Toward a new theory of feed intake regulation in ruminants 2. Costs and benefits of feed consumption: an optimization approach

Livestock

Ekvier

Pmd~c~ion

Science,

30 ( 1992 ) 297-3

I7

297

Science Publishers B.V,, Amsterdam

Toward a neui theory of feed intake regulation ruminants 2. Costs and benefits of feed consumption: an optimization approach B.J, Toikamp’ l Diymrtmcnz

qf Tropicixl

bCt*ntresfpr

and J.J.M.H.

A nind

Agrubiolugicul

in

KeteIaarsb

Prdwtion, Wageningon. Nerh~rhwhh &sear&. Wragcningerr. Nethcrlaands

(Accepted

I6 July

199 1)

GBSTRACT

nants.

B.J. and Ketelaars. J.J.M.H., 1992. Toward a new theory 2. Costs aqd benefits of feed consumption: an optimization

297-3

17.

Tolkamp,

of fed intake regulation approach. Lirw!. Prd.

in rumiSki., 30:

A new concept of feed intake regulation in ruminants is developed staning from the idea that fetd consumption presents both costs and benefits to the animal. For a non-reproducing animal, we consider the intake of net energy for maintenance and gain to be the knefits of feed consumption. and the concomitant consumption of oxygen the costs, since the use of oxygen by tissues indirectly causes an accumulation of damuge tti cell structures. a loss of vitality, ageing and a limited life span. This lcads to the hypothesis that fttd intake behaviour will be aimed at maximizing the efficiency of oxygcn utilization: from each feed an animal will consume such an amount that the intake of net energy per Iitre oxygen consumed will be maximal. Testing this hypothesis extensivdy with data from non-reproducing ruminants shows a good quantitative agreement between predicted and observed ud iibitum intake of feeds widely differing in metabolizability, nitrogen content and physical form. Changes in intake parallel to changes of bmll metabolism also agree with our hypothesis. Effects on intake of changes in maturity and physir.)l&+al state are more difficult to test due to insufficient information about the e’fects of maturity on cfficiency of mctabolizable energy utilization and uncertainty about the exact nature of costs and tinefits of feed consumption in pregnant and lactating animals. Maximization of the efficiency of oxygen utilization may reflect a more universal principle goveming the intensity of different forms of behaviour, in ruminants as well as in monogastrics. Keywords:

ruminants;

intake

regulation;

optimization

energy utilizalion

approach;

INTRODWCTlON

Common ideas about feed intake regulation portant role to cor.straints to feed consumption: Corrcswneknce to: Dr. R.J. Tolkamp. 338. 6700 AH Wageningen. Netherlands

0301-6226~92/SOS.00

S 1992 Elsvier

Department

Science

ia ruminants attribute an imfeed and animal factors which

of Tropical

Publishers

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.4nimal

AlI rights

Production.

--ed.

P.0.

Box

C;encr~It~,

haal mctrlktisrr. IS estirn;itcd from the heat prc;.. JSCUI of a t;l%tlnp animal. The ctXciency of ME utilization of ;1 feed is c&ulatecl from the r‘xjra nrcll ~II ;Inim;tI 1’radtizcs for each incrcas: in ME in;&e. .‘.n both ;:~st;ln~rti. heat production is derived from mwburements of oxygen consumption and carbon dioxide production by the animal. This means that tih;rnges in has31 met;tttism ;IS welt as in effIr*lcncy of ME utilization have a cxbrnrrwn dcrnb,mintitor in changes of oxygen c-tlnsumption. w!.~,z wnwmprbt ;~ppc;rrs to have 3 duai meaning for the animal. On 1hc tlnc h;lnrl. wxumption of oxygen is ii rlL.:.l*ssity for acrcbic organisms for the supply uf tinerg:; required for Inainten;lnw zr.nd r**?rpduc-tion of IiTc. On tht: other han6, cutisumption of oxygen ha5 dsmrlging efKccts on living organksms which are supposed to accumultilc In the course of life and to result in l(w of virality, agcing and finally death (Harman, 1986). The adverse effects Iink with the wnsumption 01. oxvg~n appear crucial for a bqtter under\ttinding of f&d intake hehaviour and perhaps, more generally, ofbehaviour, (hc intensity 01’ which C;LUSL’Sovyl en consurr.ptlon to rise progressively. This pawr starts with a brief rc~iew of harmful effects of oxygen use and the cnrrctation between oxygen ctinccznption and life span. From this we infcr that, in the course of evolution, animals will have developed mechanisms aimed at maximization of the effxiency of oxygen utilization. We will test this hypothesis by means of nrodel calculations using published data on voluntary feed intake and efficirncy of ME utilization in ruminants.

in aerobic organism,. ii&e mshr.mals, oxygen is hydrogenated to water in the process of oxidative phosphorylatic% to provide the energy for the synthesis

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of energy-rich compounds which are essential for maintenance of life. Inevitable by-products of this process are oxygen free radicals: a family of oxygencontaicing molecultis with one or more unpaired electrons (de Jong, 198 1; Miguel and Fleming, 1986; Oberley and Oberley, 1986; van Ginkel, 1988 ). These free radicals are highly reactive substances which can oxidize many different cell compounds. The living cell has a number of defence mechanisms to reduce the potential damage caused by oxygen radicals. First, a numbcr of smaller molecules like ascorbic acid (vitamin C), uric acid and glucose rcndily react with different oxygen radicals. In &c!ition, the cell has a more specific defence system, in the form of antioxidants like catalases, peroxidases, aad superolridedismutases which eliminate part of the radicals before they reach vital cetl compounds. Finally, the cell membrtine contains substances hke ar-tocopherol (vitamin E) which c&n stop certain chain reactions in the membrane initiated by the action of oxygen radicals (Koster, lY86; van Ginkel, 1988; Oberley and Oberley, 1986). The protective action of the aforementioned mechanisms is not complete: part of the free radicals oxidizes essential cell compounds like the membranes of the cell or cell organelles and DNA of cell nucleus and mitochondria. For instance, Brouwer et al. (1986) estimate the number of DNA damages in man as some thousands per cell per day. Organisms would soon lose their vitality if cells were not capable of repairing such damage. Modem azeing theories assume? however, that not all damage is repaired or that errors are made in the repair process. Especially the mitochondrial capacity to recover from ‘oxidative injury’ would be limited. This means that duting cell life there is an accumulation of damage which is not or only partly repaired. Such an accumulation results either in loss of function and death of celis or in uncontrolled division of cells and tumour development. Both will have negative repercussions for tissue and organ functioning. Finally, loss of organ function will accelerate itself and eventually cause the del;th of the organism as a whole (Qrdy, 1984; Brouwer et a!., 1986; Harman, 1986; Katz and Robinson, 1986; Koster, 1986; Miquel and Fleming, 1986; Vijg, 1987; Yu et al., 1990). The hypothesis that ageing is intimately linkec! to oxygen consumpticn was already formulated in the 1950’s by Harman and is supported by a growing number af publications (see for instance the reviews in Johnson et al., 1986; Brouwer et al., 1986; Koster, 1986). Although the scientific discipline of gerontology seems remote from the agricultural sciences, we think and hope to demonstrate that it can help to understand feeding behaviour of ruminants. OXYGEN

CONSUMPTKXJ,

VIT.ALIm,

DISEASE AND LIFE SPAN

!f the release of free radicals during oxygen use in tissues is the basic cause of loss of vitality: one may expect more rapid ageing to occur whenever daily oxygen consumption is relatively high. This is confirmed by correlations be-

twccn cumulative oxygen consumption and life span observed both between and within species. It is well documented .(e.g. Peters, 1983) that for mammsls in the mousr’ to elephant weight range, hotEl basal metabolism and average metabolic act ivit? increase proportionalIF to metrlblil’ ucight (MW;: Jt”‘.” ) while plt~ncijl lift: 5pan bnc+rc3sc’s in prrlp0rtlvn tn II.‘” ” . As maraholic activity is ;blrnOst u rmwzwo ullh i~gc’n ~on~urnptI~~n, 0crapc tutal lifetime oxy~~ uonxurrlpllr:r. ~hcrctim incm;lwts in proportion to I+‘. The rrveragc cell ~LIC does not ;~pf~‘t~cto ~nrre systematically with the size of animal species. hcncc the db ~rdgti Irft-tlrn~ cllniumpt ion crf cwygk*n by individu3l~tills is inrIc.f~c:ndcntof ~~c~t~stile. ohwr~;ltions of srnglc ~~11typos its. for cnamplc. r-~11sot’ hext musk-Iv ;rntf rrcp!r3!1~*) .z:::,:!;* 5 agree dh this gtzncral rule [,Pctcrs, 1983: I ‘alder. IW4: %hmidt-N&en. 11)114; SCC’ ~1s~Kctclaars and T~lkamp, 199 1). Rclatluni M*rrn cumulatl\‘e oxygen consumption rend p0tzntizll lift span ;~rr:nllt ;l)rsOIure: a notabk exception is man who lives rela~ivcly long taking intal ;ItiLljunt his rrvcragc mttlMiC raw. Yet, also within q..&es evidence exr-,1\ Vtlr ITIWT raptd qcing whcl;c-vcr the ralc of oxygen - ..,&jtained with IIIWL-I~slnd rodents. In Drrrsr~p~2ik.2 rrrt~lltr2olpus;w, lift span is inversely yroporlirjnal to llletabolic rate tc~~rdless of whether v;lr&ion in metabolic rate is the result of differences in genotype. temperatulc lx activity allowed. In this ymcies. sloti races of development caused by lc~wten,peratures or high IarGal L?r*;l,it: UC’ asauc’I;itcd with long lift spans (L:l;nb. 1977; Miquel and Fleming, I L)16.I -GM an other poi);iIotherms. tow tcmycratures or limited access to fcnjd. tcsulting in a decrcxcd r~xygen consumption rate, incrcasc lif’e span CI.amb, 19?? 1. Most rcscrrrch with nlamm;lls has been carried out with rats ;Ind mice. In these- experiments. oxygen ~l~nsumption has been changed by chronic dietan restrictian comparing tllc effect of restricted and ad Iibitum t;cding cjn lift ipan and dcvclopment rlf tumnurs and Mans. Withollt ewceptions it w;ls fildnd that ;it an slgc at which ad IiClilrtm fed animals had died, many of the rcstrictedlv fed animrtix were stil’ alive. These beneficial effects ‘~Pcfi~tar:, restriction mainly deperlct on the restricted calorie intake and are littIc influenced by the source of‘ calories: fat, carbohydrates or protein. A large number of disease conditions are more rare in restrictedly fed animals compared to ad libitum fed animals at the same age. Some observations suggest that the cumulative ox)*rcn consumption of ad libitum and restrictedly fed animals are little different (Berg and Simms, 1960, 196 1; Ross, 1961; Ross and Bras, 1975; Weindruch and ‘Nalford, 198.2;Kubo et al., 1984; Masore, 1988, 1990; Engclmsn ~:tal., 1990; Johnson and Good, 1990; Yu et al., 1990). Although studies of ~-II-*tLts of daily oxygen consumption on potential life

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span are still relatively scarce, the available observations are consistent with a causal relationship between oxygen consumption and yitality or life span as suggested by between-species mmparisons. Pr0ductive Iif: span of ruminants is an important parameter in some branches of livestock production, for instance dairy husbandry. However, for intensive livestock produtition it often appears more profitable to desigrt syslcms which maximize short-ten;rl produc?ivl?y without overconcern about lungevity. Obviously, the majority of our doli:estic animals is slaughtered at tin age which is only a fraction of potential life span. in a natural environment rzr under extensive livestock production conditions, longevity is of much greater importance as many individuals in a population die at an early age and reproductive parameters are generally much Icss favourable. Population models for cattle show that under extensive livestock conditions the decrease or increase in number is highly sensitive to changes in the aveisgc reproductive success of female animals (Dahl and Hjort, 1976 ). This means that the survival of the population is dependent on the reproductive success of a small group of females reaching a longer life span. Therefore, life span must have played an important role in. evolutionary processes. If we consider evolution by natural selection as an optimization process (Alexander, 1982), we may expect to find,an optimum combination of rate &‘oxygen consumption and life span in currentiy existing species. This is even more 1ikeIy if an increase in oxygen consumption rate, as a consequence of an intensification of certain behaviour, is not followed by a propor; tional increase in ‘fitness’, As we will show below. this stems to be true for feed intake behaviour. MAXIMIZXrKIN

OF THE EFFICIENCY

OF OXYGEN

I ITILIZATION

In his book ‘Optima for animals’ Alexander ( 198?) defined optimization of animal behaviour as ’ .. .the process crf minimizing costs or maximizing bcnefits, or obtaining the best possible compromise between the two’. In general terms, Alexander ( I982 1 considered cGsts and berrcfits of animal behaviour as ‘mortality or energy losses’ and ‘fecundity or energy gain’, respectiveiy. Before defining likely costs and benefits of feed intake behaviour more enplicitly, we want to stress that the use of such terminology does not imply that the animal intentionally tries to achieve a certain goal, nor that it is conscious of costs and benefits of its behaviour. Yet, we think that a theory of feeding behaviour is not complete without answering the question as to its aim (Raven. 1968 ): what is the aim of feeding behaviour? Since Darwin, we know of Mayr ( i 988) how a teleological - or ‘teleonomic’ in the +finition explanation of animal behaviour can in principle be reduced to a causal enplariation [Rust, 1988 ). The usual answer of animal nutritionists to this

The data presented by ARC ( ! 980) on the eficienoy of ME utilization mainly come from experiments with adult sheep. For this category of animals, ARC ( f 980) also prw,i LJCS separate estimates of roughage intake as related to differences in met:ib4izability (q, metabolizable energy as fraction ot‘grdss energy) of the fe&. Both data sets will be used for a first test of our hypothesis.

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Figure la shows the relation between NEI and MEI for an ‘animal fed an average quality roughage with a q-value of 0.55. NE1 and MEI have been scaled to basal metabolism (NE,). The model used for this purpose is: NEI=B*( 1 -e- B*MEr). The values for f? and p can be derived from the ef& cienc: of ME utilization for maintenance (k,) and gain (k,) according to Km and k, can be estimated from the R=X=,,,/ (km -k,) and p=k,+ln (k,/k,). +value of the roughage as &,=O.%+O,207*1q and kg= 1.32+q-0.318. Derivation of the formulae for S and p, and k,,,- and kg-values are given by ARC ( 1980). Figure 1a shows that, initially, NE1 rises rapidly as a function of’ME1 but that partial efficiency of ME utilization gradually faik Clearly, benefits (NEI ) per unit ME1 decrease as ME1 increases. Figure 1a also shows the observed voluntary ME1 and corresponding NEI, according to ARC ( 1980) (see also below). For our model calculations, the relationship between ME1 and NE1 had to be extrapolated beyond this level. Figure lb shows how heat production, again scaled to NEm, varies with ;MEl. Heat production has been calculated as MEI-NE1 + 1_The oxygen consumption is roughly proportional to heat production (see however the remarks below ). Figure 1b shows that the additional oxygen consumption per extra unit of ME consumed becomes higher as ME1 increases. From Fig. la and lb it is evident that with an increase of MEI, marginal benefits becornti progressively smaller and marginal costs progressively higher. But in our optimization approach MEI is only of secondary importance, unlike NE1 and oxygen consumption, here represented by heat production. Hence heat production is plotted against NEI in Fig. lc- According to our hypothesis! the optimum feed intake level is achieved when the ratio of benefits to costs attains its highest value. In Fig. lc this is the level of NE1 at which the tangent of the curve passes through the origin. All other levels of NE1 will result in a lower ratio ot’benefits to costs. The ratio of NE1 to total oxygen consumption is shown in Fig. Id as a function of NEI. Oxygen consumption has beea calculated from heat production as the latter is usually derived from measured oxygen consumption rates, taking into account r302 and methane production and urinary nitrogen excretion. According tn Blaxter ( 1989), heat produztion can be calculated from oxygen consumption using a figure of 19.7 kJ per litre 0: for a fasting animal which mobilizes mainly fat and a figure of 2 1.5 kJ per litre O1 for an animal which deposits large amounts of body fat. These figures have been used for conversion of heat production into oxygen consumption assuming that oxygen consumption per MJ heat produced decreases linearly from 50.36 to 46.51 Iitre when NE1 relative to NE, increases frcm 0 t3 2.0. In our example (Fig. Id). the maximum efficiency of oxygen utilization is reached at NEI/ NE n,= 1.35 and a NE1 per litre oxygen consumed equalling 14.84 kJ.l-‘. Using data of voluntaq feed consumption collected from the literature, ARC. ( f 980) caiculated a regression line relating \poluntav dq matter intake

d

1

2

Fig. 1. NE1 as a function of ME1 (a); hca~producth (HP; as ir fwction of AMEI(b); heat production as a function of NEI (c) and the effhency of oxygen utilization (NEI/Oz-consumption) ;ISa function of NEI (d). SEl, MEl, HP and O+onstimption havu been scaled to net energy for maintenance (NE,). .-\I: data apply to roughagesof metabolizability 0.55. Individual points on curves depict vall!:3 ccrrcsponding to the average observed voluntary intake crf such feeds in sheep.Al! accordir:g :
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(DMI ) of roughages to q for sheep with an average weight of 60 kg Estimated DMI for a roughage of q=OSS amounts tq 61.08.kg W-0.75-d-,1. This value can be converted to ME1 with MEI = DMI* 1B&q which gives a value of 6 17 H.kg W-0.75 .d-’ in our &le. The NE, for our reference animal can be estimated according to ARC (1980) as: Z=O.251*( IV/ 1.OB)‘-” +0.0106*W=5.74 MJ.d-’ or 266 kJ.kg W-0-75-d-‘_ Scaling MEI lo NE,,, WCfind a figure of 2.32. Inserting this value in the formula mentioned above with the appropriate values for B and p results in au average NEI/NE, of 1.38. We can further calculate a NEI per litre oxygen consumed of 14.83 kJ.l- ‘. ThiS estimate of NE1 based upon observations of ad fibitum fed animals differs only 2% from the NE1 for which the ratio between NE1 and total oxygen consumption was estimated to be maximal. Figure 2 shows the relation between the efficiency of axygm -utilization and NE1 for a number of roughages with q-values ranging from 0.45 to 0.65. These curves were calculated in the same way as explained above. The maximum value to which the effkiency of oxygen utilization can rise for any particular feed appears to increase with the metabolizability of the feed. The level of NEI at which the maximum efficiency is attained also rises with q. For a qvalue of 0.45 the maximum efficiency is found at an intake level close to

q=J.dS

Fig. 2. The effxiency of oxygen utilization (NEi/O~~onsumption) as a function of NEI for roughages ofmetabolizabiiity qzO.45, 0.50, 0.55, 0.60 artli 0.65. Individual points err cumes depict values correspondingt the a-:erage obsepcd voluntti+ intake of such f-ds in sheep. -411 accorAng 10 ARC i 1980).

.ll)lr

H.J.

I I~I.)LP~MI’.~ND

J.J.M.H.

KCI’ELAARS

I,nfortunatcI>. data sets with regard to intake- &rld efficiency of WE utili/xtwn differ i 1 .;omc rzswcts. The ‘pe!letcd dit*tc’ which &KC used for csti rnutti\ ~)t’k,,, ;~rd li, mainly comprised pelleted nlughages f,Blaxter and Boyne. I ij .+ 1 mhw. !i the ‘Zinc diets’ for which iat:lb data arc availahl~ contained r)n ~~vrrll;~t~ Jg7:, cr)i+ccntr;ltCT. EspuciaII~ for r:ilions of higher q-value. concentrates wt’rc the rnqtir ingr~dier~t. Hcr,ce. a test of the cWect of ration type is restktcd to .,ellcted rations of low mttatwlizability. Thus for a q-vaIue of O.JS the intaLc l~\~cl war c.aIculated at \rhich the efliciency of oxygen utilizat11bnbccomcs maximal, using, k,,, and I;, values for pelleted diets. The opti~tlnl intake f NEI/NE,,,= 1.67) is nnw mrtch higher than the optimum intake ti)r hmp rrqhrlgcs cjf’equa1 y (NE!.~V,= 1.05 ). This is mainly caused by a hi&r 4licicnq with which ME frrbn; pelleted feeds is utilized for gain. The ;1vw:1pc observed intake of ‘fine diets with q=O.45 appears to be 1.64 (NEI/ NE,,) and the averqe observed :~~?“G~of long roughages of similar q-value 1.02. Again, observed and predicted intake are almost identical. The estimates of k, and k,. for ‘mixed diets’ (consisting of roughage aud concentrates) g&e= 5:: ARC <1980) are, at least for the lower range of qvalues, higher than for roughages of equal q, From our hypothesis, mixed diets are thus expected to show higher intake than roughages of similar y? which is indeed conf‘lrmed 5:. the .r\KC ( 1980) regression analysis of data for cattle: irdtake is higher 3s the p~~~rtion of concentrates in a diet of a given q-value

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is higher. In the regression analysis of sheep data, the effect of concentrate portion on intake was not significant,, perhaps because concentrates on average made up only 5% of the diet. Unfortunately, a lack of data prevents fur-’ ther quantification of concentrate effects on NEI and oxygen consumption. The ARC: ( 1980) regress’ion models relating efficiency of ME utilization to rl were based upon a set of almost 1000 respiration data collected by Blaxter and Boyne ,( 1974). In a later publication (Blaxter and Boyne, 1978 ), these authors showed that apart from differences in q, also ditTerences in the nitrogen content of the feed significantly contribute to the variation in k, and k,. In the first pawr (Ketelaars and Tolkamp, 19X?) we quantified the effects of rl and nitrogen cor,tcnt un roughage intake using a set of 83 1 roughage feeding trials reported in the literature. Combining detailed information on intake and efficiency of ME utilization as affected by g and ,nitrogen content of roughages allowed a further test of our hypothesis. Calculations of optimum intake were again made for a sheep of 60 kg in the way explain4 above, except that k, and k, were now estimated from the analysis by Blaxter and Boyne ( 1978 ). Recently, Blaxter ( 1989) has summarized the results of this analysis presenting two equations: k ,=0.947-0.ooO10+(P~q)-0.128/q &,=0.9Sl -t-O.I)0037+(P/q)--.336/q, with P as the protein content of the organic matter in gakg- I. In the 831 roughage intake trials analysed by Ketelaars and Tolkamp ( 1992 ), voluntary digestible organic matter intake (DOMI, g-kg W-O.” l d * * ) appeared to be related to q and the protein content of the feed organic matter according to: DOMI = - 19.50+92.46tq+0.060+P

(r=0.89,

rsd=6.0)

In the regression analysis, the interaction between q and P was not significant. DOMI was converted to MEI (kJ.kg W-0*7s -d-l ) as MEI= 15.8+DOMX (NRC, 198 I ). Calculation of NH/NE, and the efficiency of oxygen utilization was done as before. For a number of feeds with combinations of 4 and nitrogen content. covered by both data sets, Figure 3 shows the average observed ad M&urn NE1 as compared to the predicted NE1 at which the efficiency of oxygen utilization attains its maximum value. Again, agreement between predicted and average observed intake is remarkable. Noteworthy are the data for roughages of a + value of 0.40: hot-h obsemed intake and inrake for w-hich sfflciency of oxygen.

P.J.

I-ClLYAhlP

AND

J.J.M.H.

KETELUKS

utili/;:tirm is pr~dic~ci to IX maximal lie bc!cuv maintenance IcveL Highest qualit? roughages have a predicted and obscrbcd NE1 of abou’L twice NE,. ‘Ihr niirogl;n cmtent of thr: feed bs ;i positiw cfTcct on predicted and obSSXVL’~NE11 NE, in all quality classes. On tiveragc, observed intake is 1% Iowcr than predicted. SV far only information on y and the nitrogen content of roughages has been u,cd to asknate &,, and &, bccausc rnorc detailed information is lacking. Apart .!?LNYI tfrcsc parameters other feed characteristics probably also affect the efficimcy of ME btithLii;P;. CIearl>, f;.~il intake research -would benet from a more comprehensive knowledge C! t’actors influencing the efficiency of ME utilization. EFFICIENCY BET!WEEbI

OF OXYGEN ANIMALS

UTILIZATION

AND

DIFFERENCES

IN INTAKE

In the first paper (Ketci~~rs and Tolkamp, 1992) the most important sources of animal variat6 ju intake were disc::szed. !r, the next paragraphs we will briefly analye to what extent predictions of our hypothesis agree with this variation in intake.

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In the model calculations shown above NE1 has always been scaled tq NL. This means that NE1 of ad &turn fed animals is expected to vary proportional to NE, if the efficiency of ME utilization for maintenance and gain remains constant. No evidence exists for systematic differences in k, and k, between ruminant species, at least not between sheep and cattle (ARC, 1980; Hlaxtcr, 1989). Hence, the observation of a proportionality between voluntary feed intake and basal metabolism in different genotypes (Ketelaars and Tolkamp, 1992) is in agreement with our hypothesis. The efficiency of energy utilization for gain between genotypes is negatively correlated with the proportion of energy deposited in the form of protein (e.g. Armstrong, 1982 ). Our hypothesis predicts that, as a result, also the voluntary feed intake will have a negative correlation with the proportion of protein in total energy gain. In the first paper (Ketelaars and Tolkamp, 1992) we discussed the evidence for such a negative correlation. The lc-el of voluntary feed intake relative to maintenance requirements decreases with increasing weight of the animal until finally both become t~uti in terms of net energy and an equilibrium weight is achieved. This finding deviates from the genera! rule observed between genotypes that intakti of a given feed is proportional to maintenance requirements. According to OIY hypothesis, a decrease of optimum NEI/NE, with increasing weight of the animal must be attributed to a lower efficiency of ME utilization. .4f first glance, such a conclusion seems contradictory to available literature data. However, only in a few studies have the possible effects of age or weight on the efficiency of ME utilization been examined. Part of these experiments has dealt with weight ranges still far from mature weights (Blaxter et al., 1966; Van Es et al., 1969). In some experiments which did include heavier animals: it was found that heavy and light animals did not differ in the efficiency of ME utilization; yet, in those cases, intake level’relative to maintenance requirements was not significantly different between the two types of animal (Bouvier and Vermorel, 1975; Graham; 1980). It is also worth noting that in several experiments no effect of weight on kg was found although the ratio of protein energy to fat energy in body energy gain changed with weight, sometimes considerably, for instance from 0.67 to 0.33 in the experiments of Van .Fset al. ( 1969 ). Contrary to this, Graham ( 1980 ) observed a lower & value in conjunction with a lower voluntary feed intake in young lambs, depositing mainly pro&n. compared to older and heavier sheep, depositing mainly fat. In an earlier cxpcriment, Graham ( 1969) had studied the effect of weight on the efficiency of ME utilizaCon by sheep of the -me age. He tmwluded that the efficiency was not different between lean and fat animals of 35 and 60 kg fleece-free fasted hod>. weight and tvith 5 z~d 20 kg bdl- fat. respec-

H.J. t-t,LKAMP.MitY

“1 t,)

I r;l:.111#;:1

-inil

J.J.M.H.

KETEL44RS

~:r~Jfna*Ir’l

- g iirrta1131 UL 11.)coatsinore ot’thc: ~;rtc~ufeed that1 a non-lactating .rninLd &I. ;: SIC: i%used rwre cfficitlntly f’or milk secretion than for body gain i4Kt;js ]R \’ ICWut’ the hypothesis do; A>pc~; here. a relationship bc! l\Hf’. IWCW thy twr) &rcr~~~~ionr seems obvious. In reality, no simple link can be vs!;lt;llshed. For the matuttr sheep which WL’ulced as a tefcrcnce animal in our c&ulotions so far, the Iota1 NE1 (NLm f N tY,) can be considered the benefits of fowl consumption. In this type of animal, NE1 refers tG changes in body re,‘1~crvc’s only. For a lactating animal. XIII has several components. To some cxtcnt, NL1 corresponds with changes in body reserves, and to some exte-At *.Gth chslngss in fat. prot**in and lactose sccretcd in milk. Although both components tire commonly cxprcssed ;IS SE, it is questionable whether they have the same meaning for the animal. The fact that lactating animals show a different partitioning of NE (between maintenance of bDdy reserves, gain and milk secretion) depending on genotype, stage of iact;ltion, snd feed composition suggest a negative answer to this quesiiun. Without knowledge of how the different components shck! be weighted, costs and benefits of feed consumption in lactating animals cannot be e,\paluated. Another ptobIem, of quite different nature, concerns tile commonly made Assumption that the effkkncy of ME utilization for milk production (kr) is independent of th2 Ieve! &I:’MEI. Blaxter f 1989) points to the problems involved in estimating the cttlciency of ME utilization in lactating a.nimals. A * . L I 3.:.

1.

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redu-sltion of MEI to. below its ad fibifum level causes not only a decrease of NE secretio.*AAin milk but generally also a change in energy retention. A review by ARC ( ! 980) shows that research groups have different ways of correcting for cuch changes; yet, all methods reported assume a linear relation between ME used for lactation and NE secreted in milk. Whatever the exact relation m’ay be, it will be difftcult to detect a statistically significaat departure from lincstity in view of the complications mentioned above. Simitar complications occur with regard to effects of pregnancy. Although nutrient needs may be expected to rise in the course of pregnancy, usually intake does not increase concurrently. Often, feed consumption even decreases&the final trimester of pregnancy. It is tempting to relate this to the very low et’ticicncy of ME utilization for energy retention in uterus, placenta and foetus (about 0. I 3 according to ARC, 1980). Yet, as in lactating animals, NE1 is also of quite complex nature in a pregnant animal. In addition, part of the total oxygen consumption by the pregnant animal takes place in the growing foelus. So both costs and benefits of feed consumption in pregnant animals are not easy to evaluate.

Long days and cold stress increase voluntary feed intake, and the increase in intake seems to follow rather than precede an increase in basal metabolism as discussed previously (Ketelaars and Tolkamp, 1992 1. These parallel changes in basal metabolism and intake are in complete agreement with OUT hypothesis. MAXIMIZATION PRINCIPLE?

OF THE EFFICENCY

OF OXYGEN

UTILIZ.4TION:

A UNIVERSAL

The harmful effects of oxygen consumption on vitality and poterltial life span of aerobic o:ganisms made us suppose that the intensity of animal behaviour will be controlled in such a way as to resu!! In a maximum efficiency of oxygen utilization. Feed intake regulation in ruminants appears to obey such a regulating principle. It is logical to assume that feed intake behaviotlr of other classes of animals will be controlled in a similar way. A test oi this assumptirpn is outside the scope of this paper. Yet, we can not refrain from quoting a striking analogy we found between feed intake behaviour of ruminants and foradng behaviour of a completely different species: the honeybee. The results reported by Schniid-Hempel et al. ( 1985) in a paper with the provoking title ‘Honeybees maximize their efficiency by not filling their crop’ can perfectly be understood in the light of our hypothesis (see also Ketelaars and Tuikamp. 199 E3. Se;jpile this striking analog); oytimitrltion criteria in manq’ other studies of optimal foraging hat-e ken different from ener_netic

B.J. TOL)r;r\MPAND

J.J.M.H.

KETELMRS

1982; Stephens and Krebs, 1986). A thorough evaluation in the light of the evidence presented here is clearly required. Apati from feed intake behaviour, also other types of behaviour may weil I-e controlled by the prkiple of maximizing efficiency of oxygen utilization. E\ idtrnrr may be found in studies of the rcgularion of locomatory beha\ iour. 1 IK i’c~ki,inraLc Ahab hour WCcxprcsred inlcnsity ;LSthe intake of ne-t Porgy ~wr’unit of’ timti. and the cficicncy of oxygen utilization as the intaLc tif ne: ~*nrrrgrm:r litrt” or!.grn wnsumcd. Like-wise. intrnsity of bcnmotcwj- hchavtl)llr IF mcasurrri as distwtnc’c milvcd per unit ot time. and the ttTkicncy of cwpcn utillz;llir)n as Jiutance rnllvcd per litrc oxygw r*wsumccl. The r~latiunnrhip Mwtben the twu px;rrnetcr~ has hecn studicri ;Imr,ne. others for swimmrng offis Jrrd waIkingof man (Pctcrs, 19X3: Blaxtcr. 1WI). For both ~pccic.~ optimum speed. i-c. the speed at which oxygen costs per metre moved XL’ Ioucst, apwars to agree uiith the prcfcrred speed of swimming and walkefficiency

CAlexander.

trig in rhrse sptxies,

Fig. 4. Thr cffik~cy of oxygen I:::.lization for locomotion (distance moved/oxygen consumed) in horses as a function of runni.!;; speed and type of gait (a); lines were fitted by eye. Fig. 4b shows a frquxcy disttibutio.. ; i speeds in relation to gait ofhorses which were not constrained IO a particular E.it [both Fig-;. T.&awn from Hog and Taylor, 198 I ).

I’EED

iNTAkE

REGULnTION

TN RUMINANTS

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313

sured in horses which were trained on a treadmill belt to move slower or faster than the preferred speed without changing gait. This was done for each of three different gaits: walking, trotting and galloping At least for walking and trotting, preferred speed was close to the optimum speed in terms of efflciency of oxygen utilization. For galloping this could not be confirmed with certainty due to technical problems. It is important to note a diflerence in interpretation of results. Although Hoyt and Taylor ( 198 1) actually measured oxygen consumption, they considered their findings evidence for maximization of the efficiency of energy utilization by horses. We have presented their results as an illustration of our hypothesis that animals behave so as to maximize the effjciency of oxygen utilization. From data on locomotion, a definite choice of either of the two

interpretations is not indicated. With regard to feeding behaviour, Schmid-Hempel et al. ( 1985 ) cocciuded that honeybees maximize the efficiency of energy utilization where we would see evidence for the maximization of oxygen utilization. Also in this case, wnsumption of oxygen and energy vary in a parallel way and therefore the data do not excIude either one of the interpretations. Huwever, maximizing energetic efficiency instead of net energy gain only makes sense if resources are allocated from a fixed budget (Stephens and Krebs, 1986). Indeed, Schmid-Hempel et al. ( 1985) drew at?eation to the fact that honeybees have a limited total ‘flight budget’, i.e. they can only oxidize a given amount of substrate and then the ability to forage is lost. The oxygen-free-radical theory of ageing offers an explanation for this limitation: it is not the consumption of energy per* se that causes flight metabolism to degenerate but the concomitant release of free radicals alue to oxygen conSiUiptiGn. In a para !!e! way, feed intake beh,I~~&-M~* . .VL- nfUs rrtminapte . L ._.-_- _-- rap _ he- _ pnn_I sidered to maximize efficiency of either energy or oxygen utilization. Again, maximization of efficiency of energy utilization only makes sense ifevery MJ of energy lost by oxidation can not completely be compensated for by a corn-. parable energy gain through feed consumption, but represents an irreversible prc+ loss of vitality and Iifct I~,P- In now opinion, therefore, the optimization CGSS studied here and in the work of Hoyt and Taylor ( 198 1) and SchmidHemp4 et al. ( 1985) should be interpreted in terms of maximizaticn of the efficiency of oxygen rathejr than energy utilization. The idea of a universal’principle underlying the control of widely diRering behaviour opens perspectives for new research. One of the intriguing questions is how animals succeed in cptimizing the intensity of any single behavioural activity. Still more intriguing is whether and how they succeed in optin:iGng the intensity of composite bchabiour, like for instance locomotion and feeding in grazing herbivores. As any type of behaviour is composed of a mixture of different ph>siologicaf activities. all contributing to changes in oxygen consumprion, body energy content and functional output, it ma>-k that

,; I 4

H,J. T~~LKAMt’.~NUJ.J.M.ti.

KETELAARS

similar processes are involved in the control of very different types of behaviour. A search for such a physiologic31 bxkground will b: the subject of the third paper in this series.

Hlax~c;, li.L. and A.W. Boync, 1974. ‘)uuIcd in AKC ( 1980). Hlaxrvr. li.l... and ..t.W. Ruyne. 1978. The estimation of the nurritive value of feeds as energy *IIUI~IY lbr ruminanls and the derivation offceding systems. Journal ofAgricultural Science, (knhridpcr. 90: 47-68. Rlaxr~. li.L.. 1-L. Clapperton ana F.W. Wainman. 1966. 1 ~t!iitation of the energy and protein of the fame diet by catrlc or tiiffrrcnt ages. Joumsl clr :QI icultural Science, Cambridge, 67: 67-75.

Brouwer. A., J. Vijg and D.L. Knook, lY86. Mvjisch-biologisch onderzock van het verouderingsproces. (,‘ahicts Bio-wctcnschappcn en r~I;1~‘schappij, 11: 9-15. C’zrlkr, W.rZ., IYSJ. Six. Funa:Iion, and Life Fiijllnly. Harvard University Press, Cambridge, I ISA, 43 t pp. 13ahl. G- and A. Hjort, 1Y76. Having He~,tf 1. ?;lstoral H-xd Growth and Household Economy. SroAholm kudics in Social Anthrupologv. Sruckholm, 335 pp. Engchun. R.W., N.K. Day, R.-F, Chen, 1’. Tomita, I. Bauer-Sardina, M.L. Dao and R.A. Good, lY90. ckloric consumption level ir:;Irxnces development of C3H/Ou breast adenocarcinoma with irldifference to calorie source. Proceedings of the Society for Experimental Biology and Medicine. 193: 23-30Ginkel, G. van, 1988. Zuurstof als gifstof. Natuur en Techniek, 56: 497-507, Graham. N-McC., 1969. The influc:-.Gz of body weight (fatness) on the energetic effxiency of adult sheep. .liustralian Jouma’ ! z,i.Qriculrural Research, 20: 375-385. Graham. N.McC., 1980. Variati~r! ‘11energy and nitrogen utilization by sheep between weaning and maturity. Australian JP! :r:lal of Agricultural Researr-h, 31: 335-345. Harman, D.. 1986. Free ladic:tl rhcory of aging: role of free radicals in the origination and evelution of life, aging, and Lisxss process. In: 3X. Johnson, R. Walford, D. Harman and J.

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Miquel (Editors j, Fr&Radicals, Aging, and Degenerative Diseases. Alan R. Lia, Inc., New York, pp. 3-49. Hoyt. D.F. and C.R. Taylor, 198 1. Gait and the mergetics of locomotion in horses. Science, 292: 239-240. Johnson, B.C. and R-A. Good, 1990. Chronic dietary restriction and longevity. Proceedings of the Society for Experiment&l Biology and Medicine, 193: 4-5. Johnson, J.E.. R. Walford, D. Hannan and J. Miquel (Editors), 1986. Free Radicals, Aging, and Degenerative Diseases. Alan R, Liss, !nc., yew York, 558 pp. Jont, P. de. 198 1. Hoe radicaal zijn zuumtofradicalen? Chemisch Magazine, February 198 1: 7 l-74. Katz, M.L. and W.G. Robinson, 1986. Nutritional influences on autoxidation, lipofuscin accumulation, and aging. In: J.E. Johnson, R. Walford, D. Harman and J. Miquel (Editors), Free Radicals, Aging, and Degenerative Diseases. Alan a. Liss, Inc.; New York, pp. 22 1-259. Ketclaars J.J.M.H. and B.J. Tolkamp, 1991. Toward a New Theory of Feed Intake Regulaticr. in Ruminants, Docionl thesis, Agricultural University Wageningcn. Wagcningcn, The Netherlands, 254 ppKetelaars J.J.M.H. apd B.J. Toilcamp, 1992. Toward a new theory of feed intake regulation in ruminants. 1. Causes of differences in intake; critique of culxnt views. Livest. Prod, Sci., 30: 269-236. kostcr. J-F., 1986. RidoeisrhP hacis van veroudering. De vrije radicaal-theorie. Tijdschrift voor Gcrontologic en Geriatric. 17: 99- iO3. Kubo. C.. H.C. Johnson, N.K. Day and R.A. Good, f 984. Calorie source, calorie restrictioo. immunity and aging of (NZB/NZWF)Fl mice. Journal of Nutrition, I 14: IS&I- 1899. L3mb, M.J., 1977. Biology of Ageing. Black, Glasgow and London, 184 pp. Masoro, E.J., 1988. Food restriction .;n rodents: an evaluation of its roIe in the study of aging. Journal of Gerontology: Riological Sciences, 43: B59-364. Masoro. E.J.. 1990.Asszssnlent of cz!titior,al tczpcnents in prolongation of iife and health by diet. Proceedings of the Society for Experimental Biology and Medicine, 193: 3 I-34. Mayr. E., 1988. Towz.rd a New Philosophy of Biology. Observations of an Evolutionist. The Bclknap Press of Harvard University Press, Cambridge, Massachusetts, 564 pp. hiiyucl. J. and J. Fleming. 1986. Theoretica and experimental support for an “oxygen radicalmirochondrial injury” hypothesis of cell aging. In: J.E. Johnson, R. Walford, D. Harman and J. Miquei (Editors), Free RaditiIs, Aging, and Degenerative Diseases. Alan R. Liss, Inc., New Yorli, pp. 4 I-74. NRC, 198 1. Nutrient Requirements of Goats. National kademy Press, Washington. DC. 91 PPOberley, L.W. and T.D. OberIey. 1986. Free radicals, cancer, and aging In: J.E. Johnson, R. Walford. D. Harman and J. Miquel (Editors), Free Radicals, Aging, and r)eEenerative Diseases. Ah R. Liss, Inc.. New- York, pp- 325-371. Ordy, J.M., 1984. Nutrition as modulator of rate of aging, disease. snd longerity. In’ J.M. Wordy. D. Harman and R. Alfin-Slater (Editors}, Sutrition in Geronto!ogy. Raven Press. tiew Yorkpp. l-17. Peters, R.H., 1985. ‘Inc ticological Implicstions of Bdy Size. Cambridge University Press. Cambridge. 329 pp. Raven, C.P.. 1968. Ontwikkeling ais lnformatie\erwerking. Een th~~retisch-biologi~hc stirdieWij:gerige Verkcnningen. Meulenhoff. Amsterdam. 159 pp. Ross, M-H.. 1961. Length of litheand nutrition in the rat. Journal of’Sutrition- 75: 197-ZirJ. Russ. 5I.H. and G. Br;lr. 1975. Food preference anti length or’lifc. sience. !?a: i6Z-!6? Ruse, !&I., 1918. Phitcrsophy of BioloR. Tcda:,. State L’nivrrsiry of Xc= l’ork Pre53 .Attii*>-. 155 pp.

3fb

B.J.‘I’OLL4Ml’ANLlJ-1M.H.KETELAAF.S

I LIII\ cct article nuus Piah~wns une nruvelIe hypoth& ;;1;311ti la rigularion de l’ingestion cl’alinktinlschrrLks rum;nan,s. a partir dc l’idtk que ce~c i ;;Aon amine des cotits ainsi que h-x birnk5ccs pour I’animal. Pour un animal non rcproducrcur nousconsidkons l’ingcstion d‘& ncrgic rwttc c-ommeun bGn@fireet la consommation cnnwmitantc d’oxygknc commc un cotit ti~snrdnnztiqur cc:;c~:;nwmmatinn occasionneindirg:&:mcnt une degradation acctl~tic de la \truc~u;.: III:? 4luIcs et, par cw~tiil’c!ucnt.uric rcsitricli~~lnde leur durtic de vie. Cc point de WC rww i; l’hywthk rluc 1~componement alimcntaiw serait oricnte vers une maximisation de I’cWc3c.ilL:d’u:illsaticln d’ox~g&w: l’animal mangcr;lit dc chaquc alimcnl uric quantitt tcXc que la i-onsommation d’&crgic nctlc par litrc d’oxygiwc ~lilisc serait IILLX~UA:. I.;n test approfondi & ccttc hypoth&c avtc dc*sAwmtics de la iittCraturc sur des animalrx non rcprrxlucteurs mcntrc bicn un accord quantit;;:i:‘ cntrc Its niveaux d’ingestion prkdits et obwc’c~L% dr? alimrnts qui varient considkrablrywnt cn function de Ia tcneur en &mcnts mitabolisable. dc la te~~r’urcn acute et dr la structw~ physique. De meme, les diffckenccs d’ingestion ::n rcistiun LWCEle5 difT&nctis dc nivcau du mitabolismc basal sont en accord avec notre hypr)\hkc. II c’s1plus difflcilc de tcstcr Its VILZSdc la m;llurit&. de la gestation et dc la lactation .~llr-I’ingeslion wee: notw hypothtsr parcu qu’il n’y a pas de donndes sufflsantes sur les effets de Is malurik wr I’efficGtt d’utilisztion dr I’inergie mctabolisable; le carackre exact des coti~set btSf~ces de i’ingt%ion dans les anim;luh csngestation ou lactation est Cgalemcntincertain. La maximization de I’efficacite d’utilisation d’oxygene pourrait bien etre un principe universcl gwvemant I’intensite des diff@rentesformes de comporien~nt, aussi bien de: r.:miz;;;:~ que de5monogawiques.

FEEDIKTAKE

REGUUTlONIN

RUMINANTS2

317

KURZFASSUNG Tolkamp, B.J. und Ketelaars, J.J.M.H., 1592. Zu einer neuen Theotie der Fulteraufnahmeregulation bci Wiederk9iuem. 2. Belast,ungund Nutzen der Futteraufnahme: ein Op!imierungrversueh. Livesf. Prod Sci., 30: 297-3 I 7 (auf englisch). Ln diesem Artikel entwickeln die Autorcn .eine Hypathese der Futteraufnahmeregulatian bci Wiederkiuem. Sic gehen davon aus, da0 die Futteraufnahme einerscits eine Belastungftir das Tier darstcllt und andererscits einrn Nutren bringt., Fiir ein nichtreproduzierendes Tier ist die Encrgicaufnahme als Nutzen, der gleichzcitige Sauerstoffverbrauch aber als eine Belastunganzuxhen, weil das im Ktirpergewebe indirtkt zu einer verstirkten Ijcschldigung der Zcllstruktur und damit zu Vitalititsverlust,

Alterufig und einer Beschinkung

der Lebensdauer fUhrt. Dicse

Betrachtungswcise fiihrt zu der Hypothesc, da0 die Fulteraufnahme auf eine Maximierung dcr Efflzienz dcs Sauerstoffverbrauchs abtielt: van jedem Futter wird gerade soviel aufgenommen wcrden, daB die Aufnahme von Neitmnergie pro Liter verbrauchtem Sauerstoff maximal ist. Eine ausftihrliche i)berpriifungdiescr Hypothesc mit Angaben aus der Literatur iibcc nichtreproduzierende Tiere zeigte eine entsprechende quantitative ubereinstimmung zvvischender vorausgesagten und der beobachtetcn Aufnahme von FuaerstofTen, die bcziiglich der Verdaulichkeit, des StickstofQehalts und der physikatischen Eeschaffenheit erheblich variienen. Auch der Zusammenhang der Futteraufnahme mit dem Grundstoffwechsel stimmt mit dieter Hypothese iikrrtin. Die Effekte Gcs Reifestadiums und des physiologischen Zustandes sind schwieriger zu fiberpriifen, weil nicht geniigend Ang&en iiber den EinfluD da Rciftstadiums auf die Efflzienz der Verweflung der umsetzbaren Energie vorliegen qnd wegen der ungenauen Kcnntnis der AR der B&stung und des Nutzens der Futteraufnahme in ttichtigen und Iaktierenden Tieren. Die Maximienmg der Efflzienz der Sauerstoffverwertung urird als ein allgemeines Prinzip angtiehen, da13die IntensitCr von verschiedenen Formen des Vcrhaltens SC *ahI hi Wiederkauern als such bei Monwstriden bestimmt.