Dietary flavor modifies oil preferences in the chicken

APPLIED ANIMAL BEHAVIOUR SCIENCE

ELSEVIER

Applied Animal Behaviour

Science 49 ( 1996) 2 13-22

1

Dietary flavor modifies oil preferences in the chicken Remedios T. Mabayo, Jun-ichi Okumura, Mitsuhiro Furuse Laboratory

of Animal Nutrition,

School of Agriculture,

Accepted

6 February

Nagoya Uniuersity. Nagoya 464-01,

*

Japan

1996

Abstract The effect of dietary flavor on the preference for diets containing 20% medium-chain triacylglycerol (MCT) or long-chain triacylglycerol (LCT) was investigated in the chicken. A series of experiments using birds pre-fed with a flavored basal pre-feeding diet or an MCT diet was done to identify the role of dietary flavor on the food selection of flavored LCT (FLCT) or flavored MCT (FMCT) in chickens. The basal pre-feeding diet contained 3% LCT and the MCT pre-feeding diet contained 20% MCT. Using FLCT or FMCT, the birds showed a significant preference for non-flavored diets over flavored diets. The pre-feeding diet changed the pattern of diet preference, which implies that chickens can be trained to prefer a diet which was disliked over another. It is concluded that flavor controls the preference of diets containing MCT or LCT in chickens. Keywords:

Chicken;

Feeding and nutrition;

Taste; Triglyceride

1. Introduction

A diet high in medium-chain triacylglycerol (MCT) decreases food intake in chickens as compared with a diet high in long-chain triacylglycerol (LCT) (Furuse et al., 1992b; Mabayo et al., 1994). Under self-choice feeding conditions, chickens prefer an LCT diet over an MCT diet (Furuse et al., 1993), although the same preference is not shown by rats (Furuse et al., 1992a). Species differences are an important factor in the differing results obtained from studies in which an attempt is made to modify food preferences. In mammals, most hypothalamic and amygdaloid lesions affect the manifestation or acquisition of food preferences (Le Magnen, 1992) but there is little to suggest that the hypothalamus plays a similar role in the control of food intake in fowls (Sykes, 1983).

* Corresponding

author

0168-1591/96/$15.00 Copyright PII SO168-1591(96)01047-7

0 1996 Elsevier Science B.V. All rights reserved.

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Color, taste, smell, and other physical properties of food can influence intake, especially in situations in which a choice can be made (Gentle, 1979). In birds, the sense of smell is not highly developed (Kare, 19651, but chickens do have the ability to discriminate between certain tastes or flavors (Nesheim et al., 1979). Affective responses to odors are an important part of the behavioral role of olfaction (Garcia and Brett, 1977), and it is claimed that the olfactory system of birds is functional (Tucker, 1965; Stattelman et al., 1975). The removal of the olfactory bulbs in the chicken causes a marked increase in food intake (Robinzon et al., 1977). In a preliminary experiment, the effects of olfactory bulbectomy and cutting the bilateral olfactory nerves on the food selection of chicks given dietary MCT and LCT were investigated. These treatments caused the strong preference for the LCT diet over the MCT diet to disappear (Mabayo et al., 1996). It is likely that gustatory cues play a role in the preference of diets containing MCT or LCT in chickens. In this study, therefore, the effect of dietary flavor in the preference of chickens for diets containing LCT or MCT was investigated.

2. Animals, materials and methods 2.1. General methods Day-old Single Comb White Leghorn male chicks (Hattori Hatchery, Ltd., Nagoya, Japan) were housed in a windowless house with a controlled temperature kept constantly at 30°C. Lighting was provided continuously. The birds were reared in stainless steel metabolism cages (25 cm X 21 cm X 19 cm) and were given a commercial chick mash (corn-fish meal and soybean based, 2830 kcal kg-‘, 21% crude protein; Marubeni Shiryo Co., Tokyo, Japan). Two or 3days before the start of each experiment, the chickens were fasted overnight (about 14 h) with free access to water, and were selected so that mean body weights were as uniform as possible. All chickens were offered a semipurified pre-feeding diet in uniform feeders (70 mm X 115 mm X 150 mm (depth)). The pre-feeding diet contained (in g kg-’ >: isolated soybean protein, 238; sucrose, 200; corn oil, 30; cellulose, 30; mineral mixture, 58.5; vitamin mixture, 2; choline chloride, 1.5; DL-methionine, 5; glycine, 2.5; corn starch, 432.5. During the experiment, the fasted birds were again selected and distributed into groups and all chickens in each group were allocated at random to individual metabolism cages. Each bird was offered the experimental diets in a self-choice pair of feeding troughs (70 mm X 8 mm X 50 mm (depth)) plus a waterer. Choices were made among MCT, flavored MCT (FMCT), LCT and flavored LCT (FLCT) diets. The composition of experimental non-flavored diets is shown in Table 1. Corn oil (Wake Pure Chemical Industries, Osaka, Japan) was used as LCT source and glyceryl tricaptylate was used as MCT source. The MCT source in this study was donated by Kao Corporation, to Wakayama, Japan. The 20 g corn oil kg -i diet in the MCT diet was supplemented meet the requirement for essential fatty acids. In flavored diets, the food flavor, Corn Q-4001@ (donated by Kao Corporation, Wakayama, Japan), was added to MCT or LCT diet at 0.02% (200ppm). The flavor used was to mask the smell of MCT and mimic the

R.T. Mabayo et al./Applied Table 1 Composition

of experimental

Ingredient Isolated soybean protein Mineral mixture b Vitamin mixture ’ Choline chloride Inositol L-Methionine L-Threonine Glycine Cellulose Corn starch Corn oil Coconado RK @ d

diets (g kg-

Animal Behauiour Science 49 (1996) 213-221

21.5

’) LCT a

MCT a 226 58.8 2

1.5 1 2.9 1.2 4.2 100 402.4 20 180

200 0

a MCT, medium-chain triacylglycerol; LCT, long-chain triacyiglycerol. bContained 20.7g CaHPO,.2H,O, 14.8g CaCO,, log K,HPO,, 3g KCI, 6g NaCI, 3g MgSO,, 0.5g FeS0,.7H20, 0.35g MnSO,.SH,O, 2.6mg K1, 40mg CuSO,.5H,O, 62mg ZnO, 1.7mg Na,MoO,.2HrO, 0.4mg Na,SeO, and 0.93 mg CoCl,. ’ Contained 15 mg calcium pantothenate, 6mg riboflavin, 4mg pyridoxine hydrochloride, 40mg nicotinic acid, 1.5 mg folic acid, 0.2mg biotin, 0.02mg cyanocobalamin, 3mg thiamin hydrochloride, 2001CU vitamin D,, 0.5 mg vitamin K,, and 1.93g glucose. The DL-cr-tocopheryl acetate (1OII.J) and retinyl acetate (17OOR.J) were dissolved in corn oil. d Coconado RKa, glyceryl tricaprylate (donated by Kao Corp., Wakayama, Japan).

smell of corn oil (LCT), because birds had been found to prefer the LCT diet over the MCT diet in a previous study (Furuse et al., 1993). During the experiment, birds were offered a self-choice feeding between diets specified below. Food intake was measured after 30, 60, 120, 180 and 360 min of feeding. The position of the feeders was changed after every food intake measurement to prevent the birds from pecking at one position. A paper pad was placed under the cage to collect spilled food and the collected food was returned to each feeder whenever food intake was measured. 2.2. Effects of dietary flavor on the food selection of chickens under self-choice feeding conditions The effects of dietary flavor on food selection of chickens 17-19 days of age under self-choice feeding conditions were examined. Group 1 was offered choices between FLCT and MCT (A, body weigh; with SEM, 145 f 2.2g), LCT and FMCT (B, 144 + 2.7 g) and between FLCT and FMCT (C, 143 + 1.3 g). Group 2 was given a flavored pre-feeding diet before the experiment and the birds were offered a choice between LCT and MCT, FLCT and MCT, LCT and FMCT and between FLCT and FMCT for Subgroups A (153 f 2.9g), B (153 + 2.7g), C (153 f 2.9g) and D (153 Ifr 2.8 g), respectively. Group 3 was pre-fed with MCT diet and was offered the same choices as Group 2. Mean body weights for Subgroups A, B, C and D were 159 f 3.5 g, 159 f 3.6g, 160 f 3.5 g and 160 + 3.5 g, respectively. Five birds were used per treatment.

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Time after feeding (min) Fig. 1. Cumulative food intake of birds (16days old) offered a self-choice feeding between (A) FACT and MCT, (B) LCT and FACT and (C) FLCT and FMCT diets. Values are means of five birds f SEM. ‘P < 0.05 shows significant difference between values at the same time period within panels. The effect of diet was significant in (A) (P < 0.05) and (B) (P < 0.001). Significant interaction was observed between time and diet in (B) (P < 0.001). LCT, Long-chain triacylglycerol; MCT, medium-chain triacylglycerol; FLCT, flavored long-chain triacylglycerol; FMCT, flavored medium-chain triacylglycerol.

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2.3. Comparison of food selection between flavored triacylglycerol composition in chickens

and non-flavored

diets of the same

In the preceding experiments, the birds allowed to choose between any diet and FLCT diet tended to avoid the FLCT diet. For this reason, 20 birds (ten birds per treatment; 21 days old) were offered a choice between FMCT and MCT (A, 188 + 1.7 g) and between FLCT and LCT (B, 188 f 1.7 g) to compare the food selection of chicks provided flavored and non-flavored diets of the same oil composition. 2.4. Statistics Data on food intake were analyzed by split-plot design by taking bird as a main plot and time as a subplot @AS, 1985). Comparison of means was performed by t-test only after a significant interaction between diet and time was found.

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Fig. 2. Cumulative food intake of birds (17days old) pre-fed with flavored basal pre-feeding diet for 2days and offered a self-choice feeding between (A) LCT and MCT, (B) FJCT and MCT, (C) LCT and FACT and (D) FLCT and FMCT diets. Values are means of five birds kSEM. * P < 0.05 shows significant difference between values at the same time period within panels. Significant interaction was observed between time and diet in (B) (P < 0.01). LCT, Long-chain triacylglycerol; MCT, medium-chain triacylglycerol; FLCT, flavored long-chain triacylglycerol; FMCT, flavored medium-chain triacylglycerol.

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3. Results Fig. 1 shows the cumulative food intake of chickens offered a choice between FLCT and MCT (A), FMCT and LCT (B) and between FMCT and FLCT diets (C). Fig. l(A) shows that the birds preferred the MCT diet to the FLCT diet (P < 0.05). A significant interaction between time and diet was observed for the comparison of FXCT and MCT, indicating that difference in intake between FLCT and MCT increased as time went on. Fig. l(B) shows that food intake of chickens given the LCT diet was significantly higher than that of chickens given the FMCT diet throughout the feeding period (P < 0.01). A significant interaction between diet and time was observed (P < 0.001) in this treatment. There was no significant difference in food intake of birds fed the FLCT and FMCT diets (Fig. l(C)).-

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Fig. 3. Cumulative food intake of birds (18days old) pre-fed with MCT diet for Zdays and offered a self-choice feeding between (A) LCT and MCT, (B) FACT and MCT, (C) LCT and FMCT and (D) FLCT and FMCT diets. Values are. means of five birds f SEM. * P < 0.05 shows significant difference between values at the same time. period within panels. Significant interaction was observed between time and diet in (B) (P < 0.001). LCT, Long-chain triacylglycerol; MCT, medium-chain ttiacylglycerol; FLCT, flavored long-chain triacylglycerol; FMCT, flavored medium-chain triacylglycerol.

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4. Discussion Chickens reduce their food intake when levels of MCT are high in the diet (Furuse et al., 1992b; Mabayo et al., 1994). One factor influencing this effect is the delayed forward movement of the crop contents (Mabayo et al., 1992). The mechanism of this effect is not yet understood. Under self-choice feeding conditions, chickens show a preference for an LCT over an MCT diet (Furuse et al., 1993). Recently, the role of olfaction in oil preference in rats was identified; olfactory bulbectomy reduces the preference for oil emulsions (Ramirez, 1993). Our data (Mabayo et al., 1996) show that intact and sham bulbectomized chicks have a strong preference for LCT over MCT. MCT has a rancid odor that influences avoidance in chickens. Chicks that are bulbectomized or whose bilateral olfactory nerves are cut, however, lose their strong preference for LCT and tend to feed on MCT as intensively as on LCT. The purpose of using the artificial flavor of corn oil was to confirm that the avoidance on MCT was also dependent on olfaction. The chickens, however, showed preference for non-flavored diets over flavored diets. There was no preference between FMCT and FLCT. This may mean that the flavored diets were offensive to the chickens. It is claimed that taste has not been shown to be important in making food attractive for poultry (Nesheim et al., 1979). The addition of the corn flavor to the LCT diet (which originally had a pleasant flavor) rendered it definitely unpleasant owing to its offensive taste and smell. It was not also proven that the flavor used effectively masked the odor and taste of the MCT diet, and it may only be that the flavor was different from the real corn oil flavor. The different pre-feeding diets used affected the diet preference of the chicken. When the flavored pre-feeding diet was used, the significant preference for LCT over MCT disappeared. This could have been caused by the aversive effect of the flavor used so that the birds lost their strong preference for the real LCT diet. The use of MCT diet as a pre-feeding diet conditioned the birds so that they strongly preferred MCT over FLCT. The birds offered a choice between FMCT and LCT lost their strong preference for LCT. When birds are trained to peck on a less appealing food (i.e. MCT), and then offered a choice between such food and an appealing food (i.e. LCT), the less appealing food could compete with the appealing food for consumption. Although MCT has a rancid odor, the aversion to MCT in rats (Furuse et al., 1992a) is not as intense as it is in chickens (Furuse et al., 1993). In a rat study, it was suggested that the preference for triolein over corn oil was influenced by impurities in the oil (Ramirez, 1992). In chickens, however, olfactory information was of more importance. Although it has been reported that the chicken has few taste buds and a poor sense of smell (Kare, 1965), the chicken has more taste buds than previously believed (Ganchrow and Ganchrow, 1985). Accordingly, another possibility must be considered, that the taste aversion may be induced by the flavor used in the present study apart from olfaction. Turro et al. (1994) showed that chicks are capable of associating specific food odors with negative consequences, and modify their feeding behavior as a function of such experience. This possibility remains to be investigated. In any event, it is concluded that dietary flavor modifies oil preference in the chicken.

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References Furuse, M., Choi, Y.H., Mabayo, R.T., Denbow, M., Okumura, J., 1992a. Feeding behavior in rats fed diets containing medium chain triglyceride. Physiol. Behav., 52: 815-817 Furuse, M., Mabayo, R.T., Kita, K., Okumura, J., 199213. Effects of dietary medium chain triglycerides on protein and energy utilisation of chicks. Br. Pouh. Sci., 33: 39-47 Furuse, M., Mabayo, R.T., Choi, Y.H. and Okumura, J., 1993. Feeding behavior in chicks given diets containing medium chain triglyceride. Br. Pouh. Sci., 34: 21 l-217. Ganchrow, D. and Ganchrow, J.R., 1985. Number and distribution of taste buds in the oral cavity of hatching chicks. Physiol. Behav., 34: 889-894. Garcia, J. and Brett, L.P., 1977. Conditioned responses to food odour and taste in rats and wild predators. In: M.R. Kare and 0. Maller (Editors), The Chemical Senses and Nutrition. Academic Press, NY, pp. 71-I 10. Gentle, M.J., 1979. Sensory control of food intake. In: K.N. Boorman and B.M. Freeman (Editors), Food Intake Regulation in Poultry. British Poultry Science, Edinburgh, pp. 259-273. Kare, M.R., 1965. Special senses. In: P.D. Sturkie (Editor), Avian Physiology. 2nd edn., Comstock, New York, pp. 406-466. Le Magnen, J., 1992. Neurobiology of Feeding and Nutrition. Academic Press, San Diego, CA, pp. 191-215. Mabayo, R.T., Furuse, M., Yang, S.I. and Okumura, J., 1992. Medium chain triacylglycerols enhance release of cholecystokinin in chicks. J. Nutr., 122: 1702-1705. Mabayo, R.T., Furuse, M., Murai, A. and Okumura, J., 1994. Interactions between medium chain and long chain triacylglycerols in the lipid and energy metabolism in growing chicks, Lipids, 29: 139-144. Mabayo, R.T., Okumura, J., Hirao, A., Sugita, S., Sugahara, K. and Furuse, M., 1996. The role of olfaction in oil preference in the chicken. Physiol. Behav., 59: in press. Nesheim, M.C., Austic, R.E. and Card, L.E., 1979. Poultry Production. 12th edn., Lea and Febiger, Philadelphia, PA, pp. 16-57. Ramirez, I., 1992. Chemoreception for fat: do rats sense triglycerides directly?. Appetite, 18: 193-206. Ramirez, I., 1993. Role of olfaction in starch and oil preference. Am. J. Physiol., 265: R1404R1409. Robinzon, B., Snapir, N. and Perck, M., 1977. Removal of olfactory bulbs in chickens: consequent changes in food intake and thyroid activity. Brain Res. Bull., 2: 263-271. SAS Institute, Inc., 1985. SAS User’s Guide: Statistics. SAS Institute, Inc., Gary, NC. Stattelman, A.J., Talbot, R.B. and Coulter, D.B., 1975. Olfactory thresholds of pigeons (Cohmba liuia), quail (Colinus uirginianus) and chickens (Callus gallus). Comp. B&hem. Physiol., 50A: 807-809. Sykes, A.H., 1983. Food intake and its control. In: B.M. Freeman (Editor), Physiology and Biochemistry of Domestic Fowl, Vol. 4. Academic Press, London, pp. l-29. Tucker, D., 1965. Electrophysiological evidence for olfactory function in birds. Nature, 207: 34-36. Turro, I., Porter, R.H. and Picard, M., 1994. Olfactory cues mediate food selection by young chicks. Physiol. Behav.. 55: 761-767