FIBER DIGESTIBILITY IN ROYAL ANTELOPE (NEOTRAGUS PYGMAEUS) Author(s): Debra A. Schmidt, Ph.D., Michael L. Schlegel, Ph.D., and Michael L. Galyean, Ph.D. Source: Journal of Zoo and Wildlife Medicine, 45(4):744-748. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2013-0096.1 URL: http://www.bioone.org/doi/full/10.1638/2013-0096.1

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Journal of Zoo and Wildlife Medicine 45(4): 744–748, 2014 Copyright 2014 by American Association of Zoo Veterinarians

FIBER DIGESTIBILITY IN ROYAL ANTELOPE (NEOTRAGUS PYGMAEUS) Debra A. Schmidt, Ph.D., Michael L. Schlegel, Ph.D., and Michael L. Galyean, Ph.D.

Abstract: Royal antelope (Neotragus pygmaeus) are among the smallest ungulate species and are browsing ruminants. To date, their capacities for fiber fermentation and nutrient digestion have not been quantified. This study compared apparent digestibilities of a typical high-fiber herbivore pellet (ADF 25) and a low-starch, highfiber diet (WHP) in royal antelope in a crossover design (seven subjects in the first period and four in the second). Animals on ADF 25 pellets had greater intake concentrations (P , 0.05) of dry matter, crude protein, lignin, and crude fat; however, animals fed the WHP diets had greater (P , 0.05) apparent digestibility of dry matter, acid detergent fiber, neutral detergent fiber, and crude fat. Identifying the capacity to which these smaller ruminants can degrade fiber will help to establish more appropriate feeding guidelines for small, browsing ruminants in captivity. Key words: Digestibility, fat, fiber, Neotragus pygmaeus, protein, royal antelope.

INTRODUCTION Royal antelope (Neotragus pygmaeus) are found in the rainforests of West Africa.6,9 They are the smallest bovid species, typically weighing 1.5–3 kg and classified as browsing animals, eating leaves, buds, shoots, fruits, flowers, and fungi in the wild.6,22 Grazing and browsing animals in zoos have been offered similar feeds,10 but new hypotheses suggest browsing animals are more susceptible to rumenitis than grazers and could benefit from lower-starch, higher-fiber diets.1,2,18 Rumenitis is an inflammation of the rumen. It is a problem observed in dairy and feedlot cattle and is often attributed to the feeding of readily fermentable carbohydrates (e.g., corn, wheat, and barley).3,5,7,16,21 When sufficient quantities of starch are available in the rumen, amylolytic microbes are able to reproduce rapidly and decrease the pH of the rumen through the production of volatile fatty acids and lactic acid, which can adversely affect healthy populations of other rumen microflora.3 Rumenitis is believed to be associated with mineral imbalances, laminitis, poor body condition, and poor fecal form consistency in zoo ruminants.1,12–15 The Wild Herbivore Plus diet (WHP; 5ZK4; Mazuri, Purina Mills, LLC, Saint Louis, Missouri 63166, USA) is a low-starch, high-fiber From San Diego Zoo Global, P.O. Box 120551, San Diego, California 92112, USA (Schmidt, Schlegel); and College of Agricultural Sciences and Natural Resources, Texas Tech University, Box 42123, Lubbock, Texas 79409, USA (Galyean). Present address (Schmidt): Saint Louis Zoo, One Government Drive, Saint Louis, Missouri 63110, USA. Correspondence should be directed to Dr. Schmidt ([email protected]).

diet comprised of pellets and loose beet pulp, both coated with a high-fat molasses. The highfat, high-fermentable fiber and low-lignin concentrations are important in providing small ruminants with a form of energy other than starch; however, the extent to which this small ruminant can degrade fiber has not been investigated. The purpose of this study was to determine the extent to which royal antelope ferment fiber, an important source of energy in ruminant animals.

MATERIALS AND METHODS Animals Six adult males and two adult females participated in the first phase of this crossover trial. The animals ranged from 1 to 8 yr of age; females weighed an average of 2.7 kg (2.1–3.1-kg range), and males weighed an average of 2.3 kg (1.8–2.7kg range). One male and one female were group housed and counted as one animal unit during this first phase, resulting in seven test subjects. Before the second phase of the study, two males and one female were removed from the collection, leaving four males and one female in the study. The second phase of the study did not include any paired animals. Animals were housed in off-exhibit holding pens. The pens, measuring 2.4 m 3 0.9 m or 3.7 m 3 4.9 m, had dirt floors, and animals were offered wood shavings for bedding. The trials were conducted during the months of August and September in 2007 with IACUC approval 258; pens were not heated, but it was not necessary because of warm seasonal temperatures.

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Table 1. Item

Chemical composition of all dietary items fed to royal antelope (Neotragus pygmaeus) (DM basis). ADF 25a WHPb Browse Alfalfac Leaf Eaterd Carrot Yam Collard Dandelion Romaine

DM (%) 94.4 94.1 92.2 CP (%) 17.6 17.5 10.2 ADF (%) 24.9 28.2 36.6 NDF (%) 37.5 40.8 47.3 Lignin (%) 6.3 3.6 12.7 Crude fat (%) 3.8 5.7 3.0 Ca (%) 1.7 1.0 2.8 P ( %) 1.0 0.5 0.3 Mg (%) 0.5 0.5 0.4 K (%) 1.7 1.3 1.5 Na (%) 0.8 0.8 0.8 Fe (ppm) 1,680 472 427 Zn (ppm) 163 144 323 Cu (ppm) 24 25 12 Mn (ppm) 198 83 48 Mo (ppm) 1.2 1.5 0.3

93.0 27.6 24.0 28.5 6.2 2.2 2.3 0.3 0.4 2.2 0.2 280 30 10 35 3.9

94.1 27.1 13.8 20.4 3.7 5.0 1.4 0.8 0.2 0.9 0.3 350 138 25 81 0.7

86.0 8.6 10.6 13.5 1.1 2.4 0.4 0.4 0.1 3.3 0.5 68 129 13 10 0

88.2 5.6 5.7 6.9 1.8 1.1 0.3 0.2 0.1 1.7 0.3 37 12 3 12 0.6

85.1 24.6 15.7 20.3 1.3 3.9 2.1 0.4 0.4 3.1 0.7 64 31 2 69 2.3

87.6 21.4 20.2 36.0 2.5 3.8 1.0 0.3 0.4 4.2 2.0 150 37 7 44 1.2

84.6 21.4 25.8 33.1 2.7 4.3 0.8 0.5 0.4 4.5 0.6 182 23 3 65 0.1

Kale

Spinach

87.2 34.9 18.0 20.4 1.5 4.7 2.0 0.5 0.5 2.6 1.1 117 24 3 45 2.5

90.4 39.5 13.4 17.7 1.2 3.4 1.0 0.6 1.3 4.1 2.5 249 71 10 49 0.5

ADF 25 (High Fiber Herbivore), Western Milling, Goshen, California 93227, USA. MazuritWild Herbivore Plus 5ZK4, Purina Mills, LLC, Saint Louis, Missouri 63166, USA. c Whole alfalfa was fed; however, based on visual observations, only leaves were consumed. Thus, values shown reflect the analyzed composition of alfalfa leaf samples. d Marion Leaf Eater Food (lemur), Marion Zoological, Plymouth, Minnesota 55441, USA. a

b

Diets and Preliminary Period Before the start of the study, all animals were receiving a 50 : 50 mixture of ADF 25 and Wild Herbivore (Mazuri, 5ZF1) diet. The goal was to offer isocaloric, pelleted versions of the diet, but because of a calculation error, the diets were not isocaloric. Nonetheless, animals did not consume 100% of the pellets on any day. Animals were offered either 220 g of High Fiber Herbivore (ADF 25) pellets (2.3 kcal/g ME ruminant, dry-matter basis; Western Milling, Goshen, California 93227, USA) or 125 g WHP (3.0 kcal/g ME ruminant, drymatter basis). As enrichment items, each diet also included 2 g of lemur-sized Leaf Eater Food (Marion Zoological, Plymouth, Minnesota 55441, USA), 5 g of root vegetable (carrot or yam), 20 g of leafy green vegetable (romaine lettuce, kale, spinach, collards, or dandelion greens each offered a different day). Animals were also offered approximately 30 g of a freshly cut young willow (Salix spp.) browse branch and 200 g of alfalfa hay daily. Animals had ad libitum access to water. Collection Period Animals were assigned randomly to one of two manufactured diets and were transitioned to the new diet over a 6-day period. Thereafter, the rumen microflora were then allowed to adapt to the new diet for 10 days before the 5-day digestibility trial. The animals were then transi-

tioned to the alternate diet over 6 days, allowed a 10-day adaptation period, followed by the second 5-day digestibility collection period. Other components of the diet besides the pellets (e.g., Leaf Eater, vegetables, alfalfa hay) remained the same as described for the preliminary period. Food was sampled and weighed before being offered to the antelope. After 24 hr, all uneaten feeds (orts) and feces were collected, weighed, and dried at 558C to a constant weight in a forced-air oven before analyses. Animals typically consumed all produce and Leaf Eater Food, usually leaving only pellets, alfalfa, and the browse stems for orts. Orts from browse were combined within animal for each 5-day collection period. Because animals receiving the WHP diet could be selective in choosing pellets or loose beet pulp, the WHP orts within animal were combined throughout the week. Alfalfa orts were collected, dried, and weighed, but not analyzed because of the large quantities that were recovered. On average, animals only consumed approximately 10–20 g of alfalfa daily and, per keepers, the animals only selected the alfalfa leaf material. Sample Analyses Food samples (Table 1), orts, and fecal samples were sent to Dairy One Forage Laboratory (Ithaca, New York 14850, USA) for determination of dry matter (DM), crude protein (CP), acid

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Table 2. Ingredient composition of diets consumed (%, 5-day average; DM basis 6 standard deviation) by royal antelope (Neotragus pygmaeus). Ingredient

ADF 25a

WHPb

SEc

P valued

Pelleted diet Browse Alfalfa (leaves)e Leaf Eater Foodf Carrot Yam Collard Dandelion Romaine Kale Spinach

73.78 4.33 16.19 2.20 0.27 0.26 0.47 0.58 0.53 0.73 0.60

80.92 3.15 9.63 2.48 0.31 0.29 0.52 0.65 0.61 0.75 0.68

2.286 0.626 1.989 0.075 0.008 0.009 0.016 0.017 0.035 0.031 0.033

0.11 0.26 0.10 0.06 0.02 0.03 0.02 0.01 0.01 0.55 0.06

a ADF 25 (High Fiber Herbivore), Western Milling, Goshen, California 93227, USA. Values do not total to exactly 100% because of rounding of the least-squares means. b MazuritWild Herbivore Plus 5ZK4, Purina Mills, LLC, Saint Louis, Missouri 63166, USA. c Pooled standard error of treatment means, n ¼ 6 animals/ treatment. Because of missing observations in the second period of the crossover design, the largest SE value is reported. d Probability of the F-test for the effect of diet. e Whole alfalfa was fed; however, based on visual observations, only leaves were consumed. f Marion Leaf Eater Food (lemur), Marion Zoological, Plymouth, Minnesota 55441, USA.

detergent fiber (ADF), neutral detergent fiber (NDF), lignin, and crude fat concentrations. Percent apparent nutrient digestibility was calculated by subtracting the nutrient amount excreted in the feces from the initial nutrient amount consumed; the resulting number was then divided by the initial nutrient amount consumed and multiplied by 100. Food samples were also analyzed for mineral concentrations, but as a result of the possible contamination of the feces with dirt from the pen surface, mineral digestibility was not determined. Statistical Analyses Intake of dietary components and nutrients and apparent digestibility data were analyzed with the use of the MIXED procedure of SAS (SAS Institute, Inc., Cary, North Carolina 55441, USA). The model included the fixed effects of diet (ADF 25 and WHP), period, and sequence (whether the animal received ADF 25 followed by WHP or vice versa), with animal nested within sequence as a random effect. The least-squares means and observed significance levels (P values) of the F-test for diet effects are reported in tables. Because of the missing animals in the second

Table 3. Intake and total tract apparent digestibility of nutrients by royal antelope (Neotragus pygmaeus) fed diets based on two different commercial pelleted products. Item

ADF 25a WHPb SEc P valued

Intake (g/day) Dry matter Crude protein Acid detergent fiber Neutral detergent fiber Lignin Crude fat Apparent digestibility (%) Dry matter Crude protein Acid detergent fiber Neutral detergent fiber Lignin Crude fat

87.0 17.2 20.1 29.8 5.3 3.1

76.8 15.1 20.2 28.9 3.0 3.9

2.48 0.44 0.74 1.05 0.17 0.11

0.03 0.01 0.93 0.43 0.001 0.01

58.3 71.7 31.5 37.1 21.9 73.2

68.3 72.8 52.9 58.6 25.3 88.2

1.20 1.31 2.97 1.78 3.13 1.02

0.002 0.30 0.01 0.002 0.39 0.002

a ADF 25 (High Fiber Herbivore), Western Milling, Goshen, California 93227, USA. b MazuritWild Herbivore Plus 5ZK4, Purina Mills, LLC, Saint Louis, Missouri 63166, USA. c Pooled standard error of treatment means, n ¼ 6 animal/ treatment. Because of missing observations in the second period of the crossover design, the largest SE value is reported. d Probability of the F-test for the effect of diet.

period of the crossover discussed previously, the largest standard error of the least-squares means is reported. Differences were considered statistically significant when P levels were 0.05, whereas alpha values .0.05 but 0.10 were considered to reflect important tendencies.

RESULTS The animals offered the WHP diet consumed a greater percentage (11–15%) (P , 0.05) of their diet DM from produce items (carrot, yam, collard greens, dandelion, and romaine) than the antelope offered the ADF 25 diet (Table 2). Alfalfa leaf intake, as a percentage of diet DM, tended to be greater (P ¼ 0.10) for animals offered the ADF 25 diet than those offered the WHP diet (Table 2). Royal antelope offered the WHP diet tended (P , 0.10) to consume a greater percentage of Leaf Eater Food and spinach than those offered the ADF 25 diet. Similarly, antelope offered the WHP diet consumed a greater percentage of the pelleted diet than animals offered the ADF 25 diet (Table 2), but this effect was not significant (P ¼ 0.107). Animals receiving the ADF 25 diet had greater dry matter (P ¼ 0.03), greater CP (P ¼ 0.01), and greater lignin (P ¼ 0.001) intakes than animals

SCHMIDT ET AL.—FIBER DIGESTIBILITY IN ROYAL ANTELOPE

receiving the WHP diet (Table 3). Conversely, antelope receiving the WHP diet had a greater crude fat (P ¼ 0.01) intake than those receiving the ADF 25 diet (Table 3). In terms of apparent digestibility of nutrients, the antelope receiving the WHP diet had greater dry matter (P ¼ 0.002), greater ADF (P ¼ 0.01), greater NDF (P ¼ 0.002), and greater crude fat (P ¼ 0.002) digestibilities (Table 3) than those receiving the ADF 25 diet.

DISCUSSION Typical herbivore pellets (ADF 16 and ADF 25) are ‘‘open formulas’’ and are considered nutritionally similar within feeds regardless of the manufacturer. They contain alfalfa and wheat middlings as the primary ingredients, with additional corn in the ADF 16 diet. Wheat middlings and corn add starch to the diet, and as noted previously, excessive dietary starch has been hypothesized to lead to ruminal acidosis, decreased nutrient absorption, and poor health in browsing ruminants.17,18 At the time this study was conducted, the WHP diet was a newly created diet that was formulated as a low-starch diet with high-fat molasses to increase the energy content of the diet for smaller, browsing ruminants. The main ingredients of WHP are soybean hulls, dehulled soybean meal, and beet pulp. Starch was not quantified in WHP through analyses in this study, but is reported by the manufacturer to be approximately 2.7% (DM basis; http://www.mazuri.com/product). The difference in dietary DM intake between the two treatment groups can be explained, in part, by the greater caloric content of the WHP pellets; the animals on the WHP diet did not have to consume as much alfalfa to meet their caloric needs. The lower DM intake by the animals offered the WHP diet explains why the group had a greater percentage of their consumed diet DM as produce despite being offered the same amount as the ADF 25 group. The ADF 25 diet group consumed more protein as a result of greater consumption of alfalfa (14.1 g) compared with the WHP group (7.4 g) (calculated from data in Tables 2 and 3). The greater lignin intake of the ADF 25 animals is a result of the greater consumption of alfalfa, browse, and pellets. Royal antelope seem to be able to ferment larger quantities of fiber than are typically being provided to them through the commonly fed alfalfa-based pellets. Although NDF concentrations of ADF 25 and WHP are similar (37.5% and 40.8%, respectively), the fiber composition

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within the NDF fraction is different. Neutral detergent fiber is comprised of hemicellulose, cellulose, and lignin. Lignin is the nonfermentable portion of NDF and has the propensity to bind to some of the hemicellulose fraction, making it inaccessible to rumen microbes for fermentation.20 Animals fed the ADF 25 diet had greater lignin intake (P , 0.001) with the lignin coming primarily from alfalfa-based pellets and alfalfa leaves. This increased lignin concentration is likely part of the reason there were lower digestibilities of DM, NDF, and ADF with ADF 25 versus WHP. Increasing concentrations of starch in the diets of domestic cattle has been shown to impair fiberbolytic bacteria fermentation processes in the rumen.4,8,11 Although starch was not measured in the present study, the ADF 25 pellets analyzed as part of quality control in 2007 contained 10.4% starch (DM basis), whereas the WHP diet contained 2.7% starch (DM basis). This difference in starch might have decreased the ability of the animals fed ADF 25 to ferment fiber to the same extent as those fed WHP. It has also been reported that DM and NDF apparent digestibilities are decreased as feed intake in steers increased.19 Animals fed the ADF 25 diet had greater intakes of dry matter than those receiving WHP (87.0 g vs. 76.8 g; P , 0.03) and a lower digestibilities of DM (58.3 vs. 68.3%; P , 0.0002) and NDF (37.1 vs. 58.6%; P , 0.002), which follows that reported in cattle.19 Nonetheless, the differences in DM intake evaluated by Staples et al.19 were much greater than the difference between treatments in our study, and differences in NDF and ADF intakes were minimal between the two treatments. Thus, the extent to which the difference in DM intake affected apparent digestibility estimates in the present study is open to question. Royal antelope, and possibly other small ruminants, have the ability to ferment larger dietary concentrations of NDF than are provided through the typical alfalfa-based pellet and alfalfa hay diet. Understanding that highly fermentable fiber, low-lignin, and lower-starch diets could be more appropriate for browsing species might help caretakers provide more appropriate diets for small, browsing ruminants. Acknowledgments: We thank Jo Ann Haddad, Edith Galindo, Leslie Trenary, Tammy Batson, Elaine Chu, and Curby Simerson for their assistance in conducting this project.

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LITERATURE CITED 1. Clauss M, Dierenfeld ES. The nutrition of ‘‘browsers’’. In: Fowler ME, Miller RE (eds.). Zoo and wild animal medicine current therapy 6. St. Louis (MO): Saunders; 2008. p. 444–454. 2. Clauss M, Kienzle E, Hatt JM. Feeding practices in captive wild ruminants: peculiarities in the nutrition of browsers/concentrate selectors and intermediate feeders: a review. In: Fidgett AL, Clauss M, Ganslosser U, Hatt JM, Nijoboer J (eds.). Zoo animal nutrition. 2nd ed. Fu¨rth (Germany): Filander Verlag; 2003. p. 27–52. 3. Essig HW, Huntington GB, Emerick RJ, Carlson JR. Nutritional problems related to the gastro-intestinal tract. In: Church DC (ed.). The ruminant animal. Englewood Cliffs (NJ): Prentice Hall; 1988. p. 468– 492. 4. Grant RJ. Influence of corn and sorghum starch on the in vitro kinetics of forage fiber digestion. J Dairy Sci. 1994;77:1563–1569. 5. Hall MB. Rumen acidosis: carbohydrate feeding considerations. In Proc 12th International Symposium on Lameness in Ruminants; 2002. p. 51–61. 6. Huffman B. Ultimate ungulate website [Internet]. c2012. [cited 2013 May]. Available from: http://www. ultimateungulate.com/ 7. Kahn CM (ed.). Merck veterinary manual. Whitehouse Station (NJ): Merck & Co., Inc.; 2005. p. 181– 183. 8. Kaufman W. Influence of the composition of the ration and the feeding frequency on pH regulation in the rumen and on feed intake in ruminants. Livest Prod Sci. 1976;3:103. 9. Kingdon J. The Kingdon field guide to African mammals. London (England): Academic Press; 1997. 10. Lintzenich BA, Ward AM. 1997. Hay and pellet ratios: considerations in feeding ungulates, Fact Sheet 006. Nutrition Advisory Group Handbook [Internet]. c1997 [cited 2013 April 15]. Available from: http:// nagonline.net/Technical%20Papers/technical_papers. htm 11. McCarthy RD Jr, Klusmeyer TH, Vicini JL, Clark JH, Nelson DR. Effects of source of protein and carbohydrate on ruminal fermentation and passage of

nutrients to the small intestine of lactating cows. J Dairy Sci. 1989;72:2002–2016. 12. Miller M, Weber M. Hypocalcemia, hypomagnesemia, and rumenitis in exotic ruminants. In: Fowler ME, Miller RE (eds.). Zoo and wild animal medicine current therapy 6. St. Louis (MO): Saunders; 2008. p. 404–407. 13. Miller M, Weber M, Valedes E, Fontenot D, Neiffer D, Robbins PK, Terrell S, Stetter M. Hypomagnesemia, hypocalcemia, and ruminitis in ungulates: an under-recognized syndrome? In Proc Am Assoc Zoo Vet; 2013. p. 29–33. 14. Miller M, Weber M, Valdes EV, Neiffer D, Fontenot D, Fleming G, Stetter M. Changes in serum calcium, phosphorus, and magnesium levels in captive ruminants affected by diet manipulation. J Zoo Wildl Med. 2010;41:404–408. 15. Nocek JE. Bovine acidosis: implications on laminitis. J Dairy Sci. 1997;80:1005–1028. 16. Oba M, Wertz-Lutz AE. Acidosis: new insights into the persistent problem. J Anim Sci. 2011;89:1090– 1091. 17. Schmidt DA (ed.). The Giraffe Nutrition Workshop Proceedings; 2005. 18. Schmidt DA, Kendrick EL (eds.). Ruminant Browser Nutrition Workshop; 2009. 19. Staples CR, Fernando RL, Fahey GC Jr, Berger LL, Jaster EH. Effects of intake of a mixed diet by dairy steers on digestion events. J Dairy Sci. 1984;67: 995–1006. 20. Van Soest PJ. Lignin. In: Nutritional ecology of the ruminant. 2nd ed. Ithaca (NY): Cornell University Press; 1994. p. 177–195. 21. Van Soest PJ. Feeding strategies, taxonomy, and evolution. In: Nutritional ecology of the ruminant. 2nd ed. Ithaca (NY): Cornell University Press; 1994. p. 22– 39. 22. Walther FR. Duikers and dwarf antelopes. In: Parker SP (ed.). Grzimek’s encyclopedia of mammals. New York (NY): McGraw-Hill; 1990. p. 325–343. Received for publication 4 May 2013

Fiber digestibility in royal antelope (Neotragus pygmaeus).

Royal antelope (Neotragus pygmaeus) are among the smallest ungulate species and are browsing ruminants. To date, their capacities for fiber fermentati...
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