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Background: The objective of this study was to underline that litter size as a key trait of sows needs new parameters to be evaluated and to target an individual optimum. Large individual variation in litter size affects both production and piglet’s survival and health negatively. Therefore, two new traits were suggested and analyzed. Two data sets on 5509 purebred German Landrace sows and 3926 Large White and crossing sows including at least two parental generations and at least five parities were subjected to variance components analysis. Results: The new traits for evaluating litter size were derived from the individual numbers of total born piglets (TBP) per parity: In most cases, sows reach their maximum litter size in their fourth parity. Therefore, data from at least five parities were included. The first observable maximum and minimum of TBP, and the individual variation expressed by the range were targeted. Maximum of TBP being an observable trait in pig breeding and management yielded clearly higher heritability estimates (h ~ 0.3) than those estimates predominantly reported so far. Maximum TBP gets closer to the genetic capacity for litter size than other litter traits. Minimum of TBP is positively correlated with the range of TBP (r =0.48, r > 0.6). The correlation between maximum of TBP and its individually reached frequency was negative in p g both data sets (r = − 0.28 and − 0.22, respectively). Estimated heritability coefficients for the range of TBP comprised a span of h =0.06 to 0.10. Conclusion: An optimum both for maximum and range of total born piglets in selecting sows is a way contributing to homogenous litters in order to improving the animal-related conditions both for piglets’ welfare and economic management in pig. Keywords: Pig, Litter size, Individual maximum, Variation, Heritability, Trait correlation Background Heritability of total number of piglets born per litter In pig breeding, the number of piglets born alive per (TBP) is larger than that of NBA being more sensitive parity (NBA) is a trait of economically importance, but against several long and short-term effects. But no herit- affected by multiple factors . Heritability is always re- ability estimates > 0.19 have been found in such study re- ported to be relatively low, and the wise breeding deci- ports, neither for TBP and nor for NBA. Genetic variation sion is an enduring challenge. Many biologic effects on between and within breeds was triggering substantial gen- litter size emphasize the problem: healthy conditions of etic increase in prolificacy in recent years , accompan- the sow, specific effects due to the birth process, individ- ied by increasing TBP and NBA. However, correlation ual maternal influences. Multifold environmental im- coefficients of individual litter sizes were < 0.75 . On pacts do play a role as well. One specific example on the other hand, there is much variation in these traits that intrinsic effects is the content of serum immunoglobulin can be exploited in further breeding decisions. A low vari- being lower in piglets from larger litters . ation in individual prolificacy across parities could minimize negative side effects both on survival of piglets and on management in commercial swine production. Correspondence: email@example.com Less work would be needed for managing sows having an Leibniz Institute of Farm Animal Biology (FBN), Institute for Genetics and almost constant TBP, ideally being equal to NBA, through Biometry, Wilhelm-Stahl-Allee 2, D-18196 Dummerstorf, Germany © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Freyer Journal of Animal Science and Technology (2018) 60:13 Page 2 of 7 all their parities. Nursing and feeding conditions could be individual maximum total born piglets of sows occurred stabilized. A reduced individual variation in TBP would in their fourth parities (Fig. 1). This suggests that the help to improving efficiency of piglet production and ani- true individual potential denoted by Max_TBP mostly mal welfare. Targeting an individual optimum in litter size is observable when the sow has finished at least four is presumably a thorny issue, but worth investigating. parities. The pedigree contained 30,620 individuals in total The objective of this study was on the genetic capacity of including 6168 base animals and two or more parental TBP expressed by the individual maximum TBP (Max_TBP) generations of the recorded sows in RA01. The second data and on the individual variation in TBP (Range_TBP). Two set (RACOM) meeting the same conditions as above data sets based on genetically different pools from commer- comprised 3926 German Large White purebred sows and cial swine production in Germany were subjected to analyz- sows from crossings with German Landrace, stemming ing phenotypic trait observations by means of a simple but from 436 sires (details on crossing sows: dam was Large widely used and recognized methodical approach in order to Whitefor 211sows,sirewas LargeWhite for2053 sows). estimate heritability coefficients for these new parameters for Therefore, three breed groups had to be allowed for in litter traits. RACOM. The whole pedigree was larger in RACOM, containing 37,003 individuals with 6567 base animals. Material and Methods Inbreeding was not an issue, neither in RA01 and nor in Phenotypic data RACOM. Fecundity data collected in 30 farms from January 1997 through June 2010 was provided by the Hybridschweine- Description of investigated traits and influencing factors zuchtverband Nord/Ost e.V. Malchin, Germany. In the The target trait was the individual maximum of TBP first data set, 15,271 German Landrace sows (RA01) (Max_TBP). As a secondary trait, a characteristic for de- stemming from 1425 sires belonged to about 800 con- scribing individual variation in TBP of sows should be temporarily farrowing groups. Heritability coefficients easily observable in swine production was on focus. on this large dataset based on first parities have already Range_TBP was used here on the basis of individual been reported (h = 0.10 and 0.13 for NBA respective Max_TBP and individual minimum TBP (Min_TBP). A TBP) . In the present study, 5509 sows with at least sufficient number of individual parities of each sow h five parities were considered (Table 1). Most phenotypic was necessary to calculate Table 1 Basic statistics on the investigated traits individual Range TBP ¼ Max TBP – Min TBP ; hk hi hj maximum and minimum of number total born piglets (Max_TBP and Min_TBP), and individual range of number total born piglets (Range_TBP), number of total born piglets and number of piglets where i and j denoted different parity numbers yielding born alive in first parity (TBP_first and NBA_first) in German the single maximum respective minimum of TBP and k Landrace sows (RA01) and Large White sows including crossing was the number of individually available parities. sows (RACOM) with at least five individual parities each Min_TBP and Max_TBP were in fact new traits Overall observed based on their first individual occurrence. Range_TBP Mean Standard Minimum Maximum describes a specific situation that cannot be expressed deviation by original measurements. Calculating Range_TBP is German Landrace sows (RA01, n = 5509) therefore comparable to the blood pressure amplitude Min_TBP 8.67 2.581 1 17 in medicine. Minimum and maximum were obtained Max_TBP 15.46 2.181 9 29 from different parities of a single sow. E.g., the spe- Range_TBP 7.21 2.908 1 22 cific parity number and contemporarily group of sows (expressed by herd, year and season of parity) leading to TBP_first 11.46 2.850 1 21 the specific trait observation was considered as fixed effect NBA_first 10.81 2.739 1 20 on Max_TBP and Min_TBP. A peculiarity was that the Overall parity number 6.57 1.480 5 15 year of first farrowing had a significant effect on Max_ Large White and crossing sows (RACOM, n = 3926) TBP (P < 0.0001) suggesting a targeted selection effect. Min_TBP 9.34 2.700 1 17 In Range_TBP, the situation was different in terms Max_TBP 15.63 2.260 8 26 that significance of fixed effects was found for herd, year and season related to Min_TBP. Further, the Range_TBP 6.29 2.803 1 22 number of available parities (in analyses of using TBP_first 11.53 2.905 2 20 greater than five parities) resulted in a significant ef- NBA_first 10.84 2.779 1 20 fect on Range_TBP, but not the parity number related Overall parity number 6.90 1.830 5 16 to Min_TBP or Max_TBP. Freyer Journal of Animal Science and Technology (2018) 60:13 Page 3 of 7 Fig. 1 Percentage of sows performing their individual maximum and minimum number of total born piglets (Max_TBP and Min_TBP) and number of piglets born alive (Max_NBA and Min_NBA) in a parity number related to the total number of sows in this parity group (denoted by the horizontal axis). Both unique and multifold occurrences of individual extremes were included in this diagram obtained from 5509 German landrace sows (RA01) with 36,894 phenotypic records in total All significant effects were allowed for trait specifically REML and were run on a LINUX machine [6, 7]. SAS in statistical analyses. For all targeted traits, skewness package [SAS Institute Inc., Cary, NC, US, versions 9.2 and kurtosis were negligibly small. The precondition of a and 9.4] was used for general statistics including Pearson normal distribution was fulfilled. correlation coefficients (accompanied by the error prob- NBA at first parity (NBA_first) has apparently been the ability P) and for testing fixed effects and group differ- most respected trait for production purposes so far as sug- ences by means of GLM and MIXED procedures. gested from the majority of relevant reports. Therefore, it Min_TBP and Max_TBP were considered once as was contemplated in parallel throughout the study. unique trait values at their first occurrence. A repeatabil- ity model was therefore not applied for any of the traits. Statistical analyses Results Genetic parameters of the investigated traits were esti- Heritability estimates mated on the basis of the animal model The relative additive variance components representing the heritability coefficients are shown for both samples y ¼ Xb þ Zu þ e; (Table 2). In fact, results of two analyses per sample are where y is the vector of trait observations (phenotypes), b listed: (i) results from analyses based on all parities ≥ five, vector of fixed effects (breed code, farm, herd-group, year and (ii) results based on exactly five parities. Heritability es- and season of parity, actual parity number (see also above timates of Max_TBP were within a span of 0.29 to 0.39. for further significant effects)), u vector of direct additive Standard errors were low in both samples (SE = 0.02 … 0. genetic (animal) effects, and e the vector of residual effects. 04). Heritability estimates for Min_TBP were considerably X denotes the incidence matrix of fixed effects, Z matrix of lower, namely h =0.07 … 0.11 (in most cases, SE < 0.02). direct additive-genetic effects. u and e were normally dis- Heritability estimates of Range_TBP were lowest in RA01 2 2 tributed (0, A⊗G) with numerator relationship matrix A (h =0.06± 0.01) compared to RACOM (h = 0.10 ± 0.02), and additive genetic variance-covariance structure G,and whereas the use of exactly five parities let to closer (0, I ⊗R)for e, respectively, with. I identity matrix and R results between both samples, but accompanied by e e variance-covariance structure of residuals. The symbol ⊗ larger SE (Table 2). denotes the Kronecker product. The variance components analyses aiming at estimating Frequency of individual maxima and minima in heritability coefficients and their standard errors (SE) were contemplation to Range_TBP carried out by means of univariate modeling and based on About 26 percent of sows reached their Max_TBP more one individual trait observation/trait value each for a sin- than once during their available parities. Three to four gle sow. Computer programs VCE 5.1.2 and PEST V4.0 percent yielded the same maximum more than twice. were used for the estimating heritability (and SE) based on The results were almost equal for RA01 and RACOM. Freyer Journal of Animal Science and Technology (2018) 60:13 Page 4 of 7 Table 2 Estimates of relative additive genetic variance Phenotypic and genetic trait correlations components expressing the heritability coefficients (h )and their Almost all estimated trait phenotypic correlation coeffi- standard errors (VC ± SE) on the investigated traits Min_TBP, rel cients were significant (Table 3). The estimated genetic Max_TBP and Range_TBP and in addition on NBA in first parity correlation coefficients were highly positive for Max_ based on univariate analyses TBP and Range_TBP: r =0.617 ±0.061 in RA01 and Trait Estimated variance components in relation r = 0.761 ± 0.067 in RACOM. The genetic correlation of to the total phenotypic variance Range_TBP and Min_TBP were not significant, r = 0.141 ± Additive genetic Residual 0.132 in RA01 and r = 0.214 ± 0.180 in RACOM. RA01 (German Landrace sows, n = 5509) Phenotypic correlation coefficients for piglets born (i) information on five or more parities used for estimation alive in first parity (NBA_first) and Range_TBP were Min_TBP 0.112 ± 0.014 0.888 ± 0.014 significantly negative (r = − 0.15 in RA01 and r = − 0.22 p p in RACOM, Table 3). This seems advantageous when Max_TBP 0.298 ± 0.021 0.702 ± 0.021 focusing on a very early breeding decision. However, posi- Range_TBP 0.056 ± 0.011 0.944 ± 0.011 tive genetic correlations of NBA_first and Range_TBP NBA_first 0.123 ± 0.017 0.877 ± 0.017 minimize the expectations (r = 0.33 in RA01 and r =0.31 g g (ii) information on exactly five parities used for estimation in RACOM, SE = 0.09 and 0.10, respectively). Min_TBP 0.070 ± 0.015 0.930 ± 0.015 Max_TBP 0.283 ± 0.023 0.717 ± 0.023 Discussion In commercial swine production, litter size is a key trait. Range_TBP 0.066 ± 0.012 9.934 ± 0.012 However, individual numbers of total born and piglets RACOM (Large White and crossing sows, n = 3926) born alive vary in subsequent parities. So far, this fact (i) information on five or more used for estimation has hardly been targeted as a special parameter of sows. Min_TBP 0.098 ± 0.018 0.902 ± 0.018 In this study, individual ranges of TBP were chosen to Max_TBP 0.373 ± 0.030 0.627 ± 0.030 do so as a simple trait in order to draw attention to this Range_TBP 0.104 ± 0.022 0.896 ± 0.022 problem and to suggest coping with. Selection on larger TBP increases NBA but in many NBA_ first 0.116 ± 0.020 0.884 ± 0.020 cases it also increases the number of still born piglets. (ii) information on exactly five parities used for estimation For this reason and to respecting the individual feed- Min_TBP 0.070 ± 0.024 0.930 ± 0.024 ing capacity of a sow, searching for an individual Max_TBP 0.390 ± 0.040 0.610 ± 0.040 optimum TBP should be a target in pig breeding. In Range_TBP 0.084 ± 0.026 0.916 ± 0.026 the investigated material, a clear trend of increasing investigated traits were individual maximum and minimum of number total mean performances in TBP and NBA of first parity born piglets (Max_TBP, Min_TBP), and individual variability in number total were observed during 1997 to 2008. At the same time, born piglets (Range_TBP); number of piglets born alive in first parity there was no increase in mean Range_TBP, but stand- (NBA_first) for comparing to heritability estimates from earlier studies ard deviations of Range_TBP showed an increased The relation was less for Min_TBP. 20 percent of sows trend from 1997 to 2008 very clearly (not shown in showed their Min_TBP twice or more. further detail). This suggests potential for respecting Negative phenotypic correlation coefficients being very individual variation without necessarily decreasing lit- similar in both samples were estimated for the individual ter sizes on average. frequency of Max_TBP and Range_TBP (r = − 0.25 Respecting individual Max_TBP and individual Range_ and − 0.23, P < 0.0001). The even stronger negative TBP could be a way for optimizing the management correlation of individual frequency of Min_TBP and process in swine production and improving animal wel- Range_ TBP was almost the same in RA01 and RACOM fare directly on the sow’s level. Litter size traits in pigs (r = − 0.32 and − 0.31, P < 0.0001). are likely more affected by maternal than by paternal In most cases of RA01, multiple maxima occurred for components. One might argue that the number of five Max_TBP = 13 … 16 piglets (in 996 cases, respective 69 individual parities to evaluate the genetic capacity of percent of sows with multiple maxima). In RACOM, the TBP and individual variation is a challenging limitation. “preferred span of maxima” was Max_TBP = 13 … 17 The preference on fast selection decisions in sows fo- piglets. Multiple minima were observed most frequently cuses on their performances in NBA_first. for Min_TBP = 9 … 11 in RA01 (in 56 percent of sows Which parameter really matters for evaluating a sow for with multiple minima), and Min_TBP = 10 … 12 in litter size with respect to efficiency? Observed Max_TBP RACOM. In total, RACOM was more homogenous in is an individual parameter for the genetic capacity of litter Range_TBP, confirmed by lower mean and lower stand- size as clearly suggested by larger heritability estimates ard deviation (Table 1). compared to traditionally used litter size traits (Table 2). Freyer Journal of Animal Science and Technology (2018) 60:13 Page 5 of 7 Table 3 Phenotypic correlation coefficients of individual variability in number total born piglets (Range_TBP), maximum and minimum number of total born piglets (TBP_Max and TBP_Min), and in addition both the number piglets born alive in first parity (NBA_first) and the individual relative number of still born piglets (SB_rel) obtained from RA01 (n = 5509, above diagonal) and from RACOM (n = 3926, below diagonal), Pearson correlation coefficients were significant at P < 0.0001, besides those marked by superscript letters RA01 (above diagonal) Range_TBP Max_TBP Min_TBP NBA_first SB_rel RACOM Range_TBP ———— 0.478 −0.669 − 0.145 0.079 (below diagonal) Max_TBP 0.475 ————— 0.316 0.277 0.287 Min_TBP −0.672 0.332 ————— 0.392 0.159 NBA_first −0.219 0.257 0.452 ————— 0.011 SB_rel 0.086 0.286 0.148 −0.003 ———— SB_rel was based on phenotypic on all available parities observations on still births adjusted for fixed effects of breed indicator (within RACOM), parity number, herd, year and season using the basic data set (in total, 63,000 records in RA01, 41,500 records in RACOM) for all sows included in the current study P = 0.4256 P = 0.8437 Targeting an optimum TBP does not mean selecting for percent. RACOM was more homogenous in Range_TBP highest Max_TBP. This trait should be evaluated in order than RA01. Due to the large part of crossing sows in- to find a basis for choosing the optimum. Simultaneously, cluded in RACOM, this could be a response of favorable a small individual Range_TBP should be preferred in fu- non-additive components triggering more stabilizing fac- ture breeding objectives. Comparing single sows yielding tors on expressing these traits. On the other hand, des- extremely different Range_TBP reveals the practical value pite fewer sows with trait observations, the pedigree was of low individual variation in litter size. Sows with a Max_ much larger for RACOM than for RA01, a fact that TBP of 13 to 16 showed the lowest Range_TBP and simul- could have caused higher heritability estimates. taneously the most repeatable Max_TBP, accompanied by Selecting sows with an individual optimum TBP re- fewest still births. The significant connection between still spective NBA for breeding could contribute to more births and Range_TBP is also shown by dividing sows into phenotypically (and especially environmentally) balanced range classes and by phenotypic correlations (Fig. 2,Table sustainability. Priority should be given to feeding cap- 3) and by means of eight single sows being extremely dif- acity and maternal behavior. ferent in their Range_TBP (Table 4). Birth weight of each single piglet could likely be an In the present study, the relative genetic variance (her- additional co-variable in evaluating litter size traits . itability) estimated for Range_TBP was about six to 10 However, such data was not available for this study. Table 4 Single sows from RACOM with exactly five parities and extremely low or extremely large ranges of their number in total born piglets per parity (Range_TBP), maximum number of total born piglets (Max_TBP) marked in bold, and the related absolute number of still born piglets (SB) Parity number group with respect to 1 2 3 4 5 Total Range_TBP and breed ID TBP SB TBP SB TBP SB TBP SB TBP SB TBP SB Low Range_TBP Crossing sow 196679 16 215 0 16 0 15 0 15 0 77 2 Large White 285278 13 2 13 1 13 1 14 1 13 0 66 5 Large White 106820 11 0 12 0 12 0 12 0 11 0 58 0 Crossing sow 200791 10 0 10 1 10 0 11 1 11 052 2 Large Range_TBP Large White 106324 17 5 20 2 18 6 70 50 67 13 Crossing sow 194908 10 0 17 2 18 0 17 4 1 0 63 6 Large White 107757 19 0 18 1 17 1 4 0 13 0 71 2 Large White 272177 9 0 11 0 14 2 26 13 14 1 74 16 Freyer Journal of Animal Science and Technology (2018) 60:13 Page 6 of 7 also affect the individual variation of traits related to litter size. Two candidate genes contributing to variation in TBP were reported . One of them is involved in buffering en- vironmental and genetic factors. From the same study, a genetic correlation between TBP and its variation based on boars’ breeding values was reported (r =0. 49 ). This was very similar to the phenotypic cor- relation of Range_TBP and Max_TBP in the present study (r =0.48, Table 3). The results of the study reported here suggest that an individual optimum number of total born and alive born piglets per parity of a sow can be found by respecting in- dividual Max_TBP and Range_TBP. Heritability of sows’ individual Max_TBP is higher than heritability estimates for litter size traits as published so far. More detailed in- vestigations on the basis of a genome wide association study and surely using methods allowing for genotype by environmental interactions could lead to increasing the knowledge on the responsible genes, multifold induced in- teractions and their functions. Focusing on sows being ex- tremely different in their individual variation in litter size would be of value in this continuing research process. Conclusions Using the individual maximum number of total born pig- Fig. 2 Phenotypic means of piglets born alive in first parity (a) and lets as a new trait in genetic analyses reveals considerably relative mean of still born piglets based on phenotypic observations higher heritability estimates (h ~ 0.3) than those from adjusted for fixed effects of breed indicator, litter number, herd, year and using ordinary litter size data repeatedly reported before. season (b) for all sows included in the current study (5509 sows in RA01, Information on the individual maximum is more suited to 3926 in RACOM), grouped by their ranges of total born piglets: Low reflect the genetic proliferative potential of the sow. Many ranges (difference between individual maximum and minimum number of total born piglets is1 to 4 in Range group 1), medium ranges (5 to 9 sows reached their maximum of 13 to 16 piglets in a in Range group 2) and large ranges (≤10 in Range group 3), respectively. parity more than once. Therefore, this trait is suggested to Significance of differences at P < 0.0001 in (b)only: Rangegroups1:3 find an individual optimum litter size for improving both and Range groups 2: 3 in RA01, Range groups 1: 3 in RACOM the management process and animal’s health. A sufficient evaluation of sows regarding both their individual capacity NBA in first parity was analyzed in parallel resulting in in litter size and the related individual variation (e.g. range very similar heritability estimates as reported before . as a simple secondary trait) is possible if data of at least A selection effect on sows under study was therefore not five parities is available. Individual range of litter size in suspected. 2 sows has a heritable component (h =0.06 to 0.10). No earlier reports based on individual maxima and on individual female variation of TBP have been found in Abbreviations the literature related to pig breeding. A recent study car- Max_NBA: Individual maximum number of piglets born alive related to a specific parity; Max_TBP: Individual maximum number of total born piglets of ried out in the Netherlands was based on boars’ observa- a sow related to a specific parity; Min_NBA: Individual minimum number of tions through their daughters . For a deeper insight piglets born alive related to a specific parity; Min_TBP: Individual minimum into the genetics of litter size and related traits, SNP number of total born piglets of a sow related to a specific parity; NBA: Individual number of piglets born alive per parity; NBA_first: Individual technology is being widely adapted. Such studies have number of piglets born alive in first parity; P: Error probability; RA01: Data set been reviewed , and candidate genes of reproduction from German Landrace; RACOM: Data set from Large White and crossing traits in sows were reported based on different pig popu- sows; Range_TBP: Individual range of number of total born piglets of a sow (individual variation); SB: Number of still born piglets of a sow; lations, partly with contradictory results [11–13]. SB_rel: Individual number of still born piglets in a parity adjusted for fixed Non-additive effects of single candidate genes (or effects of herd, year and season of farrowing; SE: Standard error; TBP: Total chromosomal segments) interacting with others could play number of piglets per parity; VCE : Relative variance component; Further, rel symbols on population genetic parameters were used: h - heritability a different role for TBP and NBA in first and higher parities coefficient; r and r - genetic and phenotypic correlation coefficients. Other g p . Therefore, patterns of age-dependently (inter-) acting specific symbols were used only once in the methods section (with genes, and genes affecting environmental sensitivity, could explanation) Freyer Journal of Animal Science and Technology (2018) 60:13 Page 7 of 7 Acknowledgements Data used in this study was provided by Hybridschweinezuchtverband Nord/Ost e.V. Malchin, Germany. Thanks to Dipl.-Ing. Renate Schuster and Dr. Sigfried Hoffmann for valuable communications. Funding No funding from a third party. Availability of data and materials Not applicable; data originated from a commercial pig breeding company. Authors’ contributions The author read and approved the final manuscript. Ethics approval Not applicable. Competing interests The author declares that she has no competing interests. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Received: 25 July 2017 Accepted: 1 May 2018 References 1. Lawlor PG, Lynch PB. A review of factors influencing litter size in Irish sows. Irish Veterinary J. 2007;60:359–66. 2. Nguyen K, Cassar G, Friendship RM, Dewey C, Farzan A, Kirkwood RN. An investigation of induced parturition, birth weight, birth order, litter size, and sow parity on piglet serum concentrations of immunoglobulin G. J Swine Health Prod. 2013;21(3):139–43. 3. 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Journal of Animal Science and Technology – Springer Journals
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