Learned behaviours lead to bone ingestion by phosphorus-deficient cattle
R. M. Dixon A F , M. T. Fletcher B , K. L. Goodwin C , D. J. Reid D , D. M. McNeill E , K. W. L. Yong B and J. C. Petherick A
+ Author Affiliations
- Author Affiliations
A The University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, PO Box 6014, Red Hill, Rockhampton, Qld 4701, Australia.
B The University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, Coopers Plains, Qld 4108, Australia.
C Department of Agriculture and Fisheries, Brian Pastures, PO Box 118, Gayndah, Qld 4625, Australia.
D Department of Agriculture and Fisheries, PO Box 6014, Red Hill, Rockhampton, Qld 4701, Australia.
E The University of Queensland, School of Veterinary Science, Gatton, Qld 4343, Australia.
F Corresponding author. Email: r.dixon77@uq.edu.au
Animal Production Science 59(5) 921-932 https://doi.org/10.1071/AN17251
Submitted: 22 April 2017 Accepted: 22 February 2018 Published: 28 May 2018
Abstract
Grazing cattle deficient in phosphorus (P) often seek out and chew bones, apparently to obtain dietary P. To investigate this phenomenon heifers naïve to P deficiency were either fed a P-deficient diet (LowP) or grazed P-adequate pasture (AdeqP), and preference tests examined their attraction to weathered bones or a control of wood. During Phase 1 (Days 1–145), the LowP heifers developed severe P deficiency and pica, but demonstrated little attraction to weathered bones. During Phase 2 (Days 146–155), heifers were allowed to interact with and to chew a variety of weathered bones. After this experience LowP heifers were more attracted to bones during Phase 3 (Days 156–166) than during Phase 1 (P < 0.05), and more attracted than AdeqP heifers during either phase. Subsequently, in Phase 4 (Days 167–171), LowP heifers were more attracted than AdeqP heifers (P < 0.01) to weathered bones than to a control of wood, and in Phase 5 (Days 172–176) to bones with more extended weathering. During Phase 6 (Days 177–182), attraction was reduced when bones were placed inside a cloth bag. The olfactory constituents from weathered bones were dominated by aliphatic aldehydes and ketones, consistent with long-chain fatty acid breakdown. It was concluded that attraction of P-deficient cattle to seek and ingest bones is primarily a learned response. Smell, taste and visual appearance all appear to be important cues for attraction. Pica is likely important in causing P-deficient cattle to investigate unusual materials, including bones, resulting in cattle learning by making an association between bone chewing and P ingestion.
Additional keywords: bone chewing, learned behaviour, phosphorus deficiency, post-ingestive feedback.
References
Abd-El-Aal MH, Mohamed MS (1989) A comparative study on bone fats from different species of animals. Food Chemistry 31, 93–103.| A comparative study on bone fats from different species of animals.Crossref | GoogleScholarGoogle Scholar |
AOAC (1984) ‘Official methods of analysis of the Association of Official Analytical Chemists. Section 7.099 (a).’ 14th edn (AOAC: Washington, DC)
Arsenos G, Kyriazakis I (1999) The continuum between preferences and aversions for flavoured foods in sheep conditioned by administration of casein doses. Animal Science 68, 605–616.
| The continuum between preferences and aversions for flavoured foods in sheep conditioned by administration of casein doses.Crossref | GoogleScholarGoogle Scholar |
Blair-West JR, Denton DA, Nelson JF, McKinley MJ, Radden BG, Ramshaw EH (1989) Recent studies of bone appetite in cattle. Acta Physiologica Scandinavica 136, 53–58.
Blair-West JR, Denton DA, Ramshaw EH (1990) Olfactory cueing in phosphorus deficient cattle. Proceedings of the Australian Physiological and Pharmacological Society 21, 114P
Blair-West JR, Denton DA, McKinley MJ, Radden BG, Ramshaw EH, Wark JD (1992) Behavioural and tissue responses to severe phosphorus depletion in cattle. The American Journal of Physiology 263, R656–R663.
Bowyer RT (1983) Osteophagia and antler breakage among Roosevelt elk. California Fish and Game 69, 84–88.
Bredin IP, Skinner JD, Mitchell G (2008) Can osteophagia provide giraffes with phosphorus and calcium? The Onderstepoort Journal of Veterinary Research 75, 1–9.
| Can osteophagia provide giraffes with phosphorus and calcium?Crossref | GoogleScholarGoogle Scholar |
Brothwell D (1976) Further evidence of bone chewing by ungulates: the sheep of North Ronaldsay, Orkney. Journal of Archaeological Science 3, 179–182.
| Further evidence of bone chewing by ungulates: the sheep of North Ronaldsay, Orkney.Crossref | GoogleScholarGoogle Scholar |
Burrow HM, Dillon RD (1997) Relationships between temperament and growth in a feedlot and commercial carcass traits of Bos indicus crossbreds. Australian Journal of Experimental Agriculture 37, 407–411.
| Relationships between temperament and growth in a feedlot and commercial carcass traits of Bos indicus crossbreds.Crossref | GoogleScholarGoogle Scholar |
Coates DB (1994) The effect of phosphorus as fertilizer or supplement on pasture and cattle productivity in the semi-arid tropics of north Australia. Tropical Grasslands 28, 90–108.
Coates DB, Dixon RM (2008) Development of NIRS analysis of faeces to estimate non-grass proportions in the diets selected by cattle grazing tropical pastures. Journal of Near Infrared Spectroscopy 16, 471–480.
| Development of NIRS analysis of faeces to estimate non-grass proportions in the diets selected by cattle grazing tropical pastures.Crossref | GoogleScholarGoogle Scholar |
Coates DB, Dixon RM (2011) Developing robust faecal near infrared spectroscopy calibrations to predict diet dry matter digestibility in cattle consuming tropical forages. Journal of Near Infrared Spectroscopy 19, 507–519.
| Developing robust faecal near infrared spectroscopy calibrations to predict diet dry matter digestibility in cattle consuming tropical forages.Crossref | GoogleScholarGoogle Scholar |
Coppock CE, Everett RW, Belyea RL (1976) Effect of low calcium or low phosphorus diets on free choice of calcium phosphate by lactating dairy cows. Journal of Dairy Science 59, 571–580.
| Effect of low calcium or low phosphorus diets on free choice of calcium phosphate by lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |
CSIRO (2007) ‘Nutrient requirements of domesticated ruminants.’ (CSIRO Publishing: Melbourne)
DeGreeff LE, Furton KG (2011) Collection and identification of human remains volatiles by non-contact, dynamic airflow sampling and SPME–GC/MS using various sorbent materials. Analytical and Bioanalytical Chemistry 401, 1295–1307.
| Collection and identification of human remains volatiles by non-contact, dynamic airflow sampling and SPME–GC/MS using various sorbent materials.Crossref | GoogleScholarGoogle Scholar |
Dixon RM, Coates DB (2009) NIR spectroscopy of faeces to evaluate the nutrition and physiology of herbivores. A review. Journal of Near Infrared Spectroscopy 17, 1–31.
| NIR spectroscopy of faeces to evaluate the nutrition and physiology of herbivores. A review.Crossref | GoogleScholarGoogle Scholar |
Dixon RM, Coates DB (2010) The relationship between the concentration of phosphorus in the diet and in faeces of cattle grazing tropical grass and grass–legume pastures. Advances in Animal Biosciences 2, 337
Dixon RM, Smith DM, Porch I, Petherick JC (2001) Effects of experience of young cattle on their voluntary intake of supplements. Australian Journal of Experimental Agriculture 41, 581–592.
| Effects of experience of young cattle on their voluntary intake of supplements.Crossref | GoogleScholarGoogle Scholar |
Dixon RM, White A, Fry P, Petherick JC (2003) Effects of supplement type and previous experience on variability in intake of supplements by heifers. Australian Journal of Agricultural Research 54, 529–540.
| Effects of supplement type and previous experience on variability in intake of supplements by heifers.Crossref | GoogleScholarGoogle Scholar |
Dixon RM, Coates DB, Holmes W, English B, Rolfe J (2011) Phosphorus nutrition and management: overcoming constraints to wider adoption. In ‘Proceedings of the northern beef research update conference’, 3–4 August 2011, Darwin. pp. 102–109. (North Australia Beef Research Council: Qld)
Gordon JG, Tribe DE, Graham TC (1954) The feeding behaviour of phosphorus-deficient cattle and sheep. The British Journal of Animal Behaviour 2, 72–74.
| The feeding behaviour of phosphorus-deficient cattle and sheep.Crossref | GoogleScholarGoogle Scholar |
Green HH (1925) Perverted appetites. Physiological Reviews 5, 336–348.
| Perverted appetites.Crossref | GoogleScholarGoogle Scholar |
Hills J, Kyriazakis I, Nolan JV, Hinch GN, Lynch JJ (1999) Conditioned feeding responses in sheep to flavoured foods associated with sulphur doses. Animal Science 69, 313–325.
| Conditioned feeding responses in sheep to flavoured foods associated with sulphur doses.Crossref | GoogleScholarGoogle Scholar |
Hoffman EM, Curran AM, Dulgerian N, Stockham RA, Eckenrode BA (2009) Characterization of the volatile organic compounds present in the headspace of decomposing human remains. Forensic Science International 186, 6–13.
| Characterization of the volatile organic compounds present in the headspace of decomposing human remains.Crossref | GoogleScholarGoogle Scholar |
Holmes WE (1990) Phosphorus and beef production in northern Australia. 11. A case study approach to the economic assessment of phosphorus supplementation. Tropical Grasslands 24, 250–255.
Langman VA (1978) Giraffe pica behaviour and pathology as indicators of nutritional stress. The Journal of Wildlife Management 42, 141–147.
| Giraffe pica behaviour and pathology as indicators of nutritional stress.Crossref | GoogleScholarGoogle Scholar |
Lee J, Kim D-H, Chang P, Lee J (2007) Headspace–solid phase microextraction (HS–SPME) analysis of oxidized volatiles from free fatty acids (FFA) and application for measuring hydrogen donating antioxidant activity. Food Chemistry 105, 414–420.
| Headspace–solid phase microextraction (HS–SPME) analysis of oxidized volatiles from free fatty acids (FFA) and application for measuring hydrogen donating antioxidant activity.Crossref | GoogleScholarGoogle Scholar |
Lev-Yadun S, Gutman M (2013) Carrion odor and cattle grazing: evidence for plant defense by carrion odor. Communicative & Integrative Biology 6, e26111
| Carrion odor and cattle grazing: evidence for plant defense by carrion odor.Crossref | GoogleScholarGoogle Scholar |
McCosker T, Winks L (1994) ‘Phosphorus nutrition of beef cattle in northern Australia.’ (Meat Research Corporation: Sydney)
McDowell LR (1996) Feeding minerals to cattle at pasture. Animal Feed Science and Technology 60, 247–271.
| Feeding minerals to cattle at pasture.Crossref | GoogleScholarGoogle Scholar |
Minson DJ (1990) ‘Forage in ruminant nutrition.’ (Academic Press: London)
Niethe GE (2011) New R and D for better herd health and productivity. In ‘Proceedings of the northern beef research update conference’, 3–4 August 2011, Darwin. pp. 34–40. (North Australia Beef Research Council: Qld)
Provenza FD (1995) The role of learning in food preferences of ruminants: Greenhalgh and Reid revisited. In ‘Ruminant physiology: digestion, growth and reproduction’. (Eds WV Engelhardt, S Leonhard-Marek, G Breves, D Giesecke) pp. 233–247. (Ferdinand Enke Verlag: Stuttgart, Germany)
Provenza FD (1996) Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. Journal of Animal Science 74, 2010–2020.
| Acquired aversions as the basis for varied diets of ruminants foraging on rangelands.Crossref | GoogleScholarGoogle Scholar |
Shahidi F (2001) Headspace volatile aldehydes as indicators of lipid oxidation in foods. Advances in Experimental Medicine and Biology 488, 113–123.
| Headspace volatile aldehydes as indicators of lipid oxidation in foods.Crossref | GoogleScholarGoogle Scholar |
Sweeney RA (1989) Generic combustion method for determination of crude protein in feeds. Journal – Association of Official Analytical Chemists 72, 770–774.
Theiler A (1920) The cause and prevention of lamziekte. Journal of the Department of Agriculture Union of South Africa 1, 221–244.
Theiler A, Green HH (1932) Aphosphorosis in ruminants. Nutrition Abstracts and Reviews 1, 359–385.
Villalba JJ, Provenza FD, Hall JO, Peterson C (2006) Phosphorus appetite in sheep: dissociating taste from postingestive effects. Journal of Animal Science 84, 2213–2223.
| Phosphorus appetite in sheep: dissociating taste from postingestive effects.Crossref | GoogleScholarGoogle Scholar |
Villalba JJ, Provenza FD, Hall JO (2008) Learned appetites for calcium, phosphorus, and sodium in sheep. Journal of Animal Science 86, 738–747.
| Learned appetites for calcium, phosphorus, and sodium in sheep.Crossref | GoogleScholarGoogle Scholar |
Wadsworth JC, McLean RW, Coates DB, Winter WH (1990) Phosphorus and beef production in northern Australia. 5. Animal phosphorus status and diagnosis. Tropical Grasslands 24, 185–196.
Wang J, Chen CC, Osaki S (1983) Optimization of the phosphorus–UV reagent. Clinical Chemistry 29, 1255
Winks L (1990) Phosphorus and beef production in northern Australia. 2. Responses to phosphorus by ruminants. Tropical Grasslands 24, 140–158.
Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, Hughes SI, Whittington FM (2008) Fat deposition, fatty acid composition and meat quality: a review. Meat Science 78, 343–358.
| Fat deposition, fatty acid composition and meat quality: a review.Crossref | GoogleScholarGoogle Scholar |
