Influence of winter feed restriction and summer compensation on skeletal development in red deer stags (Cervus elaphus)

~ f l u e n c eof winter feed restriction and summer cornpensatinn 0in skelcetal developn red dceer sta: ~ V U Sel;aphus) M. SUTTIE*, G. WENHAM, R. N. B. KAY, Physiology Department, Rowett Research .Institute, ucksburn, Aberdeen, AB2 9SB

he influent:e of two p lanes of nlutrition (u nrestricted ~d 70 per cent resl ricted dulring the Iwinter) on -1-6-1 ,I--.. .I,.--..-. -8.-3 :lI.."*-*, .A L-.*I.* " S A C l C l a l UCVCIUJIIIICIII IIIU~IIZIICU u y IIIC IIICLIILIII ~ U was studied in 12 red deer stag calves. At approximately three-monthly intervals from January 1978; when the stags were seven months old, until Augusl '779 when the stags were 26 months old, radiographs the right metacarpus were taken. From the rultant radiographs, diaphyseal length, diaphyseal eadth, breadth of mineralised bone, cortical bone dex and a rea of mineralised bone were measured. rowth in length was complete by August 1978. no differences in length between the lere were . . restricted and restricted stags a t that time. Di fferences in breadth, area and cortical bone index wt:re maintained throughout the study although diilferences in area of mineralised bone were the only mceasure significantlv different throughout the study. It is considered thai I tle major iinfluence olf plane of nu~tritiononI this inde,x of skelcetal develc>pment in deer. is an.~d thickness of cort ical bone, . on. tbreadth . rasuitlng in a weaker bone of the same length in the nter restrilcted stags.

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cockerels sel/ere under nutrition reduced stature, but re:tlimentatic )n restore(1 the structure of the bones to no rmal (Pratt and Mc:Cance 1961). Undernutrition p .~ g snowever reauced skeletal growth in the long nes but did not halt it entirely. Despite iabilitation, striking differences between underurished pigs and well fed controls were noted (P ratt and McCance 1964a, 1964b). Ellis and La wrence (1978) found that during a period of u ndernutrition the fore limb of filly foals grew in lenlgth but to a lesser degree than well fed controls. e proxims11 appendicular skeleton matured up to e year b efore the distal skeleton in the pig 'enharn et al 1973) and in consequence long bones, . ^___I-,. rxarlluie the metatarsus., mav . be a l e ~ ssensitive inclicator of 1post weaniIng nutritic; n a ~status than, for

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Pretent a d d r e w Invermay Agricultural Research CcWre. Private Rag. biocgiel. New Zealand

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e, the hunierus in cattle up to Iline montl :t al 1976) L-. - ..-C . . l V ~ I ~ ~ J I I ~YI U V I U C S a u b c r u ~ LCLIIIII~U~ : 1UI measur ing skeletal growth and development se:rially in livir~g animals. The aim of this study w,as to examin e the growth of the metacarpus of each a1nimal . at. .~ntervals to determine accurately the effect or ~t planes ()f nutritio:n on this tlone. Materials

and me,thods

Twel ve red d eer stags were malntalnea on a nutriticIn trial described fully by Suttie et a1 (1983). In brief, s ix stags u,ere fed to appetite for three years ,.._..__*_ -:-.-A, --A (urlrrsurlclru) and the remainder were fed 70 pel- cent of appc:the (restricted) from August to May of their first ye;i r of life, November to May thereafter a nd to appetitc:during the summer. The trial was desiigned to test Ithe hypothesis that poor winter nutritior i and subseq~ lent failure to compensate dur ing the surnmer was responsible for small red deer st;ags in Scotland compar,ed with European population:S. approximately three-monthly intervals from January 1978, when the stags were seven month!j old, until August 1979, when they were 26 months old, radiographs of the right metacarpus were taker1.. . he 1<-ray unit used was a 200 kV, 1000 mA Tr~plex Optima tic (Elema-Schonander, Sweden). Using a 37.5 x 115 cm non-screen film (Kodirex; Kodak) at a focus-tc . ...- ..)-film distance of 100 cm the exposure fartnrc -..,." for the antero-posterior projections were 70 k\ ' and 40 mA . The animals stood with the right falreleg flexed a t the elbow. The film envelope was positi oned ~ ~ n d pt he r "....%' metacarpus to include an area fron tho distal rztdius and ulna to the phalanges. A collinlator was use,d to limit the useful emission to the arc:a of the filmI. A sheet of lead rubber was placed bet ween .L- c:lLllC 111111 and the film stand to reduce the broadsc of radiaItion. The handlers adl wore p rotective ~ ar and gloves of lea(i rubber. From Ithe diaph yseal .length . ;andthe . the . resldiaphyseal .lltant radliograph . .. breadth were measlIred. The di aphyseal length was taken between the proximi21 extremity of the metacarpus and the (iistal epiphyseal growth plate. The breadth measure rnent

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Resul ength, diiaphyseal breadth, cortical Die .. . bone Index, breaatn or mineralised bone and area or miner.alised bone measul.ements fc)r each oc:casion when radiographs were tziken are slhown in T able 1. are given as well as ons measure G la: Metac;wpus of deer and dimens11 )f Mean values standard .error ..-. . . . - - ... , . ttre Done Detween epipnyses. A - u ureaorn or Done. L- u arla levels of signific:ance for Ithe differences betwren t h e X - Y Breadth of mineralissd bone t w o g roups. FIG lb: Schematic representation of ltney U test showed t hat the A cme tailed F triansverse section showing dimensions n diaph yseal length ot the unrestrlctea groul3 grew icantly faster at the 5 per cent level until 3, (as taken ,at the miclsnarr on a line drawn perper I- signif but, during part of the catch up phasieMay from 1978 icular to t he long a:(is of the bone. Along this line 3, 1978 until August 14, 1978, the re:itricted 1e cortical1 bone indlex was calculated as shown i n May . -arouc.I grew significantly faster at the 5 per cent level. Growth was complete by August 14, 1978 ana an asymptote was reached. A similar Mann-Whitney U :ortical bon e index (per cent) test on diaphyseal breadth showed no significant Barnett ar1d Nordin 1960) differences in rate of growth between the grounq. -r.-. L U + A Y = breadth of mineralised bone (cm) Diaphyseal breadth, cortical :1 )one index and breadth of mineralised t)one all showed generally AB = diaph yseal brea dth (cm) significant differences be1tween grolups due tc) plane -1 c 11U -.mition, although thelc n a > >"me indica r ; n n nf u Then an assumpt ion was Imade thalt the bonle catch up growth in bread1th of minemralised bo ne. No ould be considered as a cylir~ d e ras illustrated in meas1 re effectively reflec:ts the wici e differelIces in 'ig lb. body! weight that were (xcurring through01~t this -, . . I ne area of minerairsea Done was tnen caicu~atea stuay Are:a of miner.alised bonie (Fig 2) slhowed the largest s follows: differ ences betvveen the g~roups, alttlough dur ing the rea of min eralised bcsne (cm2): $ until No! {ember from first catch. up.ptlase, . . I May 197f , , . .-, , . -.-.. U e U Ln ([ABjL- LAB-LU-XYJL) 1978 and after it, the differences were smaller. 4

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The lacK 01,...,.. slgnlrlcant alrrerences In diaphysea~ length between the groups indicates that the effect of plane of nutrition on the length of this bone is limited. The metacarpus matures r iaplaly, '"- -ISslDly --"-'~ PC due to its important weight bearing fi~nction,a1. ~ the d asymptotic length is reached fairl!y early inI life. mon Although few radiographic studies have itored . ..skeletal development from early in lite until maturity, Wenham et al (1973) showed by Iradiography that the metacarpus of the pig was the stecond fastest maturing bone in the body of the pi15 (the fastest was the metatarsus) as it reached three quartelrs of its pc)st natal asymptote in 127 day:;. The humerlus took 1110 days to reach this stage. IVonetheless the metacarpus is more convenient to X- ray in vivo in a deer than the humerus a.nd is a rl available byproduct of slaughter . Conver mitigates for its use in radiographic studies. ., rerlecl " . No measurement of breadth reairy alterati on in plaIne of nu trition of the stags,, but breadtl1 of miner,alised borle is possit>ly the bes,t. All t ~3 b naalograpns taken In January IYII. Metacarpal bont!S of an unrestricted stag on the left and a restricted stag on t h3 ~rlght. Breadth of mlnerallsed bone IS greater at the mtd polnt of t tbe shaft (marked by horizontal llnel yet there IS llttle difference In le~ ngth of the bones

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ree measu rements o f breadth show that: although . : resrricreu2 gruup were significantly 2;mailer in nuary 1978, they caught up, but not completely, Novemk ler 1978, after which neither group owed furtiier growth. It is considered that plane of trition ha.s an important early effect on meta~ -oreadth ...-. - , but after the first period of catch u p rpus 3wth the breadth is fixed, and as the bone is narkably stable, further alteration in the plane of trition during the second winter has little or no Fect on the dimensions measuI.ed. The .area of mineralised bon e is moreI seriously other rected by plane of nutritic)n than the . ... :asures since the effects of poor early nurrlrlon are Illore permanent. This may limit the amount of catch u p growth in weight that would be possible since a smaller frame would not be able to support the potential maximum bodyweight. This presumes that :hange in nutritional circumstances, after a period undernutrition, does not influence the size of the :tacarpus if it has matured, that is if the epiphyses ve closed, at a smaller than eotential size. In fact --. se\/era1 studies have shlown that this may not be the bone of choice for shc)wing sma I1 changes in size or stress of structure caused by the .- nu . ettritional nr,:gnancy and lactation (Benz~e al 1960) or copper ficiency (Mills et a1 1976). However, Pratt and :Cance (1964a) found that the epiphyses of {erely restricted pigs opened after realimentation CO mmenced. In the present study changes in the mr:tacarpus took placc2 before I:neasureme,nt began, five months after (iietary re striction was first imposed. This indicate s the sensiltivity of th e skeleton . . nutritional restriction at tnls early stage or growrn. What is the relevance of these d&a for deer on the ottish hill? The winter restricted stags in this study mpensated fully in length of bone but not breadth area of mineralised bone, thus their thin bones were presumably weaker than thick bones of the same length. Although there was no reduction in either diaphyseal length or breadth in the present StUidy, this may be due to the relative lack of severity of the nutritional regimen. It may be that Scottish hill d eer~ eat substantially less than 70 per cent of their DOssible intake and this may be of much poorer stags. Had e qu alitv than that fed to the e x ~mrimental thf : winter undernutrition been more sevc:re in the eal length Prc:sent study then differences in diaphys~ a n d breadth might have been shc>wn ..... A guarded extrapolation may be made from this, ;uming very poor nutrition limits size, to the rest of : skeleton. It may be lighter, if not shorter, less ong and much less able t o support a large body size imal. Studlies on hill ~ . . . A : L -

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x e d seasclnal fluctu sheep 1lave show ective of I in ash content olI tne sKelr:ton irresp ~. .Inmn..rlr +uvuat ~ - - l aLuxatlua 3f pregnancy and lactation (<*.r.,awell et al 1964). No seasonal fluctuations were f 'ound in the I)resent study, possibly because of the in:sensitivity c~f the metacarpus to such changes, but: it is 1:' -...kelv that deer are subiect to seasonal fluICLUiitions iri calcium and p h o s ~ ~ilabilityo n the hill. neral The Scottish h ill biotype: is knowr .* .L---..: -:-- UI ,.c ..-..t.. UUL ulr ~IUVI>IUII supplcrlrclliar y U r l l C l r I 11, mineralIs does no~t improve the performance of hill sheep (Orr and F'raser 1932, Benzie et a1 1960); it is in only . ....when an erlergy source is fed, eg, maize, -' aaaitlon to mtnerals, that improvements are m aae. It inc:reases a stag's reproductive fitness to grc3w as large a.s the environment can maintain (CluittonBrock :t al 1982) and this entails growing as la rge a skeleto~ n as the environment can maintain. As bone breadttI does not vary much after the bone stops growin!5 in length, good early nutrition is vit al to build a strong, well mineralised skeleton on whi ch to supporlt a large b odyweight r

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Kererences J Radio1'ORY 1 1 . BARNE'TT.E. & NCI K U I N , tl. t.L. ( I ~ ~iinical 166-1 74 BENZIE, v . , tlurNE, A. W., DALGARNO, A. C., LDUCKWORTH, J.. HILL, R . WALKER, D. M. ( I W ) Journnl or Agricultural Science, Cambridge 54. 202-22 1 . & ALBOKI, S. D. c : ~ ~ ~ ~ ~ B ~ ~ " ; ~ ~ ; i ~ , " ~ ~ ~ , " ,Chicago. " ~ e ~ ;Unsiversity f r,, Chicago Press CRESSVVELL, E., BENZIE, D. & BOYNE, A. W. (1%4). lournol of .icultural Science, Cambridge 63. 387Brirish ELLIS, R. N. W. & LAWRENCE. T. L Vereri~ wry Journal 134, 322-341 MILLS, C. F., DALGARNO, A. C. & W E i u n n ~ .U. ( 1976) British Journal of Nutrition 35, ORR. J . B. & FRASER, A. H. Transactions of the Highlarnd and Agricultural Socit ld 44, 64-85 !) British Jourrnal of PRATT, C. W. M. & McCANCE N,rtririjon 15,121-129 PRATT. C. W. M. & McCANCE, R. A. (1964a) British Jobrrnal of Nutrition 18. 393-407 PRATT. C. W. M. & McCANCE, R. A. (l964b) British Jourrnal of Nutrition 18, 613-623 SUTTIE. J . M., GOODALL, E. D., PENNIE, K. & " A " R. N. B. (1983) Bri fish Journal of Nutrition 50. 737-747 WENHA,M. G.. FOWLER, V . R. & McDlDNALD, .I. JOUrn"rl of Agricult ural Science, Cambridge 110. 125-133 -

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~ e c e i v e dfor publication May r o, 1983