Gynaephora groenlandica

Gynaephora groenlandica, the Arctic woolly bear moth, is an erebid moth native to the High Arctic in the Canadian archipelago, Greenland and Wrangel Island in Russia.[3][4] It is known for its slow rate of development, as its full caterpillar life cycle may extend up to 7 years, with moulting occurring each spring.[5] This species remains in a larval state for the vast majority of its life.[4][6] Rare among Lepidoptera, it undergoes an annual period of diapause that lasts for much of the calendar year, as G. groenlandica is subject to some of the longest, most extreme winters on Earth.[7][8] In this dormant state, it can withstand temperatures as low as −70 °C.[7] The Arctic woolly bear moth also exhibits basking behavior, which aids in temperature regulation and digestion and affects both metabolism and oxygen consumption.[4][6] Females generally do not fly, while males usually do.[7]

Arctic woolly bear moth
Arctic woolly bear caterpillar, Baffin Island
Scientific classification
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Lepidoptera
Superfamily: Noctuoidea
Family: Erebidae
Genus: Gynaephora
Species:
G. groenlandica
Binomial name
Gynaephora groenlandica
(Wocke ex. Homeyer, 1874)
Synonyms[1]
  • Dasychira groenlandica Wocke ex. Homeyer, 1874[2]
  • Dicallomera kusnezovi Lukhtanov et Khruliova, 1989[3]

This species has an alpine subspecies which is notable for its geographic distribution south of the High Arctic.[9]

Taxonomy

This moth was likely first discovered on 16 June 1832 on the beach of Fury Bay, Somerset Island in northern Nunavut, Canada, by the crew of the Arctic expedition led by John Ross searching for the Northwest Passage. John Curtis, who studied the entomological specimens returned from the voyage, described the species Gynaephora rossii from the specimens obtained here, but in 1897 Harrison G. Dyar showed that when compared to the caterpillars of G. rossii he had collected from the heights of Mount Washington in New Hampshire, in fact caterpillars of G. groenlandica had been collected in 1832, and Curtis had based his description of the larvae on the wrong species.[10][11]

Before that, however, specimens were recovered in 1870 in northern Greenland by Gottlieb August Wilhelm Herrich-Schäffer on board the Germania on the Second German North Polar Expedition led by captain Karl Koldewey, and subsequently scientifically studied and described by Alexander von Homeyer in 1874 under the name Dasychira groenlandica, which Maximilian Ferdinand Wocke, who had also examined the specimens, had chosen for them earlier, and detailed in a letter to Homeyer. Herrich was able to collect a number of specimens and described the caterpillars as being like those of the Arctia moths, but the adults being extremely similar to Dasychira fascelina (now Dicallomera fascelina) but having such crippled wings as to be nearly incapable of flight. Both Wocke and Homeyer noted it was certainly a new species, but that it was closely related to the species Dasychira rossii (now Gynaephora rossii) known at that time from the geographic vicinity in Labrador.[2]

G. groenlandica was first believed to be endemic to the High Arctic,[12] until a 2013 article reported the discovery of two populations of G. groenlandica neighbouring each other in alpine environments in southwest Yukon, 900 km south of their previously known distribution. The distinct habitat, disjunct distribution, DNA haplotype and wing pattern of these two populations, were found distinctive enough to classify them as a new subspecies: G. groenlandica beringiana.[9] In 1980s moth specimens were collected on Wrangel Island, Russia. These were initially described in 1989 as a new species in the Dicallomera genus as D. kusnezovi, but further examination showed these moths were G. groenlandica, and in 2015 this taxon was subsumed as a new subspecies: G. groenlandica kusnezovi.[3]

As such, the subspecies are:

  • G. groenlandica groenlandica
  • G. groenlandica beringiana Schmidt et Cannings, 2013[3][9]
  • G. groenlandica kusnezovi (Lukhtanov et Khruliova, 1989) Lukhtanovet Khruleva 2015[3]

It has been placed in the subfamily Lymantriinae (the tussock moths) and the tribe Orgyiini.[13][14]

While G. groenlandica is a close relative of G. rossii, the two species are reproductively isolated and no hybridization occurs.[9] The two species are sympatric in many areas of Arctic parts of northern Canada[9][10][11] and Wrangel Island in Russia.[3]

Description

In general, G. groenlandica larvae are large (~300 mg) and densely coated in soft hair.[9][15][16] While they are usually a distinctive tan-brown cast, their color may vary.[9] They are characterized by a distinct hair tuft on their eighth abdominal segment, which has been described as a "rudimentary hair pencil".[7][9] Later larval instars are notable for the color pattern of this dorsal hair tuft.[9] They can also be identified by the spinulose form of their hairs, which are spineless, in contrast to the finer, feather-like (plumose) hairs of their close relative, G. rossii.[9][16] They may also be distinguished from G. rossii in terms of wing pattern: G. groenlandica lack the broad, dark band along the edge of their hind wings that is characteristic of G. rossii. In general, G. rossii also have more wing patterning than G. groenlandica.[9]

The eggs are around 1.6mm.[12]

The cocoons of this species are double-layered, with a distinct pocket of air between the two layers, as opposed to the single-layered cocoons of G. rossii.[12]

Distribution

The nominate subspecies of Arctic woolly bear moth is native to the High Arctic of Greenland and the Canadian Arctic Archipelago including Ellesmere Island, or above approximately 70°N latitude.[4][9][12][16] It is one of the most northern members of the Lepidopteran order in the Northern hemisphere.[7] It occurs as far north as Ward Hunt Island in Canada and northernmost Greenland.[16] A new subspecies G. groenlandica beringiana was described in 2013 south of the Arctic Circle in the alpine environment of the Ruby Range in southwest Yukon, 900km south of the previously known range.[9] A further subspecies G. groenlandica kusnezovi has as of 2015 only been found on Wrangel Island, Russia.[3]

Habitat

G. groenlandica is well-adapted to living in conditions of extreme cold in the High Arctic.[7]

At two distinct field sites on Ellesmere Island, it was discovered that G. groenlandica, when in a diapausal state, tend to exist in specific microhabitats rather than in a random geographic distribution. Hibernacula are frequently found secured to the base of rocks, as opposed to being attached to vegetation. At one investigation site, hibernacula were observed primarily on the leeward (on the side sheltered from the wind) side of rocks, suggesting that wind direction plays a role in the selection of hibernation sites.[8][9]

In captivity, G. groenlandica have also been observed anchoring themselves to leaf litter of Salix arctica during the diapausal period.[8]

Range

The G. groenlandica caterpillar moves up to several meters per day, primarily in order to acquire the necessary resources.[17] In comparing a group of caterpillars physically transferred between different Salix arctica (Arctic willow) plants and a second group in which each individual was restricted to a single willow for the duration of the larval active period, it was observed that transferred larvae demonstrated higher herbivory and growth rates compared to the stationary group. This implies that the acquisition of high quality resources is a primary reason for the movement of G. groenlandica larvae between host plants.[17]

Food resources
Salix arctica, the Arctic willow, is the larva's primary host plant.

G. groenlandica spends much of its life in a larval state, and food resources are necessary for development of the larvae. Salix arctica, the Arctic willow, is the primary host plant and food source for this species.[6][17] The larvae may also feed on plants of other families, such as the flowers of Saxifraga oppositifolia and the senescent leaves of Dryas integrifolia. In the nominate High Arctic subspecies, less than 3% of larvae, however, were found to choose these alternatives.[4] The lower latitude Canadian populations of G. g. beringiana of the alpine environments of southwest Yukon have larvae eating a broader spectrum of plants and proportionately less S. arctica.[9][18]

While larvae rarely eat the catkins (petal-less flower clusters) of S. arctica, they readily consume the plant's leaves. 97% of larvae which actively eat at the onset of their feeding season are consuming the new leaf buds of this plant. Comparing the nutrient concentrations of plant leaves to those of larval frass, has shown that larvae remove nitrogen and potassium from the plant.[17] Larvae appear to only feed in June, which is when the leaves of S. arctica reach their peak concentrations of nutrients and carbohydrates such as starches and sugars. The caterpillars decrease their food intake towards the end of the month and into the summer. At this time, the levels of carbohydrates and nutrients in S. arctica leaves tend to decrease, and the leaves become less palatable as concentrations of phenols and tannins increase.[4][6][19] The decrease in nutrients and carbohydrates, combined with an increase in secondary metabolites, may account for this decline in consumption.[19]

It appears to be adapted to a narrow thermal range. It is able to eat the most at temperatures intermediate to its range. [20]

Life history

The life history traits of G. groenlandica are dictated by the short, cold nature of summers in the High Arctic.[18] Due to its restricted seasonal growth period, G. groenlandica has a life cycle of approximately 7 years.[5] In contrast, its lifespan is much shorter (2–3 years) in warmer, alpine environments.[9] Arctic woolly bear moths remain larvae for the vast majority of their lives, with the exception of up to 3–4 weeks of a single summer.[6] This extended developmental period is not only attributed to low environmental temperatures, but also to the nutrition provided by its host plants .[9] While they remain in their extended larval stage, G. groenlandica experience annual winter diapauses that commence in late June or early July.[7][8] Larval mortality in an experimental caged environment on the tundra was found to be 10%.[21]

Life cycle

On Ellesmere Island the females typically lay their eggs in a mass on or in their cocoon, although they sometimes lay their eggs on the ground or on vegetation around the cocoon.[12]

This species spends the vast majority of its life as a late larval instar; its early larval and adult stages represent only 6% of its full life cycle. It is the later instars which experience multiple annual periods of diapause.[19] During this dominant stage of their lives (from the third to sixth instar phases), G. greenlandica moult annually.[5]

Larval activity is confined to a short period following snowmelt. The High Arctic presents a short growing season of 45–70 days, and the G. groenlandica cease foraging at the end of June, prior to mid-summer.[4] Larvae tend to spend 95% of their time either basking in the sun, feeding, or moving, and only 5% of their time fully immobile. More specifically, about 60% of their time as larvae is spent basking, 20% is spent feeding, and 15% is spent moving.[19]

In late June or early July, the larvae prepare to overwinter by weaving silken hibernacula and entering diapause until the subsequent snowmelt.[7][8][9] This typically occurs when daytime temperatures are at a maximum of 5-10 °C. In their diapausal state, G. groenlandica can withstand temperatures as low as -70 °C, and winter mortality is limited to, on average, a maximum of 13% of the population.[7][19][22]

The developmental stages of pupation, emergence, mating, egg laying, eclosion, and molting to the second instar stage are all confined to a period of 3–4 weeks during a single summer. Emergence and reproduction may occur within a single a 24-hour period.[4][9]

Due to the brief lifespan of fully mature adult individuals, adult moths of this species are difficult to find in the wild.[9]

Species interactions

The presence of the caterpillars eating plants in a particular area appears to have a positive correlation with herbivory of the collared pika (Ochotona collaris) in southwest Yukon.[15]

Predators

G. groenlandica has a distinct defence reaction to bat signals.[7] The Arctic moth Psychophora sabini has some of its defensive reactions to bats, presumably due to the population being isolated from this predator. G. groenlandica and G. rossii, however, continue to possess this defensive behavior. When Arctic woolly bear moths are exposed to bat-like ultrasound (26 kHz and 110 dB sound pressure level root mean square at 1 m), males respond by reversing their flight course. Responses to the sound have been observed from up to 15-25 m away. Females, however, have a degenerated bat-sensing system. There are two presumed reasons for this. Firstly, females tend to be flightless and thus do not require this adaptation. Secondly, an auditory system would compete for space with the ovaries, and the cost of this defence mechanism may outweigh the benefit of having fully functional reproductive organs.[23]

In the High Arctic these moths are preyed upon by birds. The eggs are also eaten by small foraging birds; on Ellesmere Island such birds may tear open the cocoons to feed on the egg mass usually laid inside.[12]

Parasitoids

Many G. groenlandica caterpillars perish during development due to parasitoids, namely the tachinid fly Exorista thula and the ichneumonid wasp Hyposoter diechmanni.[17][21][24] Exorista thula was described from Ellesmere Island in 2012 and is a solitary parasitoid; on the island it killed roughly 20% of the third and fourth instars of its host. Despite occurring together with the closely related Gynaephora rossii here, Exorista thula is only known to attack G. groenlandica, whereas Chetogena gelida is host specific to G. rossii.[12] In general, more than two thirds of Gynaephora are killed by parasitoids, and parasitism in G. groenlandica causes more than 50% mortality.[6][20] The probability of parasitism increases towards the end of the species' active period, which coincides with declining rates of feeding.

The hibernaculum, in which larvae spend a dominant portion of their lives, acts as a defensive barrier to parasitism.[21]

Physiology

Flight

While females of this species have fully developed wings and may take flight for a short time, they usually do not fly. It is worth noting, however, that while Arctic-inhabiting females tend to remain flightless, females of the more southern alpine subspecies are often more mobile.[7][9]

In contrast, males tend to fly high, fast, and erratically during the day.[9]

Thermoregulation

The period of maximal activity for G. groenlandica is in June, during the annual period of maximal solar radiation (24 hours of sunlight) in the High Arctic; however, temperatures at this time continue to be extremely low. Ground temperatures in June, for instance, are usually less than 10 °C.[6][19] At this time, the body temperatures of feeding larvae tend to be similar to those of molting and spinning larvae, while those of “basking” larvae tend to be higher.[6] G. groenlandica larvae spend approximately 60% of their time basking, including during periods of pupation.[19] The behavior of basking is characterized as the action of a caterpillar orienting its body so as to maximize sun exposure and avoid wind. Larvae tend to follow the direct angle of the sun’s rays in order to maintain maximal absorption of sunlight. They do this by orienting perpendicularly to the sun’s angle of insolation.[6] Through the act of basking, G. groenlandica larvae may raise their body temperature by up to 20 °C. Generally, maximal body temperature is approximately 30 °C.[4][7][6] This peak temperature is generally only reached when larvae lie in midday sun, surrounded by snow, on a day with minimal wind.[6]

Solar radiation promotes larval growth, and thus basking may increase developmental rates.[4][6] When comparing larval growth rates at 5, 10, and 30 °C, respectively, growth and metabolic rates were found to be lowest at 5 °C and maximized at 30 °C.[4] This trend exhibits a specific relationship: as body temperature increases due to basking, metabolic rates increase exponentially. This was found to hold true even when larvae were starved or seemingly inactive.[4][6]

In general, feeding larvae tend to have lower body temperatures than basking larvae. Therefore, larvae tend to feed when temperatures are highest, and they bask when they cannot reach the higher temperatures (more than 5 -10 °C) needed for activity.[4] It has been suggested that without the help of basking in 24-hour sunlight during High Arctic summers, larvae would rarely exceed their developmental threshold of ~5 °C.[19] This may account for the unique tendency of the Arctic woolly bear moth to have short feeding periods during times of peak insolation, followed by lengthier periods of basking and digestion.[19]

In early to mid-June, larval metabolism tends to be greatly impacted by food intake and rising temperature. Later in the active season, they become much more metabolically insensitive to temperature, and energy obtained via food consumption is conserved.[25]

Changes in metabolic state and body temperature also affect oxygen consumption.[4][6] Oxygen consumption was found to be much lower when larval body temperatures were below 10 °C.[6] Low oxygen consumption was also observed in inactive larvae. In contrast, it was found to be higher for caterpillars that were moving or starved, higher still for digesting larvae, and highest for feeding larvae.[4]

Digestion

Larvae frequently bask in the sunlight for roughly five hours after feeding before moving to a new site.[4][6] The consequent increase in body temperature stimulates gut enzyme activity, which enables a higher digestion rate.[6] G. groenlandica can convert ingested food at a rate of efficiency which is higher than the average value rate of efficiency of Lepidopteran species in general.[4]

Diapause

G. groenlandica experiences a period of winter diapause during which it remains dormant within a hibernaculum. In this state, it can withstand temperatures as low as -70 °C.[7] Encasing itself within a hibernaculum during diapause serves several functions: protection from parasitoids, avoidance of diminished nutrient concentration in their primary food source, Salix arctica, degradation of mitochondria linked to decreased metabolism (hypometabolism) and antifreeze production, and general conservation of energy reserves.[6][7][12]

These cocoons are made of silk and consist of two layers, into which larval hairs are incorporated.[9][22] In a 1995 study of experimentally caged larvae in the High Arctic of the Canadian Archipelago, 81% of larvae spun hibernacula.[21]

During the active season, larvae orient towards solar radiation, and each spins its respective hibernaculum over a 24-hour period.[7][8] They generally pupate with their head facing south, in a north-south orientation.[6] This cocoon helps the larvae to accumulate heat more effectively.[7]

G. groenlandica often anchor their hibernacula to the base of rocks. In captivity, G. groenlandica have also been observed to attach themselves to Salix arctica leaf litter during the diapausal period.[8] In the 1995 study mentioned above, in which larvae were kept in a cage-controlled environment on the High Arctic tundra, more hibernacula were actually observed on the predominant plant cover of Dryas integrifolia (mountain avens) and Cassiope tetragona (Arctic white heather) as opposed to on their principal host plant, S. arctica.[21] Almost half of the larvae which spun hibernacula did so in conjunction with other larvae, forming joint cocoons. Upwards of three caterpillars were occasionally observed sharing a common hibernaculum, but the most common case was that of two individuals sharing a joint cocoon. Higher rates of communal hibernacula occurred at lower population densities per cage.[21]

As temperatures decrease in the late Arctic summer, larvae begin synthesizing cryoprotective compounds, such as glycerol and betaine. Accumulation of these "antifreezes" (which protect cells from cold conditions) is aided by the bottlenecking of oxidative phosphorylation through mitochondrial degradation. While the larvae continue to produce energy from stored glycogen in their frozen state, this mitochondrial degradation causes their metabolism to drop so low as to almost stop entirely, inducing dormancy. Mitochondrial functioning may be fully restored in the spring after mere hours of resumed larval activity.[7][26]

Conservation

At warmer temperatures, arctic moth larvae generally tend to have higher respiration rates and lower growth rates. They also tend to shift their diets to more nutrient-rich foods in this type of environment. For instance, the herbivory rate of the main food source for G. groenlandica, S. arctica, is altered at elevated temperatures.[9] This implies environmentally dependent host plant plasticity in G. groenlandica. It also suggests that an increase in temperature due to global warming may have significant effects on the behavior of northern herbivore invertebrates such as G. groenlandica, as well as effects on the herbivory rates of their food sources. Thus, G. groenlandica may represent a potential indicator species for future studies on climate change.[7][18][9]

This species was highlighted in BBC's sequel to Planet Earth, called Frozen Planet.[27]

See also

References
  1. Savela, Markku (2 June 2019). "Gynaephora". Lepidoptera and some other life forms. Markku Savela. Retrieved 21 November 2019.
  2. von Homeyer, Alexander (1874). "Lepidopteren". Wissenschaftliche Ergebnisse. Die zweite Deutsche Nordpolarfahrt (in German). 2. Leipzig: F. A. Brockhaus. pp. 409–410.
  3. Lukhtanov, Vladimir A.; Khruleva, Olga (2015). "Taxonomic Position and Status of Arctic Gynaephora and Dicallomera Moths (Lepidoptera, Erebidae, Lymantriinae)" (PDF). Folia Biologica (Kraków). 63 (4): 257–261. doi:10.3409/fb63_4.257. ISSN 1734-9168. PMID 26975140. Retrieved 22 November 2019.
  4. Kukal, Olga; Dawson, Todd E. (1989-06-01). "Temperature and food quality influences feeding behavior, assimilation efficiency and growth rate of arctic woolly-bear caterpillars". Oecologia. 79 (4): 526–532. Bibcode:1989Oecol..79..526K. doi:10.1007/BF00378671. PMID 28313488.
  5. Morewood, W. Dean; Ring, Richard A. (1998-07-01). "Revision of the life history of the High Arctic moth Gynaephora groenlandica (Wocke) (Lepidoptera: Lymantriidae)". Canadian Journal of Zoology. 76 (7): 1371–1381. doi:10.1139/z98-085. ISSN 0008-4301.
  6. Kukal, Olga (March 24, 1988). "Behavioral Thermoregulation in the Freeze-Tolerant Arctic Caterpillar, Gynaephora groenlandica" (PDF). The Company of Biologists Limited.
  7. Makarova, O. L.; Sviridov, A. V.; Klepikov, M. A. (2013-04-01). "Lepidoptera (Insecta) of polar deserts". Entomological Review. 93 (2): 225–239. doi:10.1134/S0013873813020115.
  8. Bennett VA, Lee RE Jr, Nauman JS, Kukal O. Selection of overwintering microhabitats used by the arctic woollybear caterpillar, Gynaephora groenlandica. Cryo Letters. 2003 May-Jun;24(3):191-200.
  9. Barrio, Isabel C.; Schmidt, B. Christian; Cannings, Sydney; Hik, David S (December 2013). "First Records of the Arctic Moth Gynaephora groenlandica (Wocke) South of the Arctic". Arctic. 66 (4): 429–434. doi:10.14430/arctic4329. hdl:10261/142753.
  10. Curtis, John (1835). "Insects". In Ross, John (ed.). Narrative of a Second Voyage in Search of a North-west Passage, and of a Residence in the Arctic Regions during the Years 1829, 1830, 1831, 1832, 1833 - Appendix. 2. London: A.W. Webster. p. lxx, lxxi. doi:10.5962/bhl.title.11196.
  11. Dyar, Harrison G. (December 1897). "Note on Larvae of Gynaephora groenlandica and G. rossii" (PDF). Psyche. 8 (260): 153. doi:10.1155/1897/67619. Retrieved 24 November 2019.
  12. Morewood, Dean W.; Wood, Monty D. (August 2002). "Host utilization by Exorista thula Wood (sp. nov.) and Chetogena gelida (Coquillett) (Diptera: Tachinidae), parasitoids of arctic Gynaephora species (Lepidoptera: Lymantriidae)". Polar Biology. 25 (8): 575–582. doi:10.1007/s00300-002-0382-y.
  13. "Gynaephora rossii Species Information". BugGuide. Retrieved 2018-03-29.
  14. "Gynaephora rossi". Pacific Northwest Moths. Retrieved 21 November 2019.
  15. Barrio, Isabel C.; Hik, David S.; Peck, Kristen; Guillermo Bueno, C. (23 June 2013). "After the frass: foraging pikas select patches previously grazed by caterpillars". Biology Letters. 9 (3): 20130090. doi:10.1098/rsbl.2013.0090.
  16. Morewood, Dean W.; Lange, Petra (1997). "Immature stages of high arctic Gynaephora species (Lymantriidae) and notes on their biology at Alexandra Fiord, Ellesmere Island, Canada". The Journal of Research on the Lepidoptera. 34: 119–141. Retrieved 23 November 2019.
  17. Greyson-Gaito, Christopher J.; Barbour, Matthew A.; Rodriguez-Cabal, Mariano A.; Crutsinger, Gregory M.; Henry, Gregory H. R. (April 2016). "Freedom to move: Arctic caterpillar (Lepidoptera) growth rate increases with access to new willows (Salicaceae)". The Canadian Entomologist. 148 (6): 673–682. doi:10.4039/tce.2016.22.
  18. Barrio, I. C.; Hik, D. S.; Liu, J. Y. (May 2014). "Diet breadth of Gynaephora groenlandica (Lepidoptera: Erebidae): is polyphagy greater in alpine versus Arctic populations?". The Canadian Entomologist. 147 (2): 215–221. doi:10.4039/tce.2014.35.
  19. Lee, Richard (2012-12-06). Insects at Low Temperature. Springer Science & Business Media. ISBN 9781475701906.
  20. Birkemoe, Tone; Bergmann, Saskia; Hasle, Toril E.; Klanderud, Kari (2016-10-01). "Experimental warming increases herbivory by leaf-chewing insects in an alpine plant community". Ecology and Evolution. 6 (19): 6955–6962. doi:10.1002/ece3.2398. PMC 5513215. PMID 28725372.
  21. Kukal, Olga (1995-04-01). "Winter mortality and the function of larval hibernacula during the 14-year life cycle of an arctic moth, Gynaephora groenlandica". Canadian Journal of Zoology. 73 (4): 657–662. doi:10.1139/z95-077.
  22. Laity, Peter R.; Holland, Chris (2017-02-01). "Thermo-rheological behaviour of native silk feedstocks". European Polymer Journal. 87 (Supplement C): 519–534. doi:10.1016/j.eurpolymj.2016.10.054.
  23. Rydell, J.; Roininen, Heikki; Philip, Kenelm W. (22 March 2000). "Persistence of Bat Defence Reactions in High Arctic Moths (Lepidoptera)". Proceedings of the Royal Society B: Biological Sciences. 267 (1443): 553–557. doi:10.1098/rspb.2000.1036. PMC 1690572. PMID 10787157.
  24. Varkonyi, Gergely; Tomas Roslin (2013). "Freezing cold yet diverse: dissecting a high-Arctic parasitoid community associated with Lepidoptera hosts". Canadian Entomologist. 145 (2): 193–218. doi:10.4039/tce.2013.9.
  25. Hodkinson, Ian D. (2005). "Adaptations of invertebrates to terrestrial Arctic environments". Transactions of the Royal Norwegian Society of Sciences and Letters: 28–29 – via ResearchGate.
  26. Hoffmann, Klaus H. (2014-12-19). Insect Molecular Biology and Ecology. CRC Press. ISBN 9781482231892.
  27. Levin, Gary (April 8, 2008). "Another sweeping nature special when 'Planet' freezes over". USA Today. Retrieved May 25, 2010.

Further reading
  • Heinrich, Bernd (1993). The hot-blooded insects: strategies and mechanisms of thermoregulation. Harvard University Press. ISBN 9780674408388.
  • Chapman, R. F. (1998). The insects: structure and function. Cambridge University Press. p. 519. ISBN 978-0-521-57890-5.
  • Kukal, O.; Kevan, P.G. (1987). "The influence of parasitism on the life history of a high arctic insect, Gynaephora groenlandica (Wöcke) (Lepidoptera: Lymantriidae)". Can. J. Zool. 65: 156–163. doi:10.1139/z87-022.
  • Kukal, O (1988). "Caterpillars on ice". Natural History. 97: 36–41.
  • Kukal, O.; Duman, J.G.; Serianni, A.S. (1988). "Glycerol metabolism in a freeze-tolerant arctic insect: An in vivo 13-C NMR study". J. Comp. Physiol. B. 158 (2): 175–183. doi:10.1007/bf01075831. PMID 3170824.
  • Kukal, O.; Heinrich, B.; Duman, J.G. (1988). "Behavioural thermoregulation in the freeze-tolerant arctic caterpillar, Gynaephora groenlandica". J. Exp. Biol. 138: 181–193.
  • Kukal, O.; Dawson, T.E. (1989). "Temperature and food quality influences feeding behavior, assimilation efficiency and growth rate of arctic woolly-bear caterpillars". Oecologia. 79 (4): 526–532. Bibcode:1989Oecol..79..526K. doi:10.1007/bf00378671. PMID 28313488.
  • Kukal, O.; Duman, J.G.; Serianni, A.S. (1989). "Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars". J. Comp. Physiol. B. 158 (6): 661–671. doi:10.1007/bf00693004. PMID 2715455.
  • Kukal, O. 1990. Energy budget for activity of a high arctic insect, Gynaephora groenlandica (Wöcke) (Lepidoptera: Lymantriidae). In: C.R. Harington (ed) Canadian Arctic Islands: Canada's Missing Dimension. National Museum of Natural History, Ottawa, Canada.
  • Kukal, O. 1991. Behavioral and physiological adaptations to cold in a freeze-tolerant arctic insect. In: R.E. Lee and D.L. Denlinger (eds) Insects at Low Temperature. Chapman and Hall, N.Y.
  • Kukal, O. 1993. Biotic and abiotic constraints on foraging of arctic caterpillars. In: N.E. Stamp and T.M. Casey (eds) Caterpillars: Ecological and Evolutionary Constraints on Foraging. Chapman and Hall, N.Y.
  • Kevan, P.G.; Kukal, O. (1993). "A balanced life table for Gynaephora groenlandica (Lepidoptera: Lymantriidae) a long-lived high arctic insect, and implications for the stability of its populations". Can. J. Zool. 65: 156–163.
  • Danks, H.V.; Kukal, O.; Ring, R.A. (1994). "Insect cold-hardiness: Insights from the arctic". Arctic. 47 (4): 391–404. doi:10.14430/arctic1312.
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