Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T23:00:22.378Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  06 December 2012

A. Favreau-Peigné ,
R. Baumont  and
C. Ginane
A. Favreau-Peigné*
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France VetAgroSup, F-63370 Lempdes, France INRA, UMR791 Modélisation Systémique Appliquée aux Ruminants, F-75005 Paris, France AgroParisTech, UMR Modélisation Systémique Appliquée aux Ruminants, F-75005 Paris, France
R. Baumont
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France VetAgroSup, F-63370 Lempdes, France
C. Ginane
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France VetAgroSup, F-63370 Lempdes, France
*
†E-mail: [email protected]
Get access

Abstract

When domestic ruminants are faced with food diversity, they can use pre-ingestive information (i.e. food sensory characteristics perceived by the animal before swallowing the food) and post-ingestive information (i.e. digestive and metabolic consequences, experienced by the animal after swallowing the food) to evaluate the food and make decisions to select a suitable diet. The concept of palatability is essential to understand how pre- and post-ingestive information are interrelated. It refers to the hedonic value of the food without any immediate effect of post-ingestive consequences and environmental factors, but with the influence of individual characteristics, such as animal's genetic background, internal state and previous experiences. In the literature, the post-ingestive consequences are commonly considered as the main force that influences feeding behaviour whereas food sensory characteristics are only used as discriminatory agents. This discriminatory role is indeed important for animals to be aware of their feeding environment, and ruminants are able to use their different senses either singly or in combination to discriminate between different foods. However, numerous studies on ruminants’ feeding behaviour demonstrate that the role of food sensory characteristics has been underestimated or simplified; they could play at least two other roles. First, some sensory characteristics also possess a hedonic value which influences ruminants’ intake, preferences and food learning independently of any immediate post-ingestive consequences. Further, diversity of food sensory characteristics has a hedonic value, as animals prefer an absence of monotony in food sensory characteristics at similar post-ingestive consequences. Second, some of these food sensory characteristics become an indicator of post-ingestive consequences after their initial hedonic value has acquired a positive or a negative value via previous individual food learning or evolutionary processes. These food sensory characteristics thus represent cues that could help ruminants to anticipate the post-ingestive consequences of a food and to improve their learning efficiency, especially in complex environments. This review then suggests that food sensory characteristics could be of importance to provide pleasure to animals, to increase palatability of a food and to help them learn in complex feeding situations which could improve animal welfare and productivity.

Keywords

hedonic valueherbivorefood learningpalatabilitysensory cues
Type
Behaviour, welfare and health
Information
animal , Volume 7 , Issue 5 , May 2013 , pp. 806 - 813
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnold, GW 1966a. The special senses in grazing animals. I – Sight and dietary habits in sheep. Australian Journal of Agricultural Research 17, 523–529.Google Scholar
Arnold, GW 1966b. The special senses in grazing animals. II – Smell, taste, and touch and dietary habits in sheep. Australian Journal of Agricultural Research 17, 531–542.CrossRefGoogle Scholar
Arnold, GW, De Boer, ES, Boundy, CAP 1980. The influence of odour and taste on the food preferences and food intake of sheep. Australian Journal of Agricultural Research 31, 571–587.Google Scholar
Aronsson, M, Gamberale-Stille, G 2008. Domestic chicks primarily attend to colour, not pattern, when learning an aposematic coloration. Animal Behaviour 75, 417–423.Google Scholar
Arsenos, G, Hills, J, Kyriazakis, I 2000. Conditioned feeding responses of sheep towards flavoured foods associated with casein administration: the role of long delay learning. Animal Science 70, 157–169.Google Scholar
Bach, A, Villalba, JJ, Ipharraguerre, IR 2012. Interactions between mild nutrient imbalance and taste preferences in young ruminants. Journal of Animal Science 90, 1015–1025.CrossRefGoogle ScholarPubMed
Baumont, R 1996. Palatability and feeding behaviour in ruminants. A review. Annales de Zootechnie 45, 385–400.CrossRefGoogle Scholar
Baumont, R, Malbert, CH, Ruckebusch, Y 1990a. Mechanical stimulation of rumen fill and alimentary behaviour in sheep. Animal Production 50, 123–128.Google Scholar
Baumont, R, Seguier, N, Dulphy, JP 1990b. Rumen fill, forage palatability and alimentary behaviour in sheep. Journal of Agricultural Science 115, 277–284.Google Scholar
Bazely, DR 1990. Rules and cues used by sheep foraging in monocultures. In Behavioural mechanisms of food selection (ed. RN Hugues), pp. 343–367. Springer-Verlag, Berlin Heidelberg.Google Scholar
Bazely, DR, Ensor, CV 1989. Discrimination learning in sheep with cues varying in brightness and hue. Applied Animal Behaviour Science 23, 293–299.Google Scholar
Berridge, KC 1996. Food reward: brain substrates of wanting and liking. Neuroscience & Biobehavioral Reviews 20, 1–25.Google Scholar
Berridge, KC, Kringelbach, M 2008. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199, 457–480.Google Scholar
Birch, LL 1999. Development of food preferences. Annual Review of Nutrition 19, 41–62.Google Scholar
Brondel, L, Cabanac, M 2007. Alliesthesia in visual and auditory sensations from environmental signals. Physiology & Behavior 91, 196–201.CrossRefGoogle ScholarPubMed
Burritt, EA, Provenza, FD 1989. Food aversion learning: ability of lambs to distinguish safe from harmful foods. Journal of Animal Science 67, 1732–1739.Google Scholar
Burritt, EA, Provenza, FD 1992. Lambs form preferences for nonnutritive flavors paired with glucose. Journal of Animal Science 70, 1133–1136.Google Scholar
Cabanac, M 1979. Sensory pleasure. The quarterly review of biology 54, 1–29.Google Scholar
Cahn, MG, Harper, JL 1976. The biology of the leaf mark polymorphism in Trifolium repens L. Heredity 37, 327–333.Google Scholar
Cheeke, PR, Dierenfeld, ES 2010. Comparative animal nutrition and metabolism. CABI, Cambridge, UK.Google Scholar
Colucci, PE, Grovum, WL 1993. Factors affecting the voluntary intake of food by sheep. 6. The effect of monosodium glutamate on the palatability of straw diets by sham-fed and normal animals. British Journal of Nutrition 69, 37–47.CrossRefGoogle ScholarPubMed
du Toit, JT, Provenza, FD, Nastis, A 1991. Conditioned taste aversions: how sick must a ruminant get before it learns about toxicity in foods? Applied Animal Behaviour Science 30, 35–46.Google Scholar
Dumont, B 1997. Diet preferences of herbivores at pasture. Annales de Zootechnie 46, 105–116.CrossRefGoogle Scholar
Dumont, B, Dutronc, A, Petit, M 1998. How readily will sheep walk for a preferred forage? Journal of Animal Science 76, 965–971.CrossRefGoogle ScholarPubMed
Duncan, AJ, Young, SA 2002. Can goats learn about foods through conditioned food aversions and preferences when multiple food options are simultaneously available? Journal of Animal Science 80, 2091–2098.Google Scholar
Duncan, AJ, Elwert, C, Villalba, JJ, Yearsley, J, Pouloupoulou, I, Gordon, IJ 2007. How does pattern of feeding and rate of nutrient delivery influence conditioned food preferences? Oecologia 153, 617–624.Google Scholar
Edwards, GR, Newman, JA, Parsons, AJ, Krebs, JR 1997. Use of cues by grazing animals to locate food patches: an example with sheep. Applied Animal Behaviour Science 51, 59–68.Google Scholar
Favreau, A, Baumont, R, Ferreira, G, Dumont, B, Ginane, C 2010a. Do sheep use umami and bitter tastes as cues of post-ingestive consequences when selecting their diet? Applied Animal Behaviour Science 125, 115–123.Google Scholar
Favreau, A, Baumont, R, Duncan, AJ, Ginane, C 2010b. Sheep use preingestive cues as indicators of postingestive consequences to improve food learning. Journal of Animal Science 88, 1535–1544.CrossRefGoogle ScholarPubMed
Favreau, A, Ginane, C, Baumont, R 2010c. Feeding behaviour of sheep fed lucerne v. grass hays with controlled post-ingestive consequences. Animal 4, 1368–1377.Google Scholar
Forbes, JM 2010. Palatability: principles, methodology and practice for farm animals. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 5, 1–15.CrossRefGoogle Scholar
Forbes, JM, Provenza, FD 2000. Integration of learning and metabolic signals into a theory of dietary choice and food intake. In Ruminant physiology: digestion, metabolism, growth and reproduction (ed. PB Cronje), pp. 3–19. CAB International, Wallingford.Google Scholar
Forbes, JM, Mayes, RW 2002. Food choice. In Sheep nutrition (ed. M Freer and H Dove), pp. 51–69. CAB international, Wallingford.Google Scholar
Garcia, J 1989. Food for Tolman: coginition and cathexis in concert. In Aversion, avoidance, and anxiety: perspectives on aversively motivated behavior (ed. T Archer and LG Nilsson), pp. 45–85. Lawrence Erlbaum Associates, Hillsdale, NJ, USA.Google Scholar
Garcia, J, Hankins, WG 1975. The evolution of bitter and the acquisition of toxiphobia. In Olfaction and taste: 5th International Symposium (ed. D Denton and J Coghlan), pp. 39–45. Academic Press, New York.Google Scholar
Gherardi, SG, Black, JL 1991. Effect of palatability on voluntary feed intake by sheep. I – Identification of chemicals that alter the palatability of a forage. Austrian Journal of Agricultural Research 42, 571–584.CrossRefGoogle Scholar
Ginane, C, Dumont, B 2006. Generalization of conditioned food aversions in grazing sheep and its implication for food categorization. Behavioral Processes 73, 178–186.Google Scholar
Ginane, C, Baumont, R, Favreau-Peigné, A 2011. Perception and hedonic value of basic tastes in domestic ruminants. Physiology & Behavior 104, 666–674.CrossRefGoogle ScholarPubMed
Ginane, C, Baumont, R, Lassalas, J, Petit, M 2002. Feeding behaviour and intake of heifers fed on hays of various quality, offered alone or in a choice situation. Animal Research 51, 177–188.Google Scholar
Ginane, C, Duncan, AJ, Young, SA, Elston, DA, Gordon, IJ 2005. Herbivore diet selection in response to simulated variation in nutrient rewards and plant secondary compounds. Animal Behaviour 69, 541–550.Google Scholar
Glendinning, JI 1994. Is the bitter taste rejection always adaptive? Physiology & Behavior 56, 1217–1227.CrossRefGoogle ScholarPubMed
Goatcher, WD, Church, DC 1970a. Taste responses in ruminants. III. Reactions of pygmy goats, normal goats, sheep and cattle to sucrose and sodium chloride. Journal of Animal Science 31, 364–372.Google Scholar
Goatcher, WD, Church, DC 1970b. Taste responses in ruminants. IV. Reactions of pygmy goats, normal goats, sheep and cattle to acetic acid and quinine hydrochloride. Journal of Animal Science 31, 373–382.Google Scholar
Goatcher, WD, Church, DC 1970c. Review of some nutritional aspects of the sense of taste. Journal of Animal Science 31, 973–981.Google Scholar
Greenhalgh, JFD, Reid, GW 1971. Relative palatability to sheep of straw, hay and dried grass. British Journal of Nutrition 26, 107–116.Google Scholar
Grovum, WL, Chapman, HW 1988. Factors affecting the voluntary intake of food by sheep. 4. The effect of additives representing the primary tastes on sham intakes by oesophageal-fistulated sheep. British Journal of Nutrition 59, 63–72.Google Scholar
Hellekant, G, Hård Af Segerstad, C, Roberts, TW 1994. Sweet taste in the calf: III. Behavioral responses to sweeteners. Physiology & Behavior 56, 555–562.Google Scholar
Howery, LD, Bailey, DW, Ruyle, GB, Renken, WJ 2000. Cattle use visual cues to track food locations. Applied Animal Behaviour Science 67, 1–14.Google Scholar
Hutson, GD, Van Mourik, SC 1981. Food preferences of sheep. Australian Journal of Experimental Agriculture and Animal Husbandry 21, 575–582.CrossRefGoogle Scholar
Kendrick, KM, Baldwin, BA 1986. The activity of neurones in the lateral hypothalamus and zona incerta of the sheep responding to the sight or approach of food is modified by learning and satiety and reflects food preference. Brain Research 375, 320–328.Google Scholar
Kissileff, HR 1990. Some suggestions on dealing with palatability – response to Ramirez. Appetite 14, 162–166.Google Scholar
Krueger, WC, Laycock, WA, Price, DA 1974. Relationship of taste, smell, sight, and touch to forage selection. Journal of Range Management 27, 258–262.CrossRefGoogle Scholar
Kühnle, A, Müller, C 2011. Relevance of visual and olfactory cues for host location in the mustard leaf beetle Phaedon cochleariae. Physiological Entomology 36, 68–76.Google Scholar
Kyriazakis, I, Papachristou, TG, Duncan, AJ, Gordon, IJ 1997. Mild conditioned food aversions developed by sheep towards flavors associated with plant secondary compounds. Journal of Chemical Ecology 23, 727–746.Google Scholar
Launchbaugh, KL, Provenza, FD 1994. The effect of flavor concentration and toxin dose on the formation and generalization of flavor aversions in lambs. Journal of Animal Science 72, 10–13.Google Scholar
Launchbaugh, KL, Provenza, FD, Werkmeister, MJ 1997. Overcoming food neophobia in domestic ruminants through addition of a familiar flavor and repeated exposure to novel foods. Applied Animal Behaviour Science 54, 327–334.Google Scholar
Lindemann, B 2001. Receptors and transduction in taste. Nature 413, 219–225.Google Scholar
Miller-Cushon, EK, DeVries, TJ 2010. Effect of early feed type exposure on diet-selection behavior of dairy calves. Journal of Dairy Science 94, 342–350.Google Scholar
Naim, M, Ohara, I, Kare, MR, Levinson, M 1991. Interaction of MSG taste with nutrition – perspectives in consummatory behavior and digestion. Physiology & Behavior 49, 1019–1024.Google Scholar
Newman, JA, Parsons, AJ, Harvey, A 1992. Not all sheep prefer clover: diet selection revisited. Journal of Agricultural Science 119, 275–283.Google Scholar
Parsons, AJ, Newman, JA, Penning, PD, Harvey, A, Orr, RJ 1994. Diet preference of sheep: effects of recent diet, physiological state and species abundance. Journal of Animal Ecology 63, 465–478.Google Scholar
Provenza, FD 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. Journal of Range Management 48, 2–17.Google Scholar
Provenza, FD, Kimball, BA, Villalba, JJ 2000. Roles of odor, taste, and toxicity in the food preferences of lambs: implications for mimicry in plants. Oikos 88, 424–432.Google Scholar
Provenza, FD, Scott, CB, Phy, TS, Lynch, JJ 1996. Preference of sheep for foods varying in flavors and nutrients. Journal of Animal Science 74, 2355–2361.Google Scholar
Provenza, FD, Villalba, JJ, Dziba, LE, Atwood, SB, Banner, RE 2003. Linking herbivore experience, varied diets, and plant biochemical diversity. Small Ruminant Research 49, 257–274.Google Scholar
Ralphs, MH, Provenza, FD 1999. Conditioned food aversions: principles and practices, with special reference to social facilitation. Proceedings of the Nutrition Society 58, 813–820.Google Scholar
Robertson, E, Gordon, IJ, Pérez-Barbería, FJ 2006. Preferences of sheep and goats for straw pellets treated with different food-flavouring agents. Small Ruminant Research 63, 50–55.Google Scholar
Rogers, PJ 1990. Why a palatability construct is needed. Appetite 14, 167–170.Google Scholar
Rogosic, J, Estell, RE, Ivankovic, S, Kezic, J, Razov, J 2008. Potential mechanisms to increase shrub intake and performance of small ruminants in mediterranean shrubby ecosystems. Small Ruminant Research 74, 1–15.Google Scholar
Rolls, BJ 1986. Sensory-specific satiety. Nutrition Reviews 44, 93–101.Google Scholar
Rosa, Gd, Moio, L, Napolitano, F, Grasso, F, Gubitosi, L, Bordi, A 2002. Influence of flavor on goat feeding preferences. Journal of Chemical Ecology 28, 269–281.Google Scholar
Schütz, K, Davison, D, Matthews, L 2006. Do different levels of moderate feed deprivation in dairy cows affect feeding motivation? Applied Animal Behaviour Science 101, 253–263.Google Scholar
Scott, LL, Provenza, FD 1998. Variety of foods and flavors affects selection of foraging location by sheep. Applied Animal Behaviour Science 61, 113–122.Google Scholar
Simitzis, PE, Bizelis, JA, Deligeorgis, SG, Feggeros, K 2008. Effect of early dietary experiences on the development of feeding preferences in semi-intensive sheep farming systems – a brief note. Applied Animal Behaviour Science 111, 391–395.Google Scholar
Skelhorn, J, Griksaitis, D, Rowe, C 2008. Colour biases are more than a question of taste. Animal Behaviour 75, 827–835.Google Scholar
Spörndly, E, Åsberg, T 2006. Eating rate and preference of different concentrate components for cattle. Journal of Dairy Science 89, 2188–2199.Google Scholar
Swithers, SE, Davidson, TL 2008. A Role for sweet taste: calorie predictive relations in energy regulation by rats. Behavioral Neuroscience 122, 161–173.Google Scholar
Tamashiro, KLK, Hegeman, MA, Nguyen, MMN, Melhorn, SJ, Ma, LY, Woods, SC, Sakai, RR 2007. Dynamic body weight and body composition changes in response to subordination stress. Physiology & Behavior 91, 440–448.Google Scholar
Vallentine, JF 2001. Grazing management. Academic Press, San Diego, USA.Google Scholar
Van Tien, D, Lynch, JJ, Hinch, GN, Nolan, JV 1999. Grass odor and flavor overcome feed neophobia in sheep. Small Ruminant Research 32, 223–229.Google Scholar
Verbeek, E, Waas, JR, McLeay, L, Matthews, LR 2011. Measurement of feeding motivation in sheep and the effects of food restriction. Applied Animal Behaviour Science 132, 121–130.Google Scholar
Villalba, JJ, Provenza, FD 1997. Preference for wheat straw by lambs conditioned with intraruminal infusions of starch. British Journal of Nutrition 77, 287–297.Google Scholar
Villalba, JJ, Provenza, FD 2000. Roles of flavor and reward intensities in acquisition and generalization of food preferences: do strong plant signals always deter herbivory? Journal of Chemical Ecology 26, 1911–1922.Google Scholar
Villalba, JJ, Provenza, FD, Rogosic, J 1999. Preference for flavored wheat straw by lambs conditioned with intraruminal infusions of starch administered at different times after straw ingestion. Journal of Animal Science 77, 3185–3190.Google Scholar
Villalba, JJ, Bach, A, Ipharraguerre, IR 2011. Feeding behaviour and performance of lambs are influenced by flavor diversity. Journal of Animal Science 89, 2571–2581.Google Scholar
Villalba, JJ, Catanese, F, Provenza, FD, Distel, RA 2012. Relationships between early experience to dietary diversity, acceptance of novel flavors, and open field behavior in sheep. Physiology & Behavior 105, 181–187.Google Scholar
Waldern, DE, van Dyk, RD 1971. Effect of monosodium glutamate in starter rations on feed consumption and performance of early weaned calves. Journal of Dairy Science 54, 262–265.Google Scholar
Yeomans, MR, Lee, MD, Gray, RW, French, SJ 2001. Effects of test-meal palatability on compensatory eating following disguised fat and carbohydrate preloads. International Journal of Obesity 25, 1215–1224.Google Scholar
Zahorik, DM, Houpt, KA, Swartzman-Andert, J 1990. Taste-aversion learning in three species of ruminants. Applied Animal Behaviour Science 26, 27–39.Google Scholar