Friday January 25, 2013

Li Shen

Winter is a hard time for wildlife. It brings deep cold, leafless terrain, and a shortage of food and water. Animals have few choices. Most songbirds abandon the region via a perilous migration to warmer climates. Other creatures hunker down in hibernation. But there are a number of species that remain active all winter.

This is no easy task. Mammals and birds must maintain their body heat by burning (metabolizing) their body fat - or perish. For herbivores like deer and snowshoe hare, winter is especially harsh. Gone are the nutritious grasses, farm crops, and tender, growing shoots they relied on all summer. Forage is reduced to dormant twigs, buds, and evergreens. Analyses of these foods indicate that while summer forage typically contains up to 35 percent protein and less than 30 percent fiber, winter forage is only 5 percent protein but about 50 percent fiber. The rest is water. What’s more, woody browse often contains plant defense compounds that make it indigestible or even toxic.

No animal can digest cellulose, the main constituent of plant fiber. Yet deer nutrition studies suggest that a 100-pound deer is able to extract over 1,000 calories a day from its winter forage. How does it do that?

It relies on microbes, the only organisms that can break down fiber. Both deer and hare have evolved digestive systems that harness microbial power to digest the indigestible through the process of fermentation.

Deer are known as foregut fermenters because the fermentation step happens at the beginning of the digestive process. A deer stomach is divided into four in-line chambers, the first and largest chamber being the fermentation tank or rumen - hence the term "ruminant."

Unlike a human stomach, the rumen is not very acidic, which allows bacteria, protozoans, and a primitive group known as the archaea to thrive there. In this ecosystem, some bacteria break down cellulose while others feed on breakdown products and supply nutrients back to the fiber digesters. The archaea live on wastes like carbon dioxide and hydrogen, turning them into methane gas that is released by belching. Most important to the deer are the so-called short-chain fatty acids made by fermentation, like acetic acid (found in vinegar) and butyric acid (the hallmark of rancid butter), which provide the deer with a good source of energy.

Even with bacterial help, the digestion of fiber is a slow process. To increase its efficiency, deer regurgitate the rumen contents (cud) and re-chew them for several hours to break up particles, making them easier to ferment. The fermented paste passes to the lower stomach chambers where water and fatty acids are absorbed. The fourth chamber is a highly acidic "true" stomach that kills and digests the fermenters themselves. Essentially, deer grow their own food on the fiber in the rumen and then harvest it.

Different microbes are needed to break down summer and winter forage as the ecosystem of the rumen changes slowly with the seasons. Feeding deer with corn, potatoes, and the like in winter is damaging. Such foods disrupt the rumen environment causing a die-off in bacteria that allows dangerous fungi to take hold. This makes them sick and can lead to starvation.

Like deer, snowshoe hare subsist in winter on bark, twigs, and buds.

But unlike deer, the hare’s fermentation organ is in the hindgut. Fermentation happens after non-fibrous food constituents are digested in the stomach and small bowel. The fibrous bulk of the food is then shunted into the cecum, a blind sac at the junction with the large bowel. The importance of the cecum may be judged by its size: it comprises 60 percent of the digestive tract’s volume. It is populated by an ecosystem of microbes that can break down xylem, the other main constituent of wood. As the microbes digest fiber and make fatty acids, they also multiply prodigiously. The partially-digested food in the cecum is about 55 percent bacteria by dry weight; bacteria also account for most of the 24 percent protein content. The hare takes full advantage of this, in a process akin to a deer’s rumination. Soft pellets of cecal contents, called cecotrophs, are passed from the anus and eaten immediately, allowing the hare to digest the wealth of nutrients in the bacteria themselves. What’s left after re-digestion is passed as hard pellets.

Plants, of course, don’t like to be eaten, and they make themselves unpalatable with substances like tannin that renders proteins and sugars indigestible. But fermenting microbes come to the rescue by breaking down tannin. Interestingly, these tannin-busters are only found in deer rumen in winter, showing the importance of the seasonal adaptation of the rumen.

Though deer and hare are totally unrelated, they have evolved similar ways to take advantage of microbes. If these herbivores did not possess a personal fermentation tank, they would be unable to survive on their spartan winter diet.

Li Shen is an adjunct professor at the Dartmouth Medical School and the chair of the Thetford, Vt., Conservation Commission. The illustration for this column was drawn by Adelaide Tyrol. The Outside Story is assigned and edited by Northern Woodlands magazine and sponsored by the Wellborn Ecology Fund of New Hampshire Charitable Foundation: wellborn@nhcf.org.