More Than a Matter of Taste, Part II

This excerpt is from Fred Provenza’s book Nourishment: What Animals Can Teach Us About Rediscovering Our Nutritional Wisdom (Chelsea Green Publishing, 2018) and is reprinted with permission from the publisher.

Feedback from the Gut Microbiome

In 1968, near the Department of Defense’s Dugway Proving Grounds in Utah, 6,400 sheep were killed instantly by aerially applied nerve gas that drifted in the wrong direction due to a sudden shift in winds. In January 1971, over half of the sheep in a herd of 2,400 died of unknown causes in less than 24 hours near Garrison on the Utah-Nevada border. In that instance, though, nerve gas wasn’t the cause. What happened near Garrison was due to a phenomenon that had been explained in an article that had been published twenty years prior. Photos in that article showed sheep carcasses strewn across the salt desert. A dead ewe lay in the foreground while another ewe nibbled an herb with bluish green leaves. That herb was halogeton (Halogeton glomeratus), which thrives in salt desert soil that is high in sodium and chlorine. Sodium in halogeton forms salts of oxalic acid, which is exuded as residue on leaves. That residue can be toxic to herbivores.
Ironically, sheep who have experience eating halogeton can eat up to 36 percent of their diet as halogeton without any ill effects. Poisoning occurs when hungry sheep who have never eaten the plant before (researchers use the term “naive” sheep) are forced to eat too much halogeton too quickly. Historically, that occurred when sheep were trucked long distances and put in areas dominated by halogeton.
Intoxication ensues when oxalate is absorbed faster than it can be detoxified by rumen microorganisms that degrade oxalates. Sheep adapted to eating halogeton have much higher rates of oxalate degradation than do naive sheep. Successful transitions to a halogeton diet are accompanied by a ten-fold increase in the rate of oxalate metabolism by rumen microbes. Sheep need three to four days to build up an aptly large microbial population to rapidly degrade oxalate. Adapted sheep can tolerate two and a half times more oxalate than nonadapted sheep.
Scientists who study wild and domestic herbivores have long valued how diet affects the microbiome, which in turn affects the diet, as microbial ecologist Robert Hungate highlights in his classic book The Rumen and Its Microbes, published over fifty years ago. Ruminants and hindgut fermenters such as horses rely on bacteria to provide them with energy, protein, and vitamins. Bacteria digest the cell walls (cellulose) that give structure to plants. Volatile fatty acids such as propionate, butyrate, and acetate are produced from microbial fermentation of cellulose. They are absorbed directly through the rumen wall and provide most of the energy these animals require for activity and growth. The bodies of dead microbes provide 80 percent of the protein needs of ruminants. Bacteria in the rumen also synthesize B vitamins for ruminants.
Thus, the plants herbivores eat provide food for rumen microbes, which in turn feed herbivores. High-forage diets select for bacteria that digest cellulose, while high-grain feedlot diets select for bacteria that digest starch. Diets rich in secondary compounds select for microbes that enable herbivores to eat many otherwise potentially toxic plants such as halogeton. The more diverse the diet, the greater the number of different microbial species that can thrive in the gut.
A positive feedback loop also exists between a person’s food preferences, the species of microbes in their gut, and the preferences of those gut microbes for different dietary items. Microbes provide feedback to the brain through nerves, neurotransmitters, peptides (short-chain amino acids), and hormones. The same is true for rodents. Studies of rats show that certain species of gut bacteria affect the levels of the appetite-stimulating hormone ghrelin, and studies of mice show that other species of gut bacteria affect the appetite-suppressing hormone leptin.
The microbiome also affects gut motility and gut feelings through the hormone serotonin. Serotonin regulates intestinal movements and influences appetite, sleep, and mood contributing to feelings of well-being and happiness. Serotonin is primarily found in the gastrointestinal tract (95 percent),
blood platelets, and the central nervous system (5 percent) of animals, including humans. Specialized cells (enterochromaffin cells) in the gastrointestinal tract form synapses that link directly with neurons in the brain, which allows cross talk between the gut and the brain to occur in milliseconds rather than minutes. To protect the body from toxins, these cells immediately send signals to induce vomiting and diarrhea. Enterochromaffin cells express chemosensory receptors for specific compounds, they are electrically excitable, and they modulate serotonin-sensitive afferent nerve fibers through synaptic connections. That enables enterochromaffin cells to detect and transduce environmental, metabolic, and homeostatic information (gut feelings) from the gut directly to the brain.
Microbes also affect emotions. For example, gamma-aminobutyric acid (GABA) is a key neurotransmitter that dampens the fear and anxiety that mammals experience when neurons in the central nervous system are overexcited. Species of gut bacteria such as Lactobacillus rhamnosus alter expression of GABA messenger RNA in various parts of the brain via the vagus nerve, which connects the gut with the brain. Importantly, L. rhamnosus reduced stress-induced corticosterone and anxiety- and depression-related behavior. These findings highlight the key role of gut bacteria in communication of the gut with the brain and suggest gut bacteria may be useful therapeutic aides in stress-related disorders such as anxiety and depression.

Learned Preferences in Herbivores

By guiding animals to eat a variety of foods, cells and organ systems in the body ensure nutritional needs are met. The body, however, can withstand departures in intake of nutrients, and thus it’s not necessary to adjust intake of every nutrient at every meal. Homeostatic regulation needs only an increasing tendency, due to a steadily worsening imbalance, to generate behavior to correct a disorder. As nutritional state becomes inadequate, animals (including humans) sample novel foods readily—familiarity breeds contempt and novelty breeds contentedness. Once nutritional needs are again met, animals don’t experience cravings from deficits or malaise from excesses. When nutritional state is adequate, animals sample novel foods cautiously—familiarity breeds contentedness and novelty breeds contempt.
Animals prefer foods high in energy and protein, because their bodies need large amounts of energy and protein. These nutrients strongly influence food selection when animals are given choices of foods that differ in energy and protein. Lambs select diets with a higher ratio of protein to energy to meet their needs for growth, but they eat less protein as they age and their need for protein declines. Ewes increase intake of protein relative to energy as their needs for protein increase with the growth of the fetus during the last trimester of gestation, or when they are infected with parasites. When fed a diet with an imbalance between protein and energy, sheep choose to forage in locations with foods that rectify the imbalance. Dairy cows fed protein supplements during lactation avoid eating plants (for example, legumes) and plant parts (for example, new growth) that are high in protein when they forage on grass-legume pastures. They select plants and plant parts high in protein when they are fed energy-rich concentrates, such as corn grain during lactation. Lambs even become averse to diets deficient in specific amino acids and they choose to eat foods that rectify the deficit.
How do livestock maintain a balance of energy and protein in their diets? They associate the flavors of foods with nutrient-specific feedbacks. When lambs are fed a meal that consists of an “appetizer” and a “main course,” they make choices that balance the ratio of energy to protein within a meal. For example, when lambs are fed a high-energy appetizer and then offered various main course choices, they prefer the flavor previously paired with protein. Conversely, lambs fed a high-protein appetizer prefer the flavor previously paired with energy for the main course. They are even sensitive to the rates at which different sources of energy and protein ferment in the gut, as imbalances result in digestive and metabolic upsets.
The foods that animals consume to meet their needs for energy and protein usually contain vitamins and minerals, too. If animals become deficient in vitamins or minerals, however, they will select foods to rectify the deficit. Sheep deficient in vitamin E prefer food higher in vitamin E, for example. Sheep can make multiple flavor-feedback associations with minerals. We designed a study in which we made lambs deficient in one of three minerals—phosphorus, calcium, or sodium—and gave them a choice of the three differently flavored foods. The lambs had previously ingested these flavored foods with one of the three minerals. Lambs preferred the flavor previously paired with repletion of the mineral—phosphorus, calcium, or sodium—they were lacking. These findings support the practice of offering a selection of individual minerals free-choice so animals can select the particular mineral(s) that are low in the forages they are consuming. The same is true in principle and practice with medicines as I discuss in chapter 7.
Unusual foraging behaviors arise as animals sample new and often strange foods in an attempt to rectify nutritional imbalances. In the wild, sheep, caribou, and red deer rectify deficits by eating lemmings, rabbits, and birds—live or dead; sheep eat arctic terns and ptarmigan eggs; white-tailed deer dine on fish; and deer gnaw on antlers. Bighorn sheep use rodent middens as mineral licks. Cattle deficient in phosphorus eat bones, and they stop eating bones when inorganic phosphate levels in their blood rise to normal ranges. Cattle and sheep rectify mineral deficits by eating soil, licking urine patches, and eating fecal pellets and dead rabbits.
In over forty years of working with sheep, I had never seen one eat soil or feces or lick urine patches. But when I was part of a group studying sheep fed a phosphorus-deficient diet, we observed all of those behaviors. We were feeding sheep a phosphorus-deficient diet to see if they would select a food that would rectify the deficiency. However, even after a couple weeks of feeding the phosphorus-deficient diet, we couldn’t get blood phosphorus levels in the “deficient” sheep to drop. Why? They were sticking their heads through the wire panels to eat the feces of sheep in adjacent pens that were being fed a diet that was adequate in phosphorus. When we moved the phosphorus-deficient sheep into new pens, away from the phosphorus-replete sheep, they immediately began to eat the feces on the ground from a previous study. We eventually made them deficient, and they selected the food with phosphorus. Such perverted appetites or picas are adaptive behaviors that commence as animals begin to experience deficits.
This phenomenon also explains what happened when Angora goats of my early research study learned to eat woodrat houses. Inside those houses was densely packed vegetation soaked in urine, which is high in nitrogen in the form of urea. The goats had discovered that source of nonprotein nitrogen, which rumen microbes use to synthesize aminogenic (protein) and glucogenic (energy) nutrients, and they took advantage of it to help meet their needs. But as I noted, only one group of goats ate woodrat houses the first winter, and over the ensuing two winters, out of eighteen groups of goats of different breeds and from different locations, only that one group of goats ever learned to use woodrat houses as a source of nutrition. These findings illustrate the peculiar ways herbivores can discover foods that meet their nutritional needs. By learning from mother and peers, each generation benefits, and such behaviors become part of the foraging culture—the collective nutritional wisdom—of the group.

Fred Provenza is professor emeritus of Behavioral Ecology in the Department of Wildland Resources at Utah State University, where he directed an award-winning research group that pioneered an understanding of how learning influences foraging behavior and how behavior links soils and plants with herbivores and humans. Provenza is one of the founders of BEHAVE, an international network of scientists and land managers committed to integrating behavioral principles with local knowledge to enhance environmental, economic, and cultural values of rural and urban communities. His latest book Nourishment: What Animals Can Teach Us About Rediscovering Our Nutritional Wisdom will be published in November 2018.