Feeding Behavior and Performance of Lambs Are Influenced by Flavor Diversity

J. J. Villalba, A. Bach and I. R. IpharraguerreFeeding behavior and performance of lambs are influenced by flavor diversity

doi: 10.2527/jas.2010-3435 originally published online March 31, 20112011, 89:2571-2581.J ANIM SCI

http://www.journalofanimalscience.org/content/89/8/2571the World Wide Web at:

The online version of this article, along with updated information and services, is located on

www.asas.org

by guest on January 23, 2014www.journalofanimalscience.orgDownloaded from by guest on January 23, 2014www.journalofanimalscience.orgDownloaded from

Feeding behavior and performance of lambs are influenced by flavor diversity1,2

J. J. Villalba,*3 A. Bach, and I. R. Ipharraguerre

*Department of Wildland Resources, Utah State University, Logan 84322-5230; Instituci Catalana de Recerca i Estudis Avanats (ICREA) and Institut de Recerca i Tecnologia Agroalimentries (IRTA),

Ruminant Production, Caldes de Montbui 08140, Spain; and Lucta, S.A. Montorns del Valls 08170, Spain

ABSTRACT: This study determined whether early experiences of sheep with the same feed, but presented in multiple or single flavors, would influence intake, the profile of hormones involved in feed intake regulation, and the subsequent acceptability of novel feeds. Thirty-five 2-mo-old lambs were randomly assigned to 5 treat-ments (7 lambs/treatment). Lambs in 1 treatment (the diversity treatment) were simultaneously fed an unfla-vored plain ration of alfalfa (control) and barley (75:25; as-fed basis) and the same ration mixed (0.2%) with 1 of 3 flavors: 1) sweet, 2) umami, or 3) bitter. The other 4 treatments (monotonous diets) received only 1 of the 4 rations. All animals were fed their respective rations from 0800 to 1600 h for 60 d. On d 55, intake was re-corded every 30 min for 8 h. On d 58, blood samples from lambs were collected at 1 h prefeeding and at 30, 60, 210, 300, and 540 min postfeeding. Preference tests were conducted by simultaneously offering novel feeds: 1) high-energy feed, 2) high-protein feed, 3) beet pulp mixed with phytochemicals, or 4) low-quality feed. Lambs in the diversity treatment consumed more feed than did lambs in the other treatments (P < 0.001). Lambs in the diversity treatment consumed equiva-lent amounts of plain and umami feeds, with a greater amount (P < 0.001) of the umami feed being consumed than the bitter and sweet feeds. Lambs in the diversity

treatment tended to grow faster than did lambs in the other treatments (P = 0.06). On d 55, lambs in the di-versity treatment showed decreased (P < 0.05) feed in-take compared with lambs in the other treatments dur-ing the 2 peaks of food consumption (30 and 270 min from feeding) and showed a trend for the least plasma concentrations of ghrelin (P = 0.06). In contrast, lambs in the diversity treatment consumed more feed than did lambs exposed to monotonous flavors at 60, 90, 120, and 180 min from feeding (P < 0.05). Lambs in the diversity treatment also showed the least concentra-tions of cholecystokinin and glucagon-like peptide 1 (P < 0.001). There were trends for the greatest concen-trations of leptin (P = 0.14) and IGF-1 (P = 0.16) in the diversity treatment, and for the least concentration of leptin in the bitter treatment (P = 0.14). Previous experience with flavored feeds affected the preference of lambs for high-energy and low-quality feeds, and for beet pulp mixed with phytochemicals (treatment feed day effect; P < 0.05). Thus, exposure to diverse flavors has the potential to increase feed intake and induce a more even consumption of feed across time by reducing peaks and nadirs of intake compared with exposure to monotonous rations. Flavor diversity may also influence the initial acceptability of and preference for novel feeds.

Key words: diversity, eating pattern flavor, hormone, intake regulation, sheep

2011 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2011. 89:25712581 doi:10.2527/jas.2010-3435

INTRODUCTION

Ruminants evolved in diverse environments, consum-ing arrays of feeds of different chemical and physical characteristics (Provenza et al., 2007). Nevertheless, current intensive feeding systems are characterized by feeding animals monotonous diets. Evidence from rats and humans indicates that a repeated presenta-tion of the same feed may result in a reduction in feed intake (McSweeney and Swindell, 1999). At meal ini-tiation, chemical senses (i.e., smell and taste) generate oro-sensorial signals that trigger satiety (Blundell et

1 This research was supported by grants from Lucta S.A. (Mon-torns del Valls, Spain) and the Utah Agricultural Experiment Station (Logan). This paper is published with the approval of the Director, Utah Agricultural Experiment Station, and Utah State University, as journal paper number 8234.

2 We acknowledge R. Stott (Utah State University, Logan) for vet-erinary services.

3 Corresponding author: [email protected] August 16, 2010.Accepted March 17, 2011.

2571

by guest on January 23, 2014www.journalofanimalscience.orgDownloaded from

al., 1994) through a decline in wanting (related to ap-petite) or liking (related to pleasure, palatability, or hedonism) of the consumed feed. This process, known as sensory-specific satiety (Rolls et al., 1982), has been shown to play a role in regulating feed consumption in humans (Srensen et al., 2003). In contrast, diverse oro-sensorial stimuli may restore the motivation to eat (Epstein et al., 2009) by enhancing feed acceptability (Rolls, 1979; Treit et al., 1983). This effect may lead to changes in feeding frequency and in the hormonal profiles involved in feed intake regulation (Bello et al., 2009). Furthermore, offering feeds in various flavors to postpubertal heifers altered short-term feed preferences (Atwood et al., 2001). Because experiences during de-velopment induce lifelong neurological, morphological, or physiological changes (Provenza and Villalba, 2006), providing oro-sensorial diversity early in life may have more pronounced effects than doing so at later stages of life (Nolte and Provenza, 1992).

The hypothesis of this study was that providing oro-sensorial diversity to ruminants after weaning would alter feeding behavior, resulting in enhanced feed in-take and animal performance. To test this hypothesis, lambs were fed the same diet in single (monotonous) or multiple (diversity) flavors, and changes in feed intake, BW, feeding pattern, some appetite-controlling hor-mones, and preferences for novel feeds were monitored.

MATERIALS AND METHODS

The study was conducted at the Green Canyon Ecol-ogy Center, located at Utah State University in Logan, according to procedures approved by the Utah State University Institutional Animal Care and Use Commit-tee.

Animals and Dietary Treatments

During the study, 35 commercial Finn-Columbia-Polypay-Suffolk crossbred lambs of both sexes (2 mo of age) with an average initial BW of 25 1 kg were individually penned outdoors, under a protective roof,

in individual, adjacent pens measuring 2.4 3.6 m. Throughout the study, lambs had free access to fresh water and trace mineral salt blocks. Lambs were famil-iar with alfalfa and barley grain because these feeds constituted the basal diet of their mothers. Animals were weaned and introduced into their individual pens and were fed alfalfa pellets ad libitum and 300 g/d of barley grain for 12 d until the beginning of the study. Lambs were randomly divided into 5 treatments (7 lambs/treatment) and conditioned with different senso-rial experiences. Lambs in 1 treatment (diversity) were simultaneously fed an unflavored ration (plain) of al-falfa and barley [75:25; 2.9 Mcal/kg; 15% CP (AOAC, 2002)] and the same ration presented in 3 different non-nutritive flavors (0.2%): 1) sweet, 2) umami, and 3) bit-ter (Lucta, S.A., Montorns del Valls, Spain). Lambs in the other 4 treatments (monotonous diets) received only 1 of the 3 flavored feeds or the plain diet through-out the study. All lambs had ad libitum access to their respective treatment diets from 0800 to 1600 h for 60 d. Additional feed was added at 1200 h when refusals were below 10% of the amount initially offered. Daily refusals were weighed, and daily intake was expressed per kilogram of metabolic BW. Lambs were weighed on d 1, 33, and 60 of the study (Table 1).

Feeding Behavior and Blood Sampling

On d 55, lambs were fed at 0800 h and feed intake was measured every 30 min for 8 h as an estimate of feeding behavior throughout the day (Table 1). On d 56, all lambs were fed at 0800 h and 1 observer recorded eating behavior using the scan sampling method de-scribed by Altman (1974; Table 1). Scan samples were taken at 5-min intervals for a period of 8 h to record bouts of feeding and inactivity. Frequency of feeding was calculated as a percentage of the total number of scans recorded. On d 57, three randomly chosen ani-mals within each treatment were fitted with indwelling catheters in the left jugular vein (1.4 mm i.d., 1.7 mm o.d.; Abbott Laboratories, Abbott Park, IL). On d 58, 10 mL of blood was collected into heparinized tubes

Table 1. Chronology, feeds offered, and measurements in the study

Day Feeds offered Measurement

1 to 60 A plain ration of alfalfa and barley (75:25; plain treatment); the same ration mixed with sweet, umami, or bitter flavors; or a simultaneous offer of the 4 flavored feeds (diversity treatment)

Feed intake from 0800 to 1600 h (d 1 to 60); feed intake measured every 30 min from 0800 to 1600 h (d 55); scan samples at 5-min intervals from 0800 to 1600 h (d 56); blood extractions for hormone analyses (d 58); BW (d 1, 33, and 60)

61 to 105 Ad libitum intake of alfalfa pellets 106 to 109 A simultaneous offer of feeds high in energy1 Feed intake from 0800 to 0815 h110 to 113 A simultaneous offer of feeds high in protein2 Feed intake from 0800 to 0815 h114 to 117 A simultaneous offer of phytochemical-enriched feeds3 Feed intake from 0800 to 0815 h118 to 121 A simultaneous offer of feeds of low quality4 Feed intake from 0800 to 0815 h

1Oats, milo, beet pulp, and corn.2Wheat gluten meal, rabbit pellets, Calf-Manna (Manna Pro Products, Chesterfield, MO), and soybean meal.3Beet pulp mixed with condensed quebracho tannin powder (10%), quillaja bark saponin powder (2%), and sagebrush terpenes (1.8% camphor,

1.1% 1,8-cineole, and 0.1% p-cymene).4Wheat straw, wheat bran, and grape pomace.

2572 Villalba et al.


(Freeze-Dried Sodium Heparin, 143 USP units, BD Va-cutainer, Franklin Lakes, NJ) from catheters at 1 h prefeeding and at 30, 60, 210, 300, and 540 min post-feeding. Samples were immediately centrifuged at 3,000 g for 15 min at 4C to harvest plasma, and samples were subsequently stored at 30C until analyses for ghrelin, insulin, leptin, IGF-1, glucagon-like peptide 1 (GLP-1), and cholecystokinin (CCK). Insulin deter-minations were conducted using RIA with an RI-13K kit (Millipore, Bedford, MA) with intra- and interassay CV of 3.0 and 9.0%, respectively. Leptin was also ana-lyzed by RIA using an XL-85K multispecies kit (Milli-pore) with resulting intra- and interassay CV of 7.6 and 7.8%, respectively. Insulin growth factor-1 was deter-mined using ELISA with an AC-27F1 kit (IDS, Foun-tain Hills, AZ) with intra- and interassay CV of 2.0 and 3.4%, respectively. Ghrelin was analyzed by RIA with an R90 kit (Mediagnost, Reutlingen, Germany) with intra- and interassay CV of 9.3 and 6.8%, respectively. Cholecystokinin was also determined using RIA with an RB302 kit (IBL International, Hamburg, Germany) with intra- and interassay CV of 2.5 and 8.9%, respec-tively. Likewise, GLP-1 was determined by RIA with an RK-028-13 kit (Phoenix Pharmaceuticals Inc., Burlin-game, CA) with an intraassay CV of 4.0%.

Preference Tests for Novel Feeds

On d 61, all animals were offered alfalfa pellets for ad libitum intake for 45 d (Table 1). During this washout period all animals had the same basal diet and flavor experiences before being tested for their preferences for novel feeds. The aim was to ensure that differences in feeding responses to novel feeds could be attributed to the treatments that animals experienced early in life and not to the short-term effects of flavors consumed before testing.

Four series of tests were conducted to determine whether different experiences with flavors (i.e., diverse or monotonous diets) after weaning affected the pref-erence and acceptance of novel feeds (Table 1). The intake and preference for each feed were determined by simultaneously offering all tested feeds ground to 1- to 2-mm particle size to all lambs for 15 min at 0800 h to establish the initial neophobic response of the animals to the feeds. Subsequently, all lambs had ac-cess to alfalfa pellets until 1600 h. Preference tests were conducted for 4 consecutive days. In test 1, lambs were presented with feeds high in energy (whole oats, whole milo, beet pulp, and corn); in test 2, they received feeds high in protein [wheat gluten meal, rabbit pellets, Calf-Manna (Manna Pro Products, Chesterfield, MO), and soybean meal]; in test 3, animals were offered beet pulp mixed with phytochemicals [condensed quebracho tan-nin powder (10%), quillaja bark saponin powder (2%), and sagebrush terpenes (Sigma, St. Louis, MO; 1.8% camphor, 1.1% 1,8-cineole, and 0.1% p-cymene mixed in 4% vegetable oil)]; and in test 4, lambs had access to feeds of low quality (wheat straw, wheat bran, and

grape pomace; Table 2). The study began on May 26, 2009 (dietary treatments), and ended on October 4, 2009 (preference tests for novel feeds).

Statistical Analyses

Feed intake (as-fed basis; g/kg of BW0.75), ADG, eating events (as percentages of the total number of scans), plasma hormone concentrations, and preference for novel feeds [(intake of feed/total intake) 100] dur-ing the preference tests were analyzed as a split-plot design with lambs (random factor) nested within treat-ment. Treatment (diversity, sweet, umami, bitter, or plain) was the between-animal factor, novel feed (pref-erence tests for novel feeds) was the within-animal fac-tor, and time (eating behavior) or day (feed intake) was the repeated measure in the analyses (fixed factors). The fixed effect of sex was included in the model but was later removed because of a lack of significant ef-fects (P > 0.10). Separate analyses were conducted for the diversity treatment to estimate lamb preferences for each flavored feed. In this case, animal and flavored feeds (sweet, umami, bitter, or plain) were the whole-plot factors and day was the repeated measure. All analyses were computed using a mixed-effects model (SAS Inst. Inc., Cary, NC). The variance-covariance structure used was the autoregressive order-1, which yielded the smallest Bayesian information criterion.

Table 2. Metabolizable energy, digestible protein, and crude fiber of novel feeds (DM basis) offered to 5 groups of lambs exposed during a 60-d period to the same feed offered in different flavors: plain, bitter, sweet, umami, and diversity (a simultaneous offer of the 4 flavored feeds)

Feed

Nutrient composition

ME, Mcal/kg

DP, %

Crude fiber, %

Feeds high in energy1 Whole oats 2.78 10.4 12.1 Whole milo 3.18 6.8 2.5 Beet pulp 2.78 6.7 16.5 Corn 3.15 6.5 2.2Feeds high in protein Wheat gluten meal2 3.2 39.8 4.8 Rabbit pellets3 2.2 14.6 15.2 Calf-Manna4 2.5 25.0 6.0 Soybean meal1 3.07 40.9 6.6Feeds of low quality Wheat straw1 1.48 3.5 41.6 Wheat bran1 2.57 13.3 11.3 Grape pomace5 1.09 0 47.1

1From NRC (1985).2Estimated values from corn gluten (NRC, 1985).3Calculated from NRC (1985). Rabbit pellets contain 15% barley,

7.5% wheat, 8.05% canola meal, 1.2% fat, 51.9% alfalfa, 10% wheat bran, and 6.35% minerals and premixes (Intermountain Farmers As-sociation, Salt Lake City, UT).

4Manna Pro Products (Chesterfield, MO).5Van Soest (1994).

2573Oro-sensorial diversity and feeding behavior


The model diagnostics included testing for a normal distribution of the error residuals and homogeneity of variance. Means were analyzed using pairwise differ-ences of least squares means.

RESULTS AND DISCUSSION

Intake and Performance

Averaged across the 60-d period, lambs receiving the diversity treatment consumed more (P < 0.001) feed than lambs receiving the monotonous diets (Table 3). It has been hypothesized that generalist herbivores, such as sheep, prefer a diversity of feeds because no single plant species in rangelands can provide for all of the nutrient demands of the animal (Westoby, 1974, 1978), and because generalist herbivores are unable to detoxi-fy large amounts of chemically similar plant secondary metabolites (Freeland and Janzen, 1974). Nevertheless, herbivores prefer a diversity of feeds and flavors even when nutritional needs can be met with single feeds or when toxins are not a concern (Early and Provenza, 1998; Atwood et al., 2001). An alternative explanation that encompasses this observation is that preference for a specific flavor decreases during ingestion, whereas liking for uneaten feeds remains unchanged, a phenom-enon known as sensory-specific satiety (Rolls, 1986). Thus, variety reduces the rate of habituation, lead-ing to an increase in intake relative to feed monotony (Epstein et al., 2009). The process of ingesting a feed induces satiety for that particular feed, motivating ani-mals to seek alternative feeds and flavors (Provenza, 1996). Exposure, even to a nutritionally balanced feed, can decrease preference for that feed in sheep and cat-tle, and the decrease in preference is more pronounced when the feed is nutritionally unbalanced (Early and Provenza, 1998; Atwood et al., 2001).

Increases in intake caused by feed variety could be mediated by sensory signals, postingestive signals, or both; consequently, the mechanisms underlying such a response could be confounded. In the current study, the postingestive effects were controlled because the same ration was used across treatments and nonnutritive fla-

vors were provided to create diversity. Likewise, feeding rats a high-energy diet containing a variety of flavors produced an increase in energy intake and BW gains (Treit et al., 1983; Naim et al., 1986). Collectively, the positive effects of variety on intake suggest that flavor diversity reduces the sensory-specific satiety induced by repeated exposure to the same flavored feed.

Lambs in the diversity treatment consumed equiva-lent amounts of the plain and umami diets, with uma-mi being consumed in greater amounts (P < 0.001) than the bitter and sweet diets (Table 4). The plain diet was the most familiar to the lambs because they had initially been exposed to alfalfa and barley along with their mothers. Moreover, given that the umami receptors can sense several AA and simple peptides that derive from the breakdown of proteins, it can be argued that the umami taste evolved to recognize pro-tein sources (Temussi, 2009). Growing ruminants may display a particular preference for umami feeds because their requirement for protein is high, and umami sig-nals the presence of protein (Luscombe-Marsh et al., 2008). Because growing ruminants have greater needs for protein, it is likely that this effect enhanced intake of the umami-flavored diet relative to the bitter- and sweet-flavored diets. In addition, the lesser preference for the bitter-tasting ration could be attributed to the anorectic effects of bitterness (Chen et al., 2006). The incapacity of the sweet diet to stimulate feed intake in the current study differs from results described else-where, which reported an increase in DMI in response to feeding sweetened diets to steers (McMeniman et al., 2006) or calves (Montoro et al., 2010). A potential explanation for the relatively low consumption of the sweet diet could be the fact that the sweet flavor was not associated with an increased caloric supply from the ration. Likewise, lambs exposed to a noncaloric sweetener (saccharin) associated with a flavor mani-fested decreased preferences for that flavor compared with lambs exposed to the same flavor but paired with calories from glucose (Burritt and Provenza, 1992). Nevertheless, lambs still preferred the umami flavor even when its ingestion was not associated with an increased reward (e.g., protein supply). One possible

Table 3. Feed intake and performance of 5 groups of lambs exposed during a 60-d period to the same feed offered in different flavors: plain, bitter, sweet, umami, and diversity (a simultaneous offer of the 4 flavored feeds)

Item

Treatment

SE

P-value1

Plain Bitter Sweet Umami Diversity2 Trt Time Trt time

Feed intake, g/kg of BW0.75 per day

110.16c 114.28b 110.13c 114.25b 119.21a 1.22

reason for this dichotomy may reside in the different neural mechanisms by which sweet and umami tastants signal reward. For instance, dopaminergic neurons of the midbrain, which have been implicated in the re-warding aspects of food, influence sucrose consumption but do not alter the consumption of umami compounds (Shibata et al., 2009). Additionally, it has been sug-gested that the sweet taste produced by some mono- or disaccharides is different from that induced by some glucose polymers and artificial sweeteners. This differ-ence is attributed to a differential activation of brain dopamine, serotonin receptor systems, or both involved in the learning of flavor preference (Bonacchi et al., 2008).

Total feed intake of lambs in the diversity treatment was affected by an interaction (P < 0.001) between time and treatment (Figure 1). No differences among treatments were observed until d 19 of the study, and then between d 19 and 43, lambs in the diversity treat-ment had the greatest intakes among all the treatments (P < 0.05); thereafter, from d 44 until the end of the period, feed consumption once again did not differ among treatments. From d 1 to 15, lambs in the diver-sity treatment selected primarily plain (18.4 2.5 g/kg of BW0.75) and umami (21.5 2.5 g/kg of BW0.75) feeds over sweet (15.0 2.5 g/kg of BW0.75) and bitter (15.5 2.5 g/kg of BW0.75) feeds, whereas from d 19 to 43, they displayed a more even consumption of flavors: 30.9, 35.5, 34.3, and 36.1 2.5 g/kg of BW0.75 for the bitter, plain, sweet, and umami feeds, respectively (fla-vor day; P < 0.001). This generalist effect during d 19 to 43 might have contributed to an enhancement of feed intake during that period. By d 58, however, the numerically greater concentrations of plasmatic leptin in the diversity treatment (Table 5) may have reduced the differences in feed intake among treatments toward the end of the 60-d period.

No differences in ADG were found among treatments, although lambs in the diversity treatment tended (P = 0.06) to grow faster than lambs in the other treatments (Table 3). Lambs in the diversity and plain treatments also tended (P = 0.051) to show a greater feed efficien-cy than those in the rest of the treatments (Table 3). As discussed below, these tendencies toward improved performance of lambs in the diversity treatment could be linked to increases in intake and changes in the eat-ing pattern.

Eating Pattern and Plasma Hormone Concentrations

When feed consumption was recorded at 30-min in-tervals during d 55, total feed intake was different (P < 0.05) among treatments across time (Figure 2). Animals showed 2 pronounced peaks of feed intake, coinciding with 30 and 270 min postfeeding (Figure 2). Lambs receiving a diversity of flavors (diversity treatment) showed less (P < 0.05) intake than those in the other treatments during the 2 peaks of feed consumption (i.e., at 30 and 270 min postfeeding). However, in agreement with the greater total daily intakes observed in the di-versity treatment (Table 3), lambs in this treatment consumed more (P < 0.01) feed than those exposed to monotonous flavors at 60 (diversity > plain, bitter, umami), 90 (diversity > plain, sweet, umami), 120 (di-versity > plain, bitter, sweet), and 180 min (diversity > plain, bitter, sweet, umami) after feeding (Figure 2). In addition, lambs offered a diversity of flavors consumed more (P < 0.05) umami (3.12 0.20 g/kg of BW0.75) and plain (2.84 0.20 g/kg of BW0.75) feeds than sweet (2.26 0.20 g/kg of BW0.75) and bitter (2.18 0.20 g/kg of BW0.75) feeds (data not shown). This pattern was a consequence of differences in the intake of fla-vored feeds observed after 30 (plain, umami > bitter, sweet), 60 (umami > bitter), 90 (plain > bitter), 180 (plain, umami > bitter), and 270 (bitter > sweet) min of feeding the rations (flavor time; P = 0.03). Results from the present study suggest that lambs exposed to a variety of flavors achieved greater intakes than animals exposed to single rations because they consumed more (P < 0.05) feed between the 2 peaks of consumption (at 30 and 270 min postfeeding) than did lambs ex-posed to monotonous diets. Alternating consumption of flavored feeds by lambs exposed to multiple flavors likely reduced the rate of consumption at peaks of feed intake (i.e., when animals exposed to monotonous diets likely manifested their greatest intake rate capacity). The process of exercising selectivity reduces the eating rate in ruminants (Chapman et al., 2007), an inefficien-cy that could not have occurred in treatments exposed to monotonous diets because they had no alternatives. Furthermore, because the orexigenic hormone ghrelin was reported to increase as the time that elapsed since the last meal increased (Shintani et al., 2001), the least plasma ghrelin concentrations observed in lambs in the

Table 4. Feed intake by a group of lambs (diversity treatment) exposed during a 60-d period to a simultaneous offer of the same feed in different flavors: plain, bitter, sweet, or umami1

Item

Treatment

SE

P-value2

Plain Bitter Sweet Umami Trt Time Trt time

Feed intake, g/kg of BW0.75 per day 31.0b 26.6c 28.3b 33.3a 0.56

diversity treatment, compared with those in the other treatments (Table 5), could be partly responsible for the reduced intake values at the 2 peaks of feed con-sumption (i.e., 30 and 270 min postfeeding). On the other hand, although values did not differ statistically, the decreased concentrations of the anorectic peptides CCK and GLP-1 in the plasma of lambs from the di-versity treatment, compared with those in the other treatments, might have caused a reduction in satiety between peaks of consumption (i.e., 60, 90, 120, and

180 postfeeding), allowing feed intake to increase at these times (Cummings and Overduin, 2007). In ad-dition, the simultaneous offer of preferred (palatable) flavors to lambs in the diversity treatment might have enhanced the activity of the endocannabinoid system, which, in turn, could delay the induction of satiety by CCK (Di Marzo and Matias, 2005). Alternatively, the increase in feed intake observed in lambs consuming a diversity of feeds may not have represented a com-pensation for reduced intakes at peaks of consumption,

Figure 1. Daily feed intake of lambs exposed to the same feed offered in different flavors: bitter, plain, sweet, umami, and diversity (a simul-taneous offer of the 4 flavored feeds). Between d 19 and 43, lambs in the diversity treatment had the greatest intakes among all treatments (P < 0.05). Values are means for 7 lambs; SE are represented by vertical bars.

Table 5. Plasma hormone concentrations as affected by dietary treatments

Item

Treatment

SE

P-value1

Plain Bitter Sweet Umami Diversity2 Trt Time Trt time

Insulin, ng/mL 0.62 0.76 0.72 0.89 0.82 0.067 0.13

but rather an enhancement in the daily consumption of feed. Results also showed that when offering a variety of flavors, feed intake was more evenly spread through-out the day. Because ruminants do not eat continuously throughout the day but eat in bouts (Burt and Dunton, 1967; Friggens et al., 1998), flavor variety may influence daily intake through changes in the distribution of feed-ing events over time (i.e., through changes in the feed-ing pattern). In addition, changes in feeding frequency may lead to physiological changes in the animal, such as a modification in the profiles of hormones involved in the control of feed intake (Bello et al., 2009) and nutrient utilization (Bunting et al., 1987). Lambs in the diversity treatment showed the greatest leptin and IGF-1 plasma concentrations (Table 5 and Figure 3, respectively) and lambs in the plain treatment showed the least plasma insulin concentrations at 200 and 300 min postfeeding (Figure 3), which would indicate that glucose supply at these times was low. The 3 hormones, leptin, IGF-1, and insulin, have been associated with the energy status (Chilliard et al., 2005) of the animal, and it would be reasonable to expect that a greater in-take would elicit an increase in plasma concentrations of these 3 hormones.

The bitter taste reduces palatability (Grovum and Chapman, 1988; Gherardi and Black, 1991) and in-creases CCK release by enteroendocrine cells (Chen et al., 2006), a hormone that suppresses intake in rumi-nants (Baldwin, 1985). However, in the current study,

plasma CCK concentrations were greatest (P < 0.001) for the plain diet, followed by the bitter- and umami-flavored diets (Table 5). The bitter diet elicited the greatest (P < 0.001) release of CCK at 60 min post-feeding, but then it decreased below the concentrations observed with the plain diet (Figure 3). The decreased preference for the sweet-flavored diet was not expect-ed because sweetness typically enhances intake and acceptability in large ruminants (McMeniman et al., 2006; Montoro et al., 2010).

Scan Sampling

No differences among treatments were detected in the proportion of scans of eating events recorded during the feeding cycle (data not shown). Thus, the differ-ences in feed consumption observed among the differ-ent flavors within the diversity treatment were likely supported by changes in eating rate, but not eating frequency. This observation is in agreement with the notion that alterations in the amount of feed consumed in response to feed palatability are largely mediated by changes in the rate and frequency of eating (Davis and Smith, 1988). It therefore seems reasonable to sug-gest that when lambs alternated their consumption of flavored feeds when exposed to multiple flavors, they likely reduced the rate of consumption, particularly at peaks of feed intake.

Figure 2. Feed intake at 30-min intervals by lambs exposed to the same feed offered in different flavors: bitter, plain, sweet, umami, and diversity (a simultaneous offer of the 4 flavored feeds). Lambs in the diversity treatment showed the least intakes at 30 and 270 min (P < 0.05), but they consumed more feed than lambs in the plain (at 60, 90, 120, and 180 min), bitter (at 60, 120, and 180 min), umami (at 60, 90, 180 min), and sweet (at 90, 120, and 180 min; P < 0.01) treatments. Values are means for 7 lambs; SE are represented by vertical bars.



Preferences for Novel Feeds

Few experimental studies have been conducted on the effects of early experiences with feed on subse-quent feed acceptance. Generalization across sensory stimuli (e.g., flavor) seems to be an important mecha-nism by which herbivores accept novel feeds (Augner et al., 1998). Sheep are able to generalize in a qualitative and quantitative fashion across cues provided by pal-atable (Villalba and Provenza, 2000) and unpalatable (Launchbaugh and Provenza, 1993) feeds.

No differences in intake of novel high-energy feeds were detected among treatments (treatment novel feed; P = 0.49; treatment novel feed day; P = 0.86; data not shown). Likewise, no differences in pref-erences for such feeds were found among treatments (P = 0.13). However, there was an interaction between

treatment and novel feed and day (P < 0.01; Figure 4). For the first day of testing, lambs in the plain treat-ment showed a greater preference for beet pulp than did lambs fed the umami and bitter diets (Figure 4). On d 2, lambs in the plain treatment (58 7.6%) had a greater preference for milo than did lambs in the sweet (23 7.6%) and diversity treatments (27 7.6%), and lambs in the sweet treatment (39 7.6%) had a greater preference for corn than did lambs fed the plain (12 7.6%) and bitter (18 7.6%) diets. Corn contains a relatively high concentration of sucrose (Kuo et al., 1988), and lambs may have generalized the sweet taste of corn from their previous experiences with the fla-vored ration.

No differences in total intake or preferences for novel high-protein feeds were detected among treatments (P > 0.10; data not shown). Similarly, no differences in in-

Figure 3. Evolution of plasma insulin (A), cholecystokinin (CCK; B), IGF-I (C), and glucagon-like peptide 1 (GLP-1; D) concentrations in lambs exposed to the same feed offered in different flavors: bitter, diversity (a simultaneous offer of the 4 flavored feeds), plain, sweet, and umami. Values are means for 3 lambs; SE are represented by vertical bars. Asterisks indicate significant differences (P 0.05) among treatments at each particular time point.



takes of novel phytochemical-containing feeds were de-tected among treatments (P > 0.10; data not shown). However, there was a tendency (P = 0.06) for lambs in different treatments to consume different amounts of novel feeds over time. Specifically, during the last day of testing, lambs in the diversity (6.9 0.92 g/

kg of BW0.75), plain (8.8 0.92 g/kg of BW0.75), and sweet (7.1 0.92 g/kg of BW0.75) treatments tended to consume more saponin-containing feed than did lambs in the bitter treatment (4.6 0.92 g/kg of BW0.75), and lambs in the bitter (5.9 0.92 g/kg of BW0.75) and diversity treatments (6.3 0.92 g/kg of BW0.75)

Figure 4. Interactions between day, treatment, and type of novel feed on feed preferences of lambs previously exposed for 60 d to the same feed offered in different flavors: bitter, plain, sweet, umami, and diversity (a simultaneous offer of the 4 flavored feeds). Lambs in the plain treatment > lambs in the umami and bitter treatments [beet pulp (A); d 1; P < 0.05], and lambs in the sweet and diversity treatments [milo (B); d 2; P < 0.05]. Lambs in the plain and umami treatments > lambs in the bitter treatment [saponins (C); d 4; P < 0.10]. Lambs in the bitter treatment > lambs in the plain and sweet treatments [tannins (D); d 4; P < 0.10]. Lambs in the plain and bitter treatments > lambs in the diversity treatment [wheat straw (E); d 1; P < 0.05]. Lambs in the diversity treatment > lambs in the plain treatment [wheat bran (F); d 1; P < 0.05]. Treatment novel feed day; P < 0.05. Values are means for 7 lambs; SE are represented by vertical bars.



consumed more tannin-containing feed than did lambs in the umami treatment (3.7 0.92 g/kg of BW0.75). Furthermore, the evolution of feed preferences differed among treatments and novel feeds across time (P < 0.05). During the last day of testing, lambs in the plain and umami treatments showed a greater preference for saponin-containing feed than did lambs in the bitter treatment, and lambs in the bitter treatment showed a greater preference for tannin-containing feed than did lambs in the plain and sweet treatments (Figure 4). Lambs in the bitter treatment may have generalized the bitter taste of tannins from their previous experiences with the flavored ration because tannins are bitter-tast-ing compounds (Jackson et al., 1996).

Finally, no differences in total intake of novel low-quality feeds were detected among treatments (data not shown). However, for the first day of testing, lambs in the plain and bitter treatments showed a greater (P < 0.05) preference for wheat straw than did lambs in the diversity treatment, whereas lambs in the diversity treatment showed a greater (P < 0.05) preference for wheat bran than did lambs in the plain treatment (Fig-ure 4).

It has been shown that infants exposed for 8 d to a variety of fruits (not including pears) manifested a greater consumption of pears but this acceptance did not generalize to green beans (more bitter and less sweet than pears). In contrast, infants exposed for 8 d to a variety of vegetables tended to eat more green beans after exposure (Mennella et al., 2008). Likewise, infants who were exposed to different starchy vegeta-bles (not including carrots) each day ate as many car-rots after exposure as infants who were repeatedly ex-posed to carrots (Gerrish and Mennella, 2001). Thus, it seems that for the acceptance of novel feeds, the flavor of the feeds experienced in the past and how it relates to the target feed are important (Mennella et al., 2008). Some of the observed preferences in the current study are consistent with this notion. Studies of rats and hu-mans suggest that exposure to a variety of feeds is more robust when there are pronounced sensory differences between feeds (Rolls et al., 1981, 1983). Flavors in the current study were contrasting because they targeted 3 out of the 5 known primary tastes. It could be that ex-posure to such multiple sensory contrasts may enhance the transfer of diversity effect (Capretta et al., 1975), such that by providing a varied flavor experience, it would lead to a subsequent increased acceptance of novel feeds and flavors. However, the effect of experi-ence with or exposure to flavor diversity did not neces-sarily lead to a clear pattern of an improved acceptance of all the novel feeds tested.

In summary, exposure to diverse flavors, independent-ly of postingestive events, has the potential to stimulate intake, alter eating behavior, and improve animal per-formance. These differences are likely attributed to a sustained need for protein in growing animals (umami) and the rejection of toxic compounds of plant origin (bitter). Repeated exposure to flavored feeds influences

subsequent acceptance of novel feeds. Although this ef-fect is subtle, and, for many feeds, short-lived, it may have a significant effect on attenuating transient, but economically meaningful, reductions of feed intake and productivity during periods of transition when animals are introduced to novel feeds. Flavor diversity has the potential not only to enhance feed intake, but also to induce a more even spread of feed intake throughout the day. This effect could reduce rumen pH fluctuations (Sutton et al., 1986), potentially enhancing the syn-chrony of nutrient supply to the host (Hersom, 2008).

LITERATURE CITED

Altman, J. 1974. Observational study of behavior: Sampling meth-ods. Behavior 49:227265.

AOAC. 2002. Official Methods of Analysis. 17th ed. Assoc. Off. Anal. Chem., Arlington, VA.

Atwood, S. B., F. D. Provenza, R. D. Wiedmeier, and R. E. Ban-ner. 2001. Changes in preferences of gestating heifers fed un-treated or ammoniated straw in different flavors. J. Anim. Sci. 79:30273033.

Augner, M., F. D. Provenza, and J. J. Villalba. 1998. A rule of thumb in mammalian herbivores? Anim. Behav. 56:337345.

Baldwin, B. A. 1985. Food intake and its control by farm animals. Proc. Nutr. Soc. 44:303311.

Bello, N. T., A. S. Guarda, C. E. Terrillion, G. W. Redgrave, J. W. Coughlin, and T. H. Moran. 2009. Repeated binge access to a palatable food alters feeding behavior, hormone profile, and hindbrain c-Fos responses to a test meal in adult male rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:R622R631.

Blundell, J. E., S. Green, and S. V. Burley. 1994. Carbohydrates and human appetite. Am. J. Clin. Nutr. 59(Suppl.):728S734S.

Bonacchi, K. B., K. Ackroff, and A. Sclafani. 2008. Sucrose taste but not Polycose taste conditions flavor preferences in rats. Physiol. Behav. 95:235244.

Bunting, L. D., M. D. Howard, R. B. Muntifering, K. A. Dawson, and J. A. Boling. 1987. Effect of feeding frequency on forage fiber and nitrogen utilization in sheep. J. Anim. Sci. 64:11701177.

Burritt, E. A., and F. D. Provenza. 1992. Lambs form preferences for non-nutritive flavors paired with glucose. J. Anim. Sci. 70:11331136.

Burt, A. W. A., and C. R. Dunton. 1967. Effect of frequency of feeding upon food utilization by ruminants. Proc. Nutr. Soc. 26:181190.

Capretta, P. J., J. T. Petersik, and D. J. Steward. 1975. Acceptance of novel flavours is increased after early experience of diverse taste. Nature 254:689691.

Chapman, D. F., A. J. Parsons, G. P. Cosgrove, D. J. Barker, D. M. Marotti, K. J. Venning, S. M. Rutter, J. Hill, and A. N. Thompson. 2007. Impacts of spatial patterns in pasture on animal grazing behavior, intake, and performance. Crop Sci. 47:399415.

Chen, M. C., S. V. Wu, J. R. Reeve Jr., and E. Rozengurt. 2006. Bitter stimuli induce Ca2+ signaling and CCK release in entero-endocrine STC-1 cells: Role of L-type voltage-sensitive Ca2+ channels. Am. J. Physiol. Cell Physiol. 291:C726C739.

Chilliard, Y., C. Delavaud, and M. Bonnet. 2005. Leptin expres-sion in ruminants: Nutritional and physiological regulations in relation with energy metabolism. Domestic Anim. Endocrinol. 29:322.

Cummings, D. E., and J. Overduin. 2007. Gastrointestinal regula-tion of food intake. J. Clin. Invest. 117:1323.

Davis, J. D., and P. G. Smith. 1988. Analysis of lick measures the positive and negative feedback effects of carbohydrates on eat-ing. Appetite 11:229238.



Di Marzo, V., and I. Matias. 2005. Endocannabinoid control of food intake and energy balance. Nat. Neurosci. 8:585589.

Early, D. M., and F. D. Provenza. 1998. Food flavor and nutritional characteristics alter dynamics of food preference in lambs. J. Anim. Sci. 76:728734.

Epstein, L. H., J. L. Robinson, J. L. Temple, J. N. Roemmich, A. L. Marusewski, and R. L. Nadbrzuch. 2009. Variety influences habituation of motivated behavior for food and energy intake in children. Am. J. Clin. Nutr. 89:746754.

Freeland, W. J., and D. H. Janzen. 1974. Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nat. 108:269286.

Friggens, N. C., B. L. Nielsen, I. Kyriazakis, B. J. Tolkamp, and G. C. Emmans. 1998. Effects of feed composition and stage of lactation on the short-term feeding behavior of dairy cows. J. Dairy Sci. 81:32683277.

Gerrish, C. J., and J. A. Mennella. 2001. Flavor variety enhances food acceptance in formula-fed infants. Am. J. Clin. Nutr. 73:10801085.

Gherardi, S. G., and J. L. Black. 1991. Effect of palatability on voluntary feed intake by sheep. 1. Identification of chemicals that alter the palatability of a forage. Aust. J. Agric. Res. 42:571584.

Grovum, W. L., and H. W. Chapman. 1988. Factors affecting the voluntary intake of food by sheep. 4. The effect of additives rep-resenting the primary tastes on sham intakes by oesophageal-fistulated sheep. Br. J. Nutr. 59:6372.

Hersom, M.J. 2008. Opportunities to enhance performance and ef-ficiency through nutrient synchrony in forage-fed ruminants. J. Anim. Sci. 86(E-Suppl.):E306E317.

Jackson, F. S., W. C. McNabb, T. N. Barry, Y. L. Foo, and J. S. Pe-ters. 1996. The condensed tannin content of a range of subtropi-cal and temperature forages and the reactivity of condensed tannin with ribulose-1,5-bis-phosphate carboxylase (Rubisco) protein. J. Sci. Food Agric. 72:483492.

Kuo, T. M., J. F. VanMiddlesworth, and W. J. Wolf. 1988. Content of raffinose oligosaccharides and sucrose in various plant seeds. J. Agric. Food Chem. 36:3236.

Launchbaugh, K. L., and F. D. Provenza. 1993. Can plants practice mimicry to avoid grazing by mammalian herbivores? Oikos 66:501504.

Luscombe-Marsh, N. D., A. J. Smeets, and M. S. Westerterp-Plant-enga. 2008. Taste sensitivity for monosodium glutamate and an increased liking of dietary protein. Br. J. Nutr. 99:904908.

McMeniman, J. P., J. D. Rivera, P. Schlegel, W. Rounds, and M. L. Galyean. 2006. Effects of an artificial sweetener on health, performance, and dietary preference of feedlot cattle. J. Anim. Sci. 84:24912500.

McSweeney, F. K., and S. Swindell. 1999. General-process theories of motivation revisited: The role of habituation. Psychol. Bull. 125:437457.

Mennella, J. A., S. Nicklaus, A. L. Jagolino, and L. M. Yourshaw. 2008. Variety is the spice of life: Strategies for promoting fruit and vegetable acceptance in infants. Physiol. Behav. 94:2938.

Montoro, C., I.R. Ipharraguerre, and A. Bach. 2010. Blocking -opioid receptors alters short-term intake and oro-sensorial preferences of weaned calves. J. Dairy Sci. 93(E-Suppl. 1):867. (Abstr.)

Naim, M., J. G. Brand, C. M. Christensen, M. R. Kare, and S. Van Buren. 1986. Preference of rats for food flavors and texture in nutritionally controlled semi-purified diets. Physiol. Behav. 37:1521.

Nolte, D. L., and F. D. Provenza. 1992. Food preferences in lambs after exposure to flavors in solid foods. Appl. Anim. Behav. Sci. 32:337347.

NRC. 1985. Nutrient Requirements of Sheep. 6th ed. Natl. Acad. Press, Washington, DC.

Provenza, F. D. 1996. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74:20102020.

Provenza, F. D., and J. J. Villalba. 2006. Foraging in domestic verte-brates: Linking the internal and external milieu. Pages 210240 in Feeding in Domestic Vertebrates: From Structure to Func-tion. V. L. Bels, ed. CABI Publ., Oxfordshire, UK.

Provenza, F. D., J. J. Villalba, J. Haskell, J. W. MacAdam, T. C. Griggs, and R. D. Wiedmeier. 2007. The value to herbivores of plant physical and chemical diversity in time and space. Crop Sci. 47:382398.

Rolls, B. J. 1979. How variety and palatability can stimulate appe-tite. Nutr. Bull. 5:7886.

Rolls, B. J. 1986. Sensory-specific satiety. Nutr. Rev. 44:93101.Rolls, B. J., E. A. Rowe, and E. T. Rolls. 1982. How sensory proper-

ties of foods affect human feeding behavior. Physiol. Behav. 29:409417.

Rolls, B. J., E. A. Rowe, E. T. Rolls, B. Kingston, A. Megson, and R. Gunary. 1981. Variety in a meal enhances food intake in man. Physiol. Behav. 26:215221.

Rolls, B. J., P. M. Van Duijvenvoorde, and E. A. Rowe. 1983. Vari-ety in the diet enhances intake in a meal and contributes to the development of obesity in the rat. Physiol. Behav. 31:2127.

Shibata, R., M. Kameishi, T. Kondoh, and K. Torii. 2009. Bilateral dopaminergic lesions in the ventral tegmental area of rats in-fluence sucrose intake, but not umami and amino acid intake. Physiol. Behav. 96:667674.

Shintani, M., Y. Ogawa, K. Ebihara, M. Aizawa-Abe, F. Miyanaga, T. T. Hayashi, G. Inoue, K. Hosoda, M. Kojima, K. Kangawa, and K. Nakao. 2001. Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of the hypothalamic neuro-peptide Y/Y1 receptor pathways. Diabetes 50:227232.

Srensen, L. B., P. Moller, A. Flint, M. Martens, and A. Raben. 2003. Effect of sensory perception of foods on appetite and food intake: A review of studies on humans. Int. J. Obes. Relat. Metab. Disord. 27:11521166.

Sutton, J. D., I. C. Hart, W. H. Broster, R. J. Elliot, and E. Schul-ler. 1986. Feeding frequency for lactating cows: Effects on ru-men fermentation and blood metabolites and hormones. Br. J. Nutr. 56:181192.

Temussi, P. A. 2009. Sweet, bitter, and umami receptors: A complex relationship. Trends Biochem. Sci. 34:296302.

Treit, D., S. M. L. Spetch, and J. A. Deutsh. 1983. Variety in the flavor of food enhances eating in the rat: A controlled demon-stration. Physiol. Behav. 30:207211.

Van Soest, P. J. 1994. Nutritional Ecology of the Ruminant. 2nd ed. Cornell Univ. Press, Ithaca, NY.

Villalba, J. J., and F. D. Provenza. 2000. Roles of flavor and reward intensities in acquisition and generalization of food preferences: Do strong plant signals always deter herbivory? J. Chem. Ecol. 26:19111922.

Westoby, M. 1974. An analysis of diet selection by large generalist herbivores. Am. Nat. 108:290304.

Westoby, M. 1978. What are the biological bases of varied diets? Am. Nat. 112:627631.



Referenceshttp://www.journalofanimalscience.org/content/89/8/2571#BIBLThis article cites 51 articles, 13 of which you can access for free at:

Citationshttp://www.journalofanimalscience.org/content/89/8/2571#otherarticlesThis article has been cited by 2 HighWire-hosted articles:


Feeding Behavior and Performance of Lambs Are Influenced by Flavor Diversity

Documents

Transcript of Feeding Behavior and Performance of Lambs Are Influenced by Flavor Diversity