Perhaps it’s the summers I spent in college counting and identifying dragonflies and butterflies on the wing. Or maybe it was the hundreds of hours I endured in graduate school with my face dangerously close to a pan of full of muck, plucking out thousands of tiny stream insects. I reckon it’s just a lifetime of curiosity for anything six-legged that permanently etched a search image for insects in my brain.

Thus, it’s no wonder that, while enjoying a winter’s day hike to one of my favorite waterfalls near Ithaca, New York, [Taughannock Falls, above] my eyes strayed from the scenic ice-glazed landscape to the tiny, dark specks moving nimbly across the snow: winter stoneflies were on the move! [Winter Stonefly in Hand, below]

Winter stoneflies are peculiar little creatures. In the dead of winter, the stoneflies’ aquatic immature stages, called larvae or nymphs, crawl from their rocky bottom home up through cracks and crevices in the snow and ice that cover the surface of the stream they’ve inhabited for the last year and emerge as adults. Although in possession of four wings rolled neatly over their elongated abdomens, adult winter stoneflies stay close to the snow and ice, walking rather than flying, in search of mates.

All bundled up in my hat, mittens, scarf, parka, and long underwear (and still COLD), I wondered about the physiology of the winter stoneflies I observed. How can they be so active in sub-zero winter temperatures, when most of their six-legged brethren are well-hidden from the elements? And how do they avoid the lethal effects of freezing in two very different habitats, in water and on land?

Back in the cozy warmth of my home, I began to investigate some of these questions. I learned rather quickly that not much is known about the cold hardiness of aquatic insects, let alone the winter stoneflies (a name that refers specifically to two families in the order Plecoptera: Capniidae and Taeniopterygidae). In fact, in his treatise on stoneflies, the late Canadian field naturalist H.B. Noel Hynes proffered one possible reason why this is the case; adult winter stoneflies, he muses, are "most abundant early in the season before the average entomologist has emerged from hibernation."

To understand how winter stoneflies deal with freezing temperatures in water and on land, it’s useful to first examine what 60 years of research have revealed about how terrestrial insects, a more studied group, survive winter. If not clever enough to avoid winter altogether by migrating south (like those smart monarch butterflies) or seeking an insulated shelter such as your house (lady beetles and stink bugs, anyone?), terrestrial insects will prepare for the brutal cold of winter internally by undergoing a number of physiological and biochemical changes.

To understand these changes, cryobiologist Richard Lee, Jr. recommends we think of an insect as a tiny bag of water. In small, insect-sized volumes, water can actually be cooled many degrees below its standard freezing point (0°C) and still remain in liquid form, a process known as supercooling. You may have encountered supercooled liquids at some point this winter in the form of freezing rain. However, should a dust particle be introduced to a supercooled liquid, ice crystals will immediately begin to form around it in a process called nucleation. Additionally, ice can form inside the little bag of supercooled water if external ice crystals touch and subsequently invade it through any small opening, a process called inoculative nucleation.

Insects preparing for exposure to subzero winter temperatures, whether in an active or resting state, generally employ one of two strategies to achieve cold hardiness: avoid freezing or tolerate it.

Freeze-avoiding insects actively produce anti-freeze compounds – including glycerol, proteins, and sugars – that enhance their ability to supercool, allowing body fluids to remain unfrozen at temperatures even further below their freezing point. Some terrestrial insects’ supercooled body fluids can remain in a liquid state at temperatures 15 – 35°C below zero. Additionally, as winter approaches, freeze-avoiding insects will eliminate materials from their guts and body fluids that could serve as a seed around which ice crystals nucleate, including food, digestion-related bacteria, and dust.

Freeze tolerant insects, on the other hand, not only tolerate the formation of ice crystals in the fluids bathing their cells, but actively promote it. These insects produce ice-nucleating proteins in their extracellular fluid that actually limit the insects’ ability to supercool and promote ice crystal formation at higher subzero temperatures. By promoting ice crystal growth outside the cells, the ice-nucleating proteins help reduce the likelihood that the contents within the insects’ cells will freeze and burst. But with the water outside the cells bound up as ice crystals, water inside the cells will want to move into the extracellular space. To prevent subsequent cell dehydration and stabilize the cell membranes, freeze tolerant insects also produce the anti-freeze compound glycerol.

So how do these strategies translate, if at all, to aquatic insects, particularly the winter stoneflies?

Alas, before we tackle that question, let’s consider the thermodynamic properties of the aquatic environments they call home for most of their life cycle. Water, as you may recall from high school physics, has a higher specific heat than air; in other words, it takes more energy to heat water than it does to heat an equal mass of air. Consequently, the water in streams and rivers do not experience the extreme fluctuations in temperature that the air above them does and generally remains warmer than adjacent terrestrial habitats in winter. When ice forms on the surface of a water body, it actually insulates the water and substrate beneath it from sub-zero temperatures.

Dr. Lee and his cryobiology team bravely emerged from their winter hibernation to collect and compare the supercooling abilities of temperate zone aquatic and terrestrial insects in winter. Turns out, aquatic insects supercool much less than their terrestrial kin; aquatic insects supercooled to about -7°C whereas terrestrial insects in the same families supercooled to temperatures as low as -40°C! Despite reduced supercooling abilities, most aquatic insects inhabiting these temperate waters are still classified freeze avoiders; the relatively few aquatic insects known to actually tolerate freezing (specimens were actually collected directly from ice!) inhabit streams and ponds in the arctic that regularly freeze clear through the bottom. Dr. Lee and his colleagues hypothesize that overwintering aquatic insects living in the temperate zone simply do not encounter the extreme sub-zero temperatures that terrestrial insects do, rendering a super supercooling ability evolutionarily unnecessary.

Winter stonefly nymphs emerge as adults in the air pockets between the water and an insulating layer of surface ice, a fairly protected habitat that does not experience temperatures much below 0°C. Moreover, Dr. Lee and his colleagues have found that adult winter stoneflies collected in February had a significantly greater ability to supercool (i.e., they can cool to much lower temperatures without freezing) than their nymphal stages, suggesting adults can increase the amount of anti-freeze compounds in their body fluids.

Following emergence, adult winter stoneflies may seek protection in thermal refuges beneath the snow or under rocks that offer temperatures warmer than the subzero surface air. While the adults’ brownish-black body coloration may promote the absorption of solar radiation, any such gains would likely be overridden by a cold breeze due to their small body mass. And by walking about on the tips of their feet, the adult stoneflies avoid the hazards of external ice crystals potentially invading their bodies and inducing inoculative freezing.

As our winter days grow longer and warmer in anticipation of spring, your opportunities to catch winter stoneflies in action this season will soon disappear. Here’s a search image for you – Commit it to memory. Now rouse yourself from that winter hibernation and go find those supercool little bags of water!


References and Further Reading

Borror D.J., White R.E. Peterson. (1970) A field guide to insects of America north of Mexico. Houghton Mifflin Co., New York. 404 pp.

Bouchard R.W., Schuetz B.E., Ferrington L.C., Kells S.A. (2009) Cold hardiness in the adults of two winter stonefly species: Allopcapnia granulata (Claassen, 1924) and A. pygmaea (Burmeister, 1839) (Plecoptera: Capniidae). Aquatic Insects 31 (2): 145-155 doi: 10.1080/01650420902776690

Frisbie M.P., Lee R.E. (1997) Inoculative freezing and the problem of winter survival for freshwater macroinvertebrates. Journal of the North American Benthological Society 16 (3): 635-650.

Hynes H.B.N. (1976) Biology of Plecoptera. Annual Review of Entomology 21: 135-153.

Lee R.E. (1989) Insect cold-hardiness: To freeze or not to freeze. Bioscience 39 (5): 308-313

Lencioni V. (2004) Survival strategies of freshwater insects in cold environments. Journal of Limnology 63 (Suppl. 1): 45-55.

Moore M.V., Lee R.E. (1991) Surviving the big chill: Overwintering strategies of aquatic and terrestrial insects. American Entomologist 37: 111-118

Walters Jr., K.R., Sformo T., Barnes B.M., Duman J.G. (2009) Freeze tolerance in an arctic Alaska stonefly. Journal of Experimental Biology 212(2): 305-312 doi:10.1242/jeb.020701

Photo credits: Taughannock Falls and Winter Stonefly in Hand, Holly Menninger, 2008; three Allocapnia sp. Winter Stonefly Closeups, Tom D. Schultz, 2001. All photos are used with permission and licensed under the Creative Commons.

About the author: Dr. Holly Menninger is a senior extension associate at Cornell University where she helps protect New York State’s natural resources from the threats of invasive species, including a number of really big, bad bugs. With a Ph.D. in ecology and a fondness for insects with weird and wonderful life histories, she’s determined to share her enthusiasm for the natural world by any means necessary, including podcasts, tweets (@DrHolly), and posing for pictures with 17-year cicadas on her nose.

The views expressed are those of the author and are not necessarily those of Scientific American.