Abstract
The ability of grazing herbivores to assign food types to categories by relying on certain relevant criteria could considerably reduce cognitive demand and increase their foraging efficiency when selecting among many different plant items. Grasses and legumes differ functionally in vegetation communities as well as in nutritive value. We aimed to determine whether sheep can generalize an aversion they learnt for a grass or a legume species to another species of the same functional type and consequently whether botanical family is a potential level of categorization. Over four successive weeks, 12 lambs were conditioned against either a freshly cut grass (tall fescue—Festuca arundinacea, N = 6) or legume species (sainfoin—Onobrychis viciifolia, N = 6) using a negative post-ingestive stimulus (lithium chloride) on day 1. Preference of all lambs between another grass (cocksfoot—Dactylis glomerata) and another legume (alfalfa—Medicago sativa) was assessed on day 3 by measuring their relative consumptions. Preference for alfalfa progressively became lower for lambs that were conditioned against sainfoin than against tall fescue, indicating that lambs generalized the aversion between species along some perceptual gradient and classed the considered grasses and legumes in distinct categories. Beyond this original result, the question now is to identify which specific plant characteristics or functional traits the animals rely on in order to form categories.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Balogh ACV, Gamberale-Stille G, Tullberg BS, Leimar O (2010) Feature theory and the two-step hypothesis of Müllerian mimicry evolution. Evolution 64:810–822
Bazely DR (1990) Rules and cues used by sheep foraging in monocultures. In: Hughes RN (ed) Behavioural mechanisms of food selection. Springer-Verlag, Berlin, pp 343–367
Bouissou MF, Porter RH, Boyle L, Ferreira G (1996) Influence of a conspecific image of own vs. different breed on fear reactions of ewes. Behav Process 38:37–44
Bovet D, Vauclair J (1998) Functional categorization of objects and of their pictures in baboons (Papio anubis). Learn Motiv 29:309–322
Coulon M, Deputte BL, Heyman Y, Delatouche L, Richard C, Baudoin C (2007) Visual discrimination by heifers (Bos taurus) of their own species. J Comp Psychol 121:198–204
Coulon M, Deputte BL, Heyman Y, Baudoin C (2009) Individual recognition in domestic cattle (Bos taurus): evidence from 2D-images of heads from different breeds. Plos One 4:e4441
Diaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655
Dukas R, Waser NM (1994) Categorization of food types enhances foraging performance of bumblebees. Anim Behav 48:1001–1006
Edwards GR, Newman JA, Parsons AJ, Krebs JR (1997) Use of cues by grazing animals to locate food patches: an example with sheep. Appl Anim Behav Sci 51:59–68
Favreau A, Baumont R, Duncan AJ, Ginane C (2010a) Sheep use pre-ingestive cues as indicators of post-ingestive consequences to improve food learning. J Anim Sci 88:1535–1544
Favreau A, Baumont R, Ferreira G, Dumont B, Ginane C (2010b) Do sheep use umami and bitter tastes as cues of post-ingestive consequences when selecting their diet? Appl Anim Behav Sci 125:115–123
Ghirlanda S, Enquist M (2003) A century of generalization. Anim Behav 66:15–36
Ginane C, Dumont B (2006) Generalization of conditioned food aversions in grazing sheep and its implications for food categorization. Behav Process 73:178–186
Ginane C, Dumont B (2010) Do grazing sheep use species-based categorization to select their diet? Behav Process 84:622–624
Hall G (2007) Learned changes in stimulus representations (a personal history). Spanish J Psychol 10:218–229
Hanggi EB, Ingersoll JF (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn 12:451–462
Herrnstein RJ (1990) Levels of stimulus control—a functional approach. Cognition 37:133–166
Honig WK, Urcuioli PJ (1981) The legacy of Guttman and Kalish (1956)—25 years of research on stimulus-generalization. J Exp Anal Behav 36:405–445
Hughes RN, O’Brien N (2001) Shore crabs are able to transfer learned handling skills to novel prey. Anim Behav 61:711–714
Kendrick KM, Atkins K, Hinton MR, Broad KD, Fabrenys C, Keverne B (1995) Facial and vocal discrimination in sheep. Anim Behav 49:1665–1676
Launchbaugh KL, Provenza FD (1994) The effect of flavor concentration and toxin dose on the formation and generalization of flavor aversions in lambs. J Anim Sci 72:10–13
Lazareva OF, Freiburger KL, Wasserman EA (2004) Pigeons concurrently categorize photographs at both basic and superordinate levels. Psychon Bull Rev 11:1111–1117
Littel RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) Random coefficient models. In: SAS® for mixed models, 2nd edn. SAS Institute Inc., Cary, NC, USA, pp 317–341
Merchen NR, Bourquin LD (1994) Processes of digestion and factors influencing digestion and forage-based diets by ruminants. In: Fahey GC (ed) Forage quality. Evaluation and utilization. ASA CSSA SSSA. Madison, WI, USA, pp 564–612
Nicol CJ (1997) Making sense of variation: acquired functional categories and conditional discriminations. Appl Anim Behav Sci 54:59–62
O’Brien EL, Burger AE, Dawson RD (2005) Foraging decision rules and prey species preferences of northwestern crows (Corvus caurinus). Ethology 111:77–87
Penning PD, Newman JA, Parsons AJ, Harvey A, Orr RJ (1997) Diet preferences of adult sheep and goats grazing ryegrass and white clover. Small Rum Res 24:175–184
Pfister JA, Stegelmeier BL, Cheney CD, Gardner DL (2007) Effect of previous locoweed (Astragalus and Oxytropis species) intoxication on conditioned taste aversions in horses and sheep. J Anim Sci 85:1836–1841
Porter RH, Bouissou MF (1999) Discriminative responsiveness by lambs to visual images of conspecifics. Behav Process 48:101–110
Provenza FD (1995) Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J Range Manage 48:2–17
Rosch E (1978) Principles of categorization. In: Rosch E, Lloyd BB (eds) Cognition and categorization. Lawrence Erlbaum Associates, Hillsdale, New Jersey, pp 27–48
Rutter SM (2006) Diet preference for grass and legumes in free-ranging domestic sheep and cattle: current theory and future application. Appl Anim Behav Sci 97:17–35
Rutter SM, Orr RJ, Yarrow NH, Champion RA (2004) Dietary preference of dairy cows grazing ryegrass and white clover. J Dairy Sci 87:1317–1324
Sloutsky VM (2003) The role of similarity in the development of categorization. Trends Cogn Sci 7:246–251
Spehn EM, Scherer-Lorenzen M, Schmid B, Hector A, Caldeira MC, Dimitrakopoulos PG, Finn JA, Jumpponen A, O’Donnovan G, Pereira JS, Schulze ED, Troumbis AY, Körner C (2002) The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 98:205–218
Tanaka M (2001) Discrimination and categorization of photographs of natural objects by chimpanzees (Pan troglodytes). Anim Cogn 4:201–211
Tien DV, Lynch JJ, Hinch GN, Nolan JV (1999) Grass odor and flavor overcome feed neophobia in sheep. Small Rum Res 32:223–229
Urcioli PJ (2001) Categorization & acquired equivalence. In: Cook RG (ed) Avian visual cognition. http://www.pigeon.psy.tufts.edu/avc/huber/
Vauclair J, Fagot J (1996) Categorization of alphanumeric characters by baboons (Papio papio): within and between class stimulus discrimination. Current Psychol Cogn 15:449–462
Villalba JJ, Provenza FD (2000a) Roles of novelty, generalization, and postingestive feedback in the recognition of foods by lambs. J Anim Sci 78:3060–3069
Villalba JJ, Provenza FD (2000b) Roles of flavor and reward intensities in acquisition and generalization of food preferences: do strong plant signals always deter herbivory? J Chem Ecol 26:1911–1922
Villalba JJ, Provenza FD, Bryant JP (2002) Consequences of the interaction between nutrients and plant secondary metabolites on herbivore selectivity: benefits or detriments for plants? Oikos 97:282–292
Vonk J, MacDonald SE (2004) Levels of abstraction in orangutan (Pongo abelii) categorization. J Comp Psychol 118:3–13
Zayan R, Vauclair J (1998) Categories as paradigms for comparative cognition. Behav Process 42:87–99
Zentall TR, Wasserman EA, Lazareva OF, Thompson RKR, Rattermann MJ (2008) Concept learning in animals. Comp Cogn Behav Rev 3:13–45
Acknowledgments
We thank all the staff at the INRA-UR1213 experimental farm, particularly Pascal Payard for his technical assistance during tests and for animal care. Thanks also to Laurent Beaudonnat for help with plant species collection and to Aline Le Morvan and Pierre Capitan for analysing the sward samples.
Ethical note
The animals were handled by specialized personnel who applied animal care and welfare in accordance with European Union Directive No. 609/1986 under agreement number B63 345.17. The main ethical issue associated with the work was the conditioning procedure, associating handling with the administration of lithium chloride, which causes nausea and gastrointestinal malaise. Handling may have contributed to the aversiveness of the programme. However, in protocols where animals are positively conditioned, handling does not prevent the preferences from developing (Villalba and Provenza 2000b; Favreau et al. 2010b). Consequently, we can consider that the malaise caused by LiCl was the main aversive factor that changed the value of the plant species during conditionings. In order to minimize the discomfort to the level necessary to get an answer, we applied the following procedure. First, the administration rates were low (70 mg/kg) and far lower than those classically used in ruminant conditionings (100 to 200 mg/kg: Villalba et al. 2002; Pfister et al. 2007). Second, the animals did not receive the full dose if their intake during conditionings was low, and a low intake did not affect their basal diet. After conditionings, the lambs did not show any signs of distress. The most sensitive indicator would have been a decrease in basal diet consumption, and monitoring of intake revealed no such decrease.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ginane, C., Dumont, B. Do sheep (Ovis aries) categorize plant species according to botanical family?. Anim Cogn 14, 369–376 (2011). https://doi.org/10.1007/s10071-010-0371-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-010-0371-4