Animal 15 (2021) 100115 Contents lists available at ScienceDirect Animal The international journal of animal biosciences Short communication: Preweaning socialization and environmental enrichment affect short-term performance after regrouping in commercially reared pigs H.-L. Ko a,⁎, S. López-Vergé a, Q. Chong b, J. Gasa a, X. Manteca a, P. Llonch a a Department of Animal and Food Science, School of Veterinary Science, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès (Barcelona), Spain b The Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Midlothian EH25 9RG, UK a r t i c l e i n f o a b s t r a c t Article history: On-farm practices like premature weaning and frequent regrouping induce stress to pigs. Early socialization or Received 30 June 2020 environmental enrichment in piglets reduce weaning stress, as suggested in previous studies. Little research Received in revised form 9 October 2020 with both effects and in commercial settings was found. The aim was to investigate the effects of preweaning so- Accepted 13 October 2020 cialization and environmental enrichment on life-long performance in 661 Danbred pigs. Two treatments were Available online 23 December 2020 distinguished during the suckling period: control (CON, 24 litters) and enriched (ENR, 24 litters). Control piglets Keywords: were raised in barren farrowing pens; ENR piglets were provided with six enrichment objects from birth, and two Growth rate neighboring litters were socialized from Day (D) 14. Pigs were regrouped on D25 (weaning) and D71 (fattening), Intensive production while keeping the same treatment. Individual body weight was recorded on D1, 14, 23, 27, 31, 38, 69, 79, and Life-long performance after slaughter (carcass weight, CW). Pigs were slaughtered in six batches. Estimated slaughter weight (ESW) Mixing was calculated by CW × 1.25. Body weight, CW, and average daily gain (ADG) were analyzed by linear mixed Welfare models. Slaughter age was analyzed by Wilcox Rank-Sum test. Body weight and ESW were adjusted to non- linear models to obtain the predicted growth curves of CON and ENR, from birth to the targeted market weight (TMW, 105 kg). Average daily gain during the suckling, nursery, and fattening periods, and from birth to slaugh- ter, did not differ between treatments. However, ADG of ENR when moving pigs from farrowing to nursery (4- day period) and from nursery to fattening (10-day period), revealed a better performance than CON (+20.6 g/ day, P = 0.02; +53 g/day, P = 0.03, respectively). Enriched pigs tended to be slaughtered 2.8 days earlier than CON (P = 0.08). On the other hand, the predicted growth curves showed a non-significant 2-day window of reaching TMW between treatments (P = 0.23). Results suggested that enriching the neonatal environment im- proved the short-term performance after regrouping, and may benefit the life-long performance by reducing time to reach TMW. © 2020 The Authors. Published by Elsevier Inc. on behalf of The Animal Consortium. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Implications Introduction An improved performance demonstrates a crucial economic interest Intensive pig farming is often associated with poor animal welfare. and a reliable welfare indicator. It is not clear whether the benefits of Pigs are confined in stimulus-poor captive conditions, which failed to early environmental manipulations persist under commercial condi- meet their ethological needs and thwarted the expression of key behav- tions, as most studies were conducted in research facilities. According iors such as foraging and exploration (Godyń et al., 2019). These prob- to the study, raising commercially reared piglets in a physically and so- lems are exacerbated by stressful practices like early weaning and cially enriched environment, showed a sustainable weight gain after frequent mixing, resulting in poor performance and disease susceptibil- regrouping, and a tendency to be slaughtered earlier, compared to ity (Godyń et al., 2019). those in a barren neonatal environment. This represented a cheap and Prior research reported that enrichment of the neonatal environ- pragmatic strategy to ensure better adaptability of regrouping events ment can increase the resilience of piglets toward challenging situations in commercial farms. (Godyń et al., 2019). Even minor modifications such as mixing with un- familiar piglets (Salazar et al., 2018), or provision of enrichment objects (Yang et al., 2018) can reduce stress and aggression without ⁎ Corresponding author. compromising productivity. These strategies are of great interest in E-mail address: henglun.ko@uab.cat (H.-L. Ko). the swine industry, as they require few resources and installation. https://doi.org/10.1016/j.animal.2020.100115 1751-7311/© 2020 The Authors. Published by Elsevier Inc. on behalf of The Animal Consortium. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). H.-L. Ko, S. López-Vergé, Q. Chong et al. Animal 15 (2021) 100115 We aimed to study the effects of preweaning socialization and envi- tendency was considered when 0.05 < P ≤ 0.10. Results are reported ronmental enrichment on life-long performance in pigs. We hypothe- as means± SE. sized that physical and social enrichment of neonatal environment improves the life-long adaptability of pigs to novel regrouping events, Body weight, carcass weight, and average daily gain which leads to higher growth and a shorter time to reach the targeted Estimated slaughter weight (ESW) was calculated by CW × 1.25, as- market weight (TMW), compared to those in the barren environment. suming an 80% of carcass yield. Linear mixed model was the main model to compare different response variables between treatments. Details re- Material and methods garding the response variable, fixed effects, covariate, and random ef- fects of each linear mixed model are presented in Table 1. Animals, housing and diets Slaughter age and predicted growth curves The study was conducted on a commercial farm in Lleida, Spain. A Slaughter age (i.e. days from birth to slaughter) was not normally batch of 661 piglets from 48 Danbred sows (21 primiparous and 27 mul- distributed. A Wilcox Rank-Sum test was applied to compare the tiparous) was studied. Sows were moved to farrowing rooms prior to par- slaughter age between treatments. To predict the time to reach TMW turition. Piglets were individually ear-tagged and litter size was of 105 kg (T105, d), the double exponential Gompertz model in standardized between 13 and 14 piglets after parturition. Each farrowing López-Vergé et al. (2018) was applied, by adjusting all BW and ESW pen was equipped with a feeder and a drinker (ad libitum water) in the into the following formula. front of the crate for the sow, and a nipple drinker (ad libitum water) in ðb−ðc∗tÞÞ the lower part of the crate for the piglets. At weaning, 548 piglets (average BW ¼ A∗e−e 25 days of age) were moved to a nursery room, where they were regrouped according to treatment and BW, irrespective of litter origin A, b, and c are the parameters of the curve. t refers to the time (days). and sex. Each pen was equipped with three feeders (two automatic and one manual) and five nipple drinkers (ad libitum water). Results At the growing-finishing period, 442 pigs (average 71 days of age) were moved to a fattening unit until they were slaughtered. Pigs were One CON sow was removed because of lameness before farrowing. regrouped according to treatment and BW, irrespective of nursery pen Control had 10 primiparous and 13 multiparous sows, and ENR had 10 origin and sex. Each pen was equipped with a concrete box feeder con- primiparous and 14 multiparous sows. Average litter size was 14.1 ± taining ad libitum liquid feed. See Ko et al. (2020) for more details re- 0.1 (CON) and 14.0 ± 0.1 (ENR). During the suckling and nursery pe- garding the general management and housing conditions of each riods, 40 and 69 piglets were lost to follow-up, and 73 and 37 died, re- production stage. Pigs were selected by the farmer periodically and spectively. At slaughter, 100 pigs lost their traceability. were transported by truck 1 day before slaughter. There were six slaughter batches in total, with 45 days of difference between the first Body weight, carcass weight, and average daily gain and the last batch. Sows were fed with a pelleted lactation diet (2450 Kcal/kg) twice a Average BW and average daily gain (ADG) in different stages, and day. Piglets were fed with a mashed creep feed from the 2nd week CW are presented in Table 2. No difference (P > 0.1) of BW and CW until weaning. In the nursery, pigs were fed ad libitum with pelleted was found between treatments. The BW1 had a significant effect on all diets following a three-phase feeding program (2480, 2 470, and 2 460 BW (P < 0.0001), ESW (P = 0.03), and all ADG (P ≤ 0.001). Average Kcal/kg). In the growing-finishing period, pigs were fed with ad libitum daily gain in the suckling, nursery, and fattening periods, and from liquid feed diet following a two-phase feeding program (2 488 and birth to slaughter, did not differ between treatments. However, when 2477Kcal/kg). moving pigs from one facility to another (from farrowing to nursery and nursery to fattening), ADG of ENR were higher than those of CON (P = 0.02 and P = 0.03, respectively) after regrouping. There was an in- Experimental design teraction between treatment and sex in ADG from farrowing to nursery (P = 0.04), where ENR female performed better than ENR male (P = When piglets were born on Day (D) 1, litters were balanced by sow 0.02, +21.3 g/day). parity and randomly assigned to two treatments: control (CON; n = 24 litters) and enriched (ENR; n = 24 litters). Control piglets were raised in Slaughter age and predicted growth curves barren farrowing pens until weaning. Enriched piglets were provided with six enrichment objects per pen from birth (two hemp ropes, two Enriched tended to be slaughtered 2.8 days sooner than CON (194.9 rubber chew toys, and two handmade toys) and two neighboring pens ± 1.03 and 197.7 ± 1.28, P = 0.08). Fig. 1 (a) and (b) presents the pre- were socialized from D14 until weaning (see Ko et al. (2020) for details dicted growth curves by treatment and sex effect, respectively. The hor- regarding the enrichment objects). izontal line corresponds to TMW (105 kg). Neither treatment nor sex affected the time to reach TMW (P = 0.23 and P = 0.43, respectively). Weighing Numerically, ENR (192.2 ± 1.08) reached TMW 2 days earlier than CON (194.2 ± 1.21), and male (192.6 ± 1.21) reached TMW 1.3 days Pigs were individually weighed on 1, 14, 23, 27, 31, 38, 69, and earlier than female (193.9 ± 1.08). There was no interaction between 79 days of age. The BW 1–69 was obtained by Balanzas Cobos PB- treatment and sex on the time to reach TMW (P = 0.36). 4040-60 (Spain) scale [precision: 10/5 g]. The BW 79 was obtained by Meier Brakenberg (Germany) scale [precision: 100 g]. Carcass Discussion weight (CW) was obtained after the carcasses were split longitudi- nally [precision: 10 g]. We investigated the effects of enriching the neonatal environment physically and socially on life-long performance in pigs without modify- Statistical analysis ing the routine management. Based on the results, ENR showed an im- proved ADG after two regrouping events, and a tendency of 2.8-day Data were analyzed in R (R Foundation, Austria). The individual was reduction to be slaughtered, compared to CON. As evidenced in Ko the experimental unit. Statistical significance was set at P ≤ 0.05; a et al. (2020), piglets reared in an ENR environment in their early life 2 H.-L. Ko, S. López-Vergé, Q. Chong et al. Animal 15 (2021) 100115 Table 1 Variables for the linear mixed models of BW, carcass weight (CW), estimated slaughter weight (ESW), and average daily gain (ADG) of pigs. Response variable Fixed effects Covariate Random effect(s) BW1 Treatment, sex – Sow BW14, 23 Treatment, sex BW1 Sow BW27, 31, 38, 69 Treatment, sex BW1 Nursery pen BW79, ESW Treatment, sex BW1 Fattening pen CW Treatment, sex Slaughter batch Fattening pen ADG1–14, 14–23, 1–23 Treatment, sex BW1 Sow ADG23–27, 27–69 Treatment, sex BW1 Nursery pen ADG69–79, 79-ESW Treatment, sex BW1 Fattening pen ADG1-ESW Treatment, sex BW1 Sow, nursery pen, and fattening pen was better adapted to novel environments and social encounters, and in (socialization: Camerlink et al., 2018; Salazar et al., 2018; enrichment: this study, we found that these benefits also suggested a steady weight Yang et al., 2018). The trend of post-weaning growth check and subse- gain after regrouping. quent improvement in 2 weeks after weaning, corresponds to Kanaan A lack of difference in ADG between treatments during the suckling et al. (2012). period indicated that preweaning environmental manipulations had no A 4-day-period of ADG from farrowing to nursery in ENR was higher impact on performance. Similar result was reported in the literature than CON, agreeing with the results within 1-week post-weaning in Table 2 Descriptive statistics of BW, carcass weight (CW), and average daily gain (ADG) of pigs by two treatments (control (CON) and enriched (ENR)) and sex. Item Treatment n df Mean Sex SEM F-value P-value Male Female Suckling period BW1, kg CON 324 3 1.38 1.43 1.34 0.02 0.04 0.85 ENR 337 1.40 1.42 1.38 0.02 BW14, kg CON 264 4 3.43 3.43 3.43 0.06 0.01 0.49 ENR 287 3.45 3.44 3.46 0.06 BW23, kg CON 244 4 5.06 5.08 5.04 0.09 0.63 0.63 ENR 286 4.91 4.90 4.93 0.08 Nursery period BW27, kg CON 262 4 5.11 5.15 5.09 0.09 2.31 0.18 ENR 286 5.25 5.23 5.26 0.08 BW31, kg CON 253 4 5.34 5.38 5.34 0.09 3.24 0.12 ENR 278 5.45 5.48 5.42 0.08 BW38, kg CON 252 4 6.25 6.31 6.22 0.11 1.06 0.48 ENR 278 6.40 6.48 6.31 0.11 BW69, kg CON 209 4 15.36 14.87 15.67 0.25 0.14 0.81 ENR 239 15.29 15.47 15.10 0.23 Fattening period BW79, kg CON 208 4 17.35 16.78 17.71 0.29 0.76 0.50 ENR 234 17.85 17.90 17.80 0.28 CW, kg CON 153 4 91.09 90.62 90.72 0.62 0.05 0.84 ENR 187 90.48 90.34 90.59 0.59 ESW, kg1 CON 153 4 113.86 113.28 113.40 0.78 0.04 0.78 ENR 187 113.10 112.92 113.24 0.74 Suckling period ADG1–14, kg/d CON 264 4 0.154 0.151 0.156 0.004 0.14 0.49 ENR 287 0.158 0.156 0.160 0.003 ADG14–23, kg/d2 CON 244 4 0.179 0.176 0.182 0.004 1.80 0.23 ENR 285 0.162 0.161 0.164 0.004 ADG1–23, kg/d CON 224 4 0.165 0.164 0.166 0.004 0.48 0.63 ENR 286 0.160 0.158 0.161 0.003 3 ADG23–27, g/d CON 231 4 53.3 59.4 48.3 4.7 5.08 0.02 ENR 271 73.9 63.3 84.6 5.7 Nursery period ADG27–69, kg/d CON 207 4 0.249 0.241 0.253 0.005 0.14 0.60 ENR 237 0.241 0.245 0.238 0.004 ADG69–79, kg/d4 CON 206 4 0.201 0.187 0.209 0.012 4.62 0.03 ENR 232 0.254 0.247 0.261 0.013 Fattening period ADG79-ESW, kg/d CON 146 4 0.809 0.809 0.809 0.007 1.32 0.36 ENR 171 0.822 0.832 0.812 0.007 Global ADG ADG1-ESW, kg/d CON 146 4 0.568 0.565 0.570 0.004 0.70 0.43 ENR 172 0.575 0.578 0.571 0.004 1 Estimated slaughter weight (ESW) = CW × 1.25. 2 After preweaning socialization in ENR. 3 After regrouping (weaning) in CON and ENR. 4 After regrouping (from nursery to fattening) in CON and ENR. 3 H.-L. Ko, S. López-Vergé, Q. Chong et al. Animal 15 (2021) 100115 Fig. 1. Average growth curves of pigs by (a) treatment (TRT) (control vs enriched) and (b) sex (male vs female) from birth to slaughter (nCON = 133, nENR = 159; nMale = 132; and nFemale = 160). Targeted market weight was fixed at 105 kg, as the horizontal line shows. Weary et al. (2002) and Hessel et al. (2006). It was likely due to reduced J. Gasa, 0000-0002-5828-7142. aggression (Salazar et al., 2018) and smaller stress (Yang et al., 2018; Ko X. Manteca, 0000-0002-2061-4179. et al., 2020) after weaning in ENR, leading to improved performance. In P. Llonch, 0000-0001-5958-861X. Weary et al. (2002), previously socialized weaners consumed more feed, resulting in greater weight gain post-weaning. As ENR exhibited Author contributions 1.3-times more preweaning exploration than CON (Ko et al., 2020), the stimulation of chewing may be facilitated by the provision of enrich- H.-L. Ko: Conceptualization, investigation, formal analysis, original ment objects (Oostindjer et al., 2010), which could contribute to a better draft, writing – review & editing. S. López-Vergé: Methodology, formal adaptation to solid feed post-weaning. analysis, data curation, writing – review & editing. Q. Chong: Investiga- A 10-day-period of ADG from nursery to fattening in ENR was still tion, original draft. J. Gasa: Resources, data curation, writing – review & higher than CON. This could be due to better adaptability to regrouping, editing. X. Manteca: Conceptualization, supervision, writing – review & including a faster establishment of dominance relationships and less ag- editing. P. Llonch: Conceptualization, methodology, funding acquisition, onistic interactions when encountering unacquainted pigs. According to project administration, investigation, supervision, writing – review & Camerlink et al. (2018), social skills learned from socialization or re- editing. peated regrouping events could last for a long time. Godyń et al. (2019) also concluded that piglets provided with enrichment at the Declaration of interest neonatal stage were shown to perform better social behavior later in their lives. None. As we did not find a conclusive effect on long-term performance, im- proving preweaning rearing conditions might not be an ultimate solu- Acknowledgements tion to optimize pig's welfare and productivity throughout the cycle. Providing constant enrichment could contribute to successful socio- We acknowledge Ramaderies Miqueló and Applied Statistics Service cognitive development, lower stress level, and enhanced social skills, of Universitat Autònoma de Barcelona. which in turn ensures the long-term benefits regarding welfare and productivity (Godyń et al., 2019). However, our study suggested that a Financial support statement low-cost and easy-to-implement strategy could benefit pigs in the short-term without major reconstruction of current facilities. Further This work was funded by the Ministry of Economy, Industry and investigation to develop strategies with similar features is worthy to en- Competitiveness, Spain (AGL2015-68373-C2-1-R). hance welfare and productivity of commercially reared pigs. References Ethics approval Camerlink, I., Farish, M., D’Eath, R.B., Arnott, G., Turner, S.P., 2018. Long term benefits on social behaviour after early life socialization of piglets. Animals 8, 192. The ethical approval reference number is FUE-2016-00441221 by Godyń, D., Nowicki, J., Herbut, P., 2019. Effects of environmental enrichment on pig wel- Universitat Autònoma de Barcelona. fare—A review. Animals 9, 383. Hessel, E.F., Reiners, K., Van den Weghe, H.F.A., 2006. Socializing piglets before weaning: Effects on behavior of lactating sows, pre-and postweaning behavior, and perfor- Data and model availability statement mance of piglets. Journal of Animal Science 84, 2847–2855. Kanaan, V.T., Lay Jr., D.C., Richert, B.T., Pajor, E.A., 2012. Increasing the frequency of co- None of the data were deposited in an official repository. mingling piglets during the lactation period alters the development of social behavior before and after weaning. Journal of Applied Animal Welfare Science 15, 163–180. Ko, H.-L., Chong, Q., Escribano, D., Camerlink, I., Manteca, X., Llonch, P., 2020. Pre-weaning Author ORCIDs socialization and environmental enrichment affect life-long response to regrouping in commercially-reared pigs. Applied Animal Behaviour Science 229, 105044. López-Vergé, S., Gasa, J., Temple, D., Bonet, J., Coma, J., Solà-Oriol, D., 2018. Strategies to H.-L. Ko, 0000-0003-1242-791X. improve the growth and homogeneity of growing-finishing pigs: feeder space and S. López-Vergé, 0000-0002-7499-6045. feeding management. Porcine Health Management 4, 14. 4 H.-L. Ko, S. López-Vergé, Q. Chong et al. Animal 15 (2021) 100115 Oostindjer, M., Bolhuis, J.E., Mendl, M., Held, S., Gerrits, W., Van den Brand, H., Kemp, B., communal piglet area on pre-and post-weaning behaviour and performance. Applied 2010. Effects of environmental enrichment and loose housing of lactating sows on Animal Behaviour Science 76, 279–290. piglet performance before and after weaning. Journal of Animal Science 88, Yang, C.-H., Ko, H.-L., Salazar, L.C., Llonch, L., Manteca, X., Camerlink, I., Llonch, P., 2018. 3554–3562. Pre-weaning environmental enrichment increases piglets’ object play behaviour on Salazar, L.C., Ko, H.-L., Yang, C.-H., Llonch, L., Manteca, X., Camerlink, I., Llonch, P., 2018. a large scale commercial pig farm. Applied Animal Behaviour Science 202, 7–12. 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