Frederick D. Provenza

Postingestive feedback as an elementary determinant of food preference and intake in ruminants.

Ruminants select nutritious diets from a diverse array of plant species that vary in kinds and concentrations of nutrients and toxins, and meet their nutritional requirements that vary with age, physiological state. and environmental conditions. Thus, ruminants possess a degree of nutritional wisdom in the sense that they generally select foods that meet nutritional needs and avoid foods that cause toxicosis. There is little reason to believe that nutritional wisdom occurs because animals can directly taste or smell either nutrients or toxins in foods. Instead, there is increasing evidence that neurally mediated interactions between the senses (i.e., taste and smell) and the viscera enable ruminants to sense the consequences of food ingestion, and these interactions operate in subtle but profound ways to affect food selection and intake, as well as the hedonic value of food. The sensation of being satisfied to the full (i.e., satiety) occurs when animals ingest adequate kinds and amounts of nutritious foods, and animals acquire preferences (mild to strong) for foods that cause satiety. Unpleasant feelings of physical discomfort (i.e., malaise) are caused by excesses of nutrients and toxins and by nutrient deficits, and animals acquire aversions (mild to strong) to foods that cause malaise. What constitutes excesses and deficits depends on each animals morphology, physiology, and nutritional requirements. This does not mean that ruminants must maximize (optimize) intake of any particular nutrient or mix of nutrients within each meal or even on a daily basis, given that they can withstand departures from the normal average intake of nutrients (i.e., energy-rich substances, nitrogen, various minerals, and vitamins). Rather, hemostatic regulation needs only some increasing tendency, as a result of a gradually worsening deficit of some nutrient or of an excess of toxins or nutrients, to generate behavior to correct the disorder. Extreme states should cause herbivores to increase diet breadth and to acquire preferences for foods that rectify maladies. From an evolutionary standpoint, mechanisms that enable animals to experience feedback, sensations such as satiety and malaise, should be highly correlated with nutritional well being, toxicosis, and nutritional deficiencies, which are directly related with survival and reproduction.

Linking herbivore experience, varied diets, and plant biochemical diversity

Abstract We contend diets and habitats that allow animals to select among alternatives enable individuals to better meet needs for nutrients and to better cope with toxins. All plants contain toxins, and the amount of toxin an animal can ingest depends on the kinds and amounts of nutrients and toxins in the forages on offer. Nutrients and toxins both cause animals to satiate, and excesses of nutrients, nutrient imbalances, and toxins all limit food intake. Thus, individuals can better meet their needs for nutrients and regulate their intake of toxins when offered a variety of foods that differ in nutrients and toxins than when constrained to a single food, even if the food is “nutritionally balanced”. Food intake and preference also depend on differences in how individual animals are built morphologically and how they function physiologically, and marked variation is common even among closely related animals in needs for nutrients and abilities to cope with toxins. Transient food aversions compound the inefficiency of single-food diets—whether in confinement, on pastures, or on rangelands—by depressing intake among individual animals, even if they are suited “on average” to that nutrient or toxin profile. Thus, feeding and grazing practices that allow producers to capitalize on the individuality of animals are likely to improve performance of the herd by enabling the uniqueness of individuals to become manifest. Finally, past experiences play a crucial role in an animal’s propensity to learn to eat different foods. When herbivores are allowed to eat only the most preferred plants, they are not likely to learn to mix foods high in nutrients with foods that contain toxins. Conversely, herbivores encouraged to eat all plants in an area are more likely to learn to eat mixes of plants that mitigate toxicity. Experienced animals who have learned to eat a variety of foods that differ in nutrients and toxins do so even when nutritious alternatives are available, whereas naive animals familiar only with the nutritious alternatives eat only that subset of familiar foods. Different systems of management alter how animals forage. Continuous grazing at low stock densities encourages selectivity and reduces diet and habitat breadth, whereas short-duration grazing at high stock densities increases diet and habitat breadth. Thus, what was traditionally considered proper grazing management—rotational grazing at low stock densities—may have trained generations of livestock to “eat the best and leave the rest” thus inadvertently accelerating a decline in biodiversity and an increase in the abundance of less desirable plant species.

Conditioned Flavor Aversion: A Mechanism for Goats to Avoid Condensed Tannins in Blackbrush

It has been hypothesized that herbivores instinctively avoid tannin-containing plant parts in response to the adverse effects of tannins on forage digestion. However, we found that goats learned to avoid condensed tannins (CTs) from blackbrush current seasons growth by associating the flavor of foods containing CTs with aversive postingestive consequences. The aversive consequences experienced by goats apparently are not related to digestion inhibition and may depend on the structure of CTs and on how CTs are bound with other cell constituents. These observations suggest several areas of inquiry related to the interaction between CTs and herbivores. A better understanding of the physiological effects of CTs and how herbivores perceive these effects is essential to our knowledge of chemically mediated interactions between plants and mammalian herbivores. With few exceptions, the effects of food flavor have not been separated from those associated with postingestive consequences, even though our data show that postingestive consequences strongly influence palatability. We also need to know how herbivores learn which plant species to eat and which to avoid while foraging in areas that contain a variety of plant species and parts with different kinds and concentrations of CTs. Condensed tannins are pervasive in nature and can defend plants from herbivory, but since many important forages contain high levels of tannins, the presence or absence of tannins per se does not reliably indicate food quality. To predict the ability of a tannin-producing plant to deter herbivores requires a full understanding of how changes in CT structure and binding affect herbivores.

Experience early in life affects voluntary intake of blackbrush by goats.

Low nutritional quality and high levels of condensed tannins adversely affect voluntary intake of blackbrush (Coleogyne ramosissima Torr.) by goats. We studied: (1) how consumption of blackbrush or alfalfa pellets by young goats affected their consumption of those foods later in life, and (2) whether previous ingestion of blackbrush or alfalfa pellets affected the excretion of condensed tannins and total phenols from blackbrush in urine and feces, production of proline-rich proteins in saliva, excretion of nitrogen in feces, and mass of the liver, kidneys, parotid glands, and reticuloramen in goats. From 6 to 26 weeks of age, experienced goats were exposed to blackbrush, while inexperienced goats ate alfalfa pellets. Following exposure, both groups were offered older-growth blackbrush twigs (OG) or a choice between OG and current seasons blackbrush twigs (CSG). A similar feeding trial was repeated nine months after exposure, and, in addition, both groups were offered a choice between OG ad libitum and alfalfa pellets at six levels of availability. Immediately after exposure, experienced goats ingested 95% more (P < 0.01) OG per unit of body weight than inexperienced goats, but both groups rejected CSG. Nine months after exposure, experienced goats ingested 27% more (P < 0.01) OG than inexperienced goats. Experienced goats ingested 30% more OG than inexperienced goats at every level of alfalfa pellet availability. The fate of condensed tannins and total phenols was similar for both groups, but experienced goats excreted 63% more (P < 0.05) uronic acids per unit of body weight. Neither experienced nor inexperienced goats produced proline-rich proteins in saliva. Experienced goats excreted 32% more (P < 0.01) nitrogen in feces per unit of nitrogen ingested than did inexperienced goats. The mass of the reticulorumen was 30% greater (P < 0.05) for experienced than for inexperienced goats one month after exposure, but did not differ 10 months after exposure. The mass of the liver, kidneys, and parotid glands did not differ between treatments. The results show that experience early in life can have profound and persistent effects on consumption of diets high in chemical defenses and low nutrional quality. The results also suggest that several physiological and morphological factors are involved.

Applicability of Five Diet-selection Models to Various Foraging Challenges Ruminants Encounter

It is common knowledge that ruminants do not forage at random, but select a diet from the plants available to them. We believe foraging environments present at least five problems or challenges to ruminants selecting dietary items: (1) variation among dietary items in kind and amount of nutritional constituents, (2) variation among potential dietary items in kind and amount of chemical defenses, (3) plant morphological defenses, (4) temporal and spatial variation in the quantity and quality of forage, and (5) exposure of ruminants to unfamiliar foraging environments. Our objective is to assess the ability of five explanations of diet selection to provide insights into the responses of ruminants to these challenges. The models are: (1) endogenously-generated hungers (euphagia), (2) immediate sensory consequences (hedyphagia), (3) body morpho-physiology and size (morphophysiology), (4) learning through foraging consequences (learning), and (5) nutritional optimization (optimal foraging). We make the assessment by first describing the diet-selection challenges and then discussing the models and their applications to the challenges.

Ability of lambs to learn about novel foods while observing or participating with social models

We studied the influence of different social models on the intake of novel foods by lambs. The lambs were 6–7 weeks old during exposure to the novel foods. Lambs that ate novel foods for 16 min per day for 5 days with their mothers consumed about twice (P<0.05) as much of the foods after weaning as lambs that ate the foods with a dry ewe. Lambs exposed alone five times to the novel foods consumed about half (P<0.05) as much as lambs that ate with a dry ewe. Lambs did not learn to eat novel foods by observing, but not concurrently participating, while social models (mother, ewe) ate the foods. However, lambs that observed their mother eat and subsequently avoid a harmful food, ate less (P<0.05) after weaning than lambs that had observed the food only during exposure. Results were the same when lambs were tested 2 months later.

Ecological implications of condensed tannin structure: A case study

Condensed tannins were isolated from bitterbnish (Purshia tridentata) and blackbrush (Coleogyne ramosissima). Structural analyses showed that both tannins were procyanidins of similar polymer length. The overall stereochemistries at C-3 and C-4, however, differed between the two tannins. These changes in stereochemistry resulted in blackbrush tannins being less preferred than bitterbrush tannins when offered to snowshoe hares (Lepus americanus). It is unlikely that differences in protein-precipitating abilities are the cause for the preference of the bitterbrush over the blackbrush tannins. Instead, we hypothesize that condensed tannins may be depolymerized and absorbed following ingestion. Differences in tannin structure can lead to different depolymerized products and rates of depolymerization, both of which may affect herbivore preferences.

Preference for wheat straw by lambs conditioned with intraruminal infusions of starch

We hypothesized that feed preference depends on the interplay between flavour and postingestive effects, and we tested two predictions based on this hypothesis: (1) lambs acquire preferences for poorly nutritious feeds paired with starch; and (2) preferences persist when starch is no longer administered. Twenty lambs were randomly allocated to two groups and conditioned as follows: on odd-numbered days, lambs in group 1 received onion-flavoured wheat straw and lambs in group 2 received oregano-flavoured wheat straw. On even-numbered days, the flavours were switched and starch (2.5-9.4% of the digestible energy received/d) was infused into the rumen of all animals during straw consumption. Four periods of 8 d of conditioning were performed and on the 9th day of each period all animals were offered a choice between onion- and oregano-flavoured straw. After conditioning, starch administration was suspended and lambs were offered onion- and oregano-flavoured straw at weekly intervals for 8 weeks (extinction). Lambs strongly preferred the flavoured straw paired with starch, and this preference persisted during extinction. Thus, these results suggest that the postingestive effects of energy play an important role in the development of feed preferences of ruminants.

Role of Toxins in Intake of Varied Diets by Sheep

Herbivores foraging on toxic plants may consume a variety of foods that contain different toxins to increase food intake and to avoid toxicosis. We studied whether lambs offered two foods, each containing a different toxin, could ingest more food than lambs offered one food with a single toxin. Thirty-two lambs were allotted to four groups that received: (1) a ration with toxin A, (2) a ration with toxin B, (3) two rations, one with toxin A and the other with toxin B, and (4) a ration with no toxins. Toxin pairs used in the study were (1) amygdalin and lithium chloride (LiCl), (2) LiCl and LiCl, (3) sparteine and saponin, (4) oxalate and nitrate, and (5) tannin and saponin. For an hour each morning, lambs were offered their ration(s) and intakes were measured. Lambs were maintained on an alfalfa pellet or grass hay diet. Each trial lasted either five or six days. Whether or not lambs ate more when offered foods with different toxins depended on the kind and amount of toxin in the food. Lambs offered rations with amygdalin and LiCl or oxalate and nitrate consumed more food than lambs offered a ration with only one of these toxins. Lambs offered rations with sparteine and saponin or tannin and saponin did not eat more food than lambs offered a ration with either saponin or sparteine or tannin alone. Nor did lambs eat more when offered two rations both containing LiCl. In all trials, lambs offered toxins showed no signs of toxicosis, and they ate less food than lambs offered rations without toxins. Our results indicate that in some cases ruminants can increase intake of toxic foods by consuming foods containing different toxins. However, currently the only way to determine how specific toxins may interact in the body to influence intake would be to conduct feeding trials using plants or ground diets that contain toxins.

Tall Larkspur Ingestion: Can Cattle Regulate Intake Below Toxic Levels

Tall larkspur (Delphinium barbeyi) is a toxic forb often consumed by cattle on mountain rangelands, with annual fatalities averaging about 5%. This study examined the relationship between food ingestion and toxicity in cattle. Two grazing studies suggested that larkspur consumption above 25–30% of cattle diets for one or two days led to reduced larkspur consumption on subsequent days. We subsequently hypothesized that cattle can generally limit intake of larkspur to sublethal levels. This hypothesis was tested by feeding a 27% larkspur pellet in experiment 1. Cattle given a 27% larkspur pellet ad libitum showed distinct cyclic patterns of intake, where increased larkspur consumption on one or two days was followed by reduced (P < 0.025) consumption on the following day. The amount of larkspur (mean 2007 g/day; 17.8 mg toxic alkaloid/kg body wt) consumed was just below a level that would produce overt signs of toxicity. Experiment 2 was conducted to examine cattle response to a toxin dose that varied with food intake. Lithium chloride (LiCl) paired with corn ingestion was used as a model toxin, and we hypothesized that if increased (decreased) consumption was followed by a stronger (weaker) dose of LiCl, cattle would show a transient reduction (increase) in corn intake. There was no difference (P > 0.05) between controls and treatment animals at the 20 or 40 mg LiCl/kg dose in the percentage of corn consumed, but the 80 mg LiCl/kg dose induced a cyclic response (mean 46%) compared to intake by controls (mean 96%) (P < 0.001). At the 80 mg/kg dose, LiCl induced an aversion to corn; when corn intake decreased on subsequent days and LiCl dose also decreased, cattle responded by increasing corn intake and apparently extinguishing the transient food aversion. Experiment 3 was similar to the LiCl trial, except that tall larkspur was the toxin. Cattle responded to oral gavage of ground larkspur with distinct cycles; days of higher corn consumption were followed by one to three days of reduced consumption. Corn intake for controls was higher (P < 0.01) than for larkspur-treated animals (means 84 and 52%, respectively; day × treatment interaction P < 0.01). The threshold for toxic effects on corn intake was 14 mg toxic alkaloid/kg body weight. In conclusion, cattle apparently limit ingestion of some toxins so that periods of high consumption are followed by periods of reduced consumption to allow for detoxification. Cyclic consumption generally enables cattle to regulate tall larkspur consumption below a toxic threshold and allows cattle the opportunity to safely use an otherwise nutritious, but toxic, plant.