ISSN 0013-8738, Entomological Review, 2013, Vol. 93, No. 2, pp. 225–239. © Pleiades Publishing, Inc., 2013. Original Russian Text © O.L. Makarova, A.V. Sviridov, M.A. Klepikov, 2012, published in Zoologicheskii Zhurnal, 2012, Vol. 91, No. 9, pp. 1043–1057.
Lepidoptera (Insecta) of Polar Deserts O. L. Makarovaa, A. V. Sviridovb, and M. A. Klepikovc a
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russia e-mail:
[email protected] b Zoological Museum, Moscow State University, Moscow, 125009 Russia e-mail:
[email protected] c Yaroslavl State History-Architecture and Art Museum-Reserve, Yaroslavl, 150000 Russia e-mail:
[email protected] Received October 15, 2011
Abstract—Four species of Lepidoptera were found on Bolshevik Island, the Severnaya Zemlya Archipelago (the Middle-Siberian Arctic sector). The noctuid Xestia aequaeva (Benjamin, 1934) and the geometrid Psychophora cinderella Viidalepp, 2001 are considered residents, while the pickleworm Gesneria centuriella (Denis et Schiffermüller, 1775) and the plutellid Plutella xylostella (Linnaeus, 1758) were brought to the island by air currents. The records of Xestia aequaeva (78°37΄N) and Psychophora cinderella (78°56΄N) on Severnaya Zemlya are the northernmost for the families Noctuidae and Geometridae in the entire Palaearctic. The European, Middle-Siberian, and Beringian sectors of the Arctic appear to support two sympatric species of the genus Psychophora. The “last” lepidopterans along the heat gradient in the Northern Hemisphere are Psychophora spp. (including P. cinderella) and Gynaephora groenlandica (Wöcke, 1874). Both may serve as indicators in analysis of long-term climate changes in the Far North. The most important adaptations of Lepidoptera, as well as of other arthropod groups, to inhabiting the polar deserts are polyphagy and the capacity for perennial development, with female flight reduced or absent. DOI: 10.1134/S0013873813020115
Lepidoptera traditionally occupy a special place in entomological studies of the Arctic by force of their relatively high diversity and a sufficient level of knowledge of this group. In spite of the fact that the contribution of Lepidoptera to the high-latitude insect fauna decreases steadily northwards (down to 6% in the High Arctic: see Chernov, 2002), about 200 species have been recorded so far in the tundra (see Danks, 1981; Lafontaine and Wood, 1997; Kozlov et al., 2006, etc.). The actual diversity of Lepidoptera in the Arctic has been estimated at 300–450 species, of which 108 are representatives of the well studied Rhopalocera (Chernov and Tatarinov, 2006). Data on lepidopterans have been often used as the basic information during the analysis of the nature of adaptations to the Arctic conditions (Downes, 1964, 1965), solution of the important biogeographical questions (Turner et al., 1987;Downes, 1988; Mikkola et al., 1991) and discussion of the ways of the origin of the Arctic fauna as a whole (Kuznetsov, 1938). We consider the polar desert zone in its narrow interpretation, i.e., within the limits indicated by Chernov and Matveyeva (1979) and Aleksandrova (1983). The polar desert zone in the Arctic embraces a number of
northwestern islands of the Canadian Arctic Archipelago, the north extremes of Ellesmere Island, Greenland, Spitsbergen, and Novaya Zemlya, the Franz Josef Land and Severnaya Zemlya archipelagoes, the De Long Islands, and also the north of Chelyuskin Peninsula. The conditions of the polar deserts are extremely severe. The average temperature of July does not, as a rule, exceed 3.0°C, the annual precipitation is 50–300 mm, and the snow depth on the watersheds is usually less than 20 cm in winter (see Chernov et al., 2011). Development of most groups of organisms is impossible there due to the brevity of the vegetation season. Annual vascular plants are absent; the species diversity of either bryophytes or lichens exceeds that of flowering plants (Matveyeva and Zanokha, 2008; Chernov et al., 2011). Many groups of insects highly typical of the tundra zone, such as Carabidae, Curculionidae, Dytiscidae, Rhopalocera, Bombini, Syrphidae, etc., have not been reported for the zonal variants of the polar deserts (Uspensky, 1959; McAlpine, 1965; Bulavintsev and Babenko, 1983; Chernov et al., 1979; Chernov and Makarova, 2008). Many arthropod species have a patchy distribution in the landscape, mostly inhabiting microstations
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with a longer vegetation season (Makarova, 2002b; Chernov and Makarova, 2008). Because they are difficult of access, the regions of Arctic deserts are rarely visited by entomologists, and their fauna is extremely impoverished therewith; all these are resulting in the scarcity of available information on Lepidoptera (Bruggeman, 1958; McAlpine, 1965; Bulavintsev, 1999). For example, it was suggested that “lepidopterans were practically absent in the Palaearctic polar deserts” (Korotkevich, 1972) or that there were no insects at all on Severnaya Zemlya (Zaborski in: Kimble and Good, 1955; cited after Downes, 1964). No lepidopterans were recorded during special studies on Franz Josef Land (Bulavintsev and Babenko, 1983; Bulavintsev, 1999) and on Cape Chelyuskin in the north of Taimyr (Chernov et al., 1979). In the Antarctic polar deserts, the free-living insects are represented only by two species of chironomid midges (Convey and Block, 1996.) Recently, O.L. Makarova has collected data on arthropods on the Queen Elizabeth Islands (the Canadian Arctic Archipelago) and Bolshevik Island (Severnaya Zemlya), which, together with the published ones, allowed us to consider the composition of the Arctic desert faunas of many animal groups: mites (Makarova, 1999, 2002a, 2002b), collembolans (Babenko, 2000), fish (Alekseev et al., 2003), beetles (Makarova et al., 2007; Chernov and Makarova, 2008), and nematodes (Peneva et al., 2002, 2009). The severe conditions of the Arctic deserts determine the low insect diversity. Their entomofauna was presumably estimated at 30–70 species, which is comparable with, or even smaller than the diversity of the arachnid fauna (McAlpine, 1965; Makarova, 2002a; Chernov, 2004; new data on Ellef-Ringnes Island, the Queen Elizabeth Islands). The greater diversity of the class Arachnida in the polar deserts, as compared with the largest class on the Earth, Insecta, is unique for terrestrial biomes. Most insect orders are absent in the polar deserts, whereas some of them are represented by a few species in some districts: 1 species of Plecoptera (Arcynopteryx polaris Klapalek, 1912, identified by L.A. Zhiltsova), not more than 4 species of Coleoptera, and probably not more than 5 species of Hymenoptera (McAlpine, 1965; Danks, 1980; Chernov, 2004; Chernov and Makarova, 2008; our new data on Severnaya Zemlya). Representatives of Neuroptera and Homoptera are known for Severnaya Zemlya only by specimens brought occasionally by the winds (new data). By contrast, Diptera are distinguished by very high taxonomic diversity, counting 27–54 species from
15 families, among which midges of the family Chironomidae are most diverse: 16–32 species in some districts (McAlpine, 1965; Danks, 1980; Chernov, 2004; our new data on Severnaya Zemlya). The goal of the present communication is to analyze the taxonomic composition of the order Lepidoptera in the polar deserts. Research was carried out within the frame of the complex (Severtsov Institute of Ecology and Evolution and Komarov Botanical Institute of the Russian Academy of Sciences) program Comparative Ecology of the Polar Deserts supervised by Academician Yu.I. Chernov. On Severnaya Zemlya, insects were collected in July–September 1997, 1998, and 2000, in the main habitats of the maritime plain (at altitudes up to 70 m above sea level), in the south of Bolshevik Island, mainly in Solnechnaya Bay, and also in the lower reaches of the rivers Telezhnaya and Skalistaya. During 2–6 days insects were also collected in the inner areas of the island, on river terraces in the basins of the rivers Studenaya, Lagernaya, and Golysheva. According to long-term data of the polar stations, the mean annual temperature on Bolshevik Island is about –14°C, the mean temperatures of July vary from +0.9°C to +2.2°C, the mean annual precipitation (mainly snow) is 140–260 mm. The vegetation in the southern part of the island was described in detail by Matveyeva (2006). Insects were captured by hand, in soil traps, by manual examination of various substrates, and by funnel extraction (samples 125– 200 ml). The total material comprised 3652 trap-days and 649 processed samples. In all, 9 specimens of Lepidoptera were found (8 captured by hand and 1 in a trap), including 1 larva; 4 more specimens had been captured earlier on Bolshevik Island by V.I. Bulavintsev (Severtsov Institute of Ecology and Evolution). On Ellef-Ringnes Island of the Canadian Arctic Archipelago (Isachsen Bay: 78°47΄N, 103°32΄W), insects were captured during the international Biocomplexity of Frostboil Ecosystems research project supervised by D. Walker (Fairbanks, Alaska), from 19 to 31 July 2005. The material comprised 1580 trap-days and 92 extracted samples of litter and soil. Four adult specimens of Lepidoptera were captured by hand. Identification of material was performed by experts in the corresponding groups (Geometridae and Noctuidae, by A.V. Sviridov; Plutellidae and Crambidae, by M.A. Klepikov). The material is deposited in the collections of the Zoological Institute of the Russian Academy of Sciences and the Zoological Museum of Moscow State University. ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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Review of the Lepidopteran Fauna of Severnaya Zemlya
Graham-Bell Island in late July–early August 1981; pers. comm.).
Four species were found, two of which can be considered residents of the archipelago.
Biological notes. The species is a common pest of crucifers, especially Brassica cultivars; representatives of 23 more genera of Brassicaceae are listed as its food plants. Numerous findings on plants from other 11 families in most cases do not testify to feeding on them (see Robinson and Sattler, 2001). During mass invasion in the north of Norway (Finnmark), feeding on Cochlearia officinalis was recorded (Kaisila, 1973). The species serves as host to 90 species of parasitoids, mainly hymenopterans (Talekar and Shelton, 1993). A polyvoltine species with a year-round development in warm regions; the development threshold is +7.3°C (see Butts and McEwen, 1981). Development lasts about 14 days at +25.0°C, though naturalization on Marion Island in the Subantarctic (where the temperature of the warmest month, February, is only +7.9°C) indicates a labile thermopreferendum. The diamondback moth has become resistant to all the classes of insecticides, including microbial ones (Bt-toxin). All the stages can overwinter but are not resistant to cold (Talekar and Shelton, 1993). The species cannot survive winter even in many Boreal regions (the southwest of Canada, Scandinavia, the north of Japan, the south of Argentina, etc.), being almost completely eliminated in winter even on the British Isles (Chapman et al., 2002). Therefore, in spite of the presence of crucifers (Draba, Cochlearia, etc.) in the flora of the High Arctic, the species in question cannot form permanent populations there, though it has been earlier suggested that it may permanently inhabit Spitsbergen (Kaisila, 1973). [Ten species from 4 genera of crucifers, including 7 species of whitlow-grasses have been recorded on Bolshevik Island (Matveyeva and Zanokha, 2008).] This is a well-known migratory species which sometimes appears in overwhelming numbers. Migrations start in warm and dry weather. Under the laboratory conditions in Japan the optimal temperature for flight was +23°C (Shirai, 1991), but on Spitsbergen the active flight was observed at temperatures below +10°C (Coulson et al., 2002). All the findings of P. xylostella on Bolshevik Island were preceded by 2–5 days with southerly and westerly winds (S, SSW, SW, W) and the temperature as a rule considerably exceeding the climatic norm (from +8.2 to +14.4°C). One of the individuals was captured in flight on 29.VIII.2000, when the air temperature did not exceed +5°C (our new data).
Superfamily YPONOMEUTOIDEA Family Plutellidae Plutella xylostella (Linnaeus, 1758) Cerostoma maculipennis Curtis, 1832. Plutella cruciferarum Zeller, 1843. Plutella continentalis Zagulajev, 1981 (pro subsp. in P. polaris Zeller, 1880), Kozlov, 1989; Robinson, Sattler, 2001; Baraniak, 2007. Plutella polaris Zeller, 1880 (non Zeller, 1880), Coulson, Refseth, 2004; Coulson, 2007. Material. 1 ♂, Severnaya Zemlya, Bolshevik Island, Solnechnaya Bay (78°12΄N, 103°17΄E), a polygonal community with prevalence of the mosses Gymnomitrion corallioides and Racomitrium lanuginosum on a sand ridge, in a trap, 27.VII.2000; 1 ♂, same district, a zonal community on a maritime plain, in flight, 29.VIII.2000; 1 ♂, same locality, on the buttercup Ranunculus sulphureus, 3.IX.2000 (O.L. Makarova); 1 ♀, middle course of the river Golysheva (78°26΄N, 104°28΄E), a river terrace, a moss-woodrush community, in flight, 2.VIII.2000 (O.L. Makarova); 2 similar ind., same locality and date, were not captured. Two ind. of Plutellidae, possibly of the same species, were captured by V.I. Bulavintsev in Solnechnaya Bay in the summer of 1982 (pers. comm.). Distribution. A cosmopolitan species, not found in the Antarctic but recorded on some Subantarctic islands, on Marion Island the species even became denizen (Chown and Avenant, 1992; Convey, 2005). A polyzonal eurybiotic species which, however, does not develop in equatorial rain forests and under extreme Arctic and alpine conditions (Robinson and Sattler, 2001). The species is recorded regularly on Spitsbergen after southerly winds (Coulson et al., 2002), where earlier it was considered a resident (Kaisila, 1973). It may be carried by air currents to the north of Taimyr (Kozlov et al., 2006), Greenland (Wolff, 1964), Novaya Zemlya (Økland, 1921), and possibly Franz Josef Land (1 ind. of Plutellidae was recorded by V.I. Bulavintsev on Punochya dyke on ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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Superfamily PYRALOIDEA Family Crambidae Gesneria centuriella (Denis et Schiffermüller, 1775) Scoparona centuriella Denis et Schiffermüller, 1775. Material. 1 ♂ (dead adult), Severnaya Zemlya, Bolshevik Island, 4 km E of Cape Antsev, 700 m from the sea coast, snowbed, 31.VII.2000 (O.L. Makarova). Distribution. Holarctic. A polyzonal, mainly an arctoboreal species, mostly associated with mountain regions (including those of Central Europe and the Caucasus) but also recorded on the plains. It is widespread in Greenland but has not been recorded to the north of 74°15΄N (Wolff, 1964). Biological notes. The species is characteristic of both taiga forests and humid shrub tundras (Lafontaine and Wood, 2007). There are no exact data on the food plants; development on mosses was supposed (Shodotova, 2008). In Iceland, adults were found in different regions, only on Chamenerion latifolium (Ólafsson, 1981). On Severnaya Zemlya, the only individual was found dead in the snow bed, where it was evidently brought by the wind. Another representative of Pyraloidea, the polyzonal species Pyla fusca Haworth, 1811, must have been able to settle on Spitsbergen though its population is strongly localized (Coulson et al., 2003). Superfamily GEOMETROIDEA
the Northwest Territories, Melville Island), and P. suttoni Heinrich, 1942 (Quebec: the eastern coast of Hudson Bay, Little Cape Jones R.). The remaining taxa are not considered as valid at the species level. The genus demands revision with analysis of nomenclatural types and application of molecular taxonomy methods. The male genitalia in the genus Psychophora are very variable within a separate species. At the morphological level, only two species differentiated by Viidalepp (2001) may be considered reliable. It is important that these species, Psychophora cinderella Viidalepp, 2001 and Psychophora sabini (Kirby, 1824) sensu Viidalepp, 2001, are often sympatric (see below). The use of molecular methods has been attempted but it is still not clear to what extent the results are compatible with analysis of the type material necessary for solving this task (IBOL…, 2012). As for very interesting material from Ellef-Ringnes Island, the Canadian Arctic Archipelago, the identification of specimens collected there by Russian researchers in 2005 appears problematic before the revision has been made. These are the following findings of adults: 1 ind., Isachsen, on the surface of a shallow water-hole, 23.VII.2005, O.L. Makarova; 2 ind., on the moss turf in the zonal community, 24.VII.2005, N.V. Matveyeva; 1 ind., a dry polygonal community with prevalence of mosses and poppy, in a soil trap, 24.VIII.2005, O.L. Makarova. They may belong to one more species, Psychophora phocata (Möschler, 1862).
Family Geometridae
Psychophora cinderella Viidalepp, 2001
Genus PSYCHOPHORA Kirby, 1824
Material. (1) The males examined by us which allow morphological identification. 3 ♂, Severnaya Zemlya, Bolshevik Island, Akhmatov Bay (78°56΄N, 102°58΄E), 10.VIII.1991 (V.I. Bulavintsev). [Based on these specimens, we indicate the northernmost locality of the species and the family in the Palaearctic]. Besides, on Taimyr Peninsula: West Taimyr (the coast, Dikson): 4 ♂, 8 km NE of Dikson, 8.VIII.1983 (P.S. Tomkovich); 1 ♂, Medusa Bay, Willem Barents Biological Station, forb-dryas tundra, 16.VII.2001 and 2 ♂, the lower course of the Medusa river, 14.VII.2004 (M. Berezin). On Wrangel Island, Rodgers Bay, 1 ♂, a dry rubble-loam hillock, 6.VII.1988 and 1 ♂, a piedmont trail, 10.VII.1988 (O.A. Khruleva). In the mountains of North European Russia (Murmansk Province): 2 ♂, Khibiny railway station, 25.VI.1926 and 1 ♂, same locality, 17.VII.1926, and also 2 ♂: the Khibiny Mountains, Kirovsk,
Representatives of this genus have been most frequently recorded in the High Arctic (Table 1). The difficult problems of the composition and identification of species in the genus Psychophora have been long pointed out (see, e.g., Johnston, 1950). The cited author reported two species of this genus (P. sabini and P. phocata) for the Pribilof Islands (the Bering Sea) and remarked that both species demonstrated an exceptional degree of variation and that it was difficult to find a pair of similar individuals among more than 200 examined ones. In the world catalogue of the family Geometridae (Scoble, 1999), the following species are listed in the genus Psychophora (with their type localities): P. immaculata (Scinner et Mengel, 1892) (the west coast of Greenland), P. phocata (Möschler, 1862) (Labrador), P. sabini (Kirby, 1824) (Canada:
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Table 1. The diversity of Lepidoptera in the High Arctic districts with mean July temperatures no higher than +5°C Number Latitude, Island/District of species Resident species Source of data °N found Spitsbergen, Svalbard 76.6–80.1 12 (3) Plutella polaris Zeller, 1880, Stainton, 1880; Laasonen, Apamea zeta (Treitschke, 1985; Coulson, 2000, 1825), Pyla fusca (Haworth, 2007; Coulson and Ref1828) seth, 2004; Hodkinson, 2004 Severny Island, Novaya Zem74.0–77.0 4 (4) Plutella sp. (larva), Økland, 1928; Rebel, 1923 lya, north of 74°N (?) Psychophora cinderella Viidalepp, 2001 (as “?Larentia byssata Auriv.”), Psychophora sp. (as Larentia sabini), Xestia lyngei (Rebel, 1923)* North plain of Wrangel Island, 71.5 3 (3) Xestia aequaeva (Benjamin, Khruleva, 1991 lower reaches of the river 1934) (as X. brachyptera), Gidrografov Xestia liquidaria (Eversmann, 1848), Gynaephora rossii (Curtis, 1835) Lower reaches of the river Ubo73.6 (?) Xestia liquidaria, X. aequaeva Kozlov et al., 2006 inaya, NW Taimyr Melville Island, the Canadian 74.4–76.8 3 (3) Psychophora sp. (as P. sabini), Bruggeman, 1958; Arctic Archipelago Gynaephora groenlandica Ryan and Hergert, 1977 (Wöcke, 1874), Gynaephora rossii Bathurst Island, the Canadian 75.0–76.7 2 (2) Psychophora sp. (as P. sabini), Danks, 1980; Arctic Archipelago Gynaephora groenlandica Ryan and Hergert, 1977 Prince Patrick Island, the Cana76.3 2 (2) Psychophora sp. (as P. sabini), Bruggeman, 1958 dian Arctic Archipelago Gynaephora groenlandica Northern tip of Peary Land, 83.0 1 (1) Gynaephora groenlandica Wolff, 1964 Greenland Bolshevik Island, Severnaya 77.9–79.4 4 (2) Psychophora cinderella, New data Zemlya Xestia aequaeva Ward Hunt Island, the Canadian 83.0 2 (2) Psychophora sp. (as P. sabini), Bruggeman, 1958 Arctic Archipelago Gynaephora groenlandica Ellef-Ringnes Island, the Cana78.8 1 (1) Psychophora sp. (as P. sabini) McAlpine, 1965 dian Arctic Archipelago Herald Island, the Chukchi Sea 71.4 1 (1) Psychophora sp. (as P. sabini) Khruleva, 2001 Meighen Island the Canadian 79.7–80.2 0 – McAlpine, 1965 Arctic Archipelago Cape Chelyuskin, northern 77.7 0 – Chernov et al., 1979 Taimyr Bennet Island, Novosibirsk 76.7 0** – Uspensky, 1959 Islands Graham-Bell Island, Franz 80.1–80.4 1 (0) – Bulavintsev and Babenko, Josef Land 1983; Bulavintsev, pers. comm. Notes: The number of resident species is shown in parentheses; * Plutella mariae Rebel, 1923 and Psychophora cinderella were recorded, among other species, on Severny Island of the Novaya Zemlya Archipelago, to the south of 74°N (Økland, 1928; Viidalepp, 2001); ** Uspensky (1959) did not specially state that lepidopterans were absent, though after a prolonged stay on the island with extremely impoverished biota he described in detail the findings of other arthropods: planktonic crustaceans and collembolans. ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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11.VII.1946 (A.V. Tsvetaev). [Based on these specimens, we indicate the species for the first time for the European continent and Murmansk Province]. (2) Males of this species morphologically identified by its author and listed in its original description: “Holotype, male, labeled ʻNov[aya] Zemlya, Mato[chkin] Shar, Nochuev spring, 14.V.[19]25, Vakulenko,’ with a handwritten note on the back: ʻCaterpillar on the slope of Nochuev spring 20.IV.25, pupated 3.V.25, emerged 14.V.25.’ Paratypes: 1 ♀, same locality, 19.VII.[19]25, label with a handwritten note on the back: ʻMeadow on the coast;’ 2 ♂, labeled ʻUSSR, N Taimyr, 76°04΄30΄΄N, 98°32΄W, 12– 17.7.1991, Olavi Hilden leg.’” (Viidalepp, 2001). Supplementary Material on Psychophora Psychophora sabini (Kirby, 1824) sensu Viidalepp, 2001 Bombyx sabini Kirby, 1824 sensu Viidalepp, 2001. Material. (1) The males examined by us which allow morphological identification. On Taimyr Peninsula: West Taimyr (coast, Dikson): 3 ♂, Medusa Bay, hill, 10.VII.2004; 1 ♂, the lower course of the river Medusa, 14.VII.2004; 2 ♂, Medusa Bay, 17.VII.2001 (M. Berezin). On Wrangel Island, Rodgers Bay: 1 ♂, sandy-pebble floodplain, 4.VII.1988; 1 ♂, spring valley (wet moss-sedge community), 4.VII.1988; 1 ♂, a rubble north-facing slope, 12.VII.1988 (O.A. Khruleva). In the mountains of the North European Russia (Murmansk Province): 2 ♂, Khibiny Mountains, Kirovsk, 11.VII.1946 (A.V. Tsvetaev). (2) Morphologically identified males of this species which were listed by Viidalepp (2001) after he differentiated the sibling species Psychophora cinderella Viidalepp, 2001 and Psychophora sabini (Kirby, 1824) sensu Viidalepp, 2001: 1 ♂, the total photo and genitalia, Novaya Zemlya (exact locality not specified). In addition, some material of the genus Psychophora was collected on the Severnaya Zemlya Archipelago whose identification (originally made by E.M. Antonova) now needs to be verified: Material. 1 adult, Severnaya Zemlya, Bolshevik Island, the middle course of the river Studenaya (78°37΄N, 101°13΄E), a river terrace, wasteland with prevalence of Dryas punctata, Salix arctica, in flight, 13.VIII.1998 (L.L. Zanokha and O.L. Makarova); 1 adult, Bolshevik Island, near Baranov Cape, 15 km
from the sea, the river valley, a rubble area with mosslichen cover and separate clumps of higher plants, VIII.1982 (V.I. Bulavintsev). [Psychophora sp. may also be present on the terrace of the river Lagernaya, Bolshevik Island (78°22΄N, 103°31΄E), where its alleged parasitoid (see Wood in: Brodo, 2000), the bristle fly Trafoia arctica (Sack) (see Richter, 2005) was found on 7.VIII.2000 by O.L. Makarova.] Distribution. According to the reports of different authors, which should be reconsidered after the work of Viidalepp (2001), Psychophora sabini (Kirby, 1824) was also recorded on the islands Ward Hunt, Ellef-Ringnes, Cornwallis, Bathurst, Melville, Prince Patrick, Ellesmere, and Devon of the Canadian Arctic Archipelago (Bruggeman, 1958), in Greenland north of 70.5°N (Wolff, 1964), in the north of Fennoscandia (Nordström et al., 1941), Novaya Zemlya (Økland, 1928), Yamal (The Red Book…, 2004), Taimyr (Kozlov et al., 2006) [claimed to be an East-Palaearctic species, though it was described from the Nearctic!], in Magadan Province, on Chukotka Region and Kamchatka Peninsula (Sinev, 2008), Wrangel Island (Khruleva, 1989), the North Kuril Islands (Beljaev and Vasilenko, 2002), and the Pribilof Islands (Downes, 1964). Psychophora sabini (Kirby, 1824) sensu Viidalepp, 2001 has been reported from a number of these regions (see above). Biological notes. The numerous data present in the literature should now be attributed to a group of related species. The collective species typically occurs in Arctic deserts, dry and humid tundras, and also in the subarctic mountains (McAlpine, 1965; Danks, 1980; Lafontaine and Wood, 1997). The eyes are of the diurnal type (Lafontaine and Wood, 1997); the acoustic reaction to bats has been lost (Rydell et al., 2000). Some females from the Prince Patrick and Ellesmere islands of the Canadian Arctic Archipelago, and also all the females on the Pribilof Islands are brachypterous (Downes, 1964). Feeding of larvae on Saxifraga oppositifolia, Dryas integrifolia, and Papaver radicatum was observed (Danks, 1980). On Bathurst Island, the development probably takes not less than 3 years (see Danks, 2004); II–IV instar larvae can overwinter, they molt to the next instar only once a year, after wintering (Danks, 1980). In early spring, before ice breakup, the larvae are consumed by the purple sandpiper Calidris maritima, the long-tailed jaeger Stercorarius longicaudus, and obviously some other birds (Danks, 1971). The species serves as host of ichneumon wasps Meloboris sp. (Danks, 1980) and ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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probably also of the tachinid fly Trafoia arctica (Sack) (Wood in: Brodo, 2000). Superfamily NOCTUOIDEA Family Noctuidae Xestia aequaeva (Benjamin, 1934) Xestia brachyptera (Kononenko, 1981), Kononenko et al., 1996. Material. An old-instar larva, Severnaya Zemlya, Bolshevik Island, the middle course of the river Studenaya (78°37΄N, 101°13΄E), a river terrace, wasteland with prevalence of Dryas punctata and Salix arctica, in plant turf, 15.VIII.1998 (O.L. Makarova). [Based on this specimen, we indicate the northernmost locality of the species and the family in the Palaearctic]. Distribution. Novaya Zemlya, Vaigach, Yamal, Taimyr, New Siberian Islands, Wrangel Island, east of Chukchi Peninsula, Alaska, and Yukon (Lafontaine et al., 1983; Kononenko et al., 1996; Kononenko, 2005; Lafontaine and Wood, 1997). Biological notes. The species prefers well drained biotopes: dry tundras, river terraces; on Wrangel Island it reaches the highest abundance in dry sandy areas with moss-forb vegetation with a large fraction of legumes (Khruleva, 1991; Lafontaine and Wood, 1997). The life cycle probably extends over several years (Khruleva, 1989). Caterpillars may feed on plants of the genera Carex, Potentilla, and Salix but always prefer legumes (Khruleva, 1989). Specificity of the Lepidopteran Fauna of the High Arctic On Severnaya Zemlya we have found 4 species of Lepidoptera of which only two, the characteristic Arctic forms Psychophora cinderella and Xestia aequaeva, develop on the archipelago. All the findings of these species are associated with valleys of rivers in their middle course, where well-drained biotopes with a relatively high diversity of flowering plants prevail. These localities are remote from the coast and characterized by a greater number of sunny days and rarer fogs. In the periglacial zone on Severnaya Zemlya the air is 2–3° warmer than on the maritime plains (Bolshiyanov and Makeev, 1995). Plants of the genera Salix, Dryas, Carex, and Saxifraga oppositifolia which serve as food for caterpillars of the above species grow in sufficient quantities only in such intrazonal stations. ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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The findings of the well-known migrant, the diamondback moth Plutella xylostella and the pyralid Gesneria centuriella (1 dead moth) were, as a rule, preceded by strong winds blowing from the continent. Permanent residence of Plutella xylostella on Severnaya Zemlya seems to be impossible since this species cannot overwinter even in the north of the forest belt (see above). However, the population of this species on Marion Island in the Subantarctic, where the mean temperature of the coldest month is only +3.6°C, is considered to be permanent (Chown and Avenant, 1992). The larvae of P. xylostella harming crucifer cultivars in the north of Western Europe and Russia are the offspring of the moths migrating in great quantities from the south (Talekar and Shelton, 1993; Chapman et al., 2002). We have summarized the data on lepidopterans developing under the most severe conditions in the High Arctic, in particular in regions where the mean temperature of July does not exceed +5°C (Tables 1, 2). This group includes 10 species of 6 genera from the families Plutellidae, Geometridae, Lymantriidae, and Noctuidae. Representatives of Rhopalocera were not recorded in the polar desert zone, which has been noted before (Chernov and Tatarinov, 2006). They are also absent in the nival deserts of the Polar Urals (Tatarinov and Dolgin, 2001), the Putorana Plateau, and the Suntar-Khayata Range (new data), although they are rather diverse in the tundra belt of these mountain systems. Thus, the pattern of distribution of Rhopalocera in the Arctic is similar to that of carabid beetles (Chernov et al., 2000): the group includes a large complex of typical Arctic species (about 40), is fairly diverse in the southern tundra subzones and has great biocenotic significance there, becomes strongly impoverished in the northern part of the tundra zone (Chernov and Tatarinov, 2006), and is completely absent in the polar deserts. The reasons for this are still to be analyzed. Since larvae or adults of a number of rhopaloceran species are exceptionally coldresistant (Asahina et al., 1972; Miller, 1982, etc.), frost can hardly be the factor limiting their northward expansion. Association with certain food plants can hardly be the limiting factor, either. For example, among the Macrolepidoptera of Finland, the northern limits of distribution are determined by the food plant only in 3% of the 900 species (Virtanen and Neuvonen, 1999). The larvae of many diurnal butterflies from different families can overwinter twice, so that the development cycle can be extended to 2–3 years
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(Tatarinov and Dolgin, 2006). However, taking into account the extremely short and cold vegetation season in polar deserts (Chernov et al., 2011), the impossibility of further prolongation of the development period must be the most probable reason for the absence of higher Lepidoptera. As for the order as a whole, its diversity strongly depends on the amount of solar radiation (Turner et al., 1987; Virtanen and Neuvonen, 1999), the correlation coefficients between the number of diurnal lepidopteran species and the mean temperature of July in northern districts are varying within 0.87–0.99 (Chernov, 1995; Tatarinov and Dolgin, 2001). Out of 10 species included in Table 2, seven belong to the genera Psychophora, Gynaephora, and Xestia. Their representatives inhabit the Far North districts with the most extreme conditions in all the Arctic sectors. In those cases when only one lepidopteran species was recorded, it was either Gynaephora groenlandica or Psychophora sp. (“Psychophora sabini”). In the south of Verkhoyansk Ridge (the SuntarKhayata Range), the only lepidopteran specimen found by us in nival deserts at 2200 m above sea level was a cocoon of Gynaephora rossii. Thus, there is reason to dispute the opinion of the remarkable expert on Arctic lepidopterans N.Ya. Kuznetsov, who wrote that “the Arctic faunas are either too small to judge about their taxonomic composition, or do not show any taxonomic uniformity” (Kuznetsov, 1938). Already in the tundra zone, the fauna of diurnal butterflies shows a fairly noticeable increase in the participation of certain genera: Boloria, Oeneis, Erebia, and Colias (Chernov and Tatarinov, 2006). The set of lepidopteran taxa in the coldest regions of the Arctic is still more strictly determined, mainly including species with expressed polyphagy, whose larvae take several years to develop (Tables 1, 2). Females of all the lepidopteran species recorded in the polar deserts proper (the Ellef-Ringnes and Ward Hunt islands, the north extremity of Peary Land, Severnaya Zemlya, the Herald Islands) and in regions with natural conditions intermediate between the polar deserts and the arctic tundras (Bathurst Island, Tundra Akademii on Wrangel Island) either have reduced wings or practically do not fly despite the presence of normal wings, which reflects urgent need to save energy and plastic substances under these conditions (see Roff, 1990). Some representatives of the genus Xestia were assumed to develop during 2 or 3 years with repeated wintering of larvae (Mikkola, 1976; Linnaluoto and
Koponen, 1980). Analysis of well documented cases of mass flight of 9 species in even and odd years in Northwest Europe suggested that such an extended cycle of northern Xestia could be determined by the necessity to “purge” the population of larval parasites which probably have annual life cycles (Mikkola, 1976). However, in the north of Europe, the number of species with development extended to 2 years seems to be also greater in other lepidopteran groups (Krogerus, 1972; Sinev, 1988). In the territory of Finland, the fraction of Lepidoptera with repeatedly wintering larvae increases northward (Virtanen and Neuvonen, 1999), whereas for diurnal butterflies this phenomenon is mainly observed at high latitudes (Tatarinov and Dolgin, 2001). All the above points to the primary importance of the thermal factor. The “last” lepidopteran species along the thermal gradient in the Northern Hemisphere seem to be the geometrid moths of the circumpolar species complex “Psychophora spp.” and the Nearctic tussock moth Gynaephora groenlandica (Table 1). The larvae of these species can feed on plants from different families (Table 2). The larvae winter several times and have an obligate diapause. In the High Arctic (Bathurst Island), the larvae identified as Psychophora sabini molt only once at the beginning of each vegetation season, and only II–IV instar larvae can overwinter (Danks, 1980); therefore the development cycle should extend over at least 3 years. The larvae of G. groenlandica which overwinter 7 times at Ellesmere Island (Morewood and Ring, 1998) become active immediately after snowmelt but stop feeding in 3–4 weeks, when the leaves of Salix arctica, their main food plant, reduce their nutritive value (Kukal and Dawson, 1989), whereas the probability of being parasitized increases (Kukal and Kevan, 1987). Such annually “dosated” development of these species may not only synchronize emergence of males and females for copulation but also reduces the risk of being caught unprepared by the onset of winter (Danks, 2004). The importance of such adaptation cannot be overvalued since the unpredictable duration of the summer season sets the most important problem of survival under extreme conditions of the polar deserts. Appearance or disappearance of such conspicuous insects as lepidopterans can be easily recorded, that is why Psychophora spp. and Gynaephora groenlandica may serve as indicator species in analysis of long-term climate changes in the Far North. The presence of indicator species and the relative diversity of big taxa or trophic ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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groups of arthropods were suggested as the main parameters to be used in the monitoring of Arctic communities, instead of such a traditional but non-informative parameter as the number of species (Danks, 1992). Among the lepidopteran species inhabiting the most severe Arctic regions (Table 2), physiological and behavioral adaptations were studied in detail only in Gynaephora groenlandica. This High Arctic endemic occurs almost exclusively on the Canadian Arctic Archipelago and Greenland, its findings on the continent being limited to the north of Yukon (Ryan and Hergert, 1977). The species is highly adapted to living under the conditions of the utmost heat deficiency. The caterpillars are big and densely pubescent; they winter openly, weaving a special sheath before entering diapause (Morewood and Lange, 1997) and in this state they can withstand freezing to –70°C (Kukal et al., 1988b). The larvae spend 60% of their time “basking” (a special behavior ensuring the maximum exposure to the sun and avoidance of wind), due to which they may raise their body temperature by 20°C (Kukal et al., 1988a). The winter diapause is so deep that a metabolism stops almost completely due to degradation of most mitochondria (Kukal et al., 1989), which can be restored in only several hours under favorable conditions in spring (Levin et al., 2003). Unlike its Arcto-alpine equivalent Gynaephora rossii, widespread in the tundras and highlands of the Holarctic, G. groenlandica builds a two-layer cocoon which together with dense pubescence helps accumulate the summer heat more effectively (Kevan et al., 1982) and accelerates the development of pupa (Lyon and Cartar, 1996). Females of both species have fully developed wings and can take wing for a short time (Morewood and Lange, 1997) but they usually do not fly (Ferguson, 1978). [In the mountains of Hokkaido, females of G. rossii do fly and lay eggs on vertical lignified plant stems (Schaeffer and Castrovillo, 1979).] This also allows them to save energy which may be spent on the development of wing musculature (see Roff, 1990). [The females of Xestia aequaeva, “the northernmost” noctuid in the Palaearctic (78°37΄N, Bolshevik Island, Severnaya Zemlya), are brachypterous and also do not fly (Kononenko, 1981).] At the same time, both sexes of G. groenlandica and G. rossii preserve a distinct defense reaction to the signals of bats (Rydell et al., 2000), which was explained by insufficient time of their existence in the Arctic for this adaptation atrophy. The example of G. groenlandica confirms the significance of the complex of different adaptations (such ENTOMOLOGICAL REVIEW Vol. 93 No. 2 2013
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as flexibility in using resources, physiological hardiness, and development reactivity) for a survival under extreme Arctic conditions (Bale et al., 1997; Hodkinson, 2005). Polyphagy and the ability for perennial development are the most important adaptations of Lepidoptera to the extreme high latitude conditions, as it was shown for other groups of Arctic insects: chironomid midges (Butler, 1982), crane flies (McLean, 1973; Lantsov, 1982), and beetles (Chernov et al., 1994; Chernov and Makarova, 2008), and also for collembolans (Burn, 1984), oribatid mites (Block and Convey, 1995), spiders (Leech, 1966), and fish (Alekseev et al., 2003). ACKNOWLEDGMENTS The authors are grateful to the heads of the Central Arctic Prospecting Expedition A.G. Listkov, V.A. Ishkov, and V.N. Efimov (Norilsk), and also to G. Gonzales, D. Walker, and M. Reinholdt (USA) for their great help in the organization of field work on Severnaya Zemlya and Ellef-Ringnes Island; to V.I. Bulavintsev and L.L. Zanokha, for insect collections; to N.V. Matveyeva, for identification of plants and fruitful discussions; to Yu.I. Chernov, A.B. Babenko, and K.V. Makarova, for unfailing interest and advice; to O.A. Khruleva and M.V. Berezina for the possibility to study their collections of Psychophora from Wrangel Island and Taimyr; to E. Baraniak, J. Böcher, M.V. Gavrilo, O. Karsholt, M.V. Kozlov, L.L. Sluchevskaya, A. A. Marusov, J. Kullberg, A.L. Lvovsky, and D.S. Shchigel, for information support and consultations. At certain stages, the work was financially supported by grants to the first author from the Russian Foundation for Basic Research and the Russian Academy of Sciences programs “The Origin of Biosphere and the Evolution of Geobiological Systems,” “Biodiversity,” and “Wildlife.” REFERENCES 1. Aleksandrova, V.D., Vegetation of Polar Deserts in the USSR (Nauka, Leningrad, 1983) [in Russian]. 2. Alekseev, S.S., Makarova, O.L., and Smirina, E.M., “The Arctic Char Salvelinus alpinus Complex from Bolshevik Island, the Severnaya Zemlya Archipelago,” Vopr. Ikhtiol. 43 (6), 842–846 (2003). 3. Asahina, E., Ohyama Y., and Takahashi, T., “Formation of Normal Adults of a Butterfly, Aporia crataegi, Developed from Larvae Frozen to Liquid Nitrogen Temperature,” Low Temp. Sci. Ser. B 30, 91–98 (1972).
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