Sheep use preingestive cues as indicators of postingestive consequences to improve food learning12

Abstract

Previous work has shown that herbivores successfully learn to associate food sensory characteristics with postingestive consequences when the conditioning procedure is simple, whereas this ability breaks down when the learning task is made more complex. We hypothesized that sensory characteristics could act as indicators of postingestive consequences and that the presence of preingestive cues would improve the food learning of sheep in situations varying in complexity. Sixteen sheep were subjected to a first conditioning phase to associate 2 flavors added to alfalfa hay with either a positive or a negative consequence, induced by intraruminal administration of starch (330 mg/g of DMI) or LiCl (5 mg/g of DMI). Sheep progressively decreased their choice of the flavored hay associated with the negative consequence (P < 0.05). This procedure provided sheep with experience with postingestive consequences associated with the different flavors. In a second conditioning phase, the experienced sheep and 16 naïve sheep were divided into groups of 8 and subjected to either a simple or a complex conditioning procedure [i.e., the 2 flavors were offered on separate days (simple conditioning) or simultaneously within a day (complex conditioning)]. The 2 flavors applied to grass hay were associated with either positive (starch, 330 mg/g of DMI) or negative (LiCl, 10 mg/g of DMI) consequences. As hypothesized, sheep in the simple conditioning group expressed a greater aversion to the flavored hay associated with the negative consequence than did those in the complex conditioning group (0.303 +/- 0.035 vs. 0.474 +/- 0.035 respectively; P < 0.01). Experienced sheep rejected the flavor associated with the negative consequence more strongly than did naïve sheep, regardless of the conditioning procedure (0.304 +/- 0.029 vs. 0.470 +/- 0.041 respectively; P < 0.05). The initial increased preference for aniseed (0.80 +/- 0.04), however, greatly influenced food learning because sheep negatively conditioned on this flavor expressed less avoidance than those negatively conditioned on orange (0.53 +/- 0.04 vs. 0.25 +/- 0.03 respectively; P < 0.01). In conclusion, the simultaneous scenario was actually perceived as complex by all sheep, and experienced sheep were more efficient in food learning than naïve sheep in both the simple and complex learning contexts. The sheep were thus able to generalize the association between sensory cues and postingestive consequences, especially in a complex environment, and then to use these sensory cues as indicators of postingestive consequences.

Food sensory characteristics: their unconsidered roles in the feeding behaviour of domestic ruminants

“…Does the palatability of food sensory characteristics affect food learning? As mentioned above, sheep showed a higher initial preference for aniseed-flavoured orchard grass hay compared with orange-flavoured orchard grass hay (Favreau et al, 2010b). After conditioning, the preference for the flavoured hay associated with the negative post-ingestive consequence was still influenced by these initial preferences, that is, sheep negatively conditioned on aniseed expressed a lesser avoidance than sheep negatively conditioned on orange (0.53 6 0.04 v. 0.25 6 0.03, respectively; Favreau et al, 2010b).…”

“…to ensure similar post-ingestive consequences) and compared in shortterm choice tests with the same unflavoured food, animals often express clear preferences. This was the case for sheep preferring an aniseed-flavoured orchard grass hay, at a rate of 80%, compared with an orange-flavoured orchard grass hay (Favreau et al, 2010b), suggesting that the aniseed flavour has a higher hedonic value than the orange flavour in sheep. However, this result is inconsistent with those of other studies in which sheep did not express any preference between the two flavours (Kyriazakis et al, 1997;Arsenos et al, 2000).…”

“…As it is difficult to differentiate between animals' appreciation of smell (from volatile components of the food) and taste (from soluble components) because they both mix and form a flavour once the food enters the mouth (Forbes and Mayes, 2002), smell is often considered to supplement the sense of taste. Natural or artificial flavours are frequently used in conditioning experiments by adding them to a common food so as to create distinct foods from the animals' sensory perception (Provenza et al, 1996;Favreau et al, 2010b). Many experiments have thus shown that sheep discriminate between different artificial flavours, such as between orange and aniseed (Kyriazakis et al, 1997), onion and coconut (Villalba et al, 1999) or between onion flavour at different concentrations .…”

“…a calorie-free sweetener such as saccharin; Hellekant et al, 1994), (iii) by offering the different food items simultaneously since it increases the difficulty for the animal to identify which food item is responsible for which consequence (Duncan and Young, 2002;Favreau et al, 2010b), and/or (iv) by checking, with a conditioning procedure, that the intake of the added sensory modifier does not cause any post-ingestive consequence at the dose rate involved in the study (Gherardi and Black, 1991;Favreau et al, 2010a).…”

A Pharm-Ecological Perspective of Terrestrial and Aquatic Plant-Herbivore Interactions

“…Olfactory chemoreception is the most ancient sensory cue in animals and may be used for pre-ingestive avoidance of chemicals, whereas taste may be used for postingestive limitation of food intake. Although these concepts have been verified using ecologically realistic combinations of flavors and toxins (Lawler et al, 1999), there has been some doubt cast on how well animals can generalize preferences when the foraging choices become more complex both temporally and spatially in natural systems (Duncan et al, 2007;Favreau et al, 2010;Ginane et al, 2005). However, animals can discriminate mixtures of chemicals to remember and track these olfactory cues through space and time (Derby and Sorensen, 2008).…”