Postingestive feedback from starch influences the ingestive behaviour of sheep consuming wheat straw

Ž .Applied Animal Behaviour Science 66 2000 49–63www.elsevier.comrlocaterapplanim

Postingestive feedback from starch influences theingestive behaviour of sheep consuming wheat

straw

Juan J. Villalba ), Frederick D. ProvenzaDepartment of Rangeland Resources, Utah State UniÕersity, Logan, UT 84322-5230, USA

Accepted 18 August 1999

Abstract

Plant species present a complex array of biochemicals to herbivores that in conjunction with aplant’s physical structure influence intake. Our objective was to determine the role of postinges-

Ž .tive feedback from macronutrients on the ingestion of a low-quality forage by sheep OÕis aries .We compared the ingestive behaviour of two groups of lambs conditioned with intraruminal

Ž . Ž .infusions of starch 100 grlambrday; Group 1 or water 250 mlrlambrday; Group 2 while theyŽ .grazed wheat straw held erect in wooden frames; 30 cm height; Trials 1, 2 and 3 or consumed

Ž .wheat straw from food boxes 1–2 cm particle size; Trial 4 . Lambs were conditioned asŽ .individuals during Trials 1 and 4, in pairs during Trial 2, and as two groups Groups 1 and 2

during Trial 3. Ingestive behaviour – intake, intake rate, number of bites, bite size, bite rate —was assessed during individual tests that lasted 5 minrlamb. After conditioning and testing, all

Ž .animals had restricted access 80% of their daily energy requirements to a basal diet of alfalfaŽ .pellets. No differences between groups were detected during initial tests before infusing starch or

Ž . Žduring Trial 1 P)0.05 . Lambs conditioned with starch in Trial 2 consumed more straw 8 vs. 2. Ž . Ž .g; P-0.05 at higher rates 2.3 vs. 1.0 grmin; P-0.1 , and took more 13 vs. 5; P-0.1 and

Ž .larger 0.59 vs. 0.31 grbite; P-0.05 bites than lambs conditioned with water. This pattern wasŽ .maintained during Trial 3: Lambs infused with starch showed higher intake 24 vs. 5 g; P-0.01 ,

Ž . Ž . Žintake rate 5.4 vs. 1.4 grmin; P-0.001 , bites 29 vs. 10; P-0.01 , bite rate 6.7 vs. 2.6. Ž .bitesrmin; P-0.01 and bite size 0.86 vs. 0.54 grbite; P-0.05 than lambs infused with

Ž .water. In Trial 4, lambs conditioned with starch consumed more straw 21 vs. 9 g; P-0.1 , atŽ .higher rates 5.4 vs. 2.6 grmin; P-0.1 , than lambs conditioned with water. Thus, the

) Corresponding author. Tel.: q1-435-797-2539; fax: q1-435-797-3796; e-mail: [email protected]

0168-1591r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.Ž .PII: S0168-1591 99 00081-7

( )J.J. Villalba, F.D. ProÕenzarApplied Animal BehaÕiour Science 66 2000 49–6350

postingestive effects of energy played an important role in modulating rates of food intake, andour findings suggest postingestive feedback from macronutrients is a fundamental factor influenc-ing the ingestive behaviour of herbivores. q 2000 Elsevier Science B.V. All rights reserved.

Keywords: Sheep; Intake rate; Bite rate; Starch; Feeding behavior; Foraging behaviour

1. Introduction

The process of gathering food is an essential affair for living organisms. Forherbivores, behaviours directed toward finding and harvesting plants are of central

Ž .importance Shipley et al., 1994; Ungar, 1996 . Rate of food intake emerges as afundamental variable in foraging ecology since it determines the time herbivores spendgathering food to obtain required nutrients, and in an indirect manner the time they have

Ž .to invest in other activities such as mating or avoiding predators Shipley et al., 1994 .Intake rate over short periods of active grazing is determined by bite weight and bite rateŽ .Allden and Whittaker, 1970 . Traditionally, these variables have been regarded as a

Žfunction of animal morphology, behaviour and sward structure Hodgson, 1981; Black.and Kenney, 1984; Laca et al., 1994; Wilman et al., 1996 . For instance, intake per bite

is influenced primarily by the sensitivity of bite depth to variation in sward heightŽ .Hodgson et al., 1999 , and bite rate is a function of the time spent per bite on searchingŽ . Žlocomotion, recognition and decision and handling gathering herbage into the mouth,

. Ž .severing the herbage, ingestive mastication and swallowing food Laca et al., 1994 .Besides their physical characteristics, plants present a complex array of biochemicals

to herbivores. Recent research has shown that postingestive effects mediated by nutrientsŽ .and toxins strongly influence food preference Provenza, 1995a,b, 1996 . Lambs can

acquire preferences and increase consumption of low-quality forages such as wheatstraw when straw is associated with intraruminal infusions of energy and nitrogen that

Žrepresent as little as 2.5% of their daily requirements Villalba and Provenza, 1996,.1997a . Thus, it is conceivable that animals consume foods at rates that are also a

function of the foods’ postingestive actions.The majority of grazing studies have concentrated on the impact of a plant’s structure

on intake rate, with very little reference to the potential importance of a plant’sŽbiochemical composition as a factor controlling intake rate Illius and Hodgson, 1996;

.Hodgson et al., 1999 . This has occurred even though heterogeneity in the nutritionalŽ .quality of plant communities is frequent rather than peculiar Provenza et al., 1998 . The

influence of nutrients on rates of food consumption has been overlooked primarilyŽbecause research on physical plant characteristics height, bulk density, structural

.strength has controlled for plant quality and because experiments were conducted underconditions where nutritional and toxicological differences among plants were not

Ž .pronounced O’Reagain et al., 1996 .We undertook this study to determine if the postingestive actions of macronutrients

affect rates of food ingestion. We supplied lambs with intraruminal infusions of starch inassociation with the ingestion of a low-quality forage — wheat straw — whose physicalstructure is difficult to harvest and handle.

( )J.J. Villalba, F.D. ProÕenzarApplied Animal BehaÕiour Science 66 2000 49–63 51

2. Materials and methods

We conducted four trials at the Green Canyon Ecology Center, located at Utah StateUniversity in Logan. The objective of these trials was to determine if lambs modify theirrate of straw consumption when they received intraruminal infusions of starch. As thetrials progressed, we increased the degree of exposure to straw and we modified thetemporal association between food ingestion and postingestive feedback in order toenhance the association between straw and starch. Herbivores constantly manifest

Ž .dynamic and adaptive interactions with their environment Provenza et al., 1998 . WeŽshow the emergence of some of these interactions e.g., ingestive behaviour–postinges-

.tive feedback in response to the evolving experimental conditions of the study.The same animals and straw–starch or straw–water associations were maintained

Žthroughout the study. During each trial, lambs Finn–Polypay–Suffolk crossbreds of.both sexes had free access to salt blocks and fresh water. Alfalfa pellets were the basal

diet. Lambs were approximately 3 months of age at the beginning of the study.

2.1. Before conditioning

Ž .Eighteen lambs 25 kg BW were penned as a group in a 14 by 10 m plot. In order tofamiliarize the animals with the upcoming experimental procedures, every day at 0800 h

Ž .pairs of lambs were selected at random and transferred to a testing pen 3 by 4.5 m .Lambs were then offered hand-clipped plants of alfalfa held erect with clamps between

Ž w x w x w x.the major faces of the two pieces of lumber 13.5 cm H =120 cm W =3.5 cm Dthat formed a wooden frame.

Ž .Lambs were exposed in pairs during 2 consecutive days 5 minrpairrday andŽ .individually 5 minrlambrday for the ensuing 3 days. After individual exposure, all

lambs were consuming alfalfa from the wooden frames. Alfalfa plants were thenŽ .replaced by wheat straw 100 g; 30 cm height placed along the central 30 cm of the

wooden frame. During 4 consecutive days, pairs of lambs selected at random wereexposed to straw in the testing pen for a period of 5 minrpairrday.

After exposure to straw, lambs were penned as a group and received an amount ofŽ .alfalfa pellets 1270 grlambrday , which supplied about 80% of their digestible energyŽ .requirements NRC, 1985 .

2.2. Initial indiÕidual tests

The day after exposure to straw ended, lambs were tested individually between 0730and 1000 h. Each lamb in the testing pen was offered a previously weighed amount of

Ž .straw about 100 g secured in the wooden frame. We recorded the time each lamb spenteating straw during 5 min. Lambs were observed individually from a distance ofapproximately 3 m while they foraged. We excluded bouts of inactivity from calcula-tions of active feeding time. The total number of bites was recorded with a hand-counterwhile observing the lambs. We calculated intake by the difference in straw weightimmediately before and after each lamb was tested. We used these data to calculate

Ž . Ž . Ž .intake rate gramsrminute , bite rate bitesrmin , and bite size gramsrbite .


2.3. Trial 1

2.3.1. IndiÕidual testsAfter the initial determination of straw intake, lambs were sorted in decreasing order

by initial rate of straw intake and sets of two lambs were randomly assigned to twoŽ .groups Groups 1 and 2; nine lambsrgroup . Thus, differences between groups due to

initial recordings of intake rate were balanced.ŽEach lamb was offered a previously weighed amount of straw about 100 g; 30 cm

.height — secured in a wooden frame — during a 5-min period. Immediately afterbeing tested for straw consumption, lambs in Group 1 were given intraruminal infusionsof a starch suspension by oral intubation. The starch suspension was prepared by mixing100 g of starch with 250 ml tap water at room temperature. Lambs in Group 2 receivedinfusions of 250 ml tap water after consuming straw. Lambs from Groups 1 and 2 weretested in an alternate and consecutive sequence. The order in which individual lambswere tested was reversed each day. Tests were conducted between 0730 and 1000 hdaily during 3 consecutive days. We calculated intake, intake rate, number of bites, biterate and bite size during 5-min periods, as described previously. After the daily test,lambs were penned as a group and at noon they received alfalfa pellets, as describedpreviously.

2.4. Trial 2

Individual lambs were reluctant to eat straw alone in the testing pen, which reducedthe active feeding time and their exposure to straw. Consequently, during Trial 2 weattempted to increase exposure to straw — and thus enhance the association of strawwith starch — by conditioning animals in pairs.

2.4.1. Conditioning — pairsFour pairs of lambs from Group 1 and four pairs of lambs from Group 2 were formed

at random. Each pair of lambs was transferred to the testing pen and offered wheat strawŽ .100 g; 30 cm height secured in a wooden frame for 5 min. Pairs of lambs from Groups1 and 2 were tested in an alternate and consecutive order. The order of testing pairs oflambs was reversed each day. After testing, lambs in the pair received intraruminal

Ž . Ž .infusions of starch 100 grlambrday; Group 1 or water 250 mlrlambrday; Group 2 .Lambs were penned as a group and at noon they received alfalfa pellets, as described forTrial 1.

During 4 consecutive days of conditioning, we calculated intake, intake rate, numberof bites, bite rate and bite size for the 5 min period, as described for Trial 1. Pairs oflambs were the experimental units.

2.4.2. IndiÕidual testsAfter conditioning in pairs, all lambs were tested as individuals and received

Ž . Ž .intraruminal infusions of starch Group 1 or water Group 2 as described for Trial 1.Testing was performed during 1 day and we calculated intake, intake rate, number ofbites, bite rate and bite size during 5 min, as described for Trial 1.


2.5. Trial 3

During Trial 3 we attempted to enhance the association between straw and starch.First, we increased the exposure to straw by increasing the amount of time lambs wereallowed to consume straw. We also allowed lambs to consume straw while they werewith their peers.

We also modified the temporal ordering between straw offer and starch infusion byfirst infusing starch and then offering straw. This order may facilitate conditioning

Ž .because the postingestive effects of starch i.e., the effects of absorbed calories occurŽ .during rather than after straw ingestion Boakes and Lubart, 1988 .

2.5.1. Conditioning — groupsAt 0730 h, on the first day of conditioning lambs from Group 1 received intraruminal

Ž .infusions of starch 100 grlambrday by oral intubation. Lambs were then transferredto the testing pen as a group and offered straw held erect in wooden frames. Condition-ing lasted 40 minrday and every 2 min we recorded the number of animals that wereconsuming straw. After conditioning Group 1, lambs from Group 2 received intrarumi-

Ž .nal infusions of water 250 mlrlambrday and were offered straw in the same fashiondescribed for Group 1. The order in which groups were conditioned was reversed eachday. Four days of conditioning formed one conditioning period and two conditioningperiods were performed. After the daily tests, lambs were penned as a group and at noonthey received alfalfa pellets, as described for Trial 1.

The experimental area in the testing pen was prepared daily before each group ofŽ .lambs was conditioned by placing about 2.5 kg of straw 30 cm height in three wooden

frames of the same dimensions and characteristics described before.

2.5.2. IndiÕidual testsAfter each 4-day conditioning period, all lambs were tested individually, as described

Ž . Žfor Trial 1. Lambs received intraruminal infusions of starch Group 1 or water Group.2 immediately before being offered straw secured in a wooden frame. Testing was

performed during 1 day and we calculated intake, intake rate, number of bites, bite rateand bite size during a 5-min period, as described for Trial 1.

2.5.3. IndiÕidual tests without infusionsLambs were tested as described before but without starch or water administrations.

2.6. Trial 4.

2.6.1. ConditioningŽ .The day after Trial 3 ended, lambs 33 kg BW were penned individually in adjacent

Žpens of 1.6=2.2 m. Lambs from Group 1 received intraruminal infusions of starch 100. Žgrlambrday and lambs from Group 2 received intraruminal infusions of water 250.mlrlambrday . Immediately after the infusions, all lambs were offered 100 g of

Ž .chopped wheat straw 1–2 cm particle size for 40 min. Refusals were collected andweighed. Conditioning was conducted between 0800 and 0900 h daily and was repeated


Ž .during 9 consecutive days. At 1200 all lambs received alfalfa pellets 1400 grlambrdayŽthat provided approximately 80% of their daily digestible energy requirements NRC,

.1985 .

2.6.2. IndiÕidual testsAfter conditioning, and immediately before being tested for straw consumption,

Ž .lambs in Group 1 were given intraruminal infusions of a starch 100 grlambrday andŽ .lambs in Group 2 received infusions of water 250 mlrlambrday . We recorded the

time each lamb spent eating straw during 5 min. Lambs were observed individually andbouts of inactivity were excluded from calculations of feeding time. We determined theamount of straw ingested as the difference between the weight of food offered and that

Ž .remaining after 5 min. These data were used to calculate intake rate grmin . At noonall lambs were offered alfalfa pellets, as described during conditioning.

2.6.3. IndiÕidual tests without infusionsLambs were tested as described before but without starch or water administrations.

2.7. Statistical analyses

Straw intake, intake rate, number of bites, bite rate, bite size and active feeding timeŽwere analyzed as a split-plot design with lambs nested within groups. Group 1: starch

.or 2: no starch was the between-lamb factor. Pairs of lambs were the between-subjectŽ .factor when lambs were conditioned as a pair Conditioning; Trial 2 . When tests were

Ž .repeated on different days — Trial 1: 3 days; Trial 2: 4 days Conditioning — Pairs ;Ž . Ž .Trial 3: 2 days Individual Tests after Periods 1 and 2 ; Trial 4: 9 days Conditioning

— day was the repeated measure in the analysis. Means were compared using the LSDtest.

3. Results

3.1. Initial indiÕidual tests

There were no differences in straw intake between groups of lambs before applyingŽ . Ž .the treatments starch, water P)0.05 . All the measurements recorded during testing

Ž .were low and variable Table 1 .

3.2. Trial 1

During Trial 1, lambs’ ability to ingest wheat straw was not affected by infusingŽ .starch into the rumen P)0.05 . Intake values and active feeding times were still low

Ž .and variable for both groups of lambs Table 1 . For instance, several lambs in Groups 1Ž . Ž .ns4, 1, and 0 and 2 ns3, 3, and 4 consumed -1 g of straw during tests 1, 2 and3, respectively.


Table 1Straw intake, rate of straw intake, number of bites, bite rate and active feeding time by two groups of lambsthat received or not intraruminal infusions of starch associated with straw ingestion

Straw Rate of No. of Bite Intake Activeintake straw intake bites rate per bite feeding timeŽ . Ž . Ž . Ž . Ž .g grmin bitesrmin grbite min

Initial individual

cTestsG1 4 3.4 15 7.3 0.35 2.7G2 5 5.4 14 7.8 0.67 1.9S.E.M. 1.9 2.2 4.5 1.7 0.20 0.7

Trial 1Starch 6 5.7 10 6.9 0.97 1.5No starch 4 9.8 6 6.7 1.47 1.3S.E.M. 1.2 3.4 2.3 0.9 0.52 0.5

Trial 2Conditioning Pairs

a a aStarch 22 4.3 33 6.6 0.67 5.0b b bNo starch 5 0.9 17 3.5 0.29 4.9

S.E.M. 4.2 0.8 6.1 1.2 0.05 0.04Individual Tests

a a a aStarch 8 2.3 13 3.8 0.59 3.1b b b bNo starch 2 1.0 5 2.8 0.31 2.0

S.E.M. 1.9 0.5 2.8 0.5 0.07 0.7

Trial 3Individual Tests

a a a a aStarch 24 5.4 29 6.7 0.86 4.3b b b b bNo starch 5 1.4 10 2.6 0.54 3.7

S.E.M. 3.1 0.6 4.1 0.7 0.09 0.5Without infusions

a a a aStarch 14 2.8 30 6.0 0.49 5.0b b b bNo starch 2 0.6 8 1.9 0.54 4.3

S.E.M. 1.8 0.4 4.2 0.9 0.16 0.4

dTrial 4Individual Tests

a aStarch 21 5.4 – – – 3.9b bNo starch 9 2.6 – – – 3.1

S.E.M. 4.6 0.9 – – – 0.7Without infusions

a aStarch 19 4.3 – – – 4.0b bNo starch 6 2.5 – – – 2.1

S.E.M. 4.7 1.1 – – – 0.7

a,b Ž .Pairs of means within a column lacking a common superscript differ P -0.1 .cG1: Group to be conditioned with infusions of starch during Trials 1 to 4. Group 2: Group to be conditionedwith infusions of water during Trials 1 to 4.d Not measured.


3.3. Trial 2

3.3.1. Conditioning — pairsIn Trial 2, we increased the exposure to straw by conditioning animals in pairs.

Lambs also had further experience with the postingestive consequences of starch andthis treatment began to affect straw consumption. Pairs of lambs that received intrarumi-

Ž .nal infusions of starch had higher intakes, intake rates P-0.05 and larger bite sizesŽ . Ž .P-0.001 than lambs that had infusions of water Table 1 . The number of bites and

Ž .bite rate also increased, but the differences were not significant P)0.05; Table 1 .

3.3.2. IndiÕidual testsŽ . Ž .Lambs given starch ate more P-0.05 straw, at a faster rate P-0.1 , than lambs

Ž . Ž .given water Table 1 . Lambs supplemented with starch also took more bites P-0.1Ž . Ž .of larger sizes P-0.05 than lambs infused with water Table 1 .

3.4. Trial 3

3.4.1. Conditioning — groupsThe number of lambs consuming straw during conditioning declined toward the end

of the 40-min interval, particularly for the Group that was not infused with starch. The

Ž .Fig. 1. Number of lambs ingesting straw secured in wooden frames; 30 cm height during two conditioningŽ .periods of 4 days each. Lambs were conditioned as two groups Groups 1 and 2 during 40 minrday. The

number of lambs consuming straw was recorded every 2 min. Group 1 received intraruminal infusions ofŽ . Ž .starch 100 grlambrday and Group 2 intraruminal infusions of water 250 mlrlambrday before consuming

straw.


number of lambs consuming straw in the 2-min scans was in general higher for theŽ .group infused with starch than for the group infused with water Fig. 1 .

3.4.2. IndiÕidual testsThe effects of infusing starch became stronger in Trial 3 as lambs had further

experience ingesting straw and receiving starch infusions. Lambs conditioned withŽ . Ž .starch consumed more straw P-0.01 and took more bites P-0.01 than lambs

Ž .conditioned with water Table 1 . Moreover, after the second period of conditioningŽ . Ž .Period 2 , lambs infused with starch increased straw intake from 21 to 27 g; P-0.05

Ž . Žand number of bites from 24 to 35; P-0.05 compared to Period 1 Group by day.interaction, P-0.05 .

Ž .Lambs given starch ate more straw per unit of time P-0.001 , maintained a moreŽ . Ž .rapid rate of biting P-0.01 , and took larger bites P-0.05 than lambs given water.

ŽThus, active feeding time was the only variable not affected by the treatments P)0.05;.Table 1 .

3.4.3. IndiÕidual tests without infusionsŽ .Lambs given starch continued to display higher intakes P-0.001 , intake rates

Ž . Ž . Ž .P-0.001 , number of bites P-0.001 and bite rates P-0.01 than lambs givenŽ .water, even after starch was no longer administered Table 1 . Bite size and active

Ž .feeding time did not differ between groups P)0.05; Table 1 .

Ž .Fig. 2. Intake of straw 1–2 cm particle size by two groups of lambs during 9 days of conditioning. Lambs inGroup 1 received intraruminal infusions of starch and lambs in Group 2 intraruminal infusions of water

Ž .immediately before straw consumption. Means differed after day 3 P -0.05 .


3.5. Trial 4

3.5.1. ConditioningGroups did not differ in straw intake during the first 3 days of conditioning

Ž .P)0.05; Fig. 2 . After day 3, intake of straw was higher for lambs infused with starchŽ . Ž . ŽGroup 1 than for lambs infused with water Group 2 Group by day interaction,

.P-0.05; Fig. 2 . Average intake of straw across days was 44 g for lambs in Group 1Ž .and 27 g for lambs in Group 2 P)0.05; S.E.M.s10 .

3.5.2. IndiÕidual testsLambs conditioned with starch ate more straw at higher rates than lambs conditioned

Ž .with water P-0.10; Table 1 .

3.5.3. IndiÕidual tests without infusionsŽ . Ž .Lambs treated with starch ate more straw P-0.10 , at faster rates P-0.15 , and

Žspent more time feeding during the 5-min tests than lambs treated with water P-0.10;.Table 1 , even when starch infusions were suspended.

4. Discussion

4.1. PostingestiÕe feedback and ingestiÕe behaÕiour

It has been proposed that the potential rate at which a food can be eaten is largelyŽ .determined by the food’s physical characteristics Kenney and Black, 1984 . However,

under most conditions, food structure and quality are confounded because foods withhigh nutrient content are typically easy to ingest and highly digestible, whereas plantswith low nutrient content are usually difficult to ingest and poorly digestible.

Thus, we sought to isolate the effects of a plant’s structure from its postingestiveeffects. We hypothesized that rates of food intake are not only determined by thephysical structure of a forage but also by its postingestive actions. We found that groupsof lambs exposed to the same forage — wheat straw — for the same periods of timeshowed quite different patterns of ingestive behaviour, dependent on the postingestiveconsequences during straw ingestion. Lambs that received intraruminal infusions of

Ž .starch increased intake, intake rate, bite rate and intake per bite Table 1 . Lambsmanifested this behaviour even when starch was no longer supplied during testingŽ . ŽTable 1 . Lambs conditioned with starch continue to prefer flavoured straw Villalba

.and Provenza, 1997a , even when starch is no longer administered, which suggests thatthe postingestive effects of energy increase the hedonic value or liking and makepreferences — and ingestive behaviour in this study — more resistant to extinction.

Most studies of grazing have focused on the influences of food structure on intakeŽ .rate Hodgson et al., 1999 , and they have manipulated sward structure rather than sward

nutritional quality. The consensus is that other factors — nutritional and toxicologicalŽ .— being equal, intake rate is largely determined by bite mass Ungar et al., 1991 ,

Žwhich in turn is influenced by canopy structure e.g., herbage height and herbage weight


. Ž .per unit canopy volume Black and Kenney, 1984; Laca et al., 1992 . For instance,sward height has been proposed to affect bite depth and consequently intake per biteŽ .Gong et al., 1996; Hodgson et al., 1999 .

ŽIn contrast, our study shows that when physical structure is held constant e.g., same.forage, same height and density — and nutritional effects are unequal — intake rate,

bite rate and bite size are variable and largely influenced by the postingestive conse-quences of food ingestion. Rates of straw intake were low and variable when no starchwas infused in the lambs’ stomach, which supports previous work suggesting that

Ž .animals forage at variable rates, often lower than their potential Owen-Smith, 1993 .Low rates of intake are more likely to occur when foods supply low amounts ofmacronutrients and other foods of higher quality are available for consumption.

Ž .Rates of food ingestion are elastic Owen-Smith, 1993 , and influenced by anŽ .animal’s physiological state Newman et al., 1994; Villalba and Provenza, 1999a .

Fasted animals can compensate for increased nutrient demands by increasing bite rateŽ .and bite size Paterson et al., 1998 . Even though larger bites require more mastication,

Žcattle can reduce the amount of chewing to increase intake rate Greenwood and.Demment, 1988 . Increases in chewing due to increases in bite mass can also be

Žcompensated by using jaw movements for both cropping and chewing Laca et al.,.1994 .

Besides the general effects of fasting, specific nutritional needs can also modify ratesŽ .of food intake. Intake rates of an energy-dense food barley are higher in lambs after a

Ž .meal high in protein than after fasting for 15 h Villalba and Provenza, 1999a . Thisresponse is likely due to an increased need to balance the excess nitrogen supplied bythe protein-rich meal with rapidly fermentable carbohydrates in barley. In the currentstudy, energy-restricted lambs increased their rate of straw intake when straw was pairedwith starch. Collectively, these results suggest that rates of food intake are dynamic anddepend on the nutrient composition of the food and the animal’s physiological condition.

The plasticity of rates of food intake are also manifest through their dependence onan animal’s past history. Foraging skills, acquired through experience, have a significantimpact on foraging behavior by increasing the efficiency of food consumption and by

Ženhancing rates of forage intake Provenza and Balph, 1988; Flores et al., 1989;.Ortega-Reyes and Provenza, 1993 .

4.2. PostingestiÕe feedback and food choice

Food preferences also have been regarded as a function of the rate at which foods canbe ingested. Other factors being equal, plants that can be eaten quickly are likely to be

Ž .preferred to tougher species Wilman and Asiedu, 1983; Kenney and Black, 1984 .Ž . Ž .Cattle Distel et al., 1995 and sheep Black and Kenney, 1984 select those patches that

allow higher intake rates from swards that differ in height and density. Thus, inhorizontally heterogeneous pastures of similar quality, animals may be able to assess the

Ž .reward i.e., postingestive consequences from a patch by sensing the rate at which foodŽcan be obtained from the patch, and modify their preferences accordingly Distel et al.,

.1995 . However, when sward quality is variable, nutrient composition can be even moreŽ . Žimportant than structure in determining preference. Tall Bazely, 1990 or short e.g.,


.Illius et al., 1987 swards patches may be preferred when their nutritional quality ishigher. Foods that yield lower intake rates can be preferred by lambs fed unbalancedbasal diets when those foods provide ratios of energyrprotein closer to the lambs’

Ž .nutritional needs Villalba and Provenza, 1999a . Thus, rates of food intake should beconsidered an emergent property of the interaction between the structure and biochemi-cal composition of food.

A trade-off between diet quality and intake rate has been found for ewes grazingŽ .cocksfoot swards. In order to consume higher quality components leaves , ewes must

take smaller bites which promotes lower intake rates; less selective ewes take largerŽ .bites and have higher intake rates to the detriment of diet quality Prache et al., 1998 .

Thus, degree of selectivity can influence rates of food intake. Rates of food intake arethen a result, rather than a cause, of food selection. We have shown that lambs ingestwheat straw at rates lower than their potential — when offered straw paired with water,presumably because of a lack of reward during and after straw ingestion. Conversely,lambs increased straw ingestion — bite rate, bite size, number of bites — when theyreceived infusions of starch. If the food preferences of ruminants are controlled byspecific associations between a food’s flavour and the food’s postingestive actionsŽ .Provenza, 1995a,b, 1996; Villalba and Provenza, 1996, 1997a,b , then it is likely thatonce a particular food is preferred, postingestive feedback from nutrients may enhancerates of food consumption. In contrast, when preferred items become less accessible,intake per bite will decrease and animals may lower their intake rate.

4.3. PostingestiÕe feedback and palatability

Palatability is classically defined to be a function of the taste, odour and surfaceŽ .characteristics of foods Arnold, 1981 . Within this context, it has been proposed that

palatability is probably not an important determinant of intake for better-qualityŽroughages, but it may limit intake of poor-quality roughages like straw Greenhalgh and

.Reid, 1971 . This was concluded from studies where sheep were fed straw while strawwas put through a fistula in the rumen. Under these conditions, sheep were extremelyreluctant to eat straw, but they significantly increased straw intake when grass hay, a

Žmore nutritious food, was put into the rumen replacing straw Greenhalgh and Reid,.1971 .

We also found that straw intake was enhanced when lambs had an increased supplyŽ .of macronutrients to the rumen starch . However, we differ in the interpretation of the

results. Palatability is best understood as a compound phenomenon emerging from theŽ .interrelationship between the chemical senses taste, smell and postingestive feedback

Ž .Provenza, 1995a,b, 1996 . Thus, palatability per se is probably not the main reason forthe low consumption of straw displayed by sheep, but an outcome of the association

Ž .between organoleptic characteristics of straw e.g., flavour and the low amount ofnutrients supplied to the rumen during and after straw ingestion. Decreases in preferencefor straw due to a lack of nutrient feedback can explain why sheep become increasingly

Ž .reluctant to eat straw Greenhalgh and Reid, 1971 , and why lambs given waterdisplayed lower intake rates as exposure to straw increased. Conversely, lambs increase

Ž .straw intake and preference for flavoured straw Villalba and Provenza, 1997a, 1999b


when straw ingestion is followed by intraruminal infusions of starch. This increase canbe interpreted as an enhanced incentive or drive to eat straw due to its association with areadily available source of energy.

5. Conclusions

The postingestive effects of energy have a significant effect on food intake. Rates offood ingestion are not only influenced by the structure of a forage, but also by theamount of nutrients that the forage supplies. Lack of feedback from the gut during foodconsumption is one of the main reasons for the low preferences and intake ratesdisplayed for low-quality foods like straw. Thus, we suggest that food quality should beconsidered in conjunction with food structure to better understand intake rate of grazingherbivores.

Acknowledgements

This research was supported by grants from CSREES and the Utah AgriculturalExperimental Station, Utah State University. Approved as journal paper number 7160.

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Postingestive feedback from starch influences the ingestive behaviour of sheep consuming wheat straw