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1 Quarterly Journal of Experimental Physiology (1971) 56, A COMPARISON OF DIGESTION IN RED DEER AND SHEEP UNDER CONTROLLED CONDITIONS. By G. M. 0. MALoiY* and R. N. B. KAY. Physiology Department, Rowett Research Institute, Bucksburn, Aberdeen, AB2 9SB. (Received for publication 17th March 1971) Three red deer hinds and three sheep were given rations of chopped or pelleted hays. The deer apparently digested dry matter and cellulose a little less well than the sheep. Digestibility of nitrogen did not differ. In two pairs of animals fitted with rumen cannulas the volume and outflow of rumen fluid was greater in the deer than in the sheep. The ph and the concentrations of total and individual volatile fatty acids and ofammonia in the rumen fluid varied during the feeding cycle in much the same way in the deer and sheep. The rumen fluid of the deer seemed to be a little less well buffered than that of the sheep. It is concluded that digestive processes in the deer, as far as revealed in these experiments, quite closely resemble those in the sheep, though certain small differences may exist. The nutrition of wild animals depends both on the nature and quantity of food that they eat and on how well the food is digested and absorbed. The grazing behaviour ofwild red deer (Cervu8 elaphus, L.) is being studied extensively by the Nature Conservancy [1967] and some information is also available concerning park deer [Bannerman and Blaxter, 1969], but relatively little effort has been made to study digestive processeg in these animals. We have therefore compared some aspects of digestive function in tame deer and sheep under conditions which excluded behavioural differences as far as possible. Most of the digestible organic matter eaten by domestic ruminants is fermented in the forestomach and so most of our observations concerned rumen function. A preliminary account has been published [Maloiy, Kay and Goodall, 1968]. METHODS Animals. The observations were made on three red deer hinds (A, H & S) and three Scottish Blackfaced ewes (A, E & K). The deer weighed kg and the sheep kg, and all the animals were between 2 and 4 years old. Each, except Deer S, had been fitted with an ebonite rumen cannula some months before the experiments began. Details concerning fistulation of the rumen and management of the small herd of hinds of which the three deer formed a part have been given [Maloiy et al., 1968; Maloiy, 1968; Goodall, Kay and Maloiy, 1968]. During experiments the animals were kept in metabolism cages, which permitted separate collection of faeces and urine, at a room temperature of about 18 C. At other times they were housed in individual pens bedded with sawdust. Digestibility trials. The digestibilities of grass hay and lucerne hay were examined in three deer and three sheep. Two batches of rather stalky grass hay were pelleted or chopped and a single batch of lucerne hay was chopped. Various rations, providing the dry matter intakes shown in Tables I and II, were given as two equal meals daily. * Present address: Animal Physiology Division, East African Organization, Muguga, P.O. Kabete, Kenya, East Africa. Veterinary Research 257
2 258 Maloiy and Kay The animals received each diet for a preliminary period of at least 3 weeks, and then representative samples of moist faeces and urine were collected daily during a 10-day digestibility trial. Urine was preserved by addition of a few drops of toluene or 10 ml of concentrated hydrochloric acid to the urine container. The cumulative 10-day samples were stored at 10C until analysed. Composition and volume of rumen contents. The two deer and two sheep concerned were given in turn pelleted dried grass and pelleted grass hay. The deer received 1,200 g of grass and 1,400 g of hay daily, and the sheep 1,000 g of either diet. These rations approximated to the maintenance requirements of the animals, the greater intake of the deer allowing for both their greater size and their higher metabolic rate [Brockway and Maloiy, 1968]. The day's ration was given as two equal meals, at and hr. It was fully consumed, usually within 20 min. TABLE I. The intake of dry matter and the apparent digestibility of dry matter and cellulose by deer and sheep Apparent Body Dry matter dry matter Cellulose Weight intake digestibility digestibility Diet (kg) (g/24 h) () (%) Deer S Grass hay 1 (chopped) S S Grass hay 1 (pelleted) 45 1, A Grass hay 2 (chopped) 53 1, H 50 1, S Lucerne hay (chopped) 50 1, Sheep K Grass hay 1 (pelleted) K Grass hay 2 (chopped) E A Lucerne hay (chopped) Samples of rumen fluid were obtained by aspirating about 500 ml of contents from various parts of the rumen by means of a tube introduced through the cannula, and filtering immediately through surgical gauze. The solids and all but about 50 ml of the fluid were returned to the rumen. The samples were taken about 0.25 hr before the meal and at 0 5, 1-5, 3.5, 5.5, 7.5, 9-5 and sometimes 11i5 hr after offering the food. Samples were drawn in this way on 5 consecutive days. The volume and outflow of rumen fluid were measured by the method of Hyd6n [1961]. Polyethylene glycol (PEG), mol. wt. 4,000, was introduced into the rumen just before the meal as a solution of 15 g in 250 ml distilled water for the deer and 10 g in 200 ml for the sheep. The concentration of PEG in strained rumen fluid was found by analysis of samples taken, as described above, 0-25 hr before and 1-5, 3, 6, 12 and hr after dosing. This procedure was repeated on 5 consecutive days. The volume of rumen fluid was derived by calculating the concentration of PEG in the rumen at the time of dosing by extrapolating to zero time the straight line relating the logarithm of PEG concentration to time after dosing. The rate of outflow of fluid to the omasum was estimated from the slope of this line and rumen volume. Chemical analysis. The dry matter content of food and faeces was determined by heating at 1050C for 48 hr. Total nitrogen in moist samples of food and faeces and in urine was estimated by a macro-kjeldahl method. Cellulose was determined in dried samples by the method of Crampton and Maynard [1938]. The ph of the rumen fluid was measured potentiometrically within 3 min of taking
3 Digestion in Deer and Sheep 259 4'I c4 00c P O CX O i 10 _ V VC O to CO e e10 o. *'. *o *o r 11 e o oo X - O CO _ 0) (m 0 to eq _- X XM C XM 00C*cqc cq 9 CO0 0 q c 10 t-t. t oo Co Co Co m X- to C C) CO CO '-"0 CO 00 '10 ~4 104)4101 0C C* 14*1 ~I F4 E1 p~~~ 0 pt 0 04
4 260 Maloiy and Kay the sample. Ammonia was measured by the micro-diffusion method of Conway [1957]. Total volatile fatty acid (VFA) was estimated by steam-distillation using Markham stills and individual VFA by gas-liquid chromatography [James and Martin, 1952]. PEG in strained samples of rumen fluid was estimated turbidimetrically by the method of Hyd6n [1955]. RESULTS Digestibility trials. The apparent digestibilities of dry matter and cellulose are given in Table I. Grass hay 1 (chopped) was given only to Deer S. In comparing the digestibility of the remaining diets it will be seen that the three deer digested the dry matter and cellulose of the grass hays about 5 and 10 percentage units less fully than did the three sheep. On the other hand, in a single comparison lucerne hay was digested better by a deer than by a sheep. Table II gives values for the intake and excretion of nitrogen in the same trials. There was no consistent difference between the deer and the sheep in the apparent digestibility of nitrogen or in the fraction of dietary nitrogen excreted in the urine. The positive nitrogen balances correspond to the expected loss of nitrogen in the hair or fleece, 1-2 g daily. TABLE III. The volume and rate of outflow of rumen fluid in deer and 8heep (Mean value SD for 5 consecutive daily measurements) Outflow/hr Body Dry matter Rumen (as % of weight intake volume Outflow rumen (kg) (g/24 hr) (.) (ml./hr.) volume) Pelleted dried gra88 Deer A 51 1, H 49 1,086 6*8± Sheep E i *5 K '2± Pelleted grame hay Deer A 48 1, ± *1 H 46 1,235 6*0± ± Sheep E ± K ± Volume and outflow of rumen fluid. The results are summarized in Table III. The volume of fluid in the rumens of the two deer was consistently greater than in the two sheep. This difference, about 38 per cent, was greater than the difference in bodyweight (about 14 per cent), and was also greater than the difference in food intake when grass was given (20 per cent) though not when hay was given (40 per cent). The rate at which fluid flowed to the omasum, similarly, was faster in the deer
5 Digestion in Deer and Sheep 261 than in the sheep, though this difference largely disappeared when the flow was expressed as a fractional flow rate, i.e. relative to rumen fluid volume. Composition of rumen fluid. The changes in ph, total and individual VFA and ammonia that were observed in rumen fluid in the course of a feeding cycle are shown in Figs 1 and 2. The values shown are averages for the two deer (A and H) and the two sheep (E and K) during 5 successive days. It can be seen that no difference of any consequence was apparent between the pairs of animals for any of the measurements; in fact the differences within the pairs of animals were often as large as those between the pairs. As would be expected, the grass diet c 7.0 F v deer,, 6.0 Ed? o 5-0_ ffi 4.01 <-o sheep E JE 8 E,.- d = - X 80 - SO 70 - U. ~~~~~~Acetate 0 _ C Propionate 20 Butrate 10 _>= = 0 2 L TIME AFTER FEEDING(h) FIG. 1. ph, total and molar proportions of volatile fatty acids (VFA) and ammonia-n in the rumen of deer and sheep given a diet of pelleted dried grass. Each point gives the mean value for two animals. The animals were fed at 0 and 12 hr. VOL. LVI, NO I L
6 262 Maloiy and Kay (Fig. 1) gave rise to a rather more marked fermentation than the hay diet (Fig. 2), with slightly higher values for total VFA and ammonia and a lower proportion of acetate in total VFA. *_-. d"r 7.0 _- v Cheep S%O Q h I *I _ i 120 Ia.I [ : [. I. *I BI so - 70 I 60 Ị1. S0 e 4 h so l r * s e.-m _8_ Acetate P:opionate ~....,......,I Butyrate FIG. 2. I-I I I I I I I I -a = =, I 0 2 t 6 a TIME AFTER FEEDING(h) ph, total and molar proportions of volatile fatty acids (VFA) and ammonia-n in the rumen of deer and sheepgiven a diet of pelleted grass hay. Each pointgives the mean value for two animals. The animals were fed at 0 and 12 hr. Total VFA has been plotted against ruminal ph in Fig. 3. Each point represents the average of the five values obtained for each animal at each interval after feeding the grass or hay. It is apparent that the values are not distributed quite linearly, for they are affected by the sigmoid titration curve of VFA, and that the values for the deer tend to be a little more acid for a particular VFA concentration than those for the sheep.
7 Digestion in Deer and Sheep 263 The regression equations relating ph (X) to total VFA in m.mole/l. ignoring the slight non-linearity, were as follows: (Y), deer: Y = -51X+383 sheep: Y = -51X+390 The slopes are identical, but the intercepts differ significantly (P <0001). E LL I- t- 0 c: ẉe 6.0 Ruminal ph. FIG. 3. The relationship between the concentration of total volatile fatty acids (VFA) and ph in the rumen of deer and sheep fed a pelleted grass hay diet. DIscussIoN Our experiments were undertaken to compare certain aspects of digestive performance in red deer and sheep. However, it is very difficult to generalize from results obtained using only two or three animals of each species to the *
8 264 Maloiy and Kay species as a whole. The appearance of a major difference between one group of animals and the other would provide a suggestive indication of a substantial divergence between the species, provided that within-group variations were not large. On the other hand it is impossible to tell whether smaller differences between the groups, no greater than within-group variation, reflect individual idiosyncracies or a true species effect. No major difference was detected. Our deer and sheep digested their rations to a similar extent and fermentation of food in the rumen followed much the same course. This resemblance between species is important; it suggests that the differences in rumen chemistry and microbial function noted by Hobson [1969, 1970] in deer and sheep grazing the same hillside are due more to the type of food selected, the amount eaten and perhaps the diurnal grazing pattern, than to differences in digestive function. Similarly, other authors have found at most only small differences between various species of cervids and of bovids when these have been subjected to controlled digestibility trials [Bissel and Weir, 1957; Nordfeldt, Cagell and Nordkvist, 1961; Eriksson and Schmekel, 1962]. Despite this general similarity, some of the small differences that were observed may reflect true differences between the species which deserve further research. The apparent digestibility of dry matter by the deer was about 3 percentage units less than in the sheep. A somewhat greater difference, 5 percentage units, had been found in another experiment in which some of the same animals received a pelleted straw-plus-concentrate ration and this difference seemed too large to be due to the greater food intake of the deer [Maloiy, Kay, Goodall and Topps, 1970]. Similar differences have been noted in comparing three other pairs of deer and sheep receiving various long roughages [Maloiy, 1968; Kay and Goodall, unpublished observations]. In these experiments the lower apparent digestibility found in the deer seemed to be associated with a more rapid passage of food through the gut; a similar observation has been reported by Gill [1961]. While relatively rapid passage of food in deer would be expected to result in less complete digestion it might permit a greater intake of food, perhaps a net advantage to an animal forced to depend on poor roughages for part of the year. The apparent digestibility of nitrogen, and the fraction of dietary nitrogen excreted in the urine, were much the same in our deer and sheep. However, another experiment which was designed to examine nitrogen metabolism in more detail revealed certain small differences [Maloiy et al., 1970]. The volume and outflow of rumen fluid was substantially greater in the deer than in the sheep but this may be explained by the larger size together with the greater food intake of the deer. The volume of rumen fluid in the deer, , was only about a quarter as much as has been found in Polish and German deer by Gill and Jaczewski [1958] and Feustel [1967] respectively. This difference may be due partly to the relatively small rumen volumes associated with pelleted diets, and partly to the much greater size of continental red deer. The course of digestion in the rumen was very similar in both pairs of animals. The ph and the concentrations of VFA and ammonia within the rumen were closely alike, varying as much between individuals as between the pairs. The
9 Digestion in Deer and Sheep 265 relationship between ph and total VFA concentration differed significantly, however, suggesting that there may have been some difference either in the amounts of alkaline salts secreted into the rumen in the saliva or in the rate of absorption of VFA from the rumen. Short, Medin and Anderson [1966] found very acid conditions in the rumen contents of wild mule deer shot in Colorado though this may well have been due to the accumulation of VFA during the long interval between death and sampling the rumen. ACKNOWLEDGMENTS We would like to thank Mr E. D. Goodall for technical assistance and Mr R. S. Reid for analysis of VFA. REFERENCES BANNERMAN, M. M. and BTIAXTER, K. L. (1969). The Husbanding of Red Deer. Aberdeen University Press. BIssELL, H. D. and WEIR, W. C. (1957). The digestibilities of interior live oak and chamise by deer and sheep. Journal of Animal Science 16, BROCKWAY, J. M. and MALoIY, G. M. 0. (1968). Energy metabolism of the red deer. Journal of Physiology, London 194, 22-24P. CONWAY, E. J. (1957). Microdiffusion Analysis and Volumetric Error, 4th ed. London: Crosby, Lockwood and Sons Ltd. CRAMPTON, E. W. and MAYNARD, L.A. (1938). The relation of cellulose and lignin content to the nutritive value of animal feeds. Journal of Nutrition 15, ERiKssON, S. and SCHMEKEL, J. (1962). A comparison between the ability of reindeer and sheep to digest their feed. Kungl. Lantbrukshogskolans Annaler 28, FEUSTEL, G. (1967). Vergleichende Untersuchungen am Verdauungstrakt von Rothirsch (Cervus elaphus) und Reh (Capreolus capreolus) post mortem unter besonderer Berucksichtigung der Gerilstkohlenhydrate und des Ligningehaltes der Ingesta. Inaugural Dissertation, Ludwig-Maximilians-Universitat Munchen. GILL, J. (1961). Die Durchgangzeiten der Nahrung durch den Verdauungskanal und die physischen Eigenschaften des Kotes beim Rothirsch(Cervu8 elaphus L.). Transactions of the 5th Congress of the International Union of Game Biologists, Bologna. Richerche di zoologia applicata alla caccia 4, Supplement, GILL, J. and JAcZEwsxi, Z. (1958). Kapazitiit der verschiedenen Teile des Verdauungsapparates des Rothirsches (Cervus ekaphus L.). Zeitschrift fur Jagdwissenschaft 4, GOODALL, E. D., KAY, R. N. B. and MALOIY, G. M. 0. (1968). The red deer as an experimental animal. Journal of Physiology, London 194, 6-7P. HOBSON, P. N. (1969). Experimental studies of food intake and digestion. (b). Studies on the rumen metabolism and other features of red deer, hill sheep and reindeer in the Scottish hills. In The Husbanding of Red Deer, p (editors M. M. Bannerman and K. L. Blaxter). Aberdeen University Press. HOBSON, P. N. (1970). Some field experiments on the rumen functions of red deer, hill sheep and reindeer. Deer 2, HYD]hN, S. (1955). A turbidimetric method for the determination of higher polyethylene glycols in biological materials. Kungl. Lantbrukshogskolans Annaler 21, HYDAN, S. (1961). Determination of the amount of fluid in the reticulo-rumen of the sheep and its rate of passage to the omasum. Kungl. Lantbrukshigskolans Annaler 27, JAMES, A. T. and MARTIN, A. J. P. (1952). Gas-liquid partition chromatography: the separation and micro-estimation of volatile fatty acids from formic acid to dodecanoic acid. Biochemical Journal 50, MALOIY, G. M. 0. (1968). The Physiology of Digestion and Metabolism in the Red Deer (CerVus elaphus L.). Ph.D. Thesis, University of Aberdeen. MALOIY, G. M. O., KAY, R. N. B. and GOODALL, E. D. (1968). Studies on the physiology of digestion and metabolism of the red deer (Cervus elaphus). Symposia of The Zoological Society of London 21 (Comparative Nutrition of Wild Animals, editor M. A. Crawford),
10 266 Maloiy and Kay MALOIY, G. M. 0., KAY, R. N. B., GOODALL, E. D. and Topps, J. H. (1970). Digestion and nitrogen metabolism in sheep and red deer given large or small amounts of water and protein. British Journal of Nutrition 24, NATURE CONSERVANCY (1967). Red Deer Research in Scotland: Progress Report 1. Edinburgh: The Nature Conservancy. NORDFELDT, S., CAGELL, W. and NORDKVIST, M. (1961). Smaltbarhetsforsok med renar. Ojebyn Kungl. Lantbruksh6gskolan och Statens Lantbruksforsok Statens Husdjursforsbk Sdrtryck och f6rhand8meddelande. No. 151, SHORT, H. L., MEDIN, D. E. and ANDERSON, A. E. (1966). Seasonal variations in volatile fatty acids in the rumen of mule deer. Journal of Wildlife Management 30,
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