) in ice floes drifting along Severnaya Zemlya to the Arctic Basin north off Franz Josef Land and Svalbard (Pfirman et al., 1997) prove export of incorporated biological material from Ob–Enisey estuary to the northern Kara Sea. There are two major mechanisms of incorporation of materials into the sea ice, i.e. entrainment via frazil ice and anchor ice entrainment, or contact incorporation (Lisitzyn, 2022). The latter appeared to be important source of ice-rafted debris and can involve considerable amounts of bottom sediments including mollusks shells and seaweed (Darby et al., 2011). Extensive patches of frozen-in marine benthic materials included sediments, macrobenthos, eelgrass and flatfishes were reported from thick fast ice in river-mouth areas of Arctic Canada (Medcof, Thomas, 1974). In this way, larvae of S. brevipennis along with sediments can be entrained from their littoral habitats into the bottom fast ice in autumn and later, after break-up, be transported northwards and deposited on the shore of remote Vize Island. Ice-rafting from the shallow waters to the deep seas was revealed for benthic ostracods in the Laptev Sea (Stepanova et al., 2003) and the Sea of Okotsk (Ozawa, 2004), but delivery of entrained materials to other land mass was never reported to our knowledge.
Thus, to get to the location where they were sampled, the larvae have taken a long journey by ice-rafting across the Kara Sea and then a local transfer by kittiwakes from the beach to ornithogenic soil deposits beneath their colony.
If looking at the map of the distribution of S. brevipennis records and ice drift pattern in the Arctic Ocean (Fig. 7), it turns out that all findings of the species can be explained by ice rafting of larvae with littoral substrate from the mainland coastal habitats.
For the aggregate of organisms contained in the ice covering a body of water was proposed term «pagon» by S.A. Zernov (1928). He discovered 117 species in pagon, including chironomids. In some fishes, especially coregonids (Reshetnikov, Bogdanov, 2011) embryonic development is associated with freezing into ice. According to I.G. Yudanov (1939), eggs of Coregonus sardinella Vallenciennes, 1848 fertilized during the freeze-up period in the Gulf of Ob are able to freezing into ice and withstanding negative temperatures, and in the spring viable larvae hatch from they. Six species of coregonid fishes living in Eastern Siberia have developed normally from fertilized eggs while being embedded in the ice of a spawning water body (Chernyaev, 2014).
These facts indicate a high probability of transfer of S. brevipennis larvae and other organisms by ice along with frozen coastal substrate. The highest probability of inclusion of larvae in ice is contact freezing, i.e. in places where bottomfast ice forms. Bottomfast ice has the greatest extent on the shallow Siberian shelf (Dammann et al., 2019). Particularly favorable conditions for the inclusion of substrate with larvae in the ice are located in the estuaries of Arctic rivers, primarily Siberian ones, which have developed deltas and extended coastal zones that are influenced by the sea. Bottomfast sea ice plays an important part in river flood sediment distribution. River-ice jams during break-up cause substantial floods in Arctic delta plains, leading to pronounced sediment retention and biogeochemical flux exchange with thermokarst lakes (Overeem et al., 2022).
The shallow Siberian shelves of the Kara and Laptev Seas are the main source of ice formation and sediment transport, as well as the further export of sea ice and sediment to the Arctic Ocean (Stein, 2008). The Kara Sea and the eastern Laptev Sea to the western East Siberian Sea have been identified as important areas of sea ice formation and sediment trapping (Eicken et al., 2000; Pfirman et al., 1997; Tucker et al., 1999; Darby et al., 2003).
Ice formed in the Kara Sea and the Laptev Sea is carried out not only in the northeast of the Barents Sea, but is involved in the circulation in the Canadian region, which was shown by studying inclusions in ice (Darby, 2003).
Thus, the Siberian coast from the mouth of the Ob River to the Chaunskaya Bay could serve as a fan source of Smittia dispersal over the islands across the Arctic Ocean. Our genetic analysis confirms this assumption.
Bayesian tree, unique BIN BOLD number and high genetic divergence confirmed monophily and species validity of S. brevipennis. The gene COI of S. brevipennis were studied in specimens from five localities: Canada, Alaska, Svalbard, Franz Josef Land and the Vize Island. Lack of mutations in the gene COI (K2P = 0) of S. brevipennis from the vast area of some 14 mln km2 indicates a relatively recent and rapid formation of species range. Such results are a unique for chironomids collected from distant localities (minimum nearest distance varies from 400 to1600 km,) of their range compared to other orthoclads. For example, the average intraspecific divergence (K2P) for European (about 10 mln km2) orthoclads is 0,75% (Gadawski et al., 2022) while the same values for the orthoclads of the Tibetan plateau (2.5 mln km2) are 2.13% (Han et al., 2023). The complete absence of any mutations in the gene COI of S. brevipennis from the islands and mainland coast of the Arctic Ocean (area of the Arctic Ocean more than 14 mln km2) indicates a relatively recent and rapid formation of the area compared to other orthoclads. The time of S. brevipennis distribution is not known, but we have attempted to make an approximate calculation. Recent research demonstrates that the divergence rates of the COI gene in insects varies from 1.5–2.3% per 1 million years (Jamnongluk et al., 2003; Stevens et al., 2006 etc.). Slightly higher values were obtained for tenebrionid beetles equal to 3.54% per 1 million years (Papadopoulou et al., 2010). Unfortunately, similar calculations for chironomids are not known. In this study, we used for calculations of divergence time these three commonly assumed mutation rates: 1.5%, 2.3%, and 3.54%. Based on these data, we have calculated that one mutation in COI gene approximately occurs on every101.3, 66.1 or 42.9, thousand years. Thus, dispersal must have occurred during or after the last cold epoch, the LGM, ca. 10 ka BP (e.g., Hughes et al. 2016, Patton et al. 2017). In general, the age of the high-latitude Arctic archipelagos terrestrial invertebrate fauna is estimated at only 10,000 years (Makarova, 2023).