Possible factors affecting the bioavailability of copper and the copper requirements of wild, free-ranging African herbivores: A review
DOI:
https://doi.org/10.17159/sajas.v55i11.02Keywords:
antelope, bioaccessibility, hindgut fermenters, ruminants, trace elements, wildlifeAbstract
Free-ranging wild herbivores in Africa comprise 78 species of ruminants and several species of monogastric hindgut fermenters, and are classified as grazers, mixed feeders, and browsers. The objective of this review is to provide guidance to wildlife nutrition advisers by outlining key metabolic principles relevant to assessing copper nutrition in herbivores. In domestic species, copper bioavailability is influenced by dietary copper antagonists, copper solubility at absorption sites, and the homeostatic regulation of copper metabolism. Differences in the homeostatic control of copper absorption and metabolism in the liver between ruminants and monogastric species have a major effect on their tolerance to excessive copper exposure. As some elements in the diet are antagonistic to copper solubility in the digestive tract, dietary copper concentration alone has limited diagnostic value for assessing the potential copper nutrition status of a ruminant. Dietary copper is most soluble in acidic environments and factors influencing rumen pH, such as the effect of diet type on rumination and saliva flow, could thus influence copper solubility. In monogastric species, the solubility of dietary copper in the stomach can be high (up to 80% in vitro) because of the acidic environment of the stomach. Consequently, in domestic species, the bioavailability of copper varies from 1% to 10% in mature ruminants, compared with an estimated ≥30% for non-ruminants. This suggests that for wild species with similar body weights and diets, dietary copper requirements per kilogram of feed intake for maintenance should be substantially lower for monogastric species than for ruminants.
(Submitted 22 June 2025; Accepted 30 August 2025; Published 12 November 2025)
References
Abrahams, P.W., 2012. Involuntary soil ingestion and geophagia: A source and sink of mineral nutrients and potential harmful elements to consumers of earth materials. Applied Geochemistry, 27:954–968. DOI: https://doi.org/10.1016/j.apgeochem.2011.05.003
Baker, D.H. & Ammerman, C.B., 1995. Chapter 7: Copper bioavailability. In: Bioavailability of Nutrients for Animals: Amino acids, Minerals, and Vitamins. Eds: Ammerman, C.B., Baker, D.H., & Lewis, A.J., Academic Press Inc., New York. pp. 127–156.
Beasley, D.E., Koltz, A.M., Lambert, J.E., Fierer, N., & Dunn, R.R., 2015. The evolution of stomach acidity and its relevance to the human microbiome. PLoS One, 10(7):e0134116. DOI: https://doi.10.137/journal.pone.0134116
Belli, C.B., Fernandes, W.R., Torres, L.N., Sucupira, M.C.A., Marques de Sá, L.R., Maiorka, P.C., Neuenschwander, H.M., de Barros, A.de M,C., & Baccarin, R.Y.A., 2021. Copper toxicity in horses: Does it exist? Journal of Equine Veterinary Science, 106:103752. DOI: https://doi.org/10.1016/j.jevs.2021.103752
Byrne, L. & Murphy, R.A., 2022. Relative bioavailability of trace minerals in production animal nutrition: a review. Animals, 12(15):1981. DOI: https://doi.org/10.3390/ani12151981
Čadkovά, Z., Szάkovά, J., Miholovά, D., Horάkovά, B., Kopecký, O., Křivskά, D., Langrovά, I., & Tlustoš P., 2015. Bioaccessibility versus bioavailability of essential (Cu, Fe, Mn, and Zn) and toxic (Pb) elements from phyto hyperaccumulator Pistia stratiotes: Potential risk of dietary intake. Journal of Agricultural and Food Chemistry, 63:2344–2354. DOI: https://doi.org/10.1021/jf5058099
Clarkson, A.H., Paine, S., Martín-Tereso, J., & Kendall, N.R., 2020. Copper physiology in ruminants: trafficking of systemic copper, adaptations to variation in nutritional supply and thiomolybdate challenge. Nutrition Research Reviews, 33(1):43–49. DOI: https://doi.10.1017/S0954422419000180
Clauss, M., 2013. Digestive physiology and feeding behaviour of equids – a comparative approach. In: Horse Health Nutrition – European Equine Health Nutrition Congress, Gent, Belgium, 1–2 March 2013. pp. 25–33. DOI: https://doi.org/10.5167/uzh-76378
Clauss, M., Hume, I.D., & Hummel, J., 2010. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal, 4(7):979–992. DOI: https://doi.org/10.1017/S1751731110000388
Clauss, M., Müller, K., Fickel, J., Streich, W.J., Hatt, J-M., & Südekum, K-H., 2011. Macroecology of the host determines microecology of endobionts: protozoal faunas vary with wild ruminant feeding type and body mass. Journal of Zoology, 283:169–185. DOI: https://doi.org/10.1111/j.1469-7998.2010.00759x
Clauss, M., Tschuor, A., Codron, D., & Hummel, J., 2021. Reticular contraction frequency and ruminal dome development in goats do not differ between grass and browse diets. Journal of Animal Physiology and Animal Nutrition, 106(6):1208–1215. DOI: https://doi.org/10.1111/jpn.13663
Daniel, J.B. & Martín-Tereso, J., 2025. Review: Homeostatic boundaries to dietary Zn, Cu and Mn supply in cattle. Animal, 19:101532. DOI: https://doi.org/10.1016/j.animal.2025.10532
Dehority, B.A., 2002. Gastrointestinal tract of herbivores, particularly the ruminant: Anatomy, physiology and microbial digestion of plants. Journal of Applied Animal Research, 21:145–160. DOI: https://doi.org/10.1080/09712119.2002.9706367
Dierenfeld, E.S., 1997. Captive wild animal nutrition: a historical perspective. Proceedings of the Nutrition Society, 56(3):989–999. DOI: https://doi.org/10.1079/PNS19970104
Dierenfeld, E.S., Atkinson, S., Craig, A.M., Walker, K.C., Streich, W.J., & Clauss, M., 2005. Mineral concentrations in serum/plasma and liver tissue of captive and free-ranging rhinoceros species. Zoo Biology, 24:51–72. DOI: https://doi.org/10.1002/zoo.20043
Duncan, P., Foose, T.J., Gordon, L.J., Gakahu, C.G., & Lloyd, M., 1990. Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equid/bovid competition and coexistence. Oecologia, 84:411–418. DOI: https://doi.org/10.1007/BF00329768
EFSA Panel (European Food Safety Authority Panel on Additives and Products or Substances used in Animal Feed), 2016. Scientific opinion on the revision of the currently authorised maximum copper content in complete feed. EFSA Journal, 14(8):e4563100. DOI: https://doi.org/10.2903/j.efsa.2016.4563
Ettler, V., Kříbek, B., Majer, V., Knésl, I., & Mihaljevič, M., 2012. Differences in the bioaccessibility of metals/metalloids in soils from mining and smelting areas (Copperbelt, Zambia). Journal of Geochemical Exploration, 113:68–75. DOI: https://doi.org/10.1016/j.gexplo.2011.08.001
Gagnon, M. & Chew, A.E., 2000. Dietary preferences in extant African Bovidae. Journal of Mammalogy, 81(2):490–511. DOI: https://doi.org/10.1644/1545-1542(2000)081<0490:DPIEAB>2.0.CO;2
Girard, V., 2008. Trace element status and immunity. In: Trace Elements in Animal Production Systems. Eds: Schlegel, P., Durosoy, S., & Jongbloed, A.W., Wageningen Academic Publishers, The Netherlands. pp. 215–229.
Goff, J.P., 2018. Invited review: Mineral absorption mechanisms, mineral interactions that affect acid-base and antioxidant status, and diet considerations to improve mineral status. Journal of Dairy Science, 101:2763–2813. DOI: https://doi.org/10.3168/jds.2017-13112
Gould, L. & Kendall, N.R., 2011. Role of the rumen in copper and thiomolybdate absorption. Nutrition Research Reviews, 24:176–182. DOI: https://doi.org/10.1017/S0954422411000059
Hansen, S.L. & Spears, J.W., 2009. Bioaccessibility of iron from soil is increased by silage fermentation. Journal of Dairy Science, 92:2896–2905. DOI: https://doi.org/10.3168/jds.2008-1933
Hatt, J.-M., Codron, D., Müller, D.W.H., Ackermans, N.L., Martin, L.F., Kircher, P.R., Hummel, J., & Clauss, M., 2019. The rumen washes off abrasives before heavy-duty chewing in ruminants. Mammalian Biology, 97:104–111. DOI: https://doi.org/10.1016/j.mambio.2019.06.001
Hatt, J.-M., Codron, D., Ackermans, N.L., Martin, L.F., Richer, H., Kircher, P.R., Gerspach, C., Hummel, J., & Clauss, M., 2020. The effect of the rumen washing mechanism in sheep differs with concentration and size of abrasive particles. Palaeogeography, Palaeoclimatology, Palaeoecology, 550:109728. DOI: https://doi.org/10.1016/j.palaeo.2020.109728
Hill, G.M. & Shannon, M.C., 2019. Copper and zinc nutritional issues for agricultural animal production. Biological Trace Element Research, 188:148–159. DOI: https://doi.org/10.1007/s12011-018-1578-5
Hintz, H.F., 1996. Mineral requirements of growing horses. Pferdeheilkunde, 12(3):303–306.
Hoppe, P.P., 1984. Strategies of digestion in African herbivores. In: Herbivore Nutrition in the Subtropics and Tropics. Eds: Gilchrist, F.M.C. & Mackie, R.I., The Science Press (Pty) Ltd, Craighall, South Africa. pp. 222–243.
Hummel, J., Clauss, M., & Sϋdekum, K.-H., 2020. Aspects of food comminution in ungulates and their consequences for energy budget. In: Mammalian Teeth – Form and Function. Eds: Martin, T. & van Koenigswald, W., Verlag Dr. Friedrich Pfoil, Mϋnchen, Germany. pp. 87–101. DOI: http://doi.org/10.23788/mammteeth.06
Ivan, M., 1988. Effect of faunation on ruminal solubility and liver content of copper in sheep fed low or high copper diets. Journal of Animal Science, 66:1496–1501. DOI: https://doi.org/10.2527/jas1988.6661496x
Jolliff, J.S. & Mahan, D.C., 2013. Effect of dietary calcium and phosphorus levels on the total tract digestibility of innate and supplemental organic and inorganic microminerals in a corn-soybean meal-based diet of growing pigs. Journal of Animal Science, 91:2775–2783. DOI: https://doi.org/10.2527/jas.2012-5532
Kaiser, T.M., Müller, D.W.H., Fortelius, M., Schulz, E., Codron, D., & Clauss, M., 2013. Hypsodonty and tooth facet development in relation to diet and habitat in herbivorous ungulates: implications for understanding tooth wear. Mammal Review, 43(1):34–46. DOI: https://doi.org/10.1111/j.1365-2907.2011.00203.x
Kienzle, E. & Zorn, N., 2006. Bioavailability of minerals in the horse. In: Proceedings of the 3rd European Equine Nutrition & Health Congress, 17–18 March 2006, Ghent University, Merelbeke, Belgium.
Kirchgessner, M., 1993. Homeostasis and homeorhesis in trace element metabolism. In: Trace Element in Man and Animal. Eds: Anke, M., Meissner, D., & Mills, C.F., Media Touristik, Gerstorf, Germany. pp. 4–21.
Kumar, V., Pandita, S., Sidhu, G.P.S., Sharma, A., Khana, K., Kaur, P., Bali, A.S., & Setia, R., 2021. Copper bioavailability, uptake, toxicity and tolerance in plants: A comprehensive review. Chemosphere, 262:127810. DOI: https://doi.org/10.1016/j.chemosphere.2020.127810
Lauper, M., Lechner, I., Barboza, P. S., Collins, W. B., Hummel, J., Codron, D., & Clauss, M., 2013. Rumination of different-sized particles in muskoxen (Ovibos moschatus) and moose (Alces alces) on grass and browse diets, and implications for rumination in different ruminant feeding types. Mammalian Biology, 78:142–152. DOI: https://dx.doi.org/10.1016/j.mambio.2012.06.001
Lintzenich, B.A. & Ward, A.M. 1997. Hay and pellet ratios: Considerations in feeding ungulates [Online]. Nutrition Advisory Group Handbook, Fact sheet 006. Available: chrome-extension://efaidnbmnnnibpcajpcglclefindmkaj/https://nagonline.net/wp-content/uploads/2014/01/NAG-FS006-97-HayPellets-JONI-FEB-24-2002-MODIFIED.pdf
López-Alonso, M. & Miranda, M., 2020. Copper supplementation, a challenge in cattle. Animals, 10(10):1890. DOI: https://doi.org/10.3390/ani10101890
McCaughern, J.H., Mackenzie, A.M., & Sinclair, L.A., 2020. Dietary starch concentration alters reticular pH, hepatic copper concentration, and performance in lactating Holstein-Friesian dairy cows receiving added dietary sulphur and molybdenum. Journal of Dairy Science, 103:9024–9036. DOI: https://doi.org/10.3168/jds.2020-18453
Merceron, G., Ramdarshan, A., Blondel, C., Boisserie, J.-R., Brunetiere, N., Francisco, A., Gautier, D., Milhet, X., Novello, A., & Pret, D., 2016. Untangling the environmental from the dietary: dust does not matter. Proceedings of the Royal Society B: Biological Sciences, 283:20161032. DOI: https://dx.doi.org/10.1098/rspb.2016.1032
Mohieddin, A.M., 2021. Iron overload disorder in captive black rhinoceros: Comparing iron excretion with other African herbivores. MSc thesis (Veterinary Medicine), Ghent University, Belgium.
Moyo, M., Kana, E.B.G., & Nsahlai, I.V., 2017. Modelling of digesta passage rates in grazing and browsing domestic and wild ruminant herbivores. South African Journal of Animal Science, 47(3):362–377. DOI: http://dx.doi/10.4314/sajas.v47i3.13
Nakayama, S.M.M., Ikenaka, Y., Muzandu, K., Muzandu, K., Choogo, K., M’kandawire, E., Yasunda, J., & Ishizuka, M., 2012. Metal and metalloid levels and bio-accumulation characteristics in soil, sediment, land plants and hippopotami (Hippopotamus amphibius L) from the South Luangwa National Park. Ecotoxicology and Environmental Safety, 80:333–338. DOI: http://dx.doi.org/10.1016/j.ecoenv.2012.04.003
National Research Council (NRC), 2001. Chapter 6: Minerals. In: Nutrient Requirements of Dairy Cattle, 7th revised edition. The National Academy Press, Washington, DC, USA. pp. 105–161.
National Research Council (NRC), 2005. Chapter 13: Copper. In: Mineral Tolerance of Animals, 2nd revised edition The National Academy Press, Washington, DC, USA. pp. 134–153.
Nishito, Y. & Kambe, T., 2018. Absorption mechanisms of iron, copper and zinc: An overview. Journal of Nutritional Science and Vitaminology, 64:1–7. DOI: https://doi.org/10.3177/jnsv.64.1
Owen-Smith, N., 1999. Chapter 5: The animal factor in veld management. In: Veld Management in South Africa. Ed: Tainton, N.M., University of Natal Press, Pietermaritzburg, South Africa. pp. 117–138.
Pearce, S.G., Firth, E.C., Grace, N.D., & Fennessy, P.F., 1999. The effect of high pasture molybdenum concentrations on the copper status of grazing horses in New Zealand. New Zealand Journal of Agricultural Research, 42(1):93–99. DOI: https://doi.org/10.1080/00288233.1999.9513357
Przybylo, M., Hummel, J., Ortmann, S., Codron, D., Kohlschein G.-M., Kilga, D., Smithyman, J., Przybylo, U., Świerk, S., Hammer, S., Hatt, J.-M., Górka, P., & Clauss, M., 2019. Digesta passage in nondomestic ruminants: Separation mechanisms in ‘moose-type’ and ‘cattle-type’ species, and seemingly atypical browsers. Comparative Biochemistry and Physiology Part A, 235:180–192. DOI: https://doi.org/10.1016/j.cbpa.2019,06.010
Przybylo, M., Ortmann, S., Świerk, S., & Clauss, M., 2022. Fluid and particle retention in the greater kudu (Tragelaphus strepsiceros). Journal of Animal and Feed Sciences, 31(1):34–39. DOI: https://doi.org/10.22358/jafs/145755/2022
Ricketts, V., Dierenfeld, E.S., Sauer, C., & Whitehouse-Tedd, K., 2020. Feed intake and dietary composition of iron (Fe), copper (Cu), vitamin E, and tannic acid of five captive black rhinoceros (Diceros bicornis) in a UK collection. Zoo Biology, 40:52–58. DOI: https://doi.org/10.1002/zoo.21580
Ritz, J., Hofer, K., Hofer, E., Hackländer, K., Immekus, D., Codron, D., & Clauss, M., 2013. Forestomach pH in hunted roe deer (Capreolus capreolus) in relation to forestomach region, time of measurement and supplemental feeding and comparison among wild ruminant species. European Journal of Wildlife Research, 59:505–517. DOI: https://doi.org/10.1007/s10344-013-0698-7
Roy, A., Kumar, A., Bhattacharya, T., Biswas, J.K., & Watts, M., 2024. Review: Bioaccessibility of potentially harmful metals in dust and soil matrices. Exposure and Health, 16:207–236. DOI: https://doi.org/10.1007/s12403-023-00546-z
Sahu, N.P. & Kamra, D.N., 2002. Microbial eco-system of the gastro-intestinal tract of wild herbivorous animals. Journal of Applied Animal Research, 21(2):207–230. DOI: https://doi.10.1080/09712119.2002.9706370
Sanson, G.D., Kerr, S., & Read, J., 2017. Dietary exogenous and endogenous abrasives and tooth wear in African buffalo. Biosurface and Biotribology, 3:211–223. DOI: https://dx.doi.org/10.1016/j.bxbt.2017.12.006
Schiere, J.B. & De Wit, J., 1993. Feeding standards and feeding systems. Animal Feed Science and Technology, 43:121–134. DOI: https://doi.org/10.1016/0377-8401(93)90147-C
Shabbir, Z., Sardar, A., Shabbir, A., Abbas, G., Shamshad, S., Khalid, S., Natasha, Murtaza, G., Dumat, C., & Shahid, M., 2020. Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere, 259:127436. DOI: https://doi.org/10.1016/j.chemophere.2020.127436
Smit, N., 2018. Calculation of the grazing capacity and browsing capacity of game species. Wildlife Breeders Journal, 2018:108–117. Published by Wildlife Stud Services (www.ws2.co.za).
Spears, J.W. & Hansen, S.L., 2008. Bioavailability criteria for trace elements in monogastrics and ruminants. In: Trace Elements in Animal Production Systems. Eds: Schlegel, P., Durosoy, S., & Jongbloed, A.W., Wageningen Academic Publishers, The Netherlands. pp. 161–175.
Suttle, N.F., 1975a. Changes in the availability of dietary copper to young lambs associated with age and weaning. The Journal of Agricultural Science, 84:255–161. DOI: https://doi.org/10.1017/S0021859600052370
Suttle, N.F., 1975b. The role of organic sulphur in the copper-molybdenum-S interrelationship in ruminant nutrition. British Journal of Nutrition, 34:411–420. DOI: http://doi.org/10.1017/S0007114575000475
Suttle, N.F., 1994. Chapter 9: Meeting the copper requirements of ruminants. In: Recent Advances in Animal Nutrition. Eds: Carnworthy, P.C. & Cole, D.J.A., Nottingham University Press, Leicestershire, U.K. pp. 173–187.
Suttle, N.F., 2004. Assessing the needs of cattle for trace elements. In Practice, Nov/Dec 2004:553–561.
Suttle, N.F., 2022. Mineral Nutrition of Livestock, 5th edition. CABI Publishing, CABI International, Wallingford, Oxon, UK.
Van der Ent, A., Baker, A.J.M., Reeves, R.D., Pollard, A.J., & Schat, H., 2013. Hyperaccumulators of metal and metalloids trace elements: Facts and fiction. Plant and Soil, 362:319–334. DOI: http://doi.org/10.1007/s11104-012-1287-3
Van Ryssen, J.B.J. & Bath, G.F., 2024. Copper (Cu) metabolism in domestic herbivores as guide to criteria for predicting the Cu nutritional status of wild ruminants in southern Africa. Journal of the South African Veterinary Association, 95(1):26–34. DOI: https://doi.org/10.36303/JSAVA.580
Van Soest, P.J., 1994. Nutritional Ecology of the Ruminant, 2nd edition. Cornell University Press, London, UK.
Vasques, I.C.F., Lima, F.R.D., Oliveira, J.R., de Morais, E.G., Pereira, P., Guiherme, L.R.G., & Marques, J.J., 2020. Comparison of bioaccessibility methods in spiked and field Hg-contaminated soils. Chemosphere, 254:126904. DOI: https://doi.org/10.1016/j.chemosphere.2020.126904
Waghorn, G.C., Shelton, I.D., & Sinclair, B.R., 1990. Distribution of elements between solid and supernatant fractions of digesta in sheep given six diets. New Zealand Journal of Agricultural Research, 33:259–269. DOI: https://doi.org/10.1080/00288233.1990.10428418
Weiss, W.P., 1998. Requirements of fat-soluble vitamins for dairy cows: A review. Journal of Dairy Science, 81(9):2493–2501. DOI: https://doi.org/10.3168/jds.S0022-0302(98)70141-9
White, C.L., 1996. Understanding the mineral requirements of sheep. In: Detection and Treatment of Mineral Nutrition Problems in Grazing Sheep. Eds: Masters D.G. & White, C.L., ACIAR Monograph No 37, Canberra, Australia. pp. 15–29.
Windisch, W. & Ettle, T., 2008. Limitations and possibilities for progress in defining trace mineral requirements of livestock. In: Trace Elements in Animal Production Systems. Eds: Schlegel, P., Durosoy, S., & Jongbloed, A.W., Wageningen Academic Publishers, The Netherlands. pp. 187–200.
Downloads
Published
Issue
Section
License
Copyright (c) 2025 J.B.J. van Ryssen, G.F. Bath (Author)

This work is licensed under a Creative Commons Attribution 4.0 International License.

