Teacher Background

There are no obvious signs of invertebrates in the winter landscape because many avoid the harsh environment in a dormant condition.  However, conditions beneath the snow are considerably warmer, more humid, and less windy.  These "mild" conditions allow certain invertebrates to be winter active in the subnivean space, the 3-5 cm between the soil surface and the snowpack.  A snowpack thickness of about 20 cm and density of about 0.1 g/cm³ (the hiemal threshold) is the amount of snow which provides enough insulation to stabilize subnivean temperatures between 0^o and -10^oC (Aitchinson 1984, Marchand 1987). 

Soil Ecosystems

The invertebrates that are winter active under the snow are members of the soil fauna.  The soil fauna are mostly invertebrates that live in the litter or at the soil surface at some life stage.  One way of categorizing the soil fauna is according to size, as in Figure 1.

The role of many of the various soil organisms in the ecology of terrestrial ecosystems is clear:  they decompose the tons of leaf matter that falls at the end of a growing season.  In effect, they accomplish the reverse of photosynthesis; decomposition is similar to respiration on an ecosystem level (Figure 2).  Without breakdown and recycling, the above-ground ecosystem would smother in litter, as well as incur nutrient shortages.

Soil organisms are classified into feeding categories which link the ecosystem together in terms of energy flow.  Producers are organisms that convert inorganic materials and sunlight into biological material.  Usually producers are plants, and they constitute the base of most food webs or trophic pyramids (Figure 3).  Consumers are organisms that require living organic matter as a source of energy.  Organisms that feed on plants are referred to as primary consumers, which in turn are eaten by secondary consumers, and so on.  Decomposers are consumers that eat dead organic matter.  Another system of classifying organisms into feeding categories includes herbivores (feed on living plant material), carnivores (meat eaters), fungivores (feed on fungi), and detritivores (feed on dead organic matter).

The subnivean soil-litter ecosystem is unusual because the base of the food web is mainly dead material, and the fungi it supports.  Therefore, detritivore and fungivore species are common.  Carnivores, belonging to many taxonomic groups, feed upon the detritivores and fungivores.  Table 1 summarizes the kinds and the roles of typical winter-active subnivean invertebrates.  In addition to the year-round soil fauna, a few invertebrates such as aphids and leaf-hoppers, which spend the warm season in the tree canopy and migrate to the soil in autumn, are active under the snow in winter as either nymphs or adults.  A generalized subnivean trophic pyramid is summarized in Figure 3.

Table 1. Winter Active, Subnivean Invertebrates Collected in Pitfall Traps in Manitoba, Canada (Aitchison 1978a,b; 1979a, b, c, d, e, f).

The most abundant subnivean vertebrates are shrews.  As carnivores, they are the top consumer in the subnivean food web, feeding upon winter-active invertebrates.  Shrews, in turn, are important winter food for owls and weasels.  In fact, owls could not survive the winter in boreal ecosystems were it not for their ability to capture shrews, which surface periodically via ventilator shafts constructed in the snow pack.  Thus, some of the energy from subnivean ecosystems flows to organisms of the terrestrial above-snow ecosystem (Figure 4). 

Invertebrate Adaptations to Winter

Invertebrates as a group do not possess the biochemical machinery to maintain constant body temperature. Consequently, their internal temperature varies nearly directly with ambient temperature.  Winter-active invertebrates avoid freezing at subzero temperatures by their behavior; they select the warmest winter microhabitats, either beneath the snow or at the bottom of lakes and streams.  In addition, winter-active invertebrates possess physiological and biochemical mechanisms for avoiding cold injury. 

Cold-hardiness in insects may be achieved in at least three ways: (1) freezing-tolerance, the ability to withstand freezing; (2) freezing resistance, the ability to avoid freezing at below freezing temperatures by supercooling and (3) cold-acclimation (Salt 1961), physiological preparation to avoid cold-injury. The potential mechanisms involved in avoiding cold injury by insects have been reviewed by Danks (1978) and are summarized below.

Freeze-tolerant insect species are able to survive the formation of ice crystals in their tissues (Duman et al 1982); these insects are inactive all winter. Freeze-resistant species use supercooling mechanisms to decrease the temperature of their body fluids below the usual freezing point without the formation of ice crystals.

Supercooling may be accomplished by the elimination of ice nucleators, internally from the blood and externally from the gut.  These substances, usually food or soil particles, provide the initial site or "nucleus" upon which ice crystals may form.  The most efficient ice nucleators are in the gut, so many insects over-winter in an inactive state with empty digestive tracts.  While supercooling by the elimination of ice nucleators is the most common mechanism in insects for avoiding freezing, it is not generally used by winter-active invertebrates.

Supercooling by cryoprotectant production is a widespread mode of freezing avoidance in active subnivean invertebrates. Cryoprotectants are metabolites, mainly alcohols, which lower the freezing point of cells.   The most common of these cryoprotectant alcohols is glycerol -- antifreeze -- which is manufactured by many different invertebrates in winter.  Another polyhydric alcohol commonly serving as a cryoprotectant is sorbitol.  The disaccharide, trehalose, also functions in this manner.  The amounts of insect antifreeze substance produced are often prodigious -- as much as 35% of the total body mass in mid-winter.  Each of these metabolites protects the insect against freezing injury by helping to lower the temperature at which tissues freeze.  In addition, invertebrates which possess these mechanisms for freezing avoidance also make metabolic adjustments to be energetically winter-active.  

Cold acclimation involves seasonal metabolic changes that enable winter-hardy invertebrates to store some of the summer's energy for winter use.  The lipid content of an overwintering insect may be as much as 20-30% of the total body mass.  When food is low or absent, invertebrate can use this stored energy to survive.  In some insects, lipids may also serve as the base for the metabolic production of the polyhydric alcohols used as antifreeze compounds.  Thus, the main metabolites which increase in the fall and winter are lipids and polyhydric alcohols.  With these special metabolic adaptations for avoiding cold-injury, soil invertebrates can be surprisingly active in the subnivean environment.

Subnivean Invertebrate Activity

Subnivean activity implies movement beneath the snow.  In the student activity, invertebrates are captured as they move beneath the snow by using pitfall traps, cups filled with antifreeze set flush with the ground surface.  Pitfall traps mainly capture the mobile mesofauna and macrofauna (Figure 1).   

Year-round pitfall trapping has shown that most groups of invertebrates decrease in abundance in the autumn, remain low in the winter, and increase in the spring.  Despite low numbers, a remarkable variety of northern invertebrates are winter-active as Table 1 shows.  In fact, some litter-dwelling mites which are adapted to colder temperatures reach their peak abundance under the snow in the winter.  Low temperatures also stimulate the activity of some species of centipedes.  One species of spider even builds its web in snow crevices, at 0^o to -2^oC, earning its living in winter capturing springtails. 

Figure 5 shows the abundance of invertebrates caught in pitfall traps set under the snow in different habitats in central New York.  The lawn and shrub habitats are typical of those found near school yards.  The trap cups were filled with antifreeze in December shortly before the first substantial snowfall.  The invertebrates were collected from the trap ten days later and again in mid-January, during a thaw.  It is clear that an active subnivean fauna exists even in the simplest ecosystem.  Also evident are differences between habitats: the forested habitats contained higher numbers of mites and springtails, which in turn supported a population of predatory spiders.

The snowpack serves as an insulator to moderate the climatic conditions in the subnivean space.  Without the insulating snowpack, it would be too cold for most invertebrates to be active on the surface of the ground in winter.  However, it should be mentioned that a few invertebrates -- mainly insects -- are on occasion active as adults on the snowpack surface.  Collembolans (springtails) may be found jumping around in sufficient numbers to discolor the snowpack surface, hence their common name of "snow fleas".  On warm winter days, the snow scorpion fly (Mecoptera), craneflies (Diptera), and stoneflies (Plecoptera) may be found mating on top of the snowpack.  Furthermore, midges (Diptera) and the pygmy grasshopper (Orthoptera) may be found moving around on top of the snowpack in mid-winter.  All of these invertebrates that are active above the snow are darkly colored, enabling them to absorb as much heat as possible from sunlight, a mechanism of warming which is unavailable to subnivean invertebrates.

REFERENCES

Aitchison, C. W.  1978a. Spiders active under snow in southern Canada.  Symp. Zool. Soc. London 42:139-148.

Aitchison, C. W.  1978b. Notes on low temperature and winter activity of Homoptera in Manitoba.  Manitoba Entomol. 12:58-60.

Aitchison, C. W.  1979a. Winter-active subnivean invertebrates in southern Canada. I. Collembola.  Pedobiologia, 19:113-120.

Aitchison, C. W.  1979b. Winter-active subnivean invertebrates in southern Canada. II. Coleoptera. Pedobiologia, 19:121-128.

Aitchison, C. W.  1979c. Winter-active subnivean invertebrates in southern Canada. III.  Acari Pedobiologia, 19:153-160.

Aitchison, C. W.  1979d. Winter-active subnivean invertebrates in southern Canada IV. Diptera & Hymenoptera.  Pedobiologia 19:176-182.

Aitchison, C. W.  1979e. Notes on low temperature activity of oligochaetes, gastropods and centipedes in southern Canada.  Amer. Midl. Nat.  102: 

399-400.

Aitchison, C. W.  1979. Low temperature activity of pseudoscorpions and phalangids in southern Manitoba.  J. Arachnol. 7:85-86.

Danks, H. V.  1978. Modes of seasonal adaptation in the insects. I. Winter Survival.  Can. Entomol. 110:1167-1205.

Duman, J. G., K. L. Horwarth. A. Tomchaney & J. L. Patterson. 1982. Antifreeze agents of terrestrial arthropods. Comp. Biochem. Physiol. 734:545-555.

Marchand, P. J. 1987. Life in the Cold: An Introduction to Winter Ecology. Univ. Press of New England, Hanover, NH.

Salt, G. W. 1961. Principles of insect cold-hardiness. Ann. Rev. Entomol. 6:55-74.

Wallwork, J. A.  1970. Ecology of Soil Animals. McGraw-Hill, London.