Elizabeth A. Burritt

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.

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.

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.

How Goats Learn to Distinguish Between Novel Foods That Differ in Postingestive Consequences

To better understand some of the mechanisms that control selection of novel foods differing in postingestive consequences, we offered goats current seasons (CSG) and older (OG) growth twigs from the shrub blackbrush (Coleogyne ramosissima). CSG is higher than OG in nitrogen (1.04% v. 0.74%) and it is more digestible in vitro in goat rumen fluid (48% v. 38%). Nevertheless, goats acquire a preference for OG because CSG contains much higher levels of a condensed tannin that causes a learned food aversion. When CSG and OG were offered to goat naive to blackbrush, the goats did not choose either OG or CSG exclusively, but when they finally (1) ate more CSG than OG within a meal (averages of 44 g and 16 g, respectively) and (2) ate enough CSG within the meal to acquire an aversion (average of 44 g), they ingested less CSG than OG from then onward. Accordingly, the change in food selection resulting from postingestive feedback was influenced by the amount of each food ingested within a meal. This was further shown when we varied the amounts of CSG and OG that goats ingested within a meal, and then gave them by gavage the toxin lithium chloride (LiCl). They subsequently ate less of the food eaten in the greatest amount, regardless of whether it was CSG or OG. The salience of the flavor (i.e., taste and odor) of CSG and OG also played a role in the acquired aversion to CSG. Salience evidently was due to a flavor common to both OG and CSG that was more concentrated in CSG. We conclude that the relative amounts of different foods ingested within a meal, and the salience of the flavors of those foods, are both important variables that cause goats to distinguish between novel foods that differ in postingestive consequences.

Ability of lambs to learn with a delay between food ingestion and consequences given meals containing novel and familiar foods

Abstract We studied: (1) whether lambs could learn to avoid a novel food given delays of up to 8 h between food ingestion and gastrointestinal illness (long-delay study); (2) how gastrointestinal illness affected the selection of several foods differing in familiarity to lambs (mixed-meal study). Gastrointestinal illness was induced by administering encapsulated lithium chloride (LiCl; 160 mg kg −1 body weight) to lambs using a balling gun. In the long-delay study, lambs were offered a novel food for 5 min. If they consumed 10 g or more of the food, LiCl was administered 0,2,4,6, or 8 h later. Intake of the novel food was measured in 5 min trials for the next 3 days. When the delay between food ingestion and the administration of LiCl was 2 or 4 h, the lambs reduced their intake of the novel food after a single dose of LiCl. The lambs also reduced their intake of the novel food when the delay between food ingestion and the administration of LiCl was 6 or 8 h. However, LiCl was administered twice before the lambs reduced their intake of the novel food; they were also given a stronger dose (320 mg kg −1 body weight) of LiCl on Day 2 than on Day 1. Thus, repeated exposures, greater gastrointestinal distress, or both may be required before lambs reduce their intake of a novel food given delays of 6 h or more. For the mixed-meal study, we used five foods; lambs had eaten two of the foods since weaning, two of the foods for 25 days prior to the onset of the trials, and one food was novel. When lambs were offered the novel food for 5 min followed by the four familiar foods for 20 min, and then given LiCl, they refused to eat the novel food for the next 3 days. Some of the lambs also reduced their intake of the foods they had eaten for 25 days. The lambs did not decrease their intake of the foods they had eaten since weaning.

Supplemental barley and charcoal increase intake of sagebrush by lambs.

We evaluated the influence of supplemental barley and activated charcoal on the intake of sagebrush by lambs in individual pens. In 3 experiments, lambs were fed sagebrush (harvested and chopped to 2-3 cm) during the morning; they were fed a basal diet of alfalfa pellets in the afternoon. In the first experiment, lambs supplemented with activated charcoal + barley ate more A. tridentata ssp. vaseyana than lambs supplemented with barley (304 vs. 248 g; P = .071). A second set of experiments, which consisted of 3 trials, determined the effects of activated charcoal, barley, and subspecies of sagebrush on intake of sagebrush. Lambs supplemented with activated charcoal + barley ate more A. tridentata ssp. vaseyana (Trial 1; 292 vs. 225 g; P = .086), and more A. tridentata ssp. tridentata (Trial 2; 371 vs. 255 g; P = .031) than lambs supplemented with barley. In Trial 3, lambs supplemented with barley ate more sagebrush than lambs that were not supplemented (480 vs. 318 g; P = .0002). A third set of experiments compared activated charcoal + barley, barley, and no supplement in 2 trials. In Trial 1, lambs supplemented with activated charcoal + barley or barley generally ate more A. tridentata ssp. vaseyana than lambs not supplemented (P = .017). In Trial 2, lambs supplemented with activated charcoal + barley ate slightly more A. tridentata ssp. vaseyana than lambs supplemented with barley, and they ate substantially more than lambs not supplemented (P = .032). Collectively, the results suggest that energy from supplemental barley increased intake of sagebrush by lambs fed a basal ration of alfalfa pellets which are high in protein, and that activated charcoal played a minor role in further increasing intake of sagebrush. DOI:10.2458/azu_jrm_v53i4_banner

Effect of an unfamiliar location on the consumption of novel and familiar foods by sheep

We studied how moving lambs to an unfamiliar environment affected their intake of novel and familiar foods. In the first experiment, half the lambs (n = 14) were conditioned to avoid a novel food (wheat) by pairing its ingestion with lithium chloride (LiCl); the other half (n = 14) received wheat but no LiCl. Half of the lambs that received LiCl and half that did not were moved to a location unfamiliar to the lambs. Lambs at both locations were offered wheat (familiar but aversive to half the lambs), oats (novel food), and alfalfa pellets (familiar food). In the second experiment, one group of lambs (n = 16) remained at the familiar location; the other group (n = 16) was moved to a novel location. Both groups were offered alfalfa pellets (familiar food) with or without onion powder (novel flavor), wheat bran (novel food), and rye with 1% LiCl (novel and toxic food). We found that: (1) lambs consumed a familiar but aversive food (wheat) more readily at the unfamiliar location than at the familiar location (P = 0.052); (2) lambs ate less of the novel foods (oats and wheat bran) at the unfamiliar location (P = 0.09 and P < 0.001, respectively); (3) intake of the familiar food (alfalfa pellets) did not differ between locations on day 1 of either experiment. These results suggest that: (1) food neophobia is greater in unfamiliar than familiar environments, which may cause animals to eat more familiar foods in unfamiliar environments, even if the familiar foods contain toxins. They further suggest that animals should be: (2) exposed to novel foods in familiar environments to expedite intake of novel foods; (3) provided with familiar foods in novel environments to prevent declines in intake; (4) conditioned to avoid foods (e.g. fruit trees, poisonous plants) in the environments where they will forage to increase the persistence of the aversion.

Amount of experience and prior illness affect the acquisition and persistence of conditioned food aversions in lambs

We studied the acquisition of food aversions in sheep. In the first experiment, we investigated how prior illness affected the formation of a conditioned food aversion. Lambs were offered small amounts (< 200 g) of novel foods (wheat and rice) for 12 days, until lambs ate both foods readily. To establish an aversion to one of the foods, lambs were then given the toxin lithium chloride (LiCl) after eating one of the foods. On subsequent days, lambs were allowed to eat the food previously paired with LiCl until the aversion extinguished. When lambs later consumed a meal of wheat and rice and received LiCl, they avoided the food that had been paired with LiCl, but they did not reduce intake of the other food (P < 0.001). In the second experiment, we examined how amount of experience with a food affected the acquisition and persistence of a food aversion. Lambs were offered oats (novel food) at 1% body weight for either 28, 14, 7, or 1 days. An aversion was then induced by offering oats followed by LiCl. Lambs with at least 14 days exposure to novel foods formed the least persistent aversions (P = 0.002). Furthermore, the aversion to oats extinguished within 6 days in lambs offered oats for 7 days. Thus, lambs are not likely to abstain from a food they were trained to avoid (e.g. trees in orchards, poisonous plants) if they have more than 7 days experience with the food. Finally, lambs should be fed small amounts of highly nutritious novel foods (e.g. grains) during the first 7 days to avoid gastro-intestinal distress and more persistent aversions.

Socially induced diet preference ameliorates conditioned food aversion in lambs

We determined whether a socially induced diet preference could ameliorate a conditioned food aversion in lambs. To do so, one group of lambs was conditioned to avoid the shrub Cercocarpus montanus by giving them lithium chloride, a toxin that produces strong food aversions, following shrub ingestion. On Day 1 of conditioning, lambs ingested an average of 29 bites of C. montanus, but by Day 2 the number of bites had decreased to two and lambs took even fewer bites on Days 3–5. Following conditioning, averted lambs spent a substantial amount of time foraging on C. montanus when foraging with non-averted conspecifics in pasture trials (10% vs. 19% of time spent ingesting C. montanus) and in pen trials (25 vs. 35 bites). We also examined the effects of group composition during conditioning (heterogeneous vs. homogeneous) on the use of C. montanus during pasture and pen trials. In the heterogeneous groups, lambs being averted to C. montanus were exposed to the shrub in the presence of lambs not being averted to C. montanus. In the homogeneous groups all lambs were averted to C. montanus. Lambs in the heterogeneous groups took numerically more bites of C. montanus than lambs in the homogeneous groups during conditioning (25 vs. 17 bites day−1), but the trend was not significant (P>0.05). When foraging on pastures, however, lambs in the heterogeneous groups spent more (P 0.05). The capacity of social interactions to ameliorate food aversions suggests that social influences are a major determinant of diet selection in sheep.

Sagebrush Ingestion by Lambs: Effects of Experience and Macronutrients

We investigated how experience early in life and macronutrient content of the diet influenced intake of mountain big sagebrush (Artemisia tridentata Nutt. ssp. v a s e y a n a (Rydb.) Beetle) by sheep. In the first part of our study, 2-month-old lambs were exposed as a group for 2 mo to a 70% barley-30% soybean meal ration (300 g/hd/day) that contained increasing amounts sagebrush (1 to 20%). Control lambs received grain without sagebrush. All lambs had access to alfalfa hay and pellets ad libitum. When lambs were tested at 6 months of age, prior exposure had no effect on sagebrush consumption after the first 4 days of the trial. When sagebrush comprised 20% of an alfalfa/barley ration, lambs ate the sagebrush ration readily even when a nutritious alternative was offered indicating the flavor of sagebrush did not prevent lambs from feeding. Increasing the amount of sagebrush in the ration from 50% to 75% resulted in lambs eating less of the barley/sagebrush ration, but daily intake of sagebrush remained constant throughout the 4 day trial, presumably because toxins (terpenes) limited intake of sagebrush. In the second part of our study, lambs experienced with sagebrush were fed 250 g/hd/day of barley, and nutritional status was varied by offering alfalfa pellets at 33% or 80% of ad libitum (1.2 and 2.7 times maintenance, respectively) to determine if dietary energy levels affected intake of sagebrush. Each day lambs received a 50/50 sagebrush/barley supplement ad libitum for 1 hour. Lambs fed at 33% of ad libitum consumed more of the sagebrush/barley supplement than lambs fed at 80% of ad libitum. Thus, additional energy did not enable lambs to consume more sagebrush. In the last trial, lambs in both treatments were fed a basal ration of alfalfa pellets at 50% of ad libitum. Each morning for 1 hour, lambs were offered macronutrient supplements containing either 50% barley/50% sagebrush (high energy) or 25% barley/25% soybean meal/50% sagebrush (high energy and protein). Lambs consumed the same amount of sagebrush regardless of supplement. Thus, supplemental protein did not improve sagebrush consumption. We conclude lambs readily ingested a high-energy ration containing sagebrush, regardless of exposure early in life, suggesting toxins, not flavor, control intake of sagebrush. Further, supplementing lambs with energy or protein failed to improve intake of sagebrush, which suggests these macronutrients did not enhance detoxification of sagebrush.