DOI QR코드

DOI QR Code

Calcium Digestibility and Metabolism in Pigs

  • Gonzalez-Vega, J.C. (Department of Animal Sciences, University of Illinois) ;
  • Stein, H.H. (Department of Animal Sciences, University of Illinois)
  • Published : 2014.01.01

Abstract

Calcium (Ca) and phosphorus (P) are minerals that have important physiological functions in the body. For formulation of diets for pigs, it is necessary to consider an appropriate Ca:P ratio for an adequate absorption and utilization of both minerals. Although both minerals are important, much more research has been conducted on P digestibility than on Ca digestibility. Therefore, this review focuses on aspects that are important for the digestibility of Ca. Only values for apparent total tract digestibility (ATTD) of Ca have been reported in pigs, whereas values for both ATTD and standardized total tract digestibility (STTD) of P in feed ingredients have been reported. To be able to determine STTD values for Ca it is necessary to determine basal endogenous losses of Ca. Although most Ca is absorbed in the small intestine, there are indications that Ca may also be absorbed in the colon under some circumstances, but more research to verify the extent of Ca absorption in different parts of the intestinal tract is needed. Most P in plant ingredients is usually bound to phytate. Therefore, plant ingredients have low digestibility of P due to a lack of phytase secretion by pigs. During the last 2 decades, inclusion of microbial phytase in swine diets has improved P digestibility. However, it has been reported that a high inclusion of Ca reduces the efficacy of microbial phytase. It is possible that formation of insoluble calcium-phytate complexes, or Ca-P complexes, not only may affect the efficacy of phytase, but also the digestibility of P and Ca. Therefore, Ca, P, phytate, and phytase interactions are aspects that need to be considered in Ca digestibility studies.

Keywords

Calcium;Digestibility;Phosphorus;Phytase;Phytate;Pigs

References

  1. Stein, H. H., C. Pedersen, A. R. Wirt, and R. A. Bohlke. 2005. Additivity of values for apparent and standardized ileal digestibility of amino acids in mixed diets fed to growing pigs. J. Anim. Sci. 83:2387-2395.
  2. Stein, H. H., B. Seve, M. F. Fuller, P. J. Moughan, and C. F. M. de Lange. 2007. Invited review: Amino acid bioavailability and digestibility in pig feed ingredients: Terminology and application. J. Anim. Sci. 85:172-180. https://doi.org/10.2527/jas.2005-742
  3. Sulabo, R. C. and H. H. Stein. 2013. Digestibility of phosphorus and calcium in meat and bone meal fed to growing pigs. J. Anim. Sci. 91:1285-1294. https://doi.org/10.2527/jas.2011-4632
  4. Taylor, J. G. and D. A. Bushinsky. 2009. Calcium and phosphorus homeostasis. Blood Purif. 27:387-394. https://doi.org/10.1159/000209740
  5. Tryon, A. F. and B. G. Bibby. 1966. Preliminary studies on pig saliva. Arch. Oral Biol. 11:527-531. https://doi.org/10.1016/0003-9969(66)90159-2
  6. Veum, T. L. 2010. Phosphorus and calcium nutrition and metabolism. In: Phosphorus and calcium utilization and requirements in farm animals (Ed. D. M. S. S. Vitti and E. Kebreab). CAB International, London, United Kingdom. pp. 94-111.
  7. Visek, W. J., R. A. Monroe, E. W. Swanson, and C. L. Comar. 1953. Determination of endogenous fecal calcium in cattle by a simple isotope dilution method. J. Nutr. 50:23-33.
  8. Vitti, D. M. S. S. and J. C. Da Silva Filho. 2010. Isotope dilution technique. In: Phosphorus and Calcium Utilization and Requirements in Farm Animals (Ed. D. M. S. S. Vitti and E. Kebreab). CAB International, London, United Kingdom. pp. 8-17.
  9. Vitti, D. M. S. S., J. C. Da Silva Filho, H. Louvandini, R. S. Dias, I. C. S. Bueno, and E. Kebreab. 2010. Phosphorus and calcium utilization in ruminants using isotope dilution technique. In: Phosphorus and Calcium Utilization and Requirements in Farm Animals (Ed. D. M. S. S. Vitti and E. Kebreab). CAB International, London, United Kingdom. pp. 45-67.
  10. Wasserman, R. H., C. L. Comar, and M. M. Nold. 1956. The influence of amino acids and other organic compounds on the gastrointestinal absorption of calcium and strontium in the rat. J. Nutr. 59:371-383.
  11. Weaver, C. M., B. R. Martin, J. S. Ebner, and C. A. Krueger. 1987. Oxalic acid decreases calcium absorption in rats. J. Nutr. 117:1903-1906.
  12. Weaver, C. M., B. R. Martin, J. A. Story, I. Hutchinson, and L. Sanders. 2010. Novel fibers increase bone calcium content and strength beyond efficacy of large intestine fermentation. J. Agric. Food Chem. 58:8952-8957. https://doi.org/10.1021/jf904086d
  13. Widmer, M. R., L. M. McGinnis, and H. H. Stein. 2007. Energy, phosphorus, and amino acid digestibility of high-protein distillers dried grains and corn germ fed to growing pigs. J. Anim. Sci. 85:2994-3003. https://doi.org/10.2527/jas.2006-840
  14. Wise, A. 1983. Dietary factors determining the biological activities of phytate. Nutr. Abstr. Rev. 53:791-806.
  15. Rojas, O. J. and H. H. Stein. 2012. Digestibility of phosphorus by growing pigs of fermented and conventional soybean meal without and with microbial phytase. J. Anim. Sci. 90:1506-1512. https://doi.org/10.2527/jas.2011-4103
  16. Rojas, O. J., Y. Liu, and H. H. Stein. 2013. Phosphorus digestibility and concentration of digestible and metabolizable energy in corn, corn coproducts, and bakery meal fed to growing pigs. J. Anim. Sci. 91:5326-5335. https://doi.org/10.2527/jas.2013-6324
  17. Ross, R. D., G. L. Cromwell, and T. S. Stahly. 1984. Effects of source and particle size on the biological availability of calcium in calcium supplements for growing pigs. J. Anim. Sci. 59:125-134.
  18. Rostagno, H. S., L. F. T. Albino, J. L. Donzele, P. C. Gomes, R. F. de Oliveira, D. C. Lopes, A. S. Ferreira, S. L. T. Barreto, and R. F. Euclides. 2011. Brazilian tables for poultry and swine. H. S. Rostagno. 3rd. edn. Universidade Federal de Vicosa, Vicosa, Brazil.
  19. Sandberg, A. S., T. Larsen and B. Sandstrom. 1993. High dietary calcium level decreases colonic phytate degradation in pigs fed a rapeseed diet. J. Nutr. 123:559-566.
  20. Sauvant, D., J.-M. Perez, and G. Tran. 2004. Tables of composition and nutritional value of feed materials: Pigs, Poultry, Cattle, Sheep, Goats, Rabbits, Horses, Fish. (Ed. D. Sauvant, J. M. Perez, and G. Tran). Institut National de la Recherche Agronomique, Association Francaise de Zootechnie, Paris, France.
  21. Scholz-Ahrens, K. E., P. Ade, B. Marten, P. Weber, W. Timm, Y. Asil, C-C. Gluer, and J. Schrezenmeir. 2007. Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J. Nutr. 137:838S-846S.
  22. Selle, P. H., A. J. Cowieson, and V. Ravindran. 2009. Consequences of calcium interactions with phytate and phytase for poultry and pigs. Livest. Sci. 124:126-141. https://doi.org/10.1016/j.livsci.2009.01.006
  23. Sherwood, L., H. Klandorf, and P. H. Yancey. 2013. Endocrine systems. In: L. Sherwood, H. Klandorf, and P. H. Yancey, editors, Animal physiology: From genes to organism. 2nd ed. Brooks/Cole, Belmont, CA. pp. 268-334.
  24. Soares, J. H. Jr. 1995. Calcium bioavailability. In: Bioavailability of Nutrients for Animals: Amino Acids, Minerals, and Vitamins (Ed. C. B. Ammerman, D. H. Baker and A. J. Lewis). Academic Press, San Diego, California. pp. 95-118.
  25. Stein, H. H., O. Adeola, G. L. Cromwell, S. W. Kim, D. C. Mahan, and P. S. Miller. 2011. Concentration of dietary calcium supplied by calcium carbonate does not affect the apparent total tract digestibility of calcium, but reduces digestibility of phosphorus by growing pigs. J. Anim. Sci. 89:2139-2144. https://doi.org/10.2527/jas.2010-3522
  26. Stein, H. H., M. G. Boersma, and C. Pedersen. 2006. Apparent and true total tract digestibility of phosphorus in field peas (Pisum sativum L.) by growing pigs. Can. J. Anim. Sci. 86:523-525. https://doi.org/10.4141/A05-091
  27. Stein, H. H., C. T. Kadzere, S. W. Kim, and P. S. Miller. 2008. Influence of dietary phosphorus concentration on the digestibility of phosphorus in monocalcium phosphate by growing pigs. J. Anim. Sci. 86:1861-1867. https://doi.org/10.2527/jas.2008-0867
  28. Migicovsky, B. B., A. M. Nielson, M. Gluck, and R. Burgess. 1951. Penicillin and calcium absorption. Arch. Biochem. Biophys. 34:479-480. https://doi.org/10.1016/0003-9861(51)90029-X
  29. Moore, J. H. and C. Tyler. 1955a. Studies on the intestinal absorption and excretion of calcium and phosphorus in the pig. 1. A critical study of the Bergeim technique for investigating the intestinal absorption and excretion of calcium and phosphorus. Br. J. Nutr. 9:63-80. https://doi.org/10.1079/BJN19550012
  30. Moore, J. H. and C. Tyler. 1955b. Studies on the intestinal absorption and excretion of calcium and phosphorus in the pig. 2. The intestinal absorption and excretion of radioactive calcium and phosphorus. Br. J. Nutr. 9:81-93. https://doi.org/10.1079/BJN19550013
  31. National Research Council. 1998. Nutrient requirements of swine. 10th Ed. National Academy Press, Washington, DC.
  32. National Research Council. 2012. Nutrient requirements of swine. 11th Ed. National Academy Press, Washington, DC.
  33. Partridge, I. G. 1978. Studies on digestion and absorption in the intestines of growing pigs: 3. Net movements of mineral nutrients in the digestive tract. Br. J. Nutr. 39:527-537. https://doi.org/10.1079/BJN19780068
  34. Petersen, G. I. and H. H. Stein. 2006. Novel procedure for estimating endogenous losses and measurement of apparent and true digestibility of phosphorus by growing pigs. J. Anim. Sci. 84:2126-2132. https://doi.org/10.2527/jas.2005-479
  35. Pineda, L., S. Roberts, B. Kerr, R. Kwakkel, M. Verstegen, and K. Bregendahl. 2008. Maximum dietary content of corn dried distiller's grains with solubles in diets for laying hens. Effect on nitrogen balance, manure excretion, egg production, and egg quality. Iowa State University 2008 Animal Industry Report. R2334.
  36. Pointillart, A., N. Fontaine, M. Thomasset, and M. E. Jay. 1985. Phosphorus utilization, intestinal phosphatases and hormonal control of calcium metabolism in pigs fed phytic phosphorus:soyabean or rapeseed diets. Nutr. Rep. Int. 32:155-167.
  37. Poulsen, H. D., D. Carlson, J. V. Norgaard, and K. Blaabjerg. 2010. Phosphorus digestibility is highly influenced by phytase but slightly by calcium in growing pigs. Livest. Sci. 134:100-102. https://doi.org/10.1016/j.livsci.2010.06.110
  38. Qian, H., E. T. Kornegay, and D. E. Conner, Jr. 1996. Adverse effects of wide calcium:phosphorus ratios on supplemental phytase efficacy for weanling pigs fed two dietary phosphorus levels. J. Anim. Sci. 74:1288-1297.
  39. R & D Systems Inc. 2007. Calcium and phosphorus metabolism. http://www.rndsystems.com/mini_review_detail_objectname_MR07_CalciumPhosphorusMetabolism.aspx Accessed Apr. 15, 2011.
  40. Malde, M. K., I. E. Graff, H. Siljander-Rasi, E. Venalainen, K. Julshamn, J. I. Pedersen, and J. Valaja. 2010. Fish bones - a highly available calcium source for growing pigs. J. Anim. Physiol. Anim. Nutr. 94:e66-e76. https://doi.org/10.1111/j.1439-0396.2009.00979.x
  41. Martz, F. A., A. T. Belo, M. F. Weiss, and R. L. Belyea. 1999. True absorption of calcium and phosphorus from corn silage fed to nonlactating, pregnant dairy cows. J. Dairy Sci. 82:618-622. https://doi.org/10.3168/jds.S0022-0302(99)75275-6
  42. Helander, E., M. Nasi, and K. Partanen. 1996. Effects of supplementary Aspergillus niger phytase on the availability of plant phosphorus, other minerals and nutrients in growing pigs fed on high-pea diets. J. Anim. Physiol. Anim. Nutr. 76:66-79. https://doi.org/10.1111/j.1439-0396.1996.tb00677.x
  43. Kellems, R. O. and D. C. Church. 1998. Nutrients: Their metabolism and feeding standards. In: Livestock Feeds and Feeding, 4th ed. (Ed. R. O. Kellems and D. C. Church). Prentice-Hall, Inc, Upper Saddle River, New Jersey. pp. 16-39.
  44. Kemme, P. A., J. S. Radcliffe, A. W. Jongbloed, and Z. Mroz. 1997. Factors affecting phosphorus and calcium digestibility in diets for growing-finishing pigs. J. Anim. Sci. 75:2139-2146.
  45. Kerr, B. J., T. E. Weber, P. S. Miller, and L. L. Southern. 2010. Effect of phytase on apparent total tract digestibility of phosphorus in corn-soybean meal diets fed to finishing pigs. J. Anim. Sci. 88:238-247. https://doi.org/10.2527/jas.2009-2146
  46. Kil, D. Y., T. E. Sauber, D. B. Jones, and H. H. Stein. 2010. Effect of the form of dietary fat and the concentration of dietary neutral detergent fiber on ileal and total tract endogenous losses and apparent and true digestibility of fat by growing pigs. J. Anim. Sci. 88:2959-2967. https://doi.org/10.2527/jas.2009-2216
  47. Kornegay, E. T. 1985. Calcium and phosphorus in swine nutrition. In: Section 3 in NFIA Literature Review on Calcium and Phosphorus in Animal Nutrition. National Feed Ingredients Association, West Des Moines, Iowa. pp. 9.
  48. Kumar, R. 1995. Calcium transport in epithelial cells of the intestine and kidney. J. Cell. Biochem. 57:392-398. https://doi.org/10.1002/jcb.240570304
  49. Lantzsch, H. J., S. Wjst, and W. Drochner. 1995. The effect of dietary calcium on the efficacy of microbial phytase in rations for growing pigs. J. Anim. Physiol. Anim. Nutr. 73:19-26. https://doi.org/10.1111/j.1439-0396.1995.tb00399.x
  50. Lei, X. G., P. K. Ku, E. R. Miller, M. T. Yokoyama, and D. E. Ullrey. 1994. Calcium level affects the efficacy of supplemental microbial phytase in corn-soybean meal diets of weanling pigs. J. Anim. Sci. 72:139-143.
  51. Li, Z., G. Yi, J. Yin, P. Sun, D. Li, and C. Knight. 2008. Effects of organic acids on growth performance, gastrointestinal pH, intestinal microbial populations and immune responses of weaned pigs. Asian-Aust. J. Anim. Sci. 21:252-261. https://doi.org/10.5713/ajas.2008.70089
  52. Liu, J., D. W. Bollinger, D. R. Ledoux, and T. L. Veum. 1998. Lowering the dietary calcium to total phosphorus ratio increases phosphorus utilization in low-phosphorus corn-soybean meal diets supplemented with microbial phytase for growing-finishing pigs. J. Anim. Sci. 76:808-813.
  53. Liu, J., D. W. Bollinger, D. R. Ledoux, and T. L. Veum. 2000. Effects of dietary calcium:phosphorus ratios on apparent absorption of calcium and phosphorus in the small intestine, cecum, and colon of pigs. J. Anim. Sci. 78:106-109.
  54. Liu, S., S. Li, L. Lu, J. Xie, L. Zhang, Y. Jiang, and X. Luo. 2012. Development of a procedure to determine standardized mineral availabilities in soybean meal for broiler chicks. Biol. Trace Elem. Res. 148:32-37. https://doi.org/10.1007/s12011-012-9332-x
  55. Almeida, F. N. and H. H. Stein. 2012. Effects of graded levels of microbial phytase on the standardized total tract digestibility of phosphorus in corn and corn coproducts fed to pigs. J. Anim. Sci. 90:1262-1269. https://doi.org/10.2527/jas.2011-4144
  56. Ammerman, C. B. 1995. Methods for estimation of mineral bioavailability. In: Bioavailability of Nutrients for Animals: Amino Acids, Minerals, and Vitamins. (Ed. C. B. Ammerman, D. H. Baker, and A. J. Lewis). Academic Press, San Diego, California. pp. 83-94.
  57. Baker, S. R. 2011. Aspects of phosphorus nutrition in swine. Masters Thesis, University of Illinois, Urbana, Illinois.
  58. Allen, L. H. 1982. Calcium bioavailability and absorption: A review. Am. J. Clin. Nutr. 35:783-808.
  59. Almeida, F. N. and H. H. Stein. 2010. Performance and phosphorus balance of pigs fed diets formulated on the basis of values for standardized total tract digestibility of phosphorus. J. Anim. Sci. 88:2968-2977. https://doi.org/10.2527/jas.2009-2285
  60. Besancon, P. and L. Gueguen. 1969. Les principales voies du metabolisme calcique chez le porc en croissance. Ann. Biol. Anim. Bioch. Biophys. 9:537-553. https://doi.org/10.1051/rnd:19690408
  61. Bohlke, R. A., R. C. Thaler, and H. H. Stein. 2005. Calcium, phosphorus, and amino acid digestibility in low-phytate corn, normal corn, and soybean meal by growing pigs. J. Anim. Sci. 83:2396-2403.
  62. Bouillon, R., S. Van Cromphaut, and G. Carmeliet. 2003. Intestinal calcium absorption: Molecular vitamin D mediated mechanism. J. Cell. Biochem. 88:332-339. https://doi.org/10.1002/jcb.10360
  63. Brady, S. M., J. J. Callan, D. Cowan, M. McGrane, and J. V. O'Doherty. 2002. Effect of phytase inclusion and calcium/phosphorus ratio on the performance and nutrient retention of grower-finisher pigs fed barley/wheat/soya bean meal-based diets. J. Sci. Food Agric. 82:1780-1790. https://doi.org/10.1002/jsfa.1262
  64. Bringhurst, F. R. and B. Z. Leder. 2006. Regulation of calcium and phosphate homeostasis. In: Endocrinology, 5th Ed. (Ed. L. J. DeGroot and J. L. Jameson). Elsevier, Philadelphia, Pennsylvania. pp. 1465.
  65. Bronner, F. 1987. Intestinal calcium absorption: Mechanisms and implications. J. Nutr. 117:1347-1352.
  66. Bronner, F. 1998. Calcium absorption- A paradigm for mineral absorption. J. Nutr. 128:917-920.
  67. Bronner, F. and W. D. Stein. 1992. Modulation of bone calcium-binding sites regulates plasma calcium: A hypothesis. Calcif. Tissue Int. 50:483-489. https://doi.org/10.1007/BF00582159
  68. Bunzen, S., H. S. Rostagno, D. C. Lopes, F. A. Massakichi Hashimoto, P. C. Gomes, and L. R. Apolonio. 2008. Digestibilidade do fosforo de alimentos de origem vegetal determinada em suinos em crescimento e terminacao. R. Bras. Zootec. 37:1236-1242. https://doi.org/10.1590/S1516-35982008000700014
  69. Burger, E. H., J. Klein-Nulend, A. Van Der Plas, and P. J. Nijweide. 1995. Function of osteocytes in bone-Their role in mechanotransduction. J. Nutr. 125:2020S-2023S.
  70. Corradino, R. A., J. G. Ebel, P. H. Craig, A. N. Taylor, and R. H. Wasserman. 1971. Calcium absorption and the vitamin D3-dependent calcium-binding protein: 1. Inhibition by dietary Strontium. Calc. Tiss. Res. 7:81-92. https://doi.org/10.1007/BF02062596
  71. Costanzo, L. S. 2006. Endocrine physiology. In: Physiology, 3rd Ed. Saunders Elsevier, Philadelphia, Pennsylvania. pp. 377-439.
  72. Cowieson, A. J., T. Acamovic, and M. R. Bedford. 2004. The effects of phytase and phytic acid on the losss of endogenous amino acids and minerals from broiler chickens. Br. Poult. Sci. 45:101-108. https://doi.org/10.1080/00071660410001668923
  73. Crenshaw, T. D. 2001. Calcium, phosphorus, vitamin D, and vitamin K in swine nutrition. In Swine Nutrition, 2nd Ed. (Ed. A. J. Lewis and L. L. Southern). CRC Press, Boca Raton, Florida. pp. 187-212.
  74. Cromwell, G. L., R. D. Coffey, G. R. Parker, H. J. Monegue, and J. H. Randolph. 1995. Efficacy of a recombinant-derived phytase in improving the bioavailability of phosphorus in corn-soybean meal diets for pigs. J. Anim. Sci. 73:2000-2008.
  75. Dilger, R. N. and O. Adeola. 2006. Estimation of true phosphorus digestibility and endogenous phosphorus loss in growing pigs fed conventional and low-phytate soybean meals. J. Anim. Sci. 84:627-634.
  76. Ewing, W. and S. J. Charlton. 2007. Calcium. In: The Minerals Directory, 2nd ed. Context Products Ltd, Leicestershire, United Kingdom. pp. 5a-5f, and 19a.
  77. Fan, M. Z., T. Archbold, W. C. Sauer, D. Lackeyram, T. Rideout, Y. Gao, C. F. M. de Lange, and R. R. Hacker. 2001. Novel methodology allows simultaneous measurement of true phosphorus digestibility and the gastrointestinal endogenous phosphorus outputs in studies with pigs. J. Nutr. 131:2388-2396.
  78. Fernandez, J. A. 1995. Calcium and phosphorus metabolism in growing pigs. 2. Simultaneous radio-calcium and radio-phosphorus kinetics. Livest. Prod. Sci. 41:243-254. https://doi.org/10.1016/0301-6226(94)00064-E
  79. Fisher, H. 1992. Low-calcium diets enhance phytate-phosphorus availability. Nutr. Rev. 50:170-171.
  80. Frandson, R. D., W. L. Wilke, and A. D. Fails. 2009. Microscopic anatomy and growth and development of bone. In: Anatomy and Physiology of Farm Animals, 7th Ed. (Ed. R. D. Frandson, W. L. Wilke, and A. D. Fails). Wiley-Blackwell, Ames, Iowa. pp. 77-85.
  81. Gillespie, J. R. 1987. Minerals. In: Animal Nutrition and Feeding. (Ed. M. A. Bruce and C. Haller). Delmar Publishers Inc., Albany, New York. pp. 53-75.
  82. Gonzalez-Vega, J. C., C. L. Walk, Y. Liu, and H. H. Stein. 2013. Determination of endogenous intestinal losses of Ca and true total tract digestibility of calcium in canola meal fed to growing pigs. J. Anim. Sci. doi:10.2527/jas.2013-6410 https://doi.org/10.2527/jas.2013-6410
  83. Hansard, S. L., H. M. Crowder, and W. A. Lyke. 1957. The biological availability of calcium in feeds for cattle. J. Anim. Sci. 16:437-443.
  84. Hansard, S. L., W. A. Lyke, and H. M. Crowder. 1961. Absorption, excretion and utilization of calcium by swine. J. Anim. Sci. 20:292-296.
  85. Heggeness, F. W. 1959. Effect of antibiotics on the gastrointestinal absorption of calcium and magnesium in the rat. J. Nutr. 68:573-582.

Cited by

  1. The influence of calcium on phytase efficacy in non-ruminant animals vol.56, pp.8, 2016, https://doi.org/10.1071/AN15341
  2. Comparison of apparent ileal and total tract digestibility of calcium in calcium sources for pigs vol.96, pp.4, 2016, https://doi.org/10.1139/cjas-2016-0043
  3. Supplementation of pig diets in the growth and termination phases with different calcium sources pp.1573-7438, 2017, https://doi.org/10.1007/s11250-017-1456-8
  4. Do not neglect calcium: a systematic review and meta-analysis (meta-regression) of its digestibility and utilisation in growing and finishing pigs vol.119, pp.11, 2018, https://doi.org/10.1017/S0007114518000612
  5. Determining the available phosphorus release of Natuphos E 5,000 G phytase for nursery pigs vol.96, pp.3, 2018, https://doi.org/10.1093/jas/sky006