The physiological consequences of ingesting a toxic plant (Diplotaxis tenuifolia) influence subsequent foraging decisions by sheep (Ovis aries).

Toxins and nutrients interact and define herbivores' experiences with toxic plants. However, there are still open questions about the mechanisms by which nutrient-toxin interactions affect experience and as a consequence foraging decisions by consumers. This study provides a deeper insight into such mechanisms by using supplemental nutrients, a toxic plant typically avoided by herbivores (wild rocket; Diplotaxis tenuifolia), and a small ruminant (sheep; Ovis aries) as models. Thirty-six sheep were randomly assigned to four treatments (n=9) where animals consumed: wild rocket ("DT"), wild rocket followed by a protein supplement ("DT+P"), wild rocket followed by a protein supplement+a mineral supplement containing iodine and copper ("DT+P+M"), or alfalfa pellets in amounts that paired the ingestion of wild rocket by DT ("CTRL"). Towards the end of the phase of exposure (day 35), DT showed the lowest intake of wild rocket, as well as reduced levels of plasma thyroid hormones (T3 and T4), alanine aminotransferase, and a trend towards reduced hemoglobin relative to DT+P and DT+P+M. Total concentration of serum proteins and albumins were greater in sheep fed the protein supplements, which have probably elicited a protective effect on toxin ingestion. Foraging behavior was then evaluated in an experimental arena where animals could select among randomly distributed buckets containing a fixed amount of wild rocket or variable amounts of barley grain (a preferred food). Regardless of barley grain availability, DT showed lower intake and lower times spent eating wild rocket than DT+P and DT+P+M. Unexpectedly, CTRL (without previous experience with wild rocket) ingested amounts of wild rocket comparable to those observed by DT+P and DT+P+M. A negative feeding experience with wild rocket is needed for animals to display the typical pattern of aversion commonly observed in grazing conditions.

How the foraging decisions of a small ruminant are influenced by past feeding experiences with low-quality food.

Feeding experiences with low-quality foods can be improved when these foods are ingested in close temporal association with foods of higher nutritional quality. However, preference for low-quality foods in nature seems to be rather insensitive to past positive experiences and more related to their intrinsic nutritional value. An explanation for this observation is still lacking, mainly because little is known about how herbivores use information about low-quality foods during foraging. Our objective was to provide original information about this issue using a small ruminant (sheep; Ovis aries) as animal model. We manipulated the sheep's experience with a low-quality food (wheat straw) using a conditioning procedure ("oral-delay conditioning procedure"), and then we evaluated the use of this information in a simulated foraging scenario provided with wheat straw and a variable amount of a high-quality food in spatially separated feeding stations. Inclusion of wheat straw into the diet was strongly dependent on the availability of the high-quality food. We observed a threshold level in the availability of the high-quality food, which defined a zone of drastic change in the likelihood of inclusion of the wheat straw into the diet (i.e., acceptance or rejection of wheat straw). This threshold level did not change for sheep with (CS+) or without (CS-) a previous positive experience with wheat straw. However, once foraging conditions stimulated all sheep to start including the wheat straw into the diet (i.e., below the threshold level), the intake of this food was greater by CS+ sheep. This increased intake was not explained by a higher motivation to eat the wheat straw but to a greater amount of time spent foraging this food and less time spent searching for the preferred higher-quality alternative. We discuss these results based on optimal foraging models and learning models of diet selection.

Expression of conditioned preference for low-quality food in sheep is modulated by foraging costs.

Past positive experiences can increase herbivores' motivation to eat low-quality foods. However, this is not always translated into a higher preference for low-quality foods in choice tests among foods of higher nutritional quality. Foraging behavior is also affected by properties of the feeding context because the quality and abundance of foods in nature change in time and space. We hypothesized that in a choice situation, the expression of a past positive experience with a low-quality food is modulated by the costs associated with selecting a high-quality food option. A total of 24 sheep were randomly assigned into two groups (n=12). During conditioning phase, one group (CS+; i.e., conditioned group) was fed with oat hay (a low-quality food) for 20 min and immediately after a ration of soybean meal (a nutritious food), whereas the other group was also fed with oat hay but the offer of soybean meal was delayed 5 h (CS-; i.e., control group). After conditioning, we assessed sheep motivation to eat the oat hay in an experimental arena in which accessibility to alfalfa hay (a high-quality food) was increasingly restricted. When alfalfa hay was readily accessible, CS+ and CS- sheep almost exclusively selected this food, showing a small and similar preference for oat hay. However, when accessibility to alfalfa hay decreased, intake and selection of oat hay was greater in the CS+ sheep than in the CS- sheep. The latter was a consequence of differential changes in behavior between groups; for example, sheep in CS+ spent more time foraging oat hay and were more likely to switch to oat hay if they had previously been eating alfalfa hay than sheep in CS-. Our results show that behavioral expression of the conditioned preference for a low-quality food depends on parameters of the feeding context (e.g., availability). We suggest that this can be the link between learning models and optimal foraging models of diet selection.

Effects of supplementing endophyte-infected tall fescue with sainfoin and polyethylene glycol on the physiology and ingestive behavior of sheep.

Tannins in sainfoin (Onobrychis viciifolia) may bind to alkaloids in endophyte-infected tall fescue [E+; Lolium arundinaceum (Schreb.) Darbysh.] and attenuate toxicosis. If so, supplementing E+ with sainfoin will increase use of E+ by sheep, and polyethylene glycol (PEG)-a polymer that selectively binds to tannins-will reduce such response. To test these predictions, thirty-six 2-mo-old lambs were randomly assigned to 3 treatments (12 lambs/treatment). During exposure, all lambs were individually penned and fed E+ supplemented with beet pulp (CTRL), fresh-cut sainfoin and beet pulp (SAIN), or fresh-cut sainfoin plus PEG mixed in beet pulp (SAIN+PEG). Feed intake was measured daily. Rectal temperatures and jugular blood samples were taken at the beginning and end of exposure. After exposure, all lambs were offered choices between endophyte-free tall fescue (E-) and orchardgrass, and preference for E- was assessed. Then, all lambs were allowed to graze a choice of E+ and sainfoin or a monoculture of E+. The foraging behavior of lambs was recorded. When sainfoin was in mid-vegetative stage, lambs in SAIN ingested more E+ than lambs in CTRL (P = 0.05), but no differences were detected between lambs in SAIN+PEG and CTRL (P = 0.12). Sainfoin supplementation improved some physiological parameters indicative of fescue toxicosis. Lambs in SAIN had lower rectal temperatures (P = 0.02), greater numbers of leukocytes (P < 0.001) and lymphocytes (P = 0.03), and greater plasmatic concentrations of globulin (P = 0.009) and prolactin (P = 0.019) than lambs in CTRL. Some of these differences were offset by the SAIN+PEG treatment. When lambs were offered choices between E- and orchardgrass, only lambs in SAIN had greater intake of E- than lambs in CTRL (P < 0.001). When lambs were allowed to graze a choice of E+ and sainfoin, all treatments used E+ to the same extent (P > 0.05). On the other hand, when they grazed on a monoculture of E+, lambs in SAIN+PEG showed greater acceptance of E+ than lambs in SAIN or in CTRL (P < 0.05). In summary, sainfoin supplementation alleviated several of the classic signs of fescue toxicosis and increased intake of endophyte-infected tall fescue. Tannins in sainfoin partially accounted for this benefit since feeding a polymer that selectively binds to tannins (PEG) attenuated some these responses. However, sainfoin supplementation during initial exposure to E+ did not lead to an increased preference for E+ during grazing.

Induction of low-nutritious food intake by subsequent nutrient supplementation in sheep (Ovis aries).

Acceptance of and preference for a particular food depends not only on its intrinsic (e.g. nutritional) properties but also on expected or recent food experiences. An instance of this type of phenomenon has been called induction effect, which consists of an increased intake of a type of food when it precedes a hedonically preferred food in a sequence familiar to the animal, relative to controls that have access only to the less-preferred food. The purpose of our study was to assess intake induction of a low-nutritious food when followed by different high-nutritious supplements in sheep (Ovis aries). In this experiment, we ran a supplemented phase where animals fed oat hay (a low-nutritious food) in the first part of the daily feeding sessions followed by a supplement with either a high (soya bean meal; group GS) or a low (ground corn; group GC) protein-energy ratio in the second part ate more oat hay than controls that were fed oat hay in both parts of sessions (group GH). In addition, supplemented animals presented a stronger preference for oat hay over alfalfa hay than controls in a subsequent choice. When all animals received no food in the second part of the sessions (Non-supplemented phase), intake of oat hay converged to the control's intake level in all the groups, suggesting that the presence of supplements after access to oat hay was responsible for intake induction. Lastly, we repeated the supplemented phase with a different control group where animals received oat hay in the first part of the sessions and no food in the second part (group NF), thus equalizing groups in terms of the time of access to oat hay in a session. Groups GS and GC still developed higher intake of oat hay than group NF. In both supplemented phases of the experiment, we estimated animals' daily metabolizable energy (ME) and crude protein (CP) intake. CP intake was higher in group GS than in groups GC, GH and NF, but there was no difference between group GC and the controls. In turn, groups did not differ in ME intake in the First supplemented phase, and only group GS presented higher ME intake than the rest of the groups in the Second supplemented phase. Therefore, a nutritional account of the present induction effect seems insufficient. We propose that a learned association between oat hay and the post-ingestive feedback from the subsequent high-nutritious supplements underlay sheep's intake induction and increased preference for oat hay.

Early experience with diverse foods increases intake of nonfamiliar flavors and feeds in sheep.

This study determined whether early experiences by sheep with monotonous or diverse diets influence intake of unfamiliar flavors and feeds later in life. Thirty 2-mo-old lambs were randomly assigned to 3 treatment diets (n = 10): diverse (DIV), diverse with plant toxins (DIV+T), and monotonous (MON). Lambs in DIV received in 9 successive periods of exposure 4-way choice combinations of 2 foods high in energy and 2 foods high in protein from an array of 6 foods: 3 high in energy [beet pulp, oat grain, and a mix of milo:grape pomace (60:40)] and 3 high in digestible protein (DP) (soybean meal, alfalfa, corn gluten meal). Lambs in DIV+T received the same exposure as DIV, but 2 plant toxins, oxalic acid (1.5%) and quebracho tannins (10%), were randomly added to 2 of the feeds in each of the choice combinations. Lambs in MON received a monotonous balanced diet, made with a mixture of all 6 feeds detailed before. All treatments received their feed in 4 separate buckets. During exposure, treatments did not differ in total daily DMI (P = 0.31), but daily intake of ME was less (P < 0.02) and daily intake of DP was greater (P < 0.03) for lambs in DIV and DIV+T than for lambs in MON. Treatments did not differ in ADG or G:F (P > 0.05). After exposure, lambs were offered a familiar feed (wheat bran) containing novel flavors (maple, garlic, or bitter) and 2-way choices of novel feeds (fescue hay vs. corn distillers grains, rice vs. calf manna, and green peas vs. rolled oats). Intake of maple-flavored wheat bran tended (P = 0.08) to be greater for lambs in DIV than for lambs in DIV+T and MON. Intake of bitter-flavored and garlic-flavored wheat bran were greater (P = 0.03 and P = 0.04, respectively) for lambs in DIV and DIV+T than for lambs in MON. During 2-way choice trials, lambs in DIV, but not in DIV+T, showed greater intakes of fescue hay (P = 0.05) and rice (P = 0.04) than lambs in MON. Intake of green peas was greater (P = 0.03) for lambs in DIV and DIV+T than for lambs in MON. At the end of testing, lambs in DIV but not in DIV+T showed greater ADG than lambs in MON (P = 0.05). Thus, early exposure to diverse foods enhanced acceptance of novel flavors relative to early exposure to a monotonous ration. Early experience with diverse feeds plus plant toxins led to a less diverse diet than early experience with diverse feeds. Early exposure to diverse feeds may be beneficial in production systems that require rapid acceptance and high intake of unfamiliar feeds.

Devaluation of low-quality food during early experience by sheep.

A ruminant's early experience with low-quality food (LQF) is expected to increase its acceptance and preference in adulthood. Contrarily, we found that experienced sheep (ES) exposed to mature oat hay early in life ate less of this LQF than inexperienced sheep (IS). A possibility is that ES might have devaluated the LQF through continuous comparisons against high-quality food (HQF) supplements (sunflower meal and ground corn) that were simultaneously available during early experience. In this study, we tested the devaluation hypothesis with a successive negative contrast (SNC) procedure. In a consummatory SNC procedure, 'shift' subjects are unexpectedly changed from HQF to LQF, and their consumption is then compared against the consumption of 'unshift' subjects that receive LQF all throughout the SNC procedure. The magnitude of the difference in consumption between preshift and postshift is regarded as a measure of the degree to which both foods (HQF and LQF) are perceived to differ hedonically. When sheep from our previous study were 300 days old, both ES and IS were randomly assigned to either shift (ES-S and IS-S) or unshift conditions (ES-U and IS-U; n = 6 in each group). Groups ES-S and IS-S were fed HQF (alfalfa hay) during the preshift phase, and then suddenly changed to LQF (oat hay) in the postshift phase. Groups ES-U and IS-U (controls) were fed only LQF throughout the SNC procedure. Subjects in ES-S showed a significantly lower intake of LQF than those in ES-U in the first postshift session (i.e. they showed an SNC effect), which was not observed in IS. These results agree with ES subjects having devalued LQF during early experience. We discuss the possibility that high levels of nutrient supplementation can result in devaluation of LQF (i.e. decrease in preference and acceptance), whereas restricted levels of supplementation may promote a positive experience with LQF.

Role of early experience in the development of preference for low-quality food in sheep.

Domestic ruminant selectivity induces floristic changes in pasturelands, risking sustainability and limiting the subsequent availability of susceptible plant species. Development of preferences for species of lower nutritional quality may help to overcome those problems. In this study, we tested the hypothesis that early experience of sheep with a low-quality food (LQF) in a nutritional enriched context increases preference for LQF in adulthood. We predicted a higher proportional consumption of LQF in experienced lambs (EL) than in inexperienced lambs (IL) in choice situations involving LQF and alternative foods. Additionally, we determined intake of LQF by EL and IL at different levels of high-quality food (HQF) availability. From 60 to 210 days of age, EL were fed in separated feed bunks mature oat hay (LQF) simultaneously with sunflower meal (SM) and corn grain (CG), whereas IL were fed alfalfa hay (HQF) simultaneously with SM and CG. After exposure, EL and IL were offered LQF in free choice situations involving alternative foods, and also at five levels of HQF availability (100%, 75%, 50%, 25% and 0% of ad libitum intake). Proportional consumption of LQF was lower or similar in EL than IL. Intake of LQF was also lower or similar in EL than IL at all levels of HQF availability, except when the LQF was the only food available. Our results did not support the hypothesis that early experience with a LQF in a nutritional enriched context increases preference for LQF in adulthood. On the contrary, experience with LQF diminished subsequent preference for LQF in adulthood. It is proposed that, in the conditions of our study, continuous comparison between the LQF and the high-quality supplements (CG and SM) during the early exposure period lead to devaluation of LQF by EL through a simultaneous negative contrast effect.