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Applied Animal Behaviour Science 5 4 (1997) 327-334

APPLIED ANIMALBEHAVIOUR

SCIENCE

Overcoming food neophobia in domestic ruminantsthrough addition of a familiar flavor and repeated

exposure to novel foods IK.L. Launchbaugh a,* F.D. Provenza b, M.J. W erkmeister

Range Resources Department, Idaho State University, Moscow, ID 83844, USAb Rangeland Resources Department, Utah State University, Logan, UT 84322, USA

Bureau of Land Management, Farmington, NM 87401, USAAccepted 2 1 October 1996

AbstractFood neophobia, observed as a decreased intake of novel foods, can cause significant livestockproduction losses. For example, in the transition from rangeland to feedlot, livestock are usually

offered novel diets that they sample cautiously, gradually increasing intake. This familiarizationperiod can slow weight gains and increase time to slaughter. This research examines two ways toovercome food neophobia. First, we determined if the addition of a familiar flavor wou ld increasethe acceptance of a novel food. Lambs (n = 30) were fed barley, onion-flavored barley, oronion-flavored rice twice a day for 4 days. All lambs were then offered onion-flavored rice. Thelambs that had previously eaten onion-flavored barley ate more (P < 0.05) onion-flavored ricethan those that had previously eaten unflavored barley. Second, we examined if repeated exposureto novel foods increased the accepta nce of subsequ ent novel foods. Controlling for order of foodoffered, lambs (n = 72 total) were offered four novel foods (calf manna, corn, rice, and wheatbran) for 3 consecutive days each (12 days total). Lambs ate more (P < 0.05) of the fourth novelfood than of the first novel food offered. T hese results indicate that flavor gen eralization andrepeated exposure to novel foods ma y increase the acceptance of novel foods. 0 1997 ElsevierScience B.V.Keywords: Eating behavior; Flavor generalization; Intake; Neophobia; Novelty

* Corresponding author. This technical article is a contribution of the Utah Agricultural Experiment Station and the College of

Agricultural Sciences and Natural Resources at Texas Tech University (T-759). Research protocol wasapproved by the Utah State University Animal Care and Use Committee (Protocol 356).

016%1591/97/$17.00 0 1997 Elsevier Science B.V. All rights reservedPII SO168-1591(96)01194-X


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1. IntroductionRuminants almost invariably eat only a small amount of a food when it is offered for

the first time (Chapple and Lynch, 1986; Chap ple et al., 1987; Thorhallsdottir et al.,1987; Provenza et al., 19 95). This cautious samp ling or complete rejection of new foodsis called neophobia, literally fear of new. Food neophobia, not unpalatability, is themajor factor affecting intake by naive herbivores (Squibb et al., 1990).

Neopho bia has been suggested as a herbivore survival mechanism for avoidingover-consumption of toxic plants in the wild (Rozin, 1977; Provenza and Balph, 1988;Provenza et al., 1988). Nevertheless, food neophobia can cause production losses whenanim als reluctantly accept nutritious novel foods (Ortega-Reyes et al., 1992). In contem-porary livestock production systems, animals are often exposed to novel feeds orforages. Bulls, rams, or replacement females may be transported hundreds of miles aspart of breeding programs to rangelands with many unfamiliar plants. Lambs and calvesalso encounter novel foods at weaning time and when they are placed in feedlots forfattening. Low intake of feedlot diets is often observed when animals are initiallyreceived into feedlots (Cole et al., 1982; Zinn et al., 1988; Hicks et al., 1990).

This paper reports results of two experiments designed to overcome neophobia andincrease the acceptance of novel foods. The objective of the first experiment was todetermine if neophobia decreased when a familiar flavor was added to a novel food. Theobjective of the second experiment was to determine if neophobia decreased withrepeated exposure to novel foods.

2. Experiment 1: flavor generalizationGeneralization occurs w hen anim als respond in a uniform way to a group of stimuli

(Mazur, 1990). Animals generalize diet selection responses to foods with similar flavors(Launchb augh and Provenza, 1994). Generalization may therefore be impo rtant in theconsumption of novel foods because a new food may look, smell, or taste like a familiarfood that is preferred or avoided. For instance, lam bs averted to cinnamon-flavored rice,with the toxin lithium chloride, also avoided cinnamon-flavored wheat (Launchb aughand Provenza, 1994). In this experiment, we examined if the acceptance of a novel foodcould be increased by adding the flavor of a familiar acceptable food.2.1. Materials and methods

This experiment was conducted at Utah State University research facilities nearLogan, UT, with 36 crossbred lambs (both male and female) of Columbia, Rambouillet,Suffolk, Targhee, and Finnish Landrace breeds obtained as 3- to 7-day-old orphans fromthe US Sheep Experimen t Station, at Dub ois, ID. Lambs were fed a comm ercialmilk-replacer diet until 2.5 weeks of age and then were w eaned to a mix of dried milk,ground alfalfa, soybean meal, milo, and molasses. Lambs were slowly transferred onto adiet of alfalfa pellets. Lambs were exposed to only these foods before the experiment,


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K.L. Launchhaugh et al/ Appl ied Ani mal Behaciour Science 54 (1997) 327-334 329

which wa s initiated when lambs were approximately 4 months old (average weight 3 I .9kg, SE 1.1).

Three d ays before the trial, lambs were individually penned in wire pens (approxi-mately 3 m* area) set side by side. Throughout the trial, lambs were offere d ad libitumaccess to alfalfa pellets for 1 h in the morning (08:OO h) and 1 h in the evening (17:OOh). Water and salt were always available.

During a 4-day conditioning period, lamb s were offered a grain supplement for 15min twice a day at 10:00 and 19 :00 h. The specific grain offered depended on thetreatment group to which the lambs were randomly assigned (n = 12 lambs pertreatment). One treatment group received ground barley, another received ground barleywith 5% onion pow der, and the remaining group received ground rice with 5% onionpow der. On the first day of conditioning, animals were given 300 g (1.50 g in themorning and 150 g in the evening) of the grain to avoid over-consumption and possibleacidosis. The amount of grain p er day was increased to 600 g (300 g in the morning and300 g in the evening) on days 2, 3, and 4.

Following exposu re to one of three conditioning foods, all lambs w ere offered thesame food for 2 days. L ambs were offered 300 g of rice mixed with 5% onion powderfrom 10:00 to 10: 10 h on days 5 and 6. This allowed us to measure the consumption ofonion-flavored rice by lambs familiar with onion-flavored rice, familiar w ith onion butnot rice, and unfamiliar with both onion and rice.

A repeated measu res analysis of variance was used to com pare intake of onion-flavored rice by lambs in three treatments; day was the repeated measure. The effect offood eaten during conditioning (treatment) was tested with lambs nested within treat-ments. The effects of day and the treatment X day interaction were tested with theday X lamb interaction (Hicks, 1982 ). Mean separation was accom plished by the leastsignificant difference metho d (Steel and Torrie, 1 960).2.2. Resul t s and di scussi on

During the first day of conditioning, lambs ate more (P < 0.05) plain barley thanonion-flavored rice. Consumption of onion-flavored barley was intermediate betweenplain barley and onion-flavored rice. By the end of conditioning, the amount eaten didnot differ among treatments and most animals ate all they were offered. Six animals(two from each treatment) did not eat all 300 g offered by the end of conditioning and sothey were removed from the trial; resulting in ten animals per treatment.

The food eaten by lambs during conditioning strongly influenced the intake ofonion-flavored rice during testing (P < 0.05; Fig. 1). The intake of a novel food,onion-flavored rice, was greater by lambs that had previously eaten onion-flavoredbarley than by lambs ex posed to unflavored barley (P < 0.05). Lam bs that receivedonion-flavored rice during conditioning ate an amou nt of onion-flavore d rice intermedi-ate to, but not different from, the other two treatments. It is interesting that lambsfamiliar with onion-flavored rice did not eat more onion-flavored rice than the othertreatments. We suggest two possible explanations. First, lambs form stronger preferencesfor flavors associated with high energy feedback than for those associated with lessenergy fee dback (Villalba and Provenza, 1997 ). Barley has a higher digestible energy


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0 Test Day 1 Test Day 2Fig. 1. Consumption of rice flavored with onion powder by lambs that had received plain barley, onion-flavoredrice, or onion-flavored barley during a 4-day conditioning period before the test. Treatment bars, within thesame day, denoted with different letters are statistically different (P < 0.05); intervals above the treatment barsindicate standard errors of means.

and lower fiber content than rice (NR C, 1985 ). Therefore , animals conditioned withonion-flavored barley may have formed a greater preference for onion flavor than thoseoffered onion-flavored rice during conditioning. Second, the intake of a familiar fo odcan decreas e with repeated exposu re (Prov enza, 1996 ). Lamb s offered onion-flavoredrice on the test day had received it twice per day for the previous 4 days. On the testday, they ate less onion-flavored rice than they consumed the previous day, duringconditioning. This lowered intake may indicate a decrea sed preference for an overlyfamiliar food.

These results suggest that adding a familiar flavor to a novel fo od can increase itsinitial a cceptance. This principle could be useful to increase the consumption of novelfoods in livestock production systems. For examp le, to prepare animals for the feedlot, asalient flavor could be included in diets during background ing and the same salientflavor could be incorporated in the feedlot diet (Launchbaug h, 1995 ). Ortega-R eyes etal. (1992 ) dem onstrated that initial intake of newly weaned animals in drylot could beincreased by exposing animals to the feedlot diet with their mothers before weaning.How ever, livestock produce rs can seldom predict the diets their animals will receivewhen they reach the feedlot. Feedlot diets are formulated with readily available andeconomically feasible foods and it may be difficult to develop an industry standard forreceiving diets. How ever, it is conceivable that receiving diets could include a specifiedsalient flavor additive.

3. Experiment 2: repeated exposure to novel foodsAnimals show heightened neophobia after they eat a novel food that causes illness

(duToit et al., 1991 ). The opposite may also be true; neophobia may be decrea sed by


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K.L. Launchbaugh et al. Appl i ed Ani mal Behaciour Science 54 (1997) 327-334 331

several g ood experiences with novel foods. Capretta (19 77) show ed evidence for thisidea when he observed that experience with a variety of flavors by rat pups increasedtheir acceptance of a novel flavor com pared to rat pups with restricted flavor experi-ences. The purpose of experiment 2 was to determine if lambs were more likely toaccept a novel foo d after they had eaten seve ral novel food s without experiencingillness.

3.1. Materials and methods

In this experiment, 72 crossbred orphan lambs w ere obtained from the US Shee pExperiment Station and raised in the same manner as in the first experiment. Whenlambs were approximately 4 months old (average weight 3 1 O kg, SE = 0.6) they w ereindividually penned in wire pens (about 3 m* in area) set side by side. Each lamb wasoffered ad libitum access to alfalfa pellets for 1 h in the morning (07:OO h) and 1 h in theevening (17:00 h) each day . Lambs had access to water and salt at all times.

During a 12& y trial, lambs w ere offered four novel foods for 3 consecutive dayseach. The first novel food was o ffered to lambs at 11:OO h on days 1, 2, and 3. Lam bswere offered 500 g of either cra cked corn, rice, whe at bran, or calf manna. (Calf mannais a concentrate-based, pelleted food produc ed by the Manna Pro Comp any, 7711 BCarondelet Ave., St. Louis, MO .) On days 4, 5, and 6, each lamb was offered a differentfood (of the four experimental foods). For examp le, a lamb receiving corn in the firstperiod (days 1, 2, and 3) was offered either rice, w heat bran, or calf manna during thesecond period (days 4, 5, and 6). Lam bs were again offere d a different novel foo d ondays 7, 8, and 9 and the last novel food was offered on days 10, 11, and 12. There are24 possible sequences in which four foods can be offered one after another in fourordinal periods without lambs receiving the same food twice. The effect of foodpresentation sequence was controlled through blocking in a balanced simple cross-overdesign (three lambs per sequence; Gill, 1978 ). This resulted in the same number oflambs (n = 18) offered each food in each 3-day ordinal period.

A repeated measu res analysis of variance was used to determine the effect of repeatedexposu re to novel foods on the initial intake of a novel food. T he main effects of themodel were food (corn, rice, whe at bran, or calf manna) and ordinal period (first,second, third, or fourth o ffering) and the repeated measure was day within ordinalperiod. Least significant difference tests were used to com pare intake on each day ofoffering in the first, second, third, or fourth novel food (Steel and Torrie, 1960 ).

3.2. Resul t s and di scussi on

Lamb s ate more of the fourth novel food than the first novel food the first time eachfood was offered (P < 0.05; Fig. 2). There was no difference in the initial consumptionof the second or third novel foods. Consumption of the fourth novel food exceeded(P = 0.08) consumption of the second and third novel foods.Not all foods w ere equally palatable. Lamb s consum ed the same amount of rice, corn,and calf manna when it was first offered but, wheat bran was less readily accep ted


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First Second Third FourthNovel Food Presented

Fig. 2. Consumption of four novel foods the first time they were offered to lambs. Novel foods were offered infour 3-day periods (first, second, third, and fourth). An equal number of lambs received either cracked corn,rice, wheat bran, or calf manna in each ordinal period. Treatment bars denoted with different letters arestatistically different (P = 0.08); intervals above the treatment bars indicate standard errors of means.

(Table 1). Lamb s ate more on the second and third days they were offered a particularnovel food than on the first day of offering (day effe ct P < 0.01). However, ada y X food interaction was also significant (P < 0.01) because lambs did not increasesubsequent intake of whe at bran to as great an extent as corn, rice, or calf manna (Table1).

Exposing lambs to a number of safe novel foods appe ars to decreas e neophobia. Thiswill probably occur as long as consumption results in positive post-ingestive feedback .Repe ated exposu re is a useful research technique when the experimental protocolrequires high consumption of a novel food the first time it is offered (e.g. conditionedflavor-aversion trials). This principle may also explain why some animals adapt well tonovel diets when newly received into feedlot and others d o not. The dietary experienceof the animals could affec t their willingness to accept a novel feed lot ration.

Table 1Average daily intake (g f SE) of four novel foods by lambs the first, second, and third day they were offeredin a 12-day trialFood Day 1 Dav 2 Dav 3Wheat bran 36.2a f 2.8 53.ga f 3.9 67Ja f 4.2Cracked corn 124.1b f 9.9 176.2b f 11.5 191.0b f 12.1Calf manna 104.0b * 10.3 208.5 + 11.5 246.7 f 9.3Rice 121.1b f 12.4 215.3 f 12.8 250.0 + 11.4BbCMeans, within each day, followed by a different letter are different (P < 0.05).


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4. Conclusions

It is important that animals readily accept new foods in many production and researchsettings. Overcoming food neophobia by adding a familiar flavor to food or amelioratingneophobia through repeated exposure to new foods may be important methods toimprove intake of novel foods.

In addition to generalization and repeated exposure, the presence of other anima ls canprofoundly increase the consump tion of novel foods (Chap ple and Lynch, 1986;Thorhallsdottir et al., 199 0). Thus, in livestock management, it may be useful tointroduce livestock to novel foods w ith animals that are experienced at eating theparticular diet. Management strategies based on flavor generalization, repeated exposure,and social facilitation will undoubtedly be effective in increasing the acceptance ofnovel foods by ruminants.

ReferencesCapretta, P.J., 1977. Establishment of food preferences by exposure to ingestive stimuli early in life. In:

Barker, L.M., Best, M.R., Domjon, M. (Eds.), Learning Mechanisms in Food Selection. Baylor UnivesityPress, Waco, pp. 99-122.

Chapple, RX, Lynch, J.J., 1986. Behavioural factors modifying acceptance of supplementary fcods by sheep.Res. Dev. Agric. 3, 113-120.

Chapple, R.S., Wadzicka-Tomanszewska, M., Lynch, J.J., 1987. The learning behavior of sheep whenintroduced to wheat. I. Wheat acceptance by sheep and the effect of trough familiarity. Appl. Anim. Behav.Sci. 18, 157-162.

Cole, N.A., McLaren, J.B., Hutcheson, D.P., 1982. Influence of preweaning and B-vitamin supplementation ofthe feedlot receiveing diet on calves subjected to marketing and transit stress. J. Anim. Sci. 54, 911-917.

duToit, J.T., Provenza, F.D., Nastis, A., 1991. Conditioned taste aversions: how sick must a ruminant getbefore it learns about toxicity in foods? Appl. Anim. Behav. Sci. 30, 35-46.

Gill, J.L., 1978. Design and Analysis of Experiments in Animal and Medical Sciences, vol. 1. Iowa StateUniversity Press, Ames, pp. 169-259.

Hicks, C.R., 1982. Fundamental Concepts in the Design of Experiments. Saunders College Publishing, FortWorth, TX, pp. 239-244.

Hicks, R.B., Owens, F.N., Gill, D.R., Oltjen, J.W., Lake, R.P., 1990. Dry matter intake by feedlot beef steers:influence of initial weight, time on feed and season of year received in yard. J. Anim. Sci. 68, 254-265.

Launchbaugh, K.L., 1995. Effects of neophobia and aversions on food intake: why feedlot cattle sometimesrefuse to eat nutritious feeds. In: F.N. Owens (Ed.), Intake by Feedlot Cattle: Symposium Proceedings.Oklahoma Agriculture Experiment Station, Publication No. P-942, pp. 36-47.

Launchbaugh, K.L., Provenza, F.D., 1994. The effects of flavor concentration and toxin dose on the formationand generalization of flavor aversions in lambs. J. Anim. Sci. 72, 10-13.

Mazur, J.E., 1990. Learning and Behavior. Prentice Hall, Englewood Cliffs, NJ, pp. 54-81.National Research Council (NRC), 1985. Nutrient Requirements of Sheep. National Academy Press, Washing-

ton, DC, pp. 54-73.Ortega-Reyes, L., Provenza, F.D., Parker, C.F., Hatfield, P.G., 1992. Drylot performance and ruminal papillae

development of lambs exposed to a high concentration diet while nursing. Small Ruminant Res. 7,101-112.

Provenza, F.D., 1996. Acquired aversions as the basis for the varied diets of ruminants foraging on rangelands.J. Anim. Sci. 74, 2010-2020.Provenza, F.D., Balph, D.F., 1988. Development of dietary choice in livestock on rangeland and itsimplications for management. J. Anim. Sci. 66, 2356-2368.


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Provenza, F.D., Balph, D.F., Olsen, J.D., Dwyer, D.D., Ralphs, M.H., Pfister, J.A., 1988. Toward understand-ing the behavioral responses of livestock to poisonous plants. In: James, L.F., Ralphs, M.H., Nielson, D.B.(Eds.), The Ecology and Economic Impact of Poisonous Plants on Livestock Production. Westview Press,Boulder, CO, pp. 407-424.

Provenza, F.D., Lynch, J.J., Cheney, C.D., 1995. Effects of a flavor and food restriction on the response ofsheep to novel foods. Appl. Anim. Behav. Sci. 43, 83-93.

Rozin, P., 1977. The significance of learning mechanisms in food selection: some biology, psychology, andsociology of science. In: Barker, L.M., Best, M.R., Domjon, M. (Eds.), Learning Mechanisms in FoodSelection. Baylor University Press, Waco, TX, pp. 557-589.

Squibb, R.C., Provenza, F.D., Balph, D.F., 1990. Effect of age of exposure on consumption of a shrub bysheep. J. Anim. Sci. 68, 987-997.

Steel, R.G., Torrie, J.H., 1960. Principles and Procedures of Statistics: With Special Reference to theBiological Sciences. McGraw-Hill, New York, pp. 106-107.

Thorhallsdottir, A.G., Provenza, F.D., Balph, D.F., 1987. Food aversion learning in lambs with or without amother: discrimination, novelty and persistence. Appl. Anim. Behav. Sci. 18, 327-340.

Thorhallsdottir, A.G., Provenza, F.D., Balph, D.F., 1990. Ability of lambs to learn about novel foods whileobserving or participating with social models. Appl. Anim. Behav. Sci. 25, 25-33.Villalba, J.J., Provenza, F.D., 1997. Preference for wheat straw by lambs conditioned with intraruminalinfusions of starch. Br. J. Nutr. 77, 287-297.

Zinn, R.A., Dunbar, J.R., Norman, B.B., 1988. Influence of pelleting on the comparative feeding value ofcottonseed meal in receiving diets for feedlot calves. J. Anim. Sci. 66, 1335-1339.

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