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Preferences of sheep and goats for straw pellets treated with different food-flavouring agents
Small Ruminant Research 63 (2006) 50–57
Preferences of sheep and goats for straw pellets treated with different food-flavouring agents E. Robertson, I.J. Gordon ∗ , F.J. P´erez-Barber´ıa Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK Received 13 January 2004; received in revised form 4 January 2005; accepted 2 February 2005 Available online 18 March 2005
Abstract In order to assess differences in preferences for flavours between ruminant species, two-choice tests were conducted on sheep (Scottish Blackface, Ovis aries) and goats (feral hybrids, Capra hircus). Feed pellets (nutritionally improved barley straw) were treated with synthetic human food-flavouring agents representing: strawberry (ST), apple (AP), orange (OR), maple (MA), caramel (CA), truffle (TR), garlic (GA) and onion (ON) flavours. Animals were first exposed to each of the flavours and then presented with each, paired with an untreated (control) feed, and the consumption of individual feeds recorded. Preference values (PV) were calculated from the proportion of the total feed consumption derived from the flavour-treated feed. Differences in PV were found between species (P = 0.01) and between flavours (P < 0.005). Although sheep showed stronger preference for flavoured feeds than did goats, both sheep and goats showed a similar pattern of preference across the flavours offered. In general, sheep exhibited significant preference for TR, GA, ON, AP, CA, MA and OR relative to the unflavoured feeds, whereas goats showed significant preference for TR, ON, AP and GA. The findings of this research suggest that it would be of practical use to evaluate feeds flavoured with compounds representing truffle, garlic and onion as intake enhancers in goats and sheep. Only if flavouring agents are successful in enhancing intake could we recommend flavouring as a means of masking undesirable feed flavours, production of a more uniform feed from variable ingredients or in prompting feed consumption. © 2005 Elsevier B.V. All rights reserved. Keywords: Flavours; Truffle; Onion; Garlic; Goats; Sheep
1. Introduction Ruminant animals have been shown to generally select for foods on the basis of their nutrient content ∗ Corresponding author. Present address: Sustainable Ecosystems, CSIRO – Davies Laboratory, PMB PO Aitkenvale, Qld 4814, Australia. Tel.: +61 7 4753 8509; fax: +61 7 4753 8600. E-mail address: [email protected] (I.J. Gordon).
0921-4488/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2005.02.007
(e.g. Kyriazakis and Oldham, 1993; Kyriazakis et al., 1994; Burrit and Provenza, 1992) and to avoid feeds containing plant secondary compounds, e.g. tannins (Provenza and Malechek, 1984). This choice is assumed to be based on the association between sensory components of the food (e.g. taste, smell, touch and sight, Arnold, 1966a,b) and the post-ingestive consequences (e.g. positive and negative gastrointestinal feedback, Kyriazakis et al., 1997). Sheep and goats
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have been shown to consume different diets when grazing in common (e.g. Gurung et al., 1994; Kronberg and Malechek, 1997; del Pozo et al., 1998; Mysterud, 2000), which is thought to be related to differences in the ways in which the two species ingest and digest the vegetation on offer (Gordon and Illius, 1992; Kronberg and Malechek, 1997). Generally, goats appear to be less selective than sheep (Bartolom´e et al., 1998) and include a broader range of species in their diet because they include a greater proportion of browse species (Bullock, 1985; Bartolom´e et al., 1998; Pande et al., 2002). It would, therefore, be expected that sheep and goats would differ in the degree to which they associate the sensory characteristics with the post-ingestive consequences of the foods consumed. Since the sensory cue and the post-ingestive feedback are so closely linked in food choice (Provenza, 1995), it is important to adequately isolate the response due directly to the sensory cue from that due to other factors. The flavour of the food is thought to play an important sensory role in determining the preference for different foods in sheep and goats (Provenza, 1995). In this study, we fed low quality, straw pellets covered with a range of artificial flavours to test whether the innate flavour preferences differ between sheep and goats. Since goats feed on a wider variety of plants than do sheep, when grazing in common, we would predict that goats would exhibit less preference for flavours than do sheep. This would be an evolutionary advantage for the use of diverse diets and novel feeds, and consequently allow the animal greater flexibility in behaviour to adapt to new habitats and changing environmental condition (Perez-Barberia et al., 2001).
2. Materials and methods Whilst many studies of dietary learning have used artificial flavouring agents to associate the postingestive feedbacks with an ingestive sensory property of the food (e.g. Provenza et al., 1996; Kyriazakis et al., 1997; Frutos et al., 1998; Villalba and Provenza, 2000), none have systematically tested for differences in preference between sheep and goats for these flavouring agents. In general, when testing innate preferences for different flavours it is vital that the flavouring agents used have (i) no nutritional content (e.g. contain no
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energy, salt or minerals), (ii) have no (negative) postingestive consequences (e.g. from tannins or other secondary compounds), and (iii) are present in minimal quantities, as any of those factors can confound flavour preference with preference for the nutritional or postingestive consequences of the forage consumed. We investigated the flavour preferences of sheep and goats, under controlled conditions, using minute quantities (0.05 g/kg) of nutritionally inert flavouring agents combined with a relatively low quality feed. We attempted to further isolate the response by the use of minimal fasting, short-term feeding trials and the feeding of a different feed between trials (i.e. hay which would be expected to have a buffering effect). The animals used were all acclimatised to each of the flavours to minimise the effect of residual associations. Villalba and Provenza (1997) found that associations persisted for 8 weeks in lambs, but Nolte and Provenza, (1992a,b) found that associations were not extinguished until 9 months. 2.1. Design The experiment was conducted at the Macaulay Land Use Research Institute’s Glensaugh Animal Research Facility over a period of 10 days. There were two experimental periods (P1 and P2) each of four days, separated by two rest days. Tests were conducted at the same times on each day at 10:00 h (AM trial) and 15:00 h (PM trial). These times of relative inactivity within the animal facility were chosen to limit the disturbance to the animals during the tests. The same eight sheep (S1–S8) and the same eight goats (G1–G8) were used in each period. Four orthogonal 8 × 8 Latin squares (Fisher and Yates, 1957) were used (one per species per period) to allocate animals to treatments (one of the eight flavoured feeds tested against the unflavoured feed). Animals were allocated to column numbers at random and choice tests were assigned to rows. The design was balanced for the effect of the position at which the feeds were presented to the animals by alternating the relative positions of the flavoured and unflavoured feeds in every second test (i.e. right–left relative to the position of the animal in the pen). This also ensured that position effects were not confounded with time of day effects, since the former were alternated in every trial.
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2.2. Animals Eight mature castrate males of each species were used in the experiment. The Scottish Blackface sheep were 3 years old; the goats were 4-year-old feral hybrids. At the start of the experiment, mean live weights and condition scores (CS) were, respectively, 55.8 kg (S.E. ± 1.63) and CS 2.25 for sheep and 50.8 kg (S.E. ± 1.83) and CS 2.22 for goats. All animals had been housed continuously for 2 years prior to the experiment and were trained in the routines of preference tests involving chopped hays and straws but not to flavour tests per se. All animals were fed on the same diet (1.0 kg high quality grass hay per day) prior to the experiment. During the 27 days immediately prior to the experiment, all animals were accustomed to each of the flavoured feeds and the unflavoured feed by offering the feeds for a total of three days each. Between tests and between the threeday-periods animals were fed grass hay (1.0 kg per day) and had constant access to fresh water and mineral and salt licks (Rockies Yellow; Tithebarn Ltd, Southport, Merseyside, England, UK). The animals were housed in adjacent individual pens facing animals of the same species but not involved in the experiment. Pens had slatted wooden floors (area = 2.8 m2 ) with open railed front and back panels but plywoodsheeted sides. Hence, although animals remained in close visual contact with others of their own species, their choices would not have been influenced by their peers. The animal facility was provided with natural light and ventilation; the mean daily temperature during the period of the experiment was 9.9 ◦ C (S.E. ± 0.81). 2.3. Feeds 2.3.1. Preparation The basal feed used in the tests was an 8 mm (diameter) pelleted nutritionally improved straw (NIS) (Barley straw treated with ammonia; Davidson Brothers, Shotts, Lanarkshire, Scotland, UK). This feed was selected as a uniform feed with a potential to improve intake through the addition of flavours which would maximise the expression of preferences. Experimental feeds were prepared on the first day of the 27day pre-experimental period, which was considered to be sufficient time to allow the flavouring agents to be
fully absorbed into the straw pellets prior to the start of the preference tests (P. McDonald; David Moore (Flavours) Ltd. Wrexham, UK, personal communication). During the acclimatization period, daily DM intakes of all feed types (flavoured and unflavoured) were moderate (582 ± 34.5 g for sheep and 264 ± 32.9 g for goats). The flavouring agents used were synthetic watersoluble human food-flavouring complexes (maple (no. 6546; MA), caramel (no. 3708; CA), strawberry (no. 1675; ST), garlic (no. 6306; GA), apple (no. 3067/T; AP), onion (no. 0297; ON), truffle (no. 5410/T; TR) and orange (no.2884/T; OR)), (David Moore (Flavours) Ltd., Wrexham, UK.). MA and CA represent sweet flavours, GA, TR and ON represent savory flavours and ST, AP and OR represent fruity flavours. Flavouring agents were applied in liquid form as this caused no adherence problems and the flavour distributed itself evenly between and throughout pellets and caused no perceptible visual or textural changes in the pellet. The pellets were spread on a clean plastic sheet (1 per flavour) to produce an even layer, one pellet in thickness. Flavour concentrate was diluted (1 part in 20 parts unflourinated tapwater) and the resultant solution was applied evenly at a rate of 1 g per kg feed using a household plant mist sprayer. Flavoured feeds were then stored in lightproof, plastic dustbins with lids. No treatment of the control feed was carried out. Samples of each feed (control and flavoured feeds) were taken on three occasions per period to estimate the DM content and feed intakes were subsequently expressed on a dry matter basis. The samples were also analyzed for crude protein (N), gross energy (GE), fibre (acid detergent fibre (ADF) and neutral detergent fibre (NDF)) and in vitro digestibility. Nitrogen analysis was carried out with a Carlo Erba elemental analyser (Carlo Erba, Milan, Italy) as described by Pella and Colombo (1973). GE determination was by bomb calorimetry (Gallankamp, FIS, Crawley, UK) as described by Blaxter (1962). ADF was determined as described by Van Soest (1963), NDF by Van Soest and Wine (1967) and in vitro digestibility by Tilley and Terry (1963) as modified by Alexander and McGowan (1966). The addition of flavours had no significant effects on the chemical composition, GE or DM of the feeds (Table 1) and the composition of the feeds did not vary significantly between days.
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Table 1 Mean values and their standard errors (S.E.) of laboratory analyses conducted on the flavoured and unflavoured straw pellets (N = 54) Dry matter (%)
Mean S.E.
92.4 0.005
Fibre (%) NDF
ADF
66.77 0.138
50.44 0.065
Organic matter digestibility in vitro (%)
Crude protein (%)
Energy (kJ/(g DM)
54.08 0.096
4.55 0.026
16.71 0.011
2.3.2. Presentation During a test, each animal was simultaneously presented with two immediately adjacent basins, of identical size (35 cm diameter) and colour, supported in a wooden frame to prevent spillage. One of the basins contained 500 g of the control feed and the other 500 g of an allocated flavoured feed. In order to prevent crosscontamination, basins were allocated to a feed type for the duration of the experiment and labelled accordingly. The relative position of the control and flavoured feeds for each animal was alternated every second test to account for any positional effect. Each test lasted 30 min and was preceded by a 60-min fasting period. Thirty minutes after presentation to the animals the basins were removed and re-weighed. Weighing was carried out to the nearest gram. Intakes were calculated from the pre- and post-test feed weights and expressed on a DM basis (DMI). 2.4. Statistical analysis Crude preference values (cPV) were calculated by the procedure used by Bell (1959) and subsequently employed by other authors (e.g. Goatcher and Church, 1970a; Black et al., 1989; Gherhardi and Black, 1991). In this procedure, the consumption of the treated feed is expressed as a proportion of the total feed consumption and produces values ranging from 0 to 1. Instances of non-discrimination or absence of preference would both be expected to yield a value of 0.5. Goatcher and Church (1970a) classed values with a value >0.8 as strong preferences, those between 0.8 and 0.7 as moderate preferences and those between 0.7 and 0.6 as weak preferences. Similarly, a value <0.2 indicated a strong rejection, between 0.2 and 0.3 a moderate rejection and those between 0.3 and 0.4 a weak rejection. Since the impact of a one-gram change in feed intake over the range of possible PV values was not uniform (the greatest impact was at the extremes of preference),
the dataset was transformed into standardized preference values (sPV) using the following equation: sPV = loge
cPV 1 − cPV
According to the latter equation absence of preference for sPV corresponded to a value of 0. In addition to the loss of 2 data values due to feed spillage, 30 values were excluded due to the total consumption being less than the threshold set for a valid experimental unit (0.3 of the mean total DM consumption per species, i.e. 76 g for sheep and 53 g for goats). This led to an unbalanced data set that was consequently analysed by a regression approach using residual maximum likelihood (REML) algorithm in Genstat (Version 5.3, Lawes Agricultural Trust, 1993). We used sPV as the response variable; period, presentation position (right–left), species, flavour and their interactions as the fixed terms, individual body mass as a covariate and flavour within individuals as the random term in the analysis. From this model the estimated means of the sPV and their associated standard error of the differences (S.E.D.) were used to test, if the preference for each flavour differed from the unflavoured feed (zero value of sPV), and also if there were differences in preference between flavours. REML uses the Wald statistic, which has an asymptotic chi-squared distribution with degrees of freedom equal to those of the terms in the regression model (Sokal and Rohlf, 1995). Differences in preference for specific flavours between animals where calculated by a generalized linear model using a normal distribution and identity as the link function (Lawes Agricultural Trust, 1993) by fitting species + flavour + animal + species × flavour + flavour × animal. Body masses and total consumption where used untransformed in all analyses since the examination of the residuals met the criteria of homocedasticity and normality.
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In order to compare results with those in the literature, they were back-transformed using the equation: PV =
esPV 1 + esPV
3. Results Over the resulting 216 experimental tests the mean total (i.e. flavoured + unflavoured feeds) dry matter intake (DMI) over the 30 min test was higher for sheep than goats, though this difference was not significant (216.4 g versus 192.7 g, S.E.D. = 34.76; chisquare = 0.88, d.f. = 1, p = 0.349). A mean PV of 0.732 (sPV = 1.007) indicated a positive overall discrimination for the flavoured feeds (F7,236 = 25.72; P < 0.001) relative to the unflavoured feeds across the two species. The mean PV for sheep 0.820 (sPV = 1.519) was significantly greater (χ2 = 7.43, d.f. = 1, p = 0.006) than that for goats 0.634 (sPV = 0.552), (S.E.D. for transformed data = 0.3615), indicating that, although both species could discriminate between the flavoured and unflavoured feeds, the sheep exhibited stronger preferences for the flavours than did the goats (Fig. 1). No significant species by flavour interaction was found (χ2 = 0.67; d.f. = 7, p = 0.697), indicating that sheep and goats have very similar preferences for
Fig. 1. Mean and standard error standardized preference values (sPV) for flavours for sheep and goats. Maple (MA), caramel (CA), strawberry (ST), garlic (GA), apple (AP), onion (ON), truffle (TR) and orange (OR).
the eight flavours. The preferences for the different flavours were ranking as follows, TR (sPV = 1.696), GA (1.430), ON (1.308), AP (1.143), CA (0.924), MA (0.850), OR (0.561) and ST (0.370). In general, sheep exhibited significant preference for TR, GA, ON, AP, CA, MA and OR relative to the unflavoured feeds, whereas goats showed significant preference for TR, ON, AP and GA. When comparisons were carried out between flavours significant differences were found for ST against GA, AP, ON, TR and also for OR against GA, TR (S.E.D. = 0.381, α = 0.05). Although individual animals varied in the strength of their preference for the flavoured feeds (F14,100 = 4.03; p < 0.001), and there was some individual animal variation within the preferences exhibited for the flavours (0.290–0.471 for sheep and 0.228–0.381 for goats) (Fig. 1), the animal by flavour interaction was not quite significant (animal × flavour: F86,100 = 1.38, p = 0.06, NS).
4. Discussion The only experiments that have assessed the preferences for the flavours used in this experiment are those of Nolte and Provenza (1992a,b), who found onion to be more preferred by lambs than garlic although both were less preferred than the control feed (alfalfa and barley). These results differ from those reported here, both in the relative preferences for GA and ON, and in their preferences relative to the control feed, possibly due to the differences in experimental approach. Nolte and Provenza (1992a,b) used high concentrations (20–250 g per kg at 10 times natural strength) of flavours (powdered plant material), and recognized that this may have resulted in negative post-ingestive effects, especially in the case of garlic. It is also likely that any such effects would be heightened by the relatively long (overnight) fasting period used by Nolte and Provenza (1992a,b). The feed used by Nolte and Provenza (1992a) as a basal feed was a mixture of ground alfalfa and rolled barley. As a high quality feed, this would be acceptable in its untreated form and consequently less amenable to improvements in acceptability than the straw pellets used in this experiment (see also Morand-Fehr, 2003). Also, Nolte and Provenza (1992a) used powered plants whereas the current experiment involved artificial flavours, which
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may not directly replicate the flavours for ruminants and may have other unknowns (e.g. aftertaste) that could affect the preference of sheep and goats for the flavours. No specific trials have been conducted testing differences between sheep and goats for preferences between the flavours used in this experiment, with much of the research on the response of ruminants to sensory cues of taste using an approach based on the four basic taste sensations, as opposed to complex mixtures such as those used in this experiment. For example, Bell (1959) described the taste and preference thresholds for goats and sheep offered chemicals representing the sensations of sweet, sour, salty and bitter presented in drinking water. In that study, goats had a higher threshold for bitter (quinine) tastes, relative to sheep, and for both species sweet (glucose) was preferred to unflavoured tapwater over a range of concentrations. Responses to salt (sodium chloride), sour (acetic acid) and bitter flavours changed very rapidly with changes in concentration. In a separate study, Goatcher and Church (1970b) found that goats showed an increasing preference for water flavoured with sucrose as concentration increased from 2.5% to 20% whilst sheep exhibited no preferences. It might be expected, therefore, that goats would exhibit higher preferences than sheep for MA, CA, ST, OR and AP that represent “sweet” and “fruity” flavours. This was not found in this experiment. Generally, we found that sheep had a greater preference for flavoured feeds than did goats. This supports the hypothesis that goats are less affected by the flavour of the food than are sheep and this facilitates their more diverse dietary response (Bullock, 1985; Bartolom´e et al., 1998; Pande et al., 2002). Our results also demonstrate that, whilst sheep showed a greater preference for flavoured feeds than did the goats, both ruminant species showed a similar preference ranking for the flavours used in the experiment. This similarity in response suggests that both species may be receiving similar sensations from the flavours and that these sensations are innately associated with post-ingestive feedbacks associated with the consumption of a diverse range of forages. Individual animal differences in flavour preferences of the magnitude experienced here are widely reported elsewhere, with both sheep and goats and with
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a variety of flavouring agents (Morand-Fehr, 2003). Goatcher and Church (1970c), although concluding that sheep were indifferent to sweet tastes (equivalent to PV = 0.574), found individual sheep preferences varied from 0.035 to 0.845 PV equivalent. Expression of these individual differences is frequently credited with an evolutionary advantage to a social species foraging in its natural environment (e.g. Goatcher and Church, 1970c; Arnold et al., 1980). This may be of less importance in domestic animals and, if heritable, may even be selected against by modern breeding criteria. For example, Goatcher and Church (1970c) found the degree of individual variation to be consistently greater in African pygmy goats than in normal domestic goats, sheep or cattle, when comparing responses to the four basic taste sensations. In conclusion, this experiment employed synthetic food flavours to test the relative preferences of different aromatic stimuli for sheep and goats. Differences were found between flavours and between species in level of response; however, no difference was found between species in the pattern of response for the different flavours. Whilst our results do not give a clear indication that the flavour will enhance intake, they do suggest that sheep will be more responsive than goats to the flavour of the food and that there will be similar responses to flavour enhancement of food for both sheep and goats. The findings of this research suggest that it would be of practical use to evaluate feeds flavoured with compounds representing truffle, garlic and onion as intake enhancers in goats and sheep. Only if flavouring agents are successful in enhancing intake could we recommend flavouring as a means of masking undesirable feed flavours, production of a more uniform feed from variable ingredients or in prompting feed consumption.
Acknowledgements We would like to thank David Moore (Flavours) Ltd. for supplying the flavours, P. MacDonald and D. Moore for advice on their use, D. Elston, Biomathematics and Statistics Scotland, for statistical advice and R. Fawcett, A. Brown and C. MacEachern for animal care. Two referees gave valuable comments on a previous version of the manuscript.
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References Alexander, R.H., McGowan, M., 1966. The routine determination of in vitro digestibility of organic matter in forages—an investigation of the problems associated with continuous large-scale operation. J. Brit. Grassl. Soc. 21, 140–147. Arnold, G.W., 1966a. The special senses in grazing animals. I. Sight and dietary habits in sheep. Aust. J. Agric. Res. 17, 521– 529. Arnold, G.W., 1966b. The special senses in grazing animals. II. Smell, taste, and touch and dietary habits in sheep. Aust. J. Agric. Res. 17, 531–542. Arnold, G.W., de Boer, E.S., Boundy, C.A.P., 1980. The influence of odour and taste on the food preferences and food intake of sheep. Aust. J. Agric. Res. 31, 571–587. Bartolom´e, J., French, J., Plaixats, J., Selegman, N.J., 1998. Diet selection by sheep and goats on Mediterranean heath-woodland range. J. Range Manage. 51, 383–391. Bell, F.R., 1959. Preference thresholds for taste discrimination in goats. J. Agric. Sci. 52, 125–129. Black, J.L., Colebrook, W.F., Gherardi, S.G., Kenney, P.A., 1989. Diet selection and the effect of palatability on voluntary feed intake by sheep. Proc. Minn. Nutr. Conf. 50, 139–151. Blaxter, K.L., 1962. The Energy Metabolism of Ruminants. Hutchinson, London, UK, 329 pp. Bullock, D.J., 1985. Annual diets of hill sheep and feral goats in southern Scotland. J. Appl. Ecol. 22, 423–433. Burrit, E.A., Provenza, F.D., 1992. Lambs form preferences for non-nutritive flavours paired with glucose. J. Anim. Sci. 70, 1133–1136. del Pozo, M., Osoro, K., Celaya, R., 1998. Effects of complementary grazing by goats on sward composition and on sheep performance managed during lactation in perennial ryegrass and white clover pastures. Small Rumin. Res. 29, 173–184. Fisher, R.A., Yates, F., 1957. Statistical Tables for Biological, Agricultural and Medical Research, sixth edition. Longman, Harlow, UK, 156 pp. Frutos, P., Duncan, A.J., Kyriazakis, I., Gordon, I.J., 1998. Learned aversion towards oxalic acid-containing foods by goats: does rumen adaptation to oxalic acid influence diet choice? J. Chem. Ecol. 24, 383–397. Gherhardi, S.G., Black, J.L., 1991. Effect of palatability on voluntary feed intake by sheep. I. Identification of chemicals that alter the palatability of a forage. Aust. J. Agric. Res. 42, 571–584. Goatcher, W.D., Church, D.C., 1970a. Taste responses in ruminants. I. Reactions of sheep to sugars, saccharin, ethanol and salts. J. Anim. Sci. 30, 777–783. Goatcher, W.D., Church, D.C., 1970b. Taste responses in ruminants. III. Reactions of pygmy goats, normal goats, sheep and cattle to sucrose and sodium chloride. J. Anim. Sci. 31, 364– 372. Goatcher, W.D., Church, D.C., 1970c. Taste responses in ruminants. IV. Reactions of pygmy goats, normal goats, sheep and cattle to acetic acid and quinine hydrochloride. J. Anim. Sci. 31, 373– 382. Gordon, I.J., Illius, A.W., 1992. Foraging strategy: from monoculture to mosaic. In: Speedy, A. (Ed.), Progress in Sheep
and Goat Research. CAB International, Wallingford, pp. 153– 177. Gurung, N.K., Jallow, O.A., McGregor, B.A., Watson, M.J., McIlroy, B.K.M.H., Holmes, J.H.G., 1994. Complementary selection and intake of annual pastures by sheep and goats. Small Rumin. Res. 14, 185–192. Kronberg, S.L., Malechek, J.C., 1997. Relationships between nutrition and foraging behavior of free-ranging sheep and goats. J. Anim. Sci. 75, 1756–1763. Kyriazakis, I., Oldham, J.D., 1993. Diet selection in sheep: the ability of growing lambs to select a diet that meets their crude protein (nitrogen x 6.25) requirements. Brit. J. Nutr. 69, 617– 629. Kyriazakis, I., Oldham, J.D., Coop, R.L., Jackson, F.J., 1994. The effect of subclinical nematode infection on the diet selection of growing sheep. Brit. J. Nutr. 72, 665–677. Kyriazakis, I., Papachristou, T.G., Duncan, A.J., Gordon, I.J., 1997. Mild conditioned food aversions developed by sheep towards flavours associated with plant secondary compounds. J. Chem. Ecol. 23, 727–746. Lawes Agricultural Trust, 1993. Genstat 5 Reference Manual. Claredon Press, Oxford, 812 pp. Morand-Fehr, P., 2003. Dietary choices of goats at the trough. Small Rumin. Res. 49, 231–239. Mysterud, A., 2000. Diet overlap among ruminants in Fennoscandia. Oecologia 124, 130–137. Nolte, D.L., Provenza, F.D., 1992a. Food preferences in lambs after exposure to flavours in solid foods. Appl. Anim. Behav. Sci. 32, 337–347. Nolte, D.L., Provenza, F.D., 1992b. Food preferences in lambs after exposure to flavours in milk. Appl. Anim. Behav. Sci. 32, 381–389. Pande, R.S., Kemp, P.D., Hodgson, J., 2002. Preference of goats and sheep for browse species under field conditions. N. Z. J. Agric. Res. 45, 97–102. Pella, E., Colombo, B., 1973. Study of carbon, hydrogen and nitrogen determination by combustion-gas chromatography. Mikrochim. Acta 1973, 697–719. Perez-Barberia, F.J., Gordon, I.J., Nores, C., 2001. Evolutionary transitions among feeding styles and habitats in ungulates. Evol. Ecol. Res. 3, 221–230. Provenza, F.D., 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48, 2–17. Provenza, F.D., Malechek, J.C., 1984. Diet selection by domestic goats in relation to blackbrush twig chemistry. J. Appl. Ecol. 21, 831–841. Provenza, F.D., Scott, C.B., Phy, T.S., Lynch, J.J., 1996. Preference of sheep for foods varying in flavors and nutrients. J. Anim. Sci. 74, 2355–2361. Sokal, R.R., Rohlf, F.J., 1995. Biometry. Freeman, New York, 887 pp. Tilley, J.M.A., Terry, R.A., 1963. A two-stage technique for in vitro digestion of forage crops. J. Brit. Grassl. Soc. 18, 104–111. Van Soest, P.J., 1963. Use of detergents in the analysis of fibrous feeds. 2. A rapid method for the determination of fibre and lignin. J. Assoc. Off. Agric. Chem. 46, 790–829.
E. Robertson et al. / Small Ruminant Research 63 (2006) 50–57 Van Soest, P.J., Wine, R.H., 1967. Use of detergents in the analysis of fibrous feeds. 4. Determination of plant cell wall constituents. J. Assoc. Off. Agric. Chem. 50, 50–55. Villalba, J.J., Provenza, F.D., 1997. Preference for wheat straw by lambs conditioned with intraruminal infusions of starch. Brit. J. Nutr. 77, 287–297.
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Villalba, J.J., Provenza, F.D., 2000. 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.
Preferences of sheep and goats for straw pellets treated with different food-flavouring agents E. Robertson, I.J. Gordon ∗ , F.J. P´erez-Barber´ıa Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK Received 13 January 2004; received in revised form 4 January 2005; accepted 2 February 2005 Available online 18 March 2005
Abstract In order to assess differences in preferences for flavours between ruminant species, two-choice tests were conducted on sheep (Scottish Blackface, Ovis aries) and goats (feral hybrids, Capra hircus). Feed pellets (nutritionally improved barley straw) were treated with synthetic human food-flavouring agents representing: strawberry (ST), apple (AP), orange (OR), maple (MA), caramel (CA), truffle (TR), garlic (GA) and onion (ON) flavours. Animals were first exposed to each of the flavours and then presented with each, paired with an untreated (control) feed, and the consumption of individual feeds recorded. Preference values (PV) were calculated from the proportion of the total feed consumption derived from the flavour-treated feed. Differences in PV were found between species (P = 0.01) and between flavours (P < 0.005). Although sheep showed stronger preference for flavoured feeds than did goats, both sheep and goats showed a similar pattern of preference across the flavours offered. In general, sheep exhibited significant preference for TR, GA, ON, AP, CA, MA and OR relative to the unflavoured feeds, whereas goats showed significant preference for TR, ON, AP and GA. The findings of this research suggest that it would be of practical use to evaluate feeds flavoured with compounds representing truffle, garlic and onion as intake enhancers in goats and sheep. Only if flavouring agents are successful in enhancing intake could we recommend flavouring as a means of masking undesirable feed flavours, production of a more uniform feed from variable ingredients or in prompting feed consumption. © 2005 Elsevier B.V. All rights reserved. Keywords: Flavours; Truffle; Onion; Garlic; Goats; Sheep
1. Introduction Ruminant animals have been shown to generally select for foods on the basis of their nutrient content ∗ Corresponding author. Present address: Sustainable Ecosystems, CSIRO – Davies Laboratory, PMB PO Aitkenvale, Qld 4814, Australia. Tel.: +61 7 4753 8509; fax: +61 7 4753 8600. E-mail address: [email protected] (I.J. Gordon).
0921-4488/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2005.02.007
(e.g. Kyriazakis and Oldham, 1993; Kyriazakis et al., 1994; Burrit and Provenza, 1992) and to avoid feeds containing plant secondary compounds, e.g. tannins (Provenza and Malechek, 1984). This choice is assumed to be based on the association between sensory components of the food (e.g. taste, smell, touch and sight, Arnold, 1966a,b) and the post-ingestive consequences (e.g. positive and negative gastrointestinal feedback, Kyriazakis et al., 1997). Sheep and goats
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have been shown to consume different diets when grazing in common (e.g. Gurung et al., 1994; Kronberg and Malechek, 1997; del Pozo et al., 1998; Mysterud, 2000), which is thought to be related to differences in the ways in which the two species ingest and digest the vegetation on offer (Gordon and Illius, 1992; Kronberg and Malechek, 1997). Generally, goats appear to be less selective than sheep (Bartolom´e et al., 1998) and include a broader range of species in their diet because they include a greater proportion of browse species (Bullock, 1985; Bartolom´e et al., 1998; Pande et al., 2002). It would, therefore, be expected that sheep and goats would differ in the degree to which they associate the sensory characteristics with the post-ingestive consequences of the foods consumed. Since the sensory cue and the post-ingestive feedback are so closely linked in food choice (Provenza, 1995), it is important to adequately isolate the response due directly to the sensory cue from that due to other factors. The flavour of the food is thought to play an important sensory role in determining the preference for different foods in sheep and goats (Provenza, 1995). In this study, we fed low quality, straw pellets covered with a range of artificial flavours to test whether the innate flavour preferences differ between sheep and goats. Since goats feed on a wider variety of plants than do sheep, when grazing in common, we would predict that goats would exhibit less preference for flavours than do sheep. This would be an evolutionary advantage for the use of diverse diets and novel feeds, and consequently allow the animal greater flexibility in behaviour to adapt to new habitats and changing environmental condition (Perez-Barberia et al., 2001).
2. Materials and methods Whilst many studies of dietary learning have used artificial flavouring agents to associate the postingestive feedbacks with an ingestive sensory property of the food (e.g. Provenza et al., 1996; Kyriazakis et al., 1997; Frutos et al., 1998; Villalba and Provenza, 2000), none have systematically tested for differences in preference between sheep and goats for these flavouring agents. In general, when testing innate preferences for different flavours it is vital that the flavouring agents used have (i) no nutritional content (e.g. contain no
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energy, salt or minerals), (ii) have no (negative) postingestive consequences (e.g. from tannins or other secondary compounds), and (iii) are present in minimal quantities, as any of those factors can confound flavour preference with preference for the nutritional or postingestive consequences of the forage consumed. We investigated the flavour preferences of sheep and goats, under controlled conditions, using minute quantities (0.05 g/kg) of nutritionally inert flavouring agents combined with a relatively low quality feed. We attempted to further isolate the response by the use of minimal fasting, short-term feeding trials and the feeding of a different feed between trials (i.e. hay which would be expected to have a buffering effect). The animals used were all acclimatised to each of the flavours to minimise the effect of residual associations. Villalba and Provenza (1997) found that associations persisted for 8 weeks in lambs, but Nolte and Provenza, (1992a,b) found that associations were not extinguished until 9 months. 2.1. Design The experiment was conducted at the Macaulay Land Use Research Institute’s Glensaugh Animal Research Facility over a period of 10 days. There were two experimental periods (P1 and P2) each of four days, separated by two rest days. Tests were conducted at the same times on each day at 10:00 h (AM trial) and 15:00 h (PM trial). These times of relative inactivity within the animal facility were chosen to limit the disturbance to the animals during the tests. The same eight sheep (S1–S8) and the same eight goats (G1–G8) were used in each period. Four orthogonal 8 × 8 Latin squares (Fisher and Yates, 1957) were used (one per species per period) to allocate animals to treatments (one of the eight flavoured feeds tested against the unflavoured feed). Animals were allocated to column numbers at random and choice tests were assigned to rows. The design was balanced for the effect of the position at which the feeds were presented to the animals by alternating the relative positions of the flavoured and unflavoured feeds in every second test (i.e. right–left relative to the position of the animal in the pen). This also ensured that position effects were not confounded with time of day effects, since the former were alternated in every trial.
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2.2. Animals Eight mature castrate males of each species were used in the experiment. The Scottish Blackface sheep were 3 years old; the goats were 4-year-old feral hybrids. At the start of the experiment, mean live weights and condition scores (CS) were, respectively, 55.8 kg (S.E. ± 1.63) and CS 2.25 for sheep and 50.8 kg (S.E. ± 1.83) and CS 2.22 for goats. All animals had been housed continuously for 2 years prior to the experiment and were trained in the routines of preference tests involving chopped hays and straws but not to flavour tests per se. All animals were fed on the same diet (1.0 kg high quality grass hay per day) prior to the experiment. During the 27 days immediately prior to the experiment, all animals were accustomed to each of the flavoured feeds and the unflavoured feed by offering the feeds for a total of three days each. Between tests and between the threeday-periods animals were fed grass hay (1.0 kg per day) and had constant access to fresh water and mineral and salt licks (Rockies Yellow; Tithebarn Ltd, Southport, Merseyside, England, UK). The animals were housed in adjacent individual pens facing animals of the same species but not involved in the experiment. Pens had slatted wooden floors (area = 2.8 m2 ) with open railed front and back panels but plywoodsheeted sides. Hence, although animals remained in close visual contact with others of their own species, their choices would not have been influenced by their peers. The animal facility was provided with natural light and ventilation; the mean daily temperature during the period of the experiment was 9.9 ◦ C (S.E. ± 0.81). 2.3. Feeds 2.3.1. Preparation The basal feed used in the tests was an 8 mm (diameter) pelleted nutritionally improved straw (NIS) (Barley straw treated with ammonia; Davidson Brothers, Shotts, Lanarkshire, Scotland, UK). This feed was selected as a uniform feed with a potential to improve intake through the addition of flavours which would maximise the expression of preferences. Experimental feeds were prepared on the first day of the 27day pre-experimental period, which was considered to be sufficient time to allow the flavouring agents to be
fully absorbed into the straw pellets prior to the start of the preference tests (P. McDonald; David Moore (Flavours) Ltd. Wrexham, UK, personal communication). During the acclimatization period, daily DM intakes of all feed types (flavoured and unflavoured) were moderate (582 ± 34.5 g for sheep and 264 ± 32.9 g for goats). The flavouring agents used were synthetic watersoluble human food-flavouring complexes (maple (no. 6546; MA), caramel (no. 3708; CA), strawberry (no. 1675; ST), garlic (no. 6306; GA), apple (no. 3067/T; AP), onion (no. 0297; ON), truffle (no. 5410/T; TR) and orange (no.2884/T; OR)), (David Moore (Flavours) Ltd., Wrexham, UK.). MA and CA represent sweet flavours, GA, TR and ON represent savory flavours and ST, AP and OR represent fruity flavours. Flavouring agents were applied in liquid form as this caused no adherence problems and the flavour distributed itself evenly between and throughout pellets and caused no perceptible visual or textural changes in the pellet. The pellets were spread on a clean plastic sheet (1 per flavour) to produce an even layer, one pellet in thickness. Flavour concentrate was diluted (1 part in 20 parts unflourinated tapwater) and the resultant solution was applied evenly at a rate of 1 g per kg feed using a household plant mist sprayer. Flavoured feeds were then stored in lightproof, plastic dustbins with lids. No treatment of the control feed was carried out. Samples of each feed (control and flavoured feeds) were taken on three occasions per period to estimate the DM content and feed intakes were subsequently expressed on a dry matter basis. The samples were also analyzed for crude protein (N), gross energy (GE), fibre (acid detergent fibre (ADF) and neutral detergent fibre (NDF)) and in vitro digestibility. Nitrogen analysis was carried out with a Carlo Erba elemental analyser (Carlo Erba, Milan, Italy) as described by Pella and Colombo (1973). GE determination was by bomb calorimetry (Gallankamp, FIS, Crawley, UK) as described by Blaxter (1962). ADF was determined as described by Van Soest (1963), NDF by Van Soest and Wine (1967) and in vitro digestibility by Tilley and Terry (1963) as modified by Alexander and McGowan (1966). The addition of flavours had no significant effects on the chemical composition, GE or DM of the feeds (Table 1) and the composition of the feeds did not vary significantly between days.
E. Robertson et al. / Small Ruminant Research 63 (2006) 50–57
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Table 1 Mean values and their standard errors (S.E.) of laboratory analyses conducted on the flavoured and unflavoured straw pellets (N = 54) Dry matter (%)
Mean S.E.
92.4 0.005
Fibre (%) NDF
ADF
66.77 0.138
50.44 0.065
Organic matter digestibility in vitro (%)
Crude protein (%)
Energy (kJ/(g DM)
54.08 0.096
4.55 0.026
16.71 0.011
2.3.2. Presentation During a test, each animal was simultaneously presented with two immediately adjacent basins, of identical size (35 cm diameter) and colour, supported in a wooden frame to prevent spillage. One of the basins contained 500 g of the control feed and the other 500 g of an allocated flavoured feed. In order to prevent crosscontamination, basins were allocated to a feed type for the duration of the experiment and labelled accordingly. The relative position of the control and flavoured feeds for each animal was alternated every second test to account for any positional effect. Each test lasted 30 min and was preceded by a 60-min fasting period. Thirty minutes after presentation to the animals the basins were removed and re-weighed. Weighing was carried out to the nearest gram. Intakes were calculated from the pre- and post-test feed weights and expressed on a DM basis (DMI). 2.4. Statistical analysis Crude preference values (cPV) were calculated by the procedure used by Bell (1959) and subsequently employed by other authors (e.g. Goatcher and Church, 1970a; Black et al., 1989; Gherhardi and Black, 1991). In this procedure, the consumption of the treated feed is expressed as a proportion of the total feed consumption and produces values ranging from 0 to 1. Instances of non-discrimination or absence of preference would both be expected to yield a value of 0.5. Goatcher and Church (1970a) classed values with a value >0.8 as strong preferences, those between 0.8 and 0.7 as moderate preferences and those between 0.7 and 0.6 as weak preferences. Similarly, a value <0.2 indicated a strong rejection, between 0.2 and 0.3 a moderate rejection and those between 0.3 and 0.4 a weak rejection. Since the impact of a one-gram change in feed intake over the range of possible PV values was not uniform (the greatest impact was at the extremes of preference),
the dataset was transformed into standardized preference values (sPV) using the following equation: sPV = loge
cPV 1 − cPV
According to the latter equation absence of preference for sPV corresponded to a value of 0. In addition to the loss of 2 data values due to feed spillage, 30 values were excluded due to the total consumption being less than the threshold set for a valid experimental unit (0.3 of the mean total DM consumption per species, i.e. 76 g for sheep and 53 g for goats). This led to an unbalanced data set that was consequently analysed by a regression approach using residual maximum likelihood (REML) algorithm in Genstat (Version 5.3, Lawes Agricultural Trust, 1993). We used sPV as the response variable; period, presentation position (right–left), species, flavour and their interactions as the fixed terms, individual body mass as a covariate and flavour within individuals as the random term in the analysis. From this model the estimated means of the sPV and their associated standard error of the differences (S.E.D.) were used to test, if the preference for each flavour differed from the unflavoured feed (zero value of sPV), and also if there were differences in preference between flavours. REML uses the Wald statistic, which has an asymptotic chi-squared distribution with degrees of freedom equal to those of the terms in the regression model (Sokal and Rohlf, 1995). Differences in preference for specific flavours between animals where calculated by a generalized linear model using a normal distribution and identity as the link function (Lawes Agricultural Trust, 1993) by fitting species + flavour + animal + species × flavour + flavour × animal. Body masses and total consumption where used untransformed in all analyses since the examination of the residuals met the criteria of homocedasticity and normality.
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In order to compare results with those in the literature, they were back-transformed using the equation: PV =
esPV 1 + esPV
3. Results Over the resulting 216 experimental tests the mean total (i.e. flavoured + unflavoured feeds) dry matter intake (DMI) over the 30 min test was higher for sheep than goats, though this difference was not significant (216.4 g versus 192.7 g, S.E.D. = 34.76; chisquare = 0.88, d.f. = 1, p = 0.349). A mean PV of 0.732 (sPV = 1.007) indicated a positive overall discrimination for the flavoured feeds (F7,236 = 25.72; P < 0.001) relative to the unflavoured feeds across the two species. The mean PV for sheep 0.820 (sPV = 1.519) was significantly greater (χ2 = 7.43, d.f. = 1, p = 0.006) than that for goats 0.634 (sPV = 0.552), (S.E.D. for transformed data = 0.3615), indicating that, although both species could discriminate between the flavoured and unflavoured feeds, the sheep exhibited stronger preferences for the flavours than did the goats (Fig. 1). No significant species by flavour interaction was found (χ2 = 0.67; d.f. = 7, p = 0.697), indicating that sheep and goats have very similar preferences for
Fig. 1. Mean and standard error standardized preference values (sPV) for flavours for sheep and goats. Maple (MA), caramel (CA), strawberry (ST), garlic (GA), apple (AP), onion (ON), truffle (TR) and orange (OR).
the eight flavours. The preferences for the different flavours were ranking as follows, TR (sPV = 1.696), GA (1.430), ON (1.308), AP (1.143), CA (0.924), MA (0.850), OR (0.561) and ST (0.370). In general, sheep exhibited significant preference for TR, GA, ON, AP, CA, MA and OR relative to the unflavoured feeds, whereas goats showed significant preference for TR, ON, AP and GA. When comparisons were carried out between flavours significant differences were found for ST against GA, AP, ON, TR and also for OR against GA, TR (S.E.D. = 0.381, α = 0.05). Although individual animals varied in the strength of their preference for the flavoured feeds (F14,100 = 4.03; p < 0.001), and there was some individual animal variation within the preferences exhibited for the flavours (0.290–0.471 for sheep and 0.228–0.381 for goats) (Fig. 1), the animal by flavour interaction was not quite significant (animal × flavour: F86,100 = 1.38, p = 0.06, NS).
4. Discussion The only experiments that have assessed the preferences for the flavours used in this experiment are those of Nolte and Provenza (1992a,b), who found onion to be more preferred by lambs than garlic although both were less preferred than the control feed (alfalfa and barley). These results differ from those reported here, both in the relative preferences for GA and ON, and in their preferences relative to the control feed, possibly due to the differences in experimental approach. Nolte and Provenza (1992a,b) used high concentrations (20–250 g per kg at 10 times natural strength) of flavours (powdered plant material), and recognized that this may have resulted in negative post-ingestive effects, especially in the case of garlic. It is also likely that any such effects would be heightened by the relatively long (overnight) fasting period used by Nolte and Provenza (1992a,b). The feed used by Nolte and Provenza (1992a) as a basal feed was a mixture of ground alfalfa and rolled barley. As a high quality feed, this would be acceptable in its untreated form and consequently less amenable to improvements in acceptability than the straw pellets used in this experiment (see also Morand-Fehr, 2003). Also, Nolte and Provenza (1992a) used powered plants whereas the current experiment involved artificial flavours, which
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may not directly replicate the flavours for ruminants and may have other unknowns (e.g. aftertaste) that could affect the preference of sheep and goats for the flavours. No specific trials have been conducted testing differences between sheep and goats for preferences between the flavours used in this experiment, with much of the research on the response of ruminants to sensory cues of taste using an approach based on the four basic taste sensations, as opposed to complex mixtures such as those used in this experiment. For example, Bell (1959) described the taste and preference thresholds for goats and sheep offered chemicals representing the sensations of sweet, sour, salty and bitter presented in drinking water. In that study, goats had a higher threshold for bitter (quinine) tastes, relative to sheep, and for both species sweet (glucose) was preferred to unflavoured tapwater over a range of concentrations. Responses to salt (sodium chloride), sour (acetic acid) and bitter flavours changed very rapidly with changes in concentration. In a separate study, Goatcher and Church (1970b) found that goats showed an increasing preference for water flavoured with sucrose as concentration increased from 2.5% to 20% whilst sheep exhibited no preferences. It might be expected, therefore, that goats would exhibit higher preferences than sheep for MA, CA, ST, OR and AP that represent “sweet” and “fruity” flavours. This was not found in this experiment. Generally, we found that sheep had a greater preference for flavoured feeds than did goats. This supports the hypothesis that goats are less affected by the flavour of the food than are sheep and this facilitates their more diverse dietary response (Bullock, 1985; Bartolom´e et al., 1998; Pande et al., 2002). Our results also demonstrate that, whilst sheep showed a greater preference for flavoured feeds than did the goats, both ruminant species showed a similar preference ranking for the flavours used in the experiment. This similarity in response suggests that both species may be receiving similar sensations from the flavours and that these sensations are innately associated with post-ingestive feedbacks associated with the consumption of a diverse range of forages. Individual animal differences in flavour preferences of the magnitude experienced here are widely reported elsewhere, with both sheep and goats and with
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a variety of flavouring agents (Morand-Fehr, 2003). Goatcher and Church (1970c), although concluding that sheep were indifferent to sweet tastes (equivalent to PV = 0.574), found individual sheep preferences varied from 0.035 to 0.845 PV equivalent. Expression of these individual differences is frequently credited with an evolutionary advantage to a social species foraging in its natural environment (e.g. Goatcher and Church, 1970c; Arnold et al., 1980). This may be of less importance in domestic animals and, if heritable, may even be selected against by modern breeding criteria. For example, Goatcher and Church (1970c) found the degree of individual variation to be consistently greater in African pygmy goats than in normal domestic goats, sheep or cattle, when comparing responses to the four basic taste sensations. In conclusion, this experiment employed synthetic food flavours to test the relative preferences of different aromatic stimuli for sheep and goats. Differences were found between flavours and between species in level of response; however, no difference was found between species in the pattern of response for the different flavours. Whilst our results do not give a clear indication that the flavour will enhance intake, they do suggest that sheep will be more responsive than goats to the flavour of the food and that there will be similar responses to flavour enhancement of food for both sheep and goats. The findings of this research suggest that it would be of practical use to evaluate feeds flavoured with compounds representing truffle, garlic and onion as intake enhancers in goats and sheep. Only if flavouring agents are successful in enhancing intake could we recommend flavouring as a means of masking undesirable feed flavours, production of a more uniform feed from variable ingredients or in prompting feed consumption.
Acknowledgements We would like to thank David Moore (Flavours) Ltd. for supplying the flavours, P. MacDonald and D. Moore for advice on their use, D. Elston, Biomathematics and Statistics Scotland, for statistical advice and R. Fawcett, A. Brown and C. MacEachern for animal care. Two referees gave valuable comments on a previous version of the manuscript.
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References Alexander, R.H., McGowan, M., 1966. The routine determination of in vitro digestibility of organic matter in forages—an investigation of the problems associated with continuous large-scale operation. J. Brit. Grassl. Soc. 21, 140–147. Arnold, G.W., 1966a. The special senses in grazing animals. I. Sight and dietary habits in sheep. Aust. J. Agric. Res. 17, 521– 529. Arnold, G.W., 1966b. The special senses in grazing animals. II. Smell, taste, and touch and dietary habits in sheep. Aust. J. Agric. Res. 17, 531–542. Arnold, G.W., de Boer, E.S., Boundy, C.A.P., 1980. The influence of odour and taste on the food preferences and food intake of sheep. Aust. J. Agric. Res. 31, 571–587. Bartolom´e, J., French, J., Plaixats, J., Selegman, N.J., 1998. Diet selection by sheep and goats on Mediterranean heath-woodland range. J. Range Manage. 51, 383–391. Bell, F.R., 1959. Preference thresholds for taste discrimination in goats. J. Agric. Sci. 52, 125–129. Black, J.L., Colebrook, W.F., Gherardi, S.G., Kenney, P.A., 1989. Diet selection and the effect of palatability on voluntary feed intake by sheep. Proc. Minn. Nutr. Conf. 50, 139–151. Blaxter, K.L., 1962. The Energy Metabolism of Ruminants. Hutchinson, London, UK, 329 pp. Bullock, D.J., 1985. Annual diets of hill sheep and feral goats in southern Scotland. J. Appl. Ecol. 22, 423–433. Burrit, E.A., Provenza, F.D., 1992. Lambs form preferences for non-nutritive flavours paired with glucose. J. Anim. Sci. 70, 1133–1136. del Pozo, M., Osoro, K., Celaya, R., 1998. Effects of complementary grazing by goats on sward composition and on sheep performance managed during lactation in perennial ryegrass and white clover pastures. Small Rumin. Res. 29, 173–184. Fisher, R.A., Yates, F., 1957. Statistical Tables for Biological, Agricultural and Medical Research, sixth edition. Longman, Harlow, UK, 156 pp. Frutos, P., Duncan, A.J., Kyriazakis, I., Gordon, I.J., 1998. Learned aversion towards oxalic acid-containing foods by goats: does rumen adaptation to oxalic acid influence diet choice? J. Chem. Ecol. 24, 383–397. Gherhardi, S.G., Black, J.L., 1991. Effect of palatability on voluntary feed intake by sheep. I. Identification of chemicals that alter the palatability of a forage. Aust. J. Agric. Res. 42, 571–584. Goatcher, W.D., Church, D.C., 1970a. Taste responses in ruminants. I. Reactions of sheep to sugars, saccharin, ethanol and salts. J. Anim. Sci. 30, 777–783. Goatcher, W.D., Church, D.C., 1970b. Taste responses in ruminants. III. Reactions of pygmy goats, normal goats, sheep and cattle to sucrose and sodium chloride. J. Anim. Sci. 31, 364– 372. Goatcher, W.D., Church, D.C., 1970c. Taste responses in ruminants. IV. Reactions of pygmy goats, normal goats, sheep and cattle to acetic acid and quinine hydrochloride. J. Anim. Sci. 31, 373– 382. Gordon, I.J., Illius, A.W., 1992. Foraging strategy: from monoculture to mosaic. In: Speedy, A. (Ed.), Progress in Sheep
and Goat Research. CAB International, Wallingford, pp. 153– 177. Gurung, N.K., Jallow, O.A., McGregor, B.A., Watson, M.J., McIlroy, B.K.M.H., Holmes, J.H.G., 1994. Complementary selection and intake of annual pastures by sheep and goats. Small Rumin. Res. 14, 185–192. Kronberg, S.L., Malechek, J.C., 1997. Relationships between nutrition and foraging behavior of free-ranging sheep and goats. J. Anim. Sci. 75, 1756–1763. Kyriazakis, I., Oldham, J.D., 1993. Diet selection in sheep: the ability of growing lambs to select a diet that meets their crude protein (nitrogen x 6.25) requirements. Brit. J. Nutr. 69, 617– 629. Kyriazakis, I., Oldham, J.D., Coop, R.L., Jackson, F.J., 1994. The effect of subclinical nematode infection on the diet selection of growing sheep. Brit. J. Nutr. 72, 665–677. Kyriazakis, I., Papachristou, T.G., Duncan, A.J., Gordon, I.J., 1997. Mild conditioned food aversions developed by sheep towards flavours associated with plant secondary compounds. J. Chem. Ecol. 23, 727–746. Lawes Agricultural Trust, 1993. Genstat 5 Reference Manual. Claredon Press, Oxford, 812 pp. Morand-Fehr, P., 2003. Dietary choices of goats at the trough. Small Rumin. Res. 49, 231–239. Mysterud, A., 2000. Diet overlap among ruminants in Fennoscandia. Oecologia 124, 130–137. Nolte, D.L., Provenza, F.D., 1992a. Food preferences in lambs after exposure to flavours in solid foods. Appl. Anim. Behav. Sci. 32, 337–347. Nolte, D.L., Provenza, F.D., 1992b. Food preferences in lambs after exposure to flavours in milk. Appl. Anim. Behav. Sci. 32, 381–389. Pande, R.S., Kemp, P.D., Hodgson, J., 2002. Preference of goats and sheep for browse species under field conditions. N. Z. J. Agric. Res. 45, 97–102. Pella, E., Colombo, B., 1973. Study of carbon, hydrogen and nitrogen determination by combustion-gas chromatography. Mikrochim. Acta 1973, 697–719. Perez-Barberia, F.J., Gordon, I.J., Nores, C., 2001. Evolutionary transitions among feeding styles and habitats in ungulates. Evol. Ecol. Res. 3, 221–230. Provenza, F.D., 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48, 2–17. Provenza, F.D., Malechek, J.C., 1984. Diet selection by domestic goats in relation to blackbrush twig chemistry. J. Appl. Ecol. 21, 831–841. Provenza, F.D., Scott, C.B., Phy, T.S., Lynch, J.J., 1996. Preference of sheep for foods varying in flavors and nutrients. J. Anim. Sci. 74, 2355–2361. Sokal, R.R., Rohlf, F.J., 1995. Biometry. Freeman, New York, 887 pp. Tilley, J.M.A., Terry, R.A., 1963. A two-stage technique for in vitro digestion of forage crops. J. Brit. Grassl. Soc. 18, 104–111. Van Soest, P.J., 1963. Use of detergents in the analysis of fibrous feeds. 2. A rapid method for the determination of fibre and lignin. J. Assoc. Off. Agric. Chem. 46, 790–829.
E. Robertson et al. / Small Ruminant Research 63 (2006) 50–57 Van Soest, P.J., Wine, R.H., 1967. Use of detergents in the analysis of fibrous feeds. 4. Determination of plant cell wall constituents. J. Assoc. Off. Agric. Chem. 50, 50–55. Villalba, J.J., Provenza, F.D., 1997. Preference for wheat straw by lambs conditioned with intraruminal infusions of starch. Brit. J. Nutr. 77, 287–297.
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Villalba, J.J., Provenza, F.D., 2000. 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.