Whenever a food contains a toxin, an animal offered this food alone has to trade off the consequences of reducing its daily intake, thereby escaping the full effects of the toxin and suffering a lack of nutrients (bearing in mind that, in general, the only difference between a toxin and a nutrient is the concentration of the substance in the diet).
Interactions between nutrients
The ratio of VFAs administered can influence the degree of preference or aversion generated. The preference by straw-fed lambs for the associated flavoured food was greater when the ratio of acetate:propionate in the infusate was 55:45 than when it was 75:25 (Villalba and Provenza, 1997a). It is likely that sheep on the straw diet would be deficient in glucose due to low rates of production of propionate in the rumen, and this would be alleviated more effectively by the mixture with the higher proportion of propionate.
Lambs prefer a poorly nutritious flavoured food eaten during, and shortly after, an intra-ruminal infusion of energy or protein. Preloads of casein decrease preferences for flavours previously paired with casein and increase preferences for flavours paired with starch, while preloads of energy have the opposite effect. These animals can, therefore, discriminate between the post- ingestive effects of energy and protein and associate the effects with food flavours in order to regulate macronutrient ingestion.
It has been proposed that certain types of diet provide imbalances between energy and protein supply at different times of day, even though they may be balanced overall. Kyriazakis and Oldham (1997) set out to test whether such asynchrony of nutrient supply would influence diet selection, relative to a food designed to provide the same nutrient supply in a synchronous manner. Foods were formulated to provide rapidly or slowly fermentable energy with high or low ruminal degradable protein (RDP) – all foods had the same calculated contents of metabolizable energy and metabolizable protein. When choices were offered, the proportion of the low-RDP food in the selected diet was lower when the carbohydrate source was rapidly rather than slowly fermentable, which is consistent with the hypothesis that ruminants learn to select a mixture of foods that minimize metabolic imbalance.
There is thus accumulating evidence that ruminants prefer to avoid a food with an adequate nutrient balance overall that delivers different nutrients at different rates and results in temporary imbalances.
Interactions of nutrients with toxins
Animals on a high plane of nutrition are better able to withstand toxins than underfed animals. Sheep are able to eat more LiCl when on a diet high in energy and more of several toxins when on a diet high in energy and protein
(Villalba and Provenza, 2005). Presumably the higher rate of metabolism on a higher level of nutrient intake enables a faster rate of detoxification.
Conversely, dosing with toxins (terpenes, nitrates, tannins or LiCl) has caused sheep to select a diet with a higher protein:energy ratio, while treatment with cyanide causes a decrease in the protein:energy of the diet selected. Thus, there is no common response to different toxins; rather, they vary on a toxin- by-toxin basis depending on physiological state.
It sometimes happens that the plants with the highest yield of digestible nutrients are those containing toxins, and grazing animals must trade nutrients off against toxins. Deer offered pairs of foods with different ratios of phenolic toxin to digestible energy eat high-energy foods when these are low in phenolics, but low-energy foods when the high-energy ones are high in phenolics. Similarly, goats eat more low-digestibility blackbrush twigs when the high-digestibility twigs are high in toxin, and lambs prefer foods lower in readily available carbohydrate when a high-energy food has tannin added to it (Titus et al., 2000). Given PEG, which neutralizes tannin, these lambs moved their preferences to lower-energy foods to a significantly lesser extent after tannin levels were increased than those which did not receive the PEG supplement.
In most studies of conditioned preferences and aversions, access to test foods has been given one at a time, giving plenty of opportunity for animals to learn the association between each US and its attendant CS. In nature, animals are confronted with many different plants at the same time, and Duncan and Young (2002) studied the ability of goats to learn about foods when multiple foods were available simultaneously. Different conifer species were offered on separate days and animals were dosed with LiCl (20 mg/g DM foliage consumed) as a negative stimulus, sodium propionate (90 mg/g DM foliage consumed) as a positive stimulus or sodium chloride (54 mg/g DM foliage consumed) as a neutral stimulus. The goats were able to learn the associations and adjusted their diet selection accordingly (see Fig. 6.4a). However, when a different set of animals was given all three test foods and all three associated US simultaneously during the learning phase of the experiment, the animals took a mixed diet (see Fig.
6.4b), thereby reducing their chances of learning the associations. The authors state that: ‘… caution is required in extrapolating results of artificial conditioning experiments to free-ranging herbivores’.
Lambs given two foods containing different toxins (tannins, terpenes or oxalates) ate more food in total than when given only one of the foods; those offered three foods, one containing each toxin, ate even more as the intake of each individual toxin was lower than when only one of the foods was on offer (Villalba et al., 2004). This improvement is likely to arise only when the different toxins are detoxified by different mechanisms. The experience of eating these foods enhances total intake when such choices are given up to 8 months later, and emphasizes the importance of carrying out research with more than one toxin at a time and of considering the long-term as well as the short-term responses to such choices.
Learning about Food: Conditioned Preferences and Aversions 131
Interactions between ‘working’ and nutritive value
The quality of food frequently differs in different parts of the animal’s environment, and they must choose whether to stay eating a poor food or expend effort in moving to a food of better quality. In order to study this type of trade-off, Ginane et al. (2002) offered heifers a poor hay ad libitum and a limited amount of a better-quality hay on the other side of the test arena. As they depleted the limited quantity of the better food, the animals spent more time eating the poorer one; also, they were prepared to walk less to obtain the better hay when the difference in quality between the two was small, compared with when it was large. Although these heifers tended to behave in a manner likely to maximize their energy intake, their choices were sometimes suboptimal and the authors speculated that the animals desired to diversify their diet, not simply to maximize energy intake.
Fig. 6.4. Influence of post-ingestive stimulus (lithium chloride, shaded bars; sodium chloride, open bars; sodium propionate, solid bars) on intake of associated conifer species in three- way preference tests when individual conifer species were offered; (a) on separate days during conditioning weeks in the temporal separation experiment; (b) simultaneously during conditioning weeks in the simultaneous experiment (from Duncan and Young, 2002).