Overwintering Strategies of Insects in Northern Climates
Joe Nelsen Challenges in winter
● Small ectotherms
● Lack of insulation
● Food shortages (for both herbivores and predators) General strategies - energetic benefits/tradeoffs
● Diapause/dormancy
● Spatial avoidance (migration) Diapause
● Pause in development
○ various life stages
● Strategy for handling all kinds of environmental stressors
● Similar to hibernation in other animals
● Very beneficial for insects who employ this strategy - maximizes fitness ○ Conserving during the “off season” more energy for productive season Diapause - Goldenrod Gall Fly
● Egg laid in stalk of Goldenrod plant
○ Larvae hatch and stimulate gall formation
○ Larvae diapause over winter
○ Larvae pupates and adult emerges in spring
● Gall provides food and protection, but little insulation…
● Larvae produce cryoprotectants to depress freezing point, and nucleators to nucleate ice away from cells…
● Larvae can survive down to -35℃ Ice Nucleation in Gall Flies
● Employs two types of ice nucleators:
○ Fat body cells and calcium phosphate spherules - heterogeneous ice nucleation
● Calcium phosphate spherules
○ Small spheres of crystalline compound that line malpighian tubules of larvae, and nucleate ice in extracellular fluid of tubules
● Fat body cells = rare case of intracellular ice nucleation Calcium phosphate spherules
(Mugnano, 1996) Supercooling in Gall Flies
● Gall Fly larvae supercool their tissues using - polyols (sugar alcohols) ○ Sorbitol and Glycerol - primary cryoprotectants
● Lower freezing point of fluids within cells ○ Prevent ice formation in high concentrations colligitavely - by inhibiting water molecules from joining to form ice crystals intra/extracellularly
● Polyol production triggered by temperature ○ Glycerol accumulated before winter ○ Sorbitol from glycogen in response to lower temps
● Producing cryoprotectants = energetically expensive
and uses stored glycogen (Baust, 1982) Monitoring conditions in gall
● Timing to initiate physiological changes is crucial
● Environmental cues are monitored - polyol levels change in response
● Individuals that initiate and terminate diapause most efficiently will have highest fitness
(Irwin et al., 2001) Winter Clustering
● Honeybee hives are endothermic as a whole ○ Workers cluster and generate heat via flight muscles in winter ○ Individuals alternate locations on cluster to minimize losses ○ Temp. of core is very stable: 32 - 36℃
● Keeps queen and brood warm ○ Allows for continued rearing of young throughout winter
● Increases fitness of next generation workers ○ Queen/brood fitness = hive’s fitness ○ The more young that survive winter will have a larger workforce for spring ○ More workers in spring = more resources collected and stored for next winter brooding Monarch Butterflies - Latitudinal Avoidance
● Monarch Lipid Budget
○ Scarce resources for 3 months of overwintering period
○ Unable to replenish lipid reserves during this time
● Behavioral adaptations to minimize lipid depletion while overwintering in Mexico… ○ Increased resting in shade closer to point of lipid exhaustion ○ Easier to warm up flight muscles to Flight Threshold than cool down ○ Lowest lipid use per day in cooler temps
(Masters et al., 1988) Winter Ants - Vertical Avoidance
● Burrow up to 12 feet
○ Ground insulates tunnels
○ Temp stays around 65℉ in winter
○ Tunnels are in ant’s Thermoneutral - no energy expenditure
for thermoregulation (after building tunnels)
● Above ground foraging
○ Small tunnels dug to surface to warm up in when cold
○ Huge fitness advantage - most other inverts are dormant/diapausing Conclusion
● These are only a few examples…
● Overall insects = very well adapted
to surviving cold winters
● Adaptations allow for exploitation
of new niches Literature Cited
Baust, John G., and Richard E. Lee. "Environmental triggers to cryoprotectant modulation in separate populations of the gall fly, Eurost a solidaginis (Fitch)." Journal of Insect Physiology 28.5 (1982): 431-436.
Brookfield Farm Honey. "What Happens to Honeybees in the Winter?" Brookfield Farm Bees & Honey Blog. N.p., 30 Nov. 2010. Web. 02 May 2017.
Brower, Lincoln P., Linda S. Fink, and Peter Walford. "Fueling the fall migration of the monarch butterfly." Integrative and Comparative Biology 46.6 (2006): 1123-1142.
Danks, Hugh V. "Seasonal adaptations in arctic insects." Integrative and Comparative Biology 44.2 (2004): 85-94.
Hadley, Debbie. "What Is Diapause?" ThoughtCo. N.p., 9 Feb. 2017. Web. 02 May 2017.
Hahn, Daniel A., and David L. Denlinger. "Energetics of insect diapause." Annual review of entomology 56 (2011): 103-121.
Irwin, J. T., V. A. Bennett, and R. E. Lee Jr. "Diapause development in frozen larvae of the goldenrod gall fly, Eurosta solidaginis Fitch (Diptera: Tephritidae)." Journal of Comparative Physiology B 171.3 (2001): 181-188.
MAAREC. "Seasonal Cycles of Activities in Colonies." MAAREC - Mid Atlantic Apiculture Research & Extension Consortium. N.p., 08 Oct. 2010. Web. 02 May 2017.
Masters, Alan R., Stephen B. Malcolm, and Lincoln P. Brower. "Monarch butterfly (Danaus plexippus) thermoregulatory behavior and adaptations for overwintering in Mexico." Ecology 69.2 (1988): 458-467.
Mugnano, J., R. Lee, and R. Taylor. "Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae)." Journal of Experimental Biology 199.2 (1996): 465-471.
Pfister, Thomas D., and Kenneth B. Storey. "Insect freeze tolerance: Roles of protein phosphatases and protein kinase A." Insect biochemistry and molecular biology 36.1 (2006): 18-24.
Rice, Eleanor. "Prenolepis Imparis." School of Ants. NSF and HHMI, 2011. Web. 02 May 2017.
Sandro, Luke H., and Richard E. Lee Jr. "Winter biology & freeze tolerance in the goldenrod gall fly." The American Biology Teacher 68.1 (2006): 29-35.
Storey, Kenneth. "ANIMAL COLD HARDINESS." (n.d.): n. pag. The Storey Lab. Carleton University. Web. 2 May 2017.
Storey, Kenneth. "Goldenrod Gall Fly." The Storey Lab. Carleton University, 1027. Web. 02 May 2017.
Szopek, Martina, et al. "Dynamics of collective decision making of honeybees in complex temperature fields." PloS one 8.10 (2013): e76250.
Zachariassen, KARL ERIK. "Physiology of cold tolerance in insects." Physiological reviews 65.4 (1985): 799-832. Images
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