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Nitrogen isotopic fractionation as a biomarker for nitrogen use efficiency in ruminants: a meta-analysis

Published online by Cambridge University Press:  29 December 2017

G. Cantalapiedra-Hijar ,
R. J. Dewhurst ,
L. Cheng ,
A. R. J. Cabrita ,
A. J. M. Fonseca ,
P. Nozière ,
D. Makowski ,
H. Fouillet  and
I. Ortigues-Marty
G. Cantalapiedra-Hijar*
Affiliation:
INRA, VetAgro Sup, UMR Herbivores, Université Clermont Auvergne, F-63122 Saint-Genès-Champanelle, France
R. J. Dewhurst
Affiliation:
Scotland’s Rural College, King’s Buildings, West Mains Road, Edinburgh EH9 3JG, UK
L. Cheng
Affiliation:
Faculty of Veterinary and Agricultural Sciences, Dookie Campus, The University of Melbourne, Victoria 3647, Australia
A. R. J. Cabrita
Affiliation:
REQUIMTE, LAQV, Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Rua de Jorge Viterbo Ferreira n.° 228, 4050-313 Porto, Portugal
A. J. M. Fonseca
Affiliation:
REQUIMTE, LAQV, Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Rua de Jorge Viterbo Ferreira n.° 228, 4050-313 Porto, Portugal
P. Nozière
Affiliation:
INRA, VetAgro Sup, UMR Herbivores, Université Clermont Auvergne, F-63122 Saint-Genès-Champanelle, France
D. Makowski
Affiliation:
UMR Agronomie, INRA, AgroParisTech, Université Paris-Saclay, 78850 Thiverval-Grignon, France
H. Fouillet
Affiliation:
UMR Nutrition Physiology and Ingestive Behavior, AgroParisTech, INRA, Paris-Saclay University, F-75005 Paris, France
I. Ortigues-Marty
Affiliation:
INRA, VetAgro Sup, UMR Herbivores, Université Clermont Auvergne, F-63122 Saint-Genès-Champanelle, France
*
†E-mail: gonzalo.cantalapiedra@inra.fr
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Abstract

Animal proteins are naturally 15N enriched relative to the diet and the extent of this difference (Δ15Nanimal-diet or N isotopic fractionation) has been correlated to N use efficiency (NUE; N gain or milk N yield/N intake) in some recent ruminant studies. The present study used meta-analysis to investigate whether Δ15Nanimal-diet can be used as a predictor of NUE across a range of dietary conditions, particularly at the level of between-animal variation. An additional objective was to identify variables related to N partitioning explaining the link between NUE and Δ15Nanimal-diet. Individual values from eight publications reporting both NUE and Δ15Nanimal-diet for domestic ruminants were used to create a database comprising 11 experimental studies, 41 treatments and individual animal values for NUE (n=226) and Δ15Nanimal-diet (n=291). Data were analyzed by mixed-effect regression analysis taking into account experimental factors as random effects on both the intercept and slope of the model. Diets were characterized according to the INRA feeding system in terms of N utilization at the rumen, digestive and metabolic levels. These variables were used in a partial least squares regression analysis to predict separately NUE and Δ15Nanimal-diet variation, with the objective of identifying common variables linking NUE and Δ15Nanimal-diet. For individuals reared under similar conditions (within-study) and at the same time (within-period), the variance of NUE and Δ15Nanimal-diet not explained by dietary treatments (i.e. between-animal variation plus experimental error) was 35% and 55%, respectively. Mixed-effect regression analysis conducted with treatment means showed that Δ15Nanimal-diet was significantly and negatively correlated to NUE variation across diets (NUE=0.415 −0.055×Δ15Nanimal-diet). When using individual values and taking into account the random effects of study, period and diet, the relationship was also significant (NUE=0.358 −0.035×Δ15Nanimal-diet). However, there may be a biased prediction for animals close to zero, or in negative, N balance. When using a novel statistical approach, attempting to regress between-animal variation in NUE on between-animal variation in Δ15Nanimal-diet (without the influence of experimental factors), the negative relationship was still significant, highlighting the ability of Δ15Nanimal-diet to capture individual variability. Among the studied variables related to N utilization, those concerning N efficiency use at the metabolic level contributed most to predict both Δ15Nanimal-diet and NUE variation, with rumen fermentation and digestion contributing to a lesser extent. This study confirmed that on average Δ15Nanimal-diet can predict NUE variation across diets and across individuals reared under similar conditions.

Keywords

15Nruminantnitrogen use efficiencymeta-analysis
Type
Research Article
Information
animal , Volume 12 , Issue 9 , September 2018 , pp. 1827 - 1837
Copyright
© The Animal Consortium 2017 

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References

Cabrita, ARJ, Fonseca, AJM and Dewhurst, RJ 2014. Short communication: relationship between the efficiency of utilization of feed nitrogen and 15 N enrichment in casein from lactating dairy cows. Journal of Dairy Science 97, 7225–7229.Google Scholar
Cantalapiedra-Hijar, G, Fouillet, H, Huneau, JF, Fanchone, A, Doreau, M, Nozière, P and Ortigues-Marty, I 2016. Relationship between efficiency of nitrogen utilization and isotopic nitrogen fractionation in dairy cows: contribution of digestion v. metabolism? Animal 10, 221–229.Google Scholar
Cantalapiedra-Hijar, G, Ortigues-Marty, I, Sepchat, B, Agabriel, J, Huneau, JF and Fouillet, H 2015. Diet–animal fractionation of nitrogen stable isotopes reflects the efficiency of nitrogen assimilation in ruminants. British Journal of Nutrition 113, 1158–1169.Google Scholar
Cheng, L, Edwards, GR, Dewhurst, RJ, Nicol, AM and Pacheco, D 2016. The effect of dietary water soluble carbohydrate to nitrogen ratio on nitrogen partitioning and isotopic fractionation of lactating goats offered a high-nitrogen diet. Animal 10, 779–785.Google Scholar
Cheng, L, Kim, EJ, Merry, RJ and Dewhurst, RJ 2011. Nitrogen partitioning and isotopic fractionation in dairy cows consuming diets based on a range of contrasting forages. Journal of Dairy Science 94, 2031–2041.Google Scholar
Cheng, L, Nicol, AM, Dewhurst, RJ and Edwards, GR 2013a. The effects of dietary nitrogen to water-soluble carbohydrate ratio on isotopic fractionation and partitioning of nitrogen in non-lactating sheep. Animal 7, 1274–1279.Google Scholar
Cheng, L, Sheahan, AJ, Gibbs, SJ, Rius, AG, Kay, JK, Meier, S, Edwards, R, Dewhurst, RJ and Roche, JR 2013b. Technical note: nitrogen isotopic fractionation can be used to predict nitrogen-use efficiency in dairy cows fed temperate pasture. Journal of Animal Science 91, 5785–5788.Google Scholar
Cheng, L, Woodward, SL, Dewhurst, RJ, Zhou, H and Edwards, GR 2014. Nitrogen partitioning, energy use efficiency and isotopic fractionation measurements from cows differing in genetic merit fed low-quality pasture in late lactation. Animal Production Science 54, 1651–1656.Google Scholar
Dijkstra, J, Reynolds, CK, Kebreab, E, Bannink, A, Ellis, JL, France, J and Van Vuuren, AM 2013. Challenges in ruminant nutrition: towards minimal nitrogen losses in cattle. In Energy and protein metabolism and nutrition in sustainable animal production. (ed. JW Oltjen, E Kebreab, H Lapièrre), pp. 47–58. Wageningen Academic Publishers, Wageningen, Netherlands.Google Scholar
Fuller, BT, Fuller, JL, Sage, NE, Harris, DA, O’Connell, TC and Hedges, RE 2004. Nitrogen balance and δ15N: why you’re not what you eat during pregnancy. Rapid Communications in Mass Spectrometry 18, 2889–2896.Google Scholar
Gaye‐Siessegger, J, Focken, U, Abe, HJ and Becker, K 2007. Starvation and low feeding levels result in an enrichment of 13C in lipids and 15N in protein of Nile tilapia Oreochromis niloticus L. Journal of Fish Biology 71, 90–100.Google Scholar
Gaye-Siessegger, J, Focken, U, Muetzel, S, Abe, H and Becker, K 2004. Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138, 175–183.Google Scholar
Hartman, G 2011. Are elevated δ15N values in herbivores in hot and arid environments caused by diet or animal physiology? Functional Ecology 25, 122–131.Google Scholar
Hobson, KA, Alisauskas, RT and Clark, RG 1993. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. The Condor 95, 388–394.Google Scholar
Hof, G, Vervoorn, MD, Lenaers, PJ and Tamminga, S 1997. Milk urea nitrogen as a tool to monitor the protein nutrition of dairy cows. Journal of Dairy Science 80, 3333–3340.Google Scholar
Hristov, AN, Etter, RP, Ropp, JK and Grandeen, KL 2004. Effect of dietary crude protein level and degradability on ruminal fermentation and nitrogen utilization in lactating dairy cows. Journal of Animal Science 82, 3219–3229.Google Scholar
Huhtanen, P and Hristov, AN 2009. A meta-analysis of the effects of dietary protein concentration and degradability on milk protein yield and milk N efficiency in dairy cows. Journal of Dairy Science 92, 3222–3232.Google Scholar
Huhtanen, P, Cabezas-Garcia, EH, Krizsan, SJ and Shingfield, KJ 2015. Evaluation of between-cow variation in milk urea and rumen ammonia nitrogen concentrations and the association with nitrogen utilization and diet digestibility in lactating cows. Journal of Dairy Science 98, 3182–3196.Google Scholar
Jenkins, SG, Partridge, ST, Stephenson, TR, Farley, SD and Robbins, CT 2001. Nitrogen and carbon isotope fractionation between mothers, neonates and nursing offspring. Oecologia 129, 336–341.Google Scholar
Kauffman, AJ and St-Pierre, NR 2001. The relationship of milk urea nitrogen to urine nitrogen excretion in Holstein and jersey cows1. Journal of Dairy Science 84, 2284–2294.Google Scholar
Kohn, RA, Dinneen, MM and Russek-Cohen, E 2005. Using blood urea nitrogen to predict nitrogen excretion and efficiency of nitrogen utilization in cattle, sheep, goats, horses, pigs and rats. Journal of Animal Science 83, 879–889.Google Scholar
Martínez del Rio, C, Wolf, N, Carleton, SA and Gannes, LZ 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84, 91–111.Google Scholar
Minagawa, M and Wada, E 1984. Stepwise enrichment of 1519N along food chains: further evidence and the relation between δ 15 N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.Google Scholar
Nousiainen, J, Shingfield, KJ and Huhtanen, P 2004. Evaluation of milk urea nitrogen as a diagnostic of protein feeding. Journal of Dairy Science 87, 386–398.Google Scholar
Pinheiro, JC and Bates, DM 2000. Linear mixed-effects models. In Mixed-effects models in S ans S-PLUS (ed. J Chambers, W Eddy, Härdle, S Sheather, L Tierney), pp. 3–56. Springer, New York, USA.Google Scholar
Phuong, H N, Friggens, NC, De Boer, IJM and Schmidely, P 2013. Factors affecting energy and nitrogen efficiency of dairy cows: a meta-analysis. Journal of Dairy Science 96, 7245–7259.Google Scholar
Poupin, N, Bos, C, Mariotti, F, Huneau, JF, Tomé, D and Fouillet, H 2011. The nature of the dietary protein impacts the tissue-to-diet 15N discrimination factors in laboratory rats. PloS ONE 6, e28046.Google Scholar
Poupin, N, Mariotti, F, Huneau, JF, Hermier, D and Fouillet, H 2014. Natural isotopic signatures of variations in body nitrogen fluxes: a compartmental model analysis. PLoS Computational Biology 10, e1003865.Google Scholar
R Development Core Team 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved on 10 November 2016. http://www.R-project.org.Google Scholar
Richardson, EC and Herd, RM 2004. Biological basis for variation in residual feed intake in beef cattle. 2. Synthesis of results following divergent selection. Australian Journal of Experimental Agriculture 44, 431–440.Google Scholar
Sauvant, D and Nozière, P 2016. Quantification of the main digestive processes in ruminants: the equations involved in the renewed energy and protein feed evaluation systems. Animal 10, 755–770.Google Scholar
Sears, J, Hatch, SA and O’Brien, DM 2009. Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159, 41–48.Google Scholar
Sick, H, Roos, N, Saggau, E, Haa, K, Meyn, V, Walch, B and Trugo, N 1997. Amino acid utilization and isotope discrimination of amino nitrogen in nitrogen metabolism of rat liver in vivo . Zeitschrift für Ernährungswissenschaft 36, 340–346.Google Scholar
Sponheimer, M, Robinson, T, Ayliffe, L, Passey, B, Roeder, B, Shipley, L, Lopez, E, Cerling, T, Dearing, D and Ehleringer, J 2003a. An experimental study of carbon-isotope fractionation between diet, hair and feces of mammalian herbivores. Canadian Journal of Zoology 8, 871–876.Google Scholar
Sponheimer, M, Robinson, TF, Roeder, BL, Passey, BH, Ayliffe, LK, Cerling, TE, Dearing, MD and Ehleringer, JR 2003b. An experimental study of nitrogen flux in llamas: is 14 N preferentially excreted? Journal of Archaeological Science 30, 1649–1655.Google Scholar
Sutoh, M, Obara, Y and Yoneyama, T 1993. The effects of feeding regimen and dietary sucrose supplementation on natural abundance of 15N in some components of ruminal fluid and plasma of sheep. Journal of Animal Science 71, 226–231.Google Scholar
Vallimont, JE, Dechow, CD, Daubert, JM, Dekleva, MW, Blum, JW, Barlieb, CM, Liu, W, Varga, GA, Heinrichs, AJ and Baumrucker, CR 2010. Genetic parameters of feed intake, production, body weight, body condition score and selected type traits of Holstein cows in commercial tie-stall barns. Journal of Dairy Science 93, 4892–4901.Google Scholar
Vanderklift, MA and Ponsard, S 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136, 169–182.Google Scholar
Warinner, C and Tuross, N 2010. Brief communication: tissue isotopic enrichment associated with growth depression in a pig: Implications for archaeology and ecology. American Journal of Physical Anthropology 141, 486–493.Google Scholar
Wattiaux, MA and Reed, JD 1995. Fractionation of nitrogen isotopes by mixed ruminal bacteria. Journal of Animal Science 73, 257–266.Google Scholar
Wheadon, NM, McGee, M, Edwards, GR and Dewhurst, RJ 2014. Plasma nitrogen isotopic fractionation and feed efficiency in growing beef heifers. British Journal of Nutrition 111, 1705–1711.Google Scholar
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