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Digestive efficiency in two small, wild ruminants: the dik-dik and suni antelopes
Comparative Biochemistry and Physiology Part A 124 (1999) 149 – 153 www.elsevier.com/locate/cbpa
Digestive efficiency in two small, wild ruminants: the dik-dik and suni antelopes G.M.O. Maloiy a, E.T. Clemens b,* b
a Institute of Animal Physiology and Biotechnology Research, P.O. Box 34206, Nairobi, Kenya, South Africa Department of Animal and Veterinary Science, Uni6ersity of Nebraska-Lincoln, Lincoln, NB 68583 -0908, USA
Received 29 April 1999; received in revised form 16 July 1999; accepted 19 July 1999
Abstract A comparative study, using six dik-dik and eight suni antelope, was undertaken to identify similarities and differences that may exist in the digestive process of these two small, East African ruminant browsers. The suni antelope was the more select feeder, preferring the native, Grewia sinilis leaves over that of lucerne hay. Daily forage consumption rate, per unity body weight, was greater in the dik-dik (40.4 g/kg) than for the suni (30.6 g/kg), while daily fluid intake was considerably less (i.e. dik-dik, 68 ml/kg versus suni, 106 ml/kg body weight). Rumen fermentation studies suggested that the suni antelope attained the more rapid rumen and caecal fermentation activities, when compared to the dik-dik antelope. The difference in ruminal and caecal digestive process of the two antelope is suggested to be partly the result of the dik-dik’s arid-adaptation strategies of less fluid intake and a more diverse (less selective) browse consumption, relative to the suni antelope. © 1999 Elsevier Science Inc. All rights reserved. Keywords: Caecal; Dik-dik antelope; Fermentation; Forage intake; Grewia leaves; Lucerne hay; Rumen; Suni antelope
1. Introduction The dik-dik (Rhynchotragus kirkii ) and the suni (Neotragus moschatus) antelope are two of East Africa’s smallest ruminants. Each will range in size from 3.0 to 4.8 kg adult body weight, and each is known to inhabit arid and semi-arid scrub areas in Eastern, Central and Southern Africa. During the rainy seasons these small ruminants prefer to feed on succulent, easily fermentable browse, of high protein content [9,10,16,27,28]. Yet during periods of drought (May– October) available forage is scarce and of low nutritional quality [7,19,22]. The ability of these small ruminants to survive, and flourish, under extended periods of low quality forage intake is of particular interest to those within both the agricultural and the wild-life communities. Of importance to note is that both the dik-dik and suni antelope adapt well to captivity and have been used frequently in controlled research set Journal Series No. 12604, Agricultural research division, University of Nebraska-Lincoln, Lincoln, NE 68583-0702, USA. * Corresponding author. Tel.: + 1-402-472-6219; fax: + 1-402-4726362.
tings [11,13,16,18–22]. The study being presented was undertaken to determine the digestive efficiency and nutritional value of low quality forage fed to the dikdik and suni antelope under controlled conditions. Particular emphasis was placed upon rumen and caecal fermentation and the available short-chain fatty acids resulting from fermentation within each species.
2. Materials and methods
2.1. Animals Experiments were undertaken using six dik-dik (3.89 0.6 kg mean body weight) and eight suni antelope (3.4 9 0.4 kg mean body weight) under controlled laboratory conditions, in accordance with guidelines set forth by the American Physiological Society [1]. All the animals were collected from their natural habitat in conjunction with the Department of Wildlife Conservation and Management programs. All dik-dik and suni antelope were group housed, according to species, for a period of 3 weeks before being used for digestion studies. The preliminary period was used to
1095-6433/99/$ - see front matter © 1999 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3 ( 9 9 ) 0 0 0 9 6 - 3
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permit the animals to adapt to their captive environment, the animal handlers and to their experimental diets. Each animal was weighed regularly, using a Salter Spring Balance (25 kg capacity) to insure proper weight maintenance and to provide frequent human/animal interaction. During the experimental phase of the study, each antelope was housed in an individual metabolic cage which allowed for automatic separation of urine and faecal materials. The metabolic cages were maintained in a climatic control chamber where the temperature and relative humidity were regulated at 22°C and 30% humidity, respectively.
2.2. Diets A basal diet consisting of Grewia sinilis leaves and early weaning calf pellets (6.2 fiber and 20.1% crude protein; Unga Lts., Nairobi), along with a mineral block, was provided to the antelope during their captive adaptation period. However, the mineral block and calf pellets were removed prior to beginning the fiber-quality digestive studies. During the metabolic study periods the antelope were fed one of three experimental diets based upon crude fiber and crude protein content (Table 1). Animals were randomly assigned diets and experimental period, such that each animal was tested on each diet [25]. During the digestibility studies, forage and water were provided ad libitum in feeding trays attached to the front of each metabolic cage. Daily food intake, water intake, and urine and faecal output were recorded at 09:00 h throughout the 10-day metabolic study for each animal and for each diet.
2.3. Chemical analysis General proximate analysis procedures were used to determine the dry matter and nutrient composition of the forage sources [2]. Individual daily faecal and urine excretions were collected and the weight and volume determined, respectively. Samples of each were taken for laboratory analysis of dry matter and energy determination. The dry matter content of the food and faeces were determined by drying a representative sample of a known weight in a forced air oven to a constant weight at 105°C. The energy content of the Table 1 Basic composition of forage fed to the dik-dik and suni antelope during the digestive studiesa Dry matter (%) Fibre (%) Star grass hay 86 Lucerne leaves 82 G. sinilis leaves 92
28 26 12
Crude protein (%) 7 20 14
a Grewia and lucerne leaves were collected fresh weekly and dried in the sun before feeding.
feed and faeces were determined using a Galanekamp Balistic Bomb Calorimeter.
2.4. Rumen, abomasal and caecal contents After completion of all digestibility studies all dik-dik and suni antelope were readapted to their basal diet of G. sinilis leaves for a period of 10 days. The calf pellets and mineral block were not offered during this period. Each antelope was euthanized, via sodium pentobarbital IV, and the abdominal cavity of each animal opened immediately after death. Ligatures were used to tie-off the oesophagus at the cardia and the large bowel at the rectal-anal junction, after which the entire gastrointestinal tract was then removed. The gastrointestinal tract of each antelope was further separated by ligatures into select segments which included: the reticulo-rumen, abomasum and caecum. The total contents were removed from each segment, weighed, and a representative sample refrigerated for later analysis. Additional samples were strained through cheese cloth, the supernatant acidified with concentrated H2SO4 (approx. 0.5 per 20 ml sample), and refrigerated for later analyses of short-chain fatty acids. Dry matter content was determined by drying a portion of each sample to a constant weight in a forced-air oven at 105°C. Additional samples of whole gut contents were centrifuged and the supernatant collected for laboratory analysis of: osmolality, lactic acid and short-chain fatty acid concentrations as described by Maloiy and co-workers [20,21]. Rumen and caecal fermentation rates of each animal were determined by measurement of the rate of in vitro gas production, according to methods previously described [8,14,15]. All samples were analyzed in duplicate. Analysis of variance and Duncan’s Multiple Range Test were used to determine significant differences [25]. The level of statistical difference was set at P B0.05.
3. Results The average body weights of the six dik-dik (3.8 kg9 0.6 SEM) and suni antelope (3.4 kg9 0.4 SEM) did not change appreciably during the adaptation period, nor during the fibre feeding trial. Food and water intake, as well as, the dry matter and energy digestibility values obtained for the dik-dik and suni antelope fed each of the forage sources is reported in Table 2. The feeding of star grass hay resulted in a significant (PB 0.05) reduction in food and water intake for both the dik-dik and suni antelope when compared to these same animals fed the lucerne or Grewia leaves. The reduced intake was further reflected in a significantly (PB 0.05) lower digestible dry matter and digestible energy value for both species, again when compared to
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Table 2 Intake and digestibility values obtained for the dik-dik and suni antelope fed various sources of foragea
Dik-dik
Suni
a
Forage
Food intake (g/day)
Water intake (ml/day)
Dry matter digestibility (%)
Energy digestibility (%)
Star grass Lucerne Grewia Star grass Lucerne Grewia
1289 16* 1589 12** 1499 3** 889 2* 989 6** 1109 4***
162920* 266918** 25198** 264 9 16* 356932** 368940**
58 9 0.6* 67 9 1.2** 68 9 1.7** 57 91.6* 71 9 0.2** 70 9 1.1**
56 91.2* 68 90.8** 70 91.6** 5891.2* 72 90.4** 70 90.8**
Values represent the mean 9 SEM for six dik-dik and eight suni antelope. Values with unlike superscripts are statistically different (PB0.05).
Table 3 In vitro rumen fermentation rate, dry matter and rumen content values for the dik-dik and suni antelope fed G. sinilis leavesa
Dik-dik Suni
Dry matter (%)
Fermentation rateb
Rumen pH
Short-chain fatty acid (mmol/l)
Lactic acid (mmol/l)
Osmolality (mOsm/kg)
16.49 0.6 15.9 9 1.5
348918 3729 21
6.629 0.4 6.67 9 0.1
166 918 178 9 9
3.2 9 0.8 3.3 91.4
317936 341921
a Values represent the mean 9 SEM for six dik-dik and eight suni antelope. Statistical differences were not observed for any of the above parameters measured (P\0.05). b Fermentation rate reported as mmol gas/g dry matter/h.
Table 4 In vitro caecal fermentation rate, dry matter and caecal content values for dik-dik and suni antelope fed G. sinilis leavesa
Dik-dik Suni a b
Dry matter (%)
Fermentation rateb
Caecal pH
Short-chain fatty acid (mmol/l)
Lactic acid (mmol/l)
Osmolality (mOsm/kg)
15.3 90.4* 10.49 0.5**
76.2 9 6 80.79 8
7.059 0.04 7.039 0.03
68.6 94 74.1 96
2.2 9 0.2* 1.2 9 0.2**
31994 324 92
Values represent the mean 9 SEM for six dik-dik and eight suni antelope. Values with unlike superscripts are statistically different (PB0.05). Fermentation rate expressed as mmol gas/g dry matter/h.
the consumption of lucerne or Grewia leaves (Table 2). While statistical differences were not generally observed for the feeding of lucerne and Grewia leaves, within each species of antelope, there was the suggestion of a dietary preference, when comparing these two forages. The dik-dik antelope consumed a slightly greater quantity of lucerne leaves, while the suni antelope consumed more of the Grewia leaves. When dry matter intake was reported on a per kg body weight basis for all forage feeding periods, the dik-dik consumed slightly more (mean 40.5 g dm/kg body weight), than did the suni (mean 33.8 g dm/kg body weight). These values were statistically different and represent a daily dry matter intake of approximately 4.0 and 3.4% of body weight for the dik-dik and suni, respectively. Daily fluid intake of the two species were statistically different (P B 0.05), with the dik-dik averaging 136 ml water/kg body weight, and the suni, 213 ml water/kg body weight, per day. The resulting data for the in vitro fermentation studies of the dik-dik and suni antelope rumen and caecal contents is reported in Tables 3 and 4, respectively. Statistical differences were not detected (P \ 0.05) when
comparing rumen fermentation values for the dik-dik and suni antelope. However, rumen fermentation rate, as measured by in vitro gas production, rumen shortchain fatty acid (SCFA) concentration, and rumen osmolality, all suggest that the suni antelope may have a slightly more rapid ruminal digestive rate than that of the dik-dik antelope. Caecal fermentation for the dik-dik and suni antelope, like that of rumen fermentation, was not different between species (Table 4). However, when comparing the two species of antelope, statistical differences (PB 0.05) for the dik-dik and suni antelope were noted in the dry matter content and the lactic acid concentration, observed within this segment of gut. As was observed for the rumen fermentation studies, caecal fermentation rate, caecal short-chain fatty acid concentration and caecal osmolality all suggest a more rapid rate of fibre digestion occurring within the caecum of the suni antelope. Statistical differences were not observed (P \0.05) for any of the parameters for dik-dik and suni antelope abomasal content (Table 5).
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Table 5 Abomasal dry matter, pH, organic acid and osmolality values for the dik-dik and suni antelope fed G. sinilis leavesa
Dik-dik Suni a
Dry matter (%)
Abomasal pH
Short-chain fatty acid (mmol/l)
Lactic acid (mmol/l)
Osmolality (mOsm/kg)
13.0 9 1.6 12.4 9 2.0
3.429 0.2 3.869 0.3
18.5 9 3.5 16.6 91.5
2.0 9 0.9 2.9 90.6
308 9 26 328 9 9
Values represent the mean 9 SEM for six dik-dik and eight suni antelope.
4. Discussion East African suni antelope and the dik-dik antelope have become popular animals for research studies. These small, wild ruminants adapt well to captivity, are easily handled, can be maintained economically, and serve as both a unique and a comparable species of rumen function studies. The dik-dik antelope is, of the two, the most frequently studied [11,16,18 – 24], while the suni antelope is perhaps less so [11,13,16]. Both are arid, or semi-arid, inhabitants living in an environment that alters from lush, abundant vegetation to periods of severe drought [16,20]. In nature both are select browsers [9,16]. The present study was undertaken as a comparative study, to identify similarities and differences that may exist in the plant material digestive process of these two species. The study, while undertaken with somewhat limited knowledge of the natural, specific diets of these antelope [9,29], used three sources of forage materials: star grass hay (both a forage source non-typical of that of a ‘browser’ (i.e. grass hay), and a forage source high in fibre and low in crude protein content), lucerne leaves (a browse, high in fibre and in protein content, yet not typically native to the antelope’s diet), and G. sinilis leaves (a browse, low in fibre and high in protein content, and one typically found in the antelope’s natural diet) [16]. It is generally accepted that forage high in fibre and low in protein content, such as noted for the grass hay, are considered low-quality forages. The ratio of fibre to protein content of the Grewia leaves would be considered a high-quality forage source. While both antelope species consumed and maintained body weight on all test diets, food consumption, dry matter digestive efficiency, and energy digestibility was significantly less for these antelope when consuming the star grass hay. The suni antelope demonstrated a preference for the Grewia leaves, as determined by food intake studies. The dik-dik antelope consumed the lucerne and Grewia browse at similar rates. When considering only the feed intake for the two sources of browse (i.e. lucerne and Grewia leaves), the dik-dik antelope were observed to consume forage at a rate of 40.4 g/kg body weight, and the suni, 30.6 g/kg body weight. Water intake showed the opposite relationship, i.e. dik-dik, 68 ml/kg body weight and the suni, 106 ml/kg body weight. Several investigators have suggested that the dik-dik, relative to
the suni, is the more arid adapted antelope of the two species [22,23]. Prior to the rumen function studies both species of antelope were readapted to, and fed, their native G. sinilis leaves. Subsequent analysis of the rumen contents (i.e. dry matter, pH, SCFA and lactic acid concentrations, and rumen fluid osmolality, as well as the in vitro fermentation studies), suggest that, while statistical differences were not observed (P \ 0.05) for any of the individual parameters, the combined data would suggest that the suni antelope had the more rapid rumen fermentation activities. The data is in agreement with the in vitro fermentation studies of suni and dik-dik collected in the wild, showing suni fermentation rates being more rapid [16]. One might conclude that the observed feeding pattern of the suni antelope contributed to this effect (i.e. a lower volume intake, and presumably more select browse, along with greater fluid consumption would favor a more rapid fermentation process). It is important to note, as suggested by Hoppe and co-workers [16], that rumen fermentation rates of the captive-fed antelope are lower than those of wildcollected animals. However, the rumen dry matter content of these captive and wild antelope were very similar (i.e. 15–16%). Hoppe and co-workers [12,14–16] have clearly shown that the rate of rumen fermentation is inversely rated to that of body size, with the larger species having the lower rates. Thus, the amount of ingested forage escaping foregut fermentation and entering the lower bowel is greater in the ruminant of a larger body size (i.e. a direct relationship). Furthermore, within foregut fermenters, such as the true ruminants, the extent of hindgut (caecal) fermentation would be expected to be less than that of simple-stomach herbivores with limited foregut fermentation [3,5,26]. Caecal fermentation rates of the suni and dik-dik antelope averaged 22% of that observed in the rumen, with caecal SCFA concentrations approximately 59% less than those concentrations observed in the rumen. Prior studies of the African buffalo (850 kg), Grant’s gazelle (42 kg) and Grey duiker (12 kg) revealed caecal fermentation rates averaging 47, 39 and 23% of their rumen fermentation rates, respectively [4,17]. The average volume of dik-dik and suni rumen (0.3 kg) and caecal contents ( B 0.1 kg), was reported earlier [6]. From this information, that of the fermentation rate, and SCFA concentrations in the
G.M.O. Maloiy, E.T. Clemens / Comparati6e Biochemistry and Physiology, Part A 124 (1999) 149–153
present study, it is calculated that caecal digestion contributes approximately 23% of the fermentative activities of these two antelope. Lactic acid production accounts for less than 2% of the organic acids produced. It is concluded that the weight and size of the dik-dik and suni antelope are sufficiently similar, that body size is not a factor in foregut or caecal fermentation [12]. However, the preferred, select browse consumption of the suni, in association with their greater fluid consumption provides for an enhanced fermentation rate, dry matter and energy digestibilities noted in the suni antelope relative to that of the dik-dik.
References [1] American Physiological Society. Guide for the Care and Use of Laboratory Animals. Bethesda: Office of Science and Health Reports, 1980 [DRR.NIH, Publ. No. 80–23]. [2] A.O.A.C. Official Methods of Analysis. 9th ed. Washington, DC: Association of Official Agricultural Chemists, 1985. [3] Arman P, Hopcraft D. Nutritional studies on East African herbivores. I. Digestibilities of dry matter, crude fibre and crude protein in antelope, cattle and sheep. Brit J Nutr 1975;33:255 – 64. [4] Boomker EA. A Study of the Digestive Processes of the Common Duiker, Syl6icapra grimmia. University of Pretoria: Thesis, 1981. [5] Choshniok I, Arnon H, Shkolink A. Digestive efficiency in a wild goat: the Nubian ibex. Can J Anim Sci 1984;64:160 – 1. [6] Clemens ET, Maloiy GMO. Digestive physiology of East African wild ruminants. Comp Biochem Physiol 1983;76A:319 – 33. [7] Estes RD. The Behavior Guide to African Mammals. NC, USA: Wake Forest Stadium Book, 1991. [8] Giesecke D, van Gylswyk NO. A study of feeding types and certain rumen functions in six species of South African wild ruminants. J Argic Sci Camb 1975;85:75–83. [9] Hofmann RR. The Ruminant Stomach. East African Literature Bureau. Nairobi, Kenya, East Africa, 1973. [10] Hofmann R, Musangi RS. Comparative digestibility coefficients of domestic and game ruminants from marginal lands in East Africa. Bull Epiz Dis Africa 1973;21:385–8. [11] Hoppe PP. Comparison of voluntary food and water consumption and digestion in Kirki’s dik-dik and suni. East Africa Wildl J 1977;15:41 – 8.
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[12] Hoppe PP. Rumen fermentation and body weight in African ruminants. Proc Songr Game Biol 1977;13:141 – 50. [13] Hoppe PP, Gwynne MD. Food retention time in the digestive tract of the suni antelope (Neotragus moschatus). Saugetier Kdl 1978;26:236 – 7. [14] Hoppe PP, Ovortrup SA, Woodford MH. Rumen fermentation and food selection in East African sheep, goats, Thomson’s gazelle, Grant’s gazelle and impala. J Arctic Sci Camb 1977;89:129 – 35. [15] Hoppe PP, Ovortrup SA, Woodford MH. Rumen fermentation and food selection in East African Zebu cattle, wildebeest, Coke’s hartebeest and topi. J Zool Lond 1977;181:1 – 9. [16] Hoppe PP, van Hoven W, von Engelhardt W, Prins RA, Lankhorst A, Gwynne MD. Pregastric and caecal fermentation in dik-dik (Madoqua kirkii ) and suni (Neotragus moschatus). Comp Biochem Physiol 1983;75A:517 – 24. [17] Hungate R, Phillips GD, McGregor A, Hungate DP, Buechner HK. Microbial fermentations in certain mammals. Science 1959;130:1192– 4. [18] Kamau JMZ, Maloiy GMO. The fasting metabolism of a small East African antelope: dik-dik. J Physiol Lond 1981;319:50–1P. [19] Maloiy GMO. The water metabolism of a small East African antelope: the dik-dik. Proc Rol Soc Lond 1973;184:167–78. [20] Maloiy GMO, Clemens ET. Aspects of digestion and in vitro fermentation in the caecum of some East African herbivores. J Zool Lond 1991;224:293 – 300. [21] Maloiy GMO, Clemens ET, Kamau JMZ. Aspects of digestion and in vitro rumen fermentation rate in six species of East African wild ruminants. J Zool Lond 1982;197:345 – 53. [22] Maloiy GMO, Rugangazi BM, Clemens ET. The physiology of the dik-dik antelope. Comp Biochem Physiol 1988;91:1–8. [23] Maloiy GMO, Rugangazi BM, Clemens ET. Nitrogen metabolism and renal function in the dik-dik antelope (Rhynchotragus kirkii ), Comp. Biochem. Physiol. 1999;(in review). [24] Rugangazi BM. Renal Excretion of Urea and Electrolytes in a Small Wild Ruminant: the Dik-dik Antelope (Rhynchotragus kirkii ). University of Nairobi, Kenya, East Africa: M.Sc. Thesis, 1985. [25] Snedecor GW, Cochran WG. Statistical Methods. 6th ed. Ames, Iowa: The Iowa State University Press, 1967. [26] Stevens CE, Hume ID. Comparative Physiology of the Vertebrate Digestive System. 2nd ed. Cambridge University Press, 1995. p. 203 – 15. [27] Tinley KL. Dik-dik (Madoqua kirki ) in South West Africa: notes on distribution, ecology and behavior. Madoqua 1969;1:7–33. [28] Van Hoven W. Rumen fermentation and methane production in the African buffalo (Syncerus caffer) in the Kruger National Park. Koedoe 18 1980;23:45 – 55. [29] Walker EP. Mammals of the World. Baltimore, MD: Johns Hopkins University Press, 1983:1276 – 7.
Digestive efficiency in two small, wild ruminants: the dik-dik and suni antelopes G.M.O. Maloiy a, E.T. Clemens b,* b
a Institute of Animal Physiology and Biotechnology Research, P.O. Box 34206, Nairobi, Kenya, South Africa Department of Animal and Veterinary Science, Uni6ersity of Nebraska-Lincoln, Lincoln, NB 68583 -0908, USA
Received 29 April 1999; received in revised form 16 July 1999; accepted 19 July 1999
Abstract A comparative study, using six dik-dik and eight suni antelope, was undertaken to identify similarities and differences that may exist in the digestive process of these two small, East African ruminant browsers. The suni antelope was the more select feeder, preferring the native, Grewia sinilis leaves over that of lucerne hay. Daily forage consumption rate, per unity body weight, was greater in the dik-dik (40.4 g/kg) than for the suni (30.6 g/kg), while daily fluid intake was considerably less (i.e. dik-dik, 68 ml/kg versus suni, 106 ml/kg body weight). Rumen fermentation studies suggested that the suni antelope attained the more rapid rumen and caecal fermentation activities, when compared to the dik-dik antelope. The difference in ruminal and caecal digestive process of the two antelope is suggested to be partly the result of the dik-dik’s arid-adaptation strategies of less fluid intake and a more diverse (less selective) browse consumption, relative to the suni antelope. © 1999 Elsevier Science Inc. All rights reserved. Keywords: Caecal; Dik-dik antelope; Fermentation; Forage intake; Grewia leaves; Lucerne hay; Rumen; Suni antelope
1. Introduction The dik-dik (Rhynchotragus kirkii ) and the suni (Neotragus moschatus) antelope are two of East Africa’s smallest ruminants. Each will range in size from 3.0 to 4.8 kg adult body weight, and each is known to inhabit arid and semi-arid scrub areas in Eastern, Central and Southern Africa. During the rainy seasons these small ruminants prefer to feed on succulent, easily fermentable browse, of high protein content [9,10,16,27,28]. Yet during periods of drought (May– October) available forage is scarce and of low nutritional quality [7,19,22]. The ability of these small ruminants to survive, and flourish, under extended periods of low quality forage intake is of particular interest to those within both the agricultural and the wild-life communities. Of importance to note is that both the dik-dik and suni antelope adapt well to captivity and have been used frequently in controlled research set Journal Series No. 12604, Agricultural research division, University of Nebraska-Lincoln, Lincoln, NE 68583-0702, USA. * Corresponding author. Tel.: + 1-402-472-6219; fax: + 1-402-4726362.
tings [11,13,16,18–22]. The study being presented was undertaken to determine the digestive efficiency and nutritional value of low quality forage fed to the dikdik and suni antelope under controlled conditions. Particular emphasis was placed upon rumen and caecal fermentation and the available short-chain fatty acids resulting from fermentation within each species.
2. Materials and methods
2.1. Animals Experiments were undertaken using six dik-dik (3.89 0.6 kg mean body weight) and eight suni antelope (3.4 9 0.4 kg mean body weight) under controlled laboratory conditions, in accordance with guidelines set forth by the American Physiological Society [1]. All the animals were collected from their natural habitat in conjunction with the Department of Wildlife Conservation and Management programs. All dik-dik and suni antelope were group housed, according to species, for a period of 3 weeks before being used for digestion studies. The preliminary period was used to
1095-6433/99/$ - see front matter © 1999 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3 ( 9 9 ) 0 0 0 9 6 - 3
G.M.O. Maloiy, E.T. Clemens / Comparati6e Biochemistry and Physiology, Part A 124 (1999) 149–153
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permit the animals to adapt to their captive environment, the animal handlers and to their experimental diets. Each animal was weighed regularly, using a Salter Spring Balance (25 kg capacity) to insure proper weight maintenance and to provide frequent human/animal interaction. During the experimental phase of the study, each antelope was housed in an individual metabolic cage which allowed for automatic separation of urine and faecal materials. The metabolic cages were maintained in a climatic control chamber where the temperature and relative humidity were regulated at 22°C and 30% humidity, respectively.
2.2. Diets A basal diet consisting of Grewia sinilis leaves and early weaning calf pellets (6.2 fiber and 20.1% crude protein; Unga Lts., Nairobi), along with a mineral block, was provided to the antelope during their captive adaptation period. However, the mineral block and calf pellets were removed prior to beginning the fiber-quality digestive studies. During the metabolic study periods the antelope were fed one of three experimental diets based upon crude fiber and crude protein content (Table 1). Animals were randomly assigned diets and experimental period, such that each animal was tested on each diet [25]. During the digestibility studies, forage and water were provided ad libitum in feeding trays attached to the front of each metabolic cage. Daily food intake, water intake, and urine and faecal output were recorded at 09:00 h throughout the 10-day metabolic study for each animal and for each diet.
2.3. Chemical analysis General proximate analysis procedures were used to determine the dry matter and nutrient composition of the forage sources [2]. Individual daily faecal and urine excretions were collected and the weight and volume determined, respectively. Samples of each were taken for laboratory analysis of dry matter and energy determination. The dry matter content of the food and faeces were determined by drying a representative sample of a known weight in a forced air oven to a constant weight at 105°C. The energy content of the Table 1 Basic composition of forage fed to the dik-dik and suni antelope during the digestive studiesa Dry matter (%) Fibre (%) Star grass hay 86 Lucerne leaves 82 G. sinilis leaves 92
28 26 12
Crude protein (%) 7 20 14
a Grewia and lucerne leaves were collected fresh weekly and dried in the sun before feeding.
feed and faeces were determined using a Galanekamp Balistic Bomb Calorimeter.
2.4. Rumen, abomasal and caecal contents After completion of all digestibility studies all dik-dik and suni antelope were readapted to their basal diet of G. sinilis leaves for a period of 10 days. The calf pellets and mineral block were not offered during this period. Each antelope was euthanized, via sodium pentobarbital IV, and the abdominal cavity of each animal opened immediately after death. Ligatures were used to tie-off the oesophagus at the cardia and the large bowel at the rectal-anal junction, after which the entire gastrointestinal tract was then removed. The gastrointestinal tract of each antelope was further separated by ligatures into select segments which included: the reticulo-rumen, abomasum and caecum. The total contents were removed from each segment, weighed, and a representative sample refrigerated for later analysis. Additional samples were strained through cheese cloth, the supernatant acidified with concentrated H2SO4 (approx. 0.5 per 20 ml sample), and refrigerated for later analyses of short-chain fatty acids. Dry matter content was determined by drying a portion of each sample to a constant weight in a forced-air oven at 105°C. Additional samples of whole gut contents were centrifuged and the supernatant collected for laboratory analysis of: osmolality, lactic acid and short-chain fatty acid concentrations as described by Maloiy and co-workers [20,21]. Rumen and caecal fermentation rates of each animal were determined by measurement of the rate of in vitro gas production, according to methods previously described [8,14,15]. All samples were analyzed in duplicate. Analysis of variance and Duncan’s Multiple Range Test were used to determine significant differences [25]. The level of statistical difference was set at P B0.05.
3. Results The average body weights of the six dik-dik (3.8 kg9 0.6 SEM) and suni antelope (3.4 kg9 0.4 SEM) did not change appreciably during the adaptation period, nor during the fibre feeding trial. Food and water intake, as well as, the dry matter and energy digestibility values obtained for the dik-dik and suni antelope fed each of the forage sources is reported in Table 2. The feeding of star grass hay resulted in a significant (PB 0.05) reduction in food and water intake for both the dik-dik and suni antelope when compared to these same animals fed the lucerne or Grewia leaves. The reduced intake was further reflected in a significantly (PB 0.05) lower digestible dry matter and digestible energy value for both species, again when compared to
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Table 2 Intake and digestibility values obtained for the dik-dik and suni antelope fed various sources of foragea
Dik-dik
Suni
a
Forage
Food intake (g/day)
Water intake (ml/day)
Dry matter digestibility (%)
Energy digestibility (%)
Star grass Lucerne Grewia Star grass Lucerne Grewia
1289 16* 1589 12** 1499 3** 889 2* 989 6** 1109 4***
162920* 266918** 25198** 264 9 16* 356932** 368940**
58 9 0.6* 67 9 1.2** 68 9 1.7** 57 91.6* 71 9 0.2** 70 9 1.1**
56 91.2* 68 90.8** 70 91.6** 5891.2* 72 90.4** 70 90.8**
Values represent the mean 9 SEM for six dik-dik and eight suni antelope. Values with unlike superscripts are statistically different (PB0.05).
Table 3 In vitro rumen fermentation rate, dry matter and rumen content values for the dik-dik and suni antelope fed G. sinilis leavesa
Dik-dik Suni
Dry matter (%)
Fermentation rateb
Rumen pH
Short-chain fatty acid (mmol/l)
Lactic acid (mmol/l)
Osmolality (mOsm/kg)
16.49 0.6 15.9 9 1.5
348918 3729 21
6.629 0.4 6.67 9 0.1
166 918 178 9 9
3.2 9 0.8 3.3 91.4
317936 341921
a Values represent the mean 9 SEM for six dik-dik and eight suni antelope. Statistical differences were not observed for any of the above parameters measured (P\0.05). b Fermentation rate reported as mmol gas/g dry matter/h.
Table 4 In vitro caecal fermentation rate, dry matter and caecal content values for dik-dik and suni antelope fed G. sinilis leavesa
Dik-dik Suni a b
Dry matter (%)
Fermentation rateb
Caecal pH
Short-chain fatty acid (mmol/l)
Lactic acid (mmol/l)
Osmolality (mOsm/kg)
15.3 90.4* 10.49 0.5**
76.2 9 6 80.79 8
7.059 0.04 7.039 0.03
68.6 94 74.1 96
2.2 9 0.2* 1.2 9 0.2**
31994 324 92
Values represent the mean 9 SEM for six dik-dik and eight suni antelope. Values with unlike superscripts are statistically different (PB0.05). Fermentation rate expressed as mmol gas/g dry matter/h.
the consumption of lucerne or Grewia leaves (Table 2). While statistical differences were not generally observed for the feeding of lucerne and Grewia leaves, within each species of antelope, there was the suggestion of a dietary preference, when comparing these two forages. The dik-dik antelope consumed a slightly greater quantity of lucerne leaves, while the suni antelope consumed more of the Grewia leaves. When dry matter intake was reported on a per kg body weight basis for all forage feeding periods, the dik-dik consumed slightly more (mean 40.5 g dm/kg body weight), than did the suni (mean 33.8 g dm/kg body weight). These values were statistically different and represent a daily dry matter intake of approximately 4.0 and 3.4% of body weight for the dik-dik and suni, respectively. Daily fluid intake of the two species were statistically different (P B 0.05), with the dik-dik averaging 136 ml water/kg body weight, and the suni, 213 ml water/kg body weight, per day. The resulting data for the in vitro fermentation studies of the dik-dik and suni antelope rumen and caecal contents is reported in Tables 3 and 4, respectively. Statistical differences were not detected (P \ 0.05) when
comparing rumen fermentation values for the dik-dik and suni antelope. However, rumen fermentation rate, as measured by in vitro gas production, rumen shortchain fatty acid (SCFA) concentration, and rumen osmolality, all suggest that the suni antelope may have a slightly more rapid ruminal digestive rate than that of the dik-dik antelope. Caecal fermentation for the dik-dik and suni antelope, like that of rumen fermentation, was not different between species (Table 4). However, when comparing the two species of antelope, statistical differences (PB 0.05) for the dik-dik and suni antelope were noted in the dry matter content and the lactic acid concentration, observed within this segment of gut. As was observed for the rumen fermentation studies, caecal fermentation rate, caecal short-chain fatty acid concentration and caecal osmolality all suggest a more rapid rate of fibre digestion occurring within the caecum of the suni antelope. Statistical differences were not observed (P \0.05) for any of the parameters for dik-dik and suni antelope abomasal content (Table 5).
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Table 5 Abomasal dry matter, pH, organic acid and osmolality values for the dik-dik and suni antelope fed G. sinilis leavesa
Dik-dik Suni a
Dry matter (%)
Abomasal pH
Short-chain fatty acid (mmol/l)
Lactic acid (mmol/l)
Osmolality (mOsm/kg)
13.0 9 1.6 12.4 9 2.0
3.429 0.2 3.869 0.3
18.5 9 3.5 16.6 91.5
2.0 9 0.9 2.9 90.6
308 9 26 328 9 9
Values represent the mean 9 SEM for six dik-dik and eight suni antelope.
4. Discussion East African suni antelope and the dik-dik antelope have become popular animals for research studies. These small, wild ruminants adapt well to captivity, are easily handled, can be maintained economically, and serve as both a unique and a comparable species of rumen function studies. The dik-dik antelope is, of the two, the most frequently studied [11,16,18 – 24], while the suni antelope is perhaps less so [11,13,16]. Both are arid, or semi-arid, inhabitants living in an environment that alters from lush, abundant vegetation to periods of severe drought [16,20]. In nature both are select browsers [9,16]. The present study was undertaken as a comparative study, to identify similarities and differences that may exist in the plant material digestive process of these two species. The study, while undertaken with somewhat limited knowledge of the natural, specific diets of these antelope [9,29], used three sources of forage materials: star grass hay (both a forage source non-typical of that of a ‘browser’ (i.e. grass hay), and a forage source high in fibre and low in crude protein content), lucerne leaves (a browse, high in fibre and in protein content, yet not typically native to the antelope’s diet), and G. sinilis leaves (a browse, low in fibre and high in protein content, and one typically found in the antelope’s natural diet) [16]. It is generally accepted that forage high in fibre and low in protein content, such as noted for the grass hay, are considered low-quality forages. The ratio of fibre to protein content of the Grewia leaves would be considered a high-quality forage source. While both antelope species consumed and maintained body weight on all test diets, food consumption, dry matter digestive efficiency, and energy digestibility was significantly less for these antelope when consuming the star grass hay. The suni antelope demonstrated a preference for the Grewia leaves, as determined by food intake studies. The dik-dik antelope consumed the lucerne and Grewia browse at similar rates. When considering only the feed intake for the two sources of browse (i.e. lucerne and Grewia leaves), the dik-dik antelope were observed to consume forage at a rate of 40.4 g/kg body weight, and the suni, 30.6 g/kg body weight. Water intake showed the opposite relationship, i.e. dik-dik, 68 ml/kg body weight and the suni, 106 ml/kg body weight. Several investigators have suggested that the dik-dik, relative to
the suni, is the more arid adapted antelope of the two species [22,23]. Prior to the rumen function studies both species of antelope were readapted to, and fed, their native G. sinilis leaves. Subsequent analysis of the rumen contents (i.e. dry matter, pH, SCFA and lactic acid concentrations, and rumen fluid osmolality, as well as the in vitro fermentation studies), suggest that, while statistical differences were not observed (P \ 0.05) for any of the individual parameters, the combined data would suggest that the suni antelope had the more rapid rumen fermentation activities. The data is in agreement with the in vitro fermentation studies of suni and dik-dik collected in the wild, showing suni fermentation rates being more rapid [16]. One might conclude that the observed feeding pattern of the suni antelope contributed to this effect (i.e. a lower volume intake, and presumably more select browse, along with greater fluid consumption would favor a more rapid fermentation process). It is important to note, as suggested by Hoppe and co-workers [16], that rumen fermentation rates of the captive-fed antelope are lower than those of wildcollected animals. However, the rumen dry matter content of these captive and wild antelope were very similar (i.e. 15–16%). Hoppe and co-workers [12,14–16] have clearly shown that the rate of rumen fermentation is inversely rated to that of body size, with the larger species having the lower rates. Thus, the amount of ingested forage escaping foregut fermentation and entering the lower bowel is greater in the ruminant of a larger body size (i.e. a direct relationship). Furthermore, within foregut fermenters, such as the true ruminants, the extent of hindgut (caecal) fermentation would be expected to be less than that of simple-stomach herbivores with limited foregut fermentation [3,5,26]. Caecal fermentation rates of the suni and dik-dik antelope averaged 22% of that observed in the rumen, with caecal SCFA concentrations approximately 59% less than those concentrations observed in the rumen. Prior studies of the African buffalo (850 kg), Grant’s gazelle (42 kg) and Grey duiker (12 kg) revealed caecal fermentation rates averaging 47, 39 and 23% of their rumen fermentation rates, respectively [4,17]. The average volume of dik-dik and suni rumen (0.3 kg) and caecal contents ( B 0.1 kg), was reported earlier [6]. From this information, that of the fermentation rate, and SCFA concentrations in the
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present study, it is calculated that caecal digestion contributes approximately 23% of the fermentative activities of these two antelope. Lactic acid production accounts for less than 2% of the organic acids produced. It is concluded that the weight and size of the dik-dik and suni antelope are sufficiently similar, that body size is not a factor in foregut or caecal fermentation [12]. However, the preferred, select browse consumption of the suni, in association with their greater fluid consumption provides for an enhanced fermentation rate, dry matter and energy digestibilities noted in the suni antelope relative to that of the dik-dik.
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