Response to environmental enrichment of weanling pigs on growth, behaviour and welfare after weaning

A total of 360 weaning pigs (Landrace × Yorkshire × Duroc [LYD]: average initial BW 6.56 ± 0.17 kg) were randomly allotted to one of the three treatments based on initial BW. A completely randomized design was used in this study. There were ten pigs per pen, with six replicates per treatment. The experimental treatments were the control, EE-1 (inclusion of play object until one week after weaning), EE-2 (inclusion of play object until two weeks after weaning), and EE-4 (inclusion of play object until four weeks after weaning). For environmental enrichment, the play object was anchored to the floor near a self-feeder (spring play object; Taewoo Livestock, Seoungju, Korea). Experimental diets were provided using commercial feed products. The experimental phases were phase 1 (d 0–14 post weaning) and phase 2 (d 15–28 post weaning). All pens contained a self-feeder and nipple drinker to provide ad libitum to feed and water.

The amount of feed supplemented was measured throughout the experimental period to calculate the average daily feed intake (ADFI). The average daily gain (ADG), ADFI, and gain-to-feed ratio (G/F) were calculated at the end of each phase (phase 1: d 14, phase 2: d 28, and overall: d 0–28 after weaning).

Coefficient of variation (CV) of BW was calculated at the end of each phase (phase 1: d 14, phase 2: d 28) as the CV by dividing the individual BW standard deviation by the mean BW.

The incidence of diarrhea was measured three times (on d 7, 14, and 28). The criteria for collecting data on the incidence of diarrhea were as follows: 1 = hard, dry pellets in a small, hard mass; 2 = hard, formed stool that remained firm and soft; 3 = soft, formed, and moist stool that retained its shape; 4 = soft, unformed stool that assumed the shape of the container; and 5 = watery, liquid stool that could be poured [12].

Piglet behavior was recorded at the end of each phase (d 14 and 28) by installing cameras (FIX Extreme Action Camera, Wuhan Tao Cheng Network Technology, Hubei, China) above each pen. The cameras were arranged through a cable duct located at the top of the middle of each pen to record behavior over the entire area. The video was recorded for 8 h, and the recorded video files were extracted and saved on a high-capacity USB flash drive for analysis. The observation days were at the end of each phase (phase 1: d 14, phase 2: d 28) after weaning and included an 8 h observation period (10:00–18:00). Each behavior was evaluated for 8 h using the video footage, and the number of behavioral observations was shown as the number per hour [13]. The criteria for analyzing the behavior traits are shown in Table 1.

Evaluation of lesions on the body (ear, front, middle, hindquarters, and legs) or tail was conducted by inspecting the two sides of experimental weaning pigs at the end of each phase (d 14 and 28) after weaning [14].

Saliva and hair samples were prepared and harvested at the end of phase 2 (d 28 after weaning). Medical cotton was attached to the fence of each experimental pen with string to collect saliva samples. After weaning, the pigs chewed the medical cotton for 5 to 10 min until fully wet. The cotton was retrieved using the string, and the ear tag of the pig was recorded during the chewing process. Supernatant of the saliva sample (~7–8 mL) was prepared by centrifugation at 3,000×g at 4°C for 10 min and was stored at −20°C until analysis. Salivary cortisol concentration was measured using a commercial ELISA kit (ADI-90-071, Enzo Life Sciences, Farmingdale, NY, USA) [15]. Freshly grown hair from individual weaning pigs was collected and used for the analysis of hair cortisol concentrations. The collected hair samples were washed three times with isopropanol, followed by drying in a vacuum dryer at 35°C, and then placed in an EML plastic tube containing steel pellets and a bead beater (tacoTMPrep, 50/60 Hz 2A, GeneReach Taichung, Taichung, Taiwan). Hair cortisol was extracted using methanol after crushing at Biotechnology Corp., Taiwan. A cortisol ELISA kit (ADI-900-071, Enzo Life Sciences) was used to determine the cortisol concentrations in the extracted sample [16].

Data generated in the present study were subjected to a statistical analysis system (SAS Institute, Cary, NC, USA) using the general linear model procedure in a completely randomized design. When significant differences were identified among the treatment means, they were separated using Tukey’s Honest Significant Difference test. Statistical significance was set at p < 0.05.

The effects of environmental enrichment on growth performance are summarized in Table 2. In phase 1, pigs raised in EE-2 and EE-4 had greater ADG (p = 0.002) than those raised in the control. In phase 2, pigs raised in EE-4 had greater ADG (p = 0.039) than pigs raised in the control. Overall, pigs from EE-2 and EE-4 showed a greater ADG (p = 0.006) than the control. In phase 1, the ADFI of pigs in the EE-2 was higher (p = 0.016) than the control. In phase 2, pigs treated with EE-2 showed higher ADFI (p = 0.030) than pigs reared in the control. Overall, pigs raised in the EE-4 treatment had a greater ADFI (p = 0.014) than the control. However, G/F did not exhibit any significant differences in phase 1, phase 2, or the overall period. The effects of environmental enrichment on group CV are presented in Table 3. Pigs raised in EE-2 and EE-4 had lower uniformity than the pigs raised in the control group in phases 1 (p = 0.006) and 2 (p < 0.001), and overall (p < 0.001).

The effects of environmental enrichment on the incidence of diarrhea are shown in Table 4. The incidence of diarrhea was lower (p < 0.001) in pigs raised in EE-2 and EE-4 than the control treatment in early phase 1 (the first week after weaning). However, environmental enrichment did not exhibit any significant differences among the treatments at the end of phase 1 and phase 2.

The effects of environmental enrichment on behavioral traits are shown in Table 5. Pigs raised in EE-2 and EE-4 exhibited lower biting (p = 0.018), tail biting (p = 0.001), and ear biting (p = 0.016). However, there were no significant differences in behavioral traits in phase 2.

The effects of environmental enrichment on skin lesion scores are shown in Table 6. Pigs raised in EE-4 had lower skin lesion scores (p = 0.015) than those raised in the control. However, there was no significant difference between the treatments in phase 2.

The effects of environmental enrichment on salivary and hair cortisol concentrations are shown in Table 7. Pigs reared in EE-4 had lower (p = 0.032) hair cortisol concentrations than pigs reared in the control. However, there was no significant difference in the cortisol levels of the saliva among the treatments.

Concerns regarding animals’ welfare and growth have led to an increased focus on stress management. In particular, the agonistic behavior induced by the early weaning period is related to growth retardation during the growing and finishing phases of pigs [17]. Environmental enrichment as a play object installation resulted in an increase in growth performance, that is, ADG and ADFI, compared to the control group during the current study, although the enrichment effect on growth was the highest in the EE-2 group. This may result in different responses of the piglets to the object, and interest in the enriched environment appears to diminish with age during the weaning phase [18,19]. Similarly, the growth of weaning pigs raised in an enriched environment was higher than that of those raised in a commercial barren environment; however, the enriched environment did not affect growth performance until 20 weeks of age [20]. As a crucial period, the weaning process is strongly connected to the growth of weaning pigs, but it is also linked to the timing of the final market weight and profitability of the producer. Accordingly, the management CV of BW just before or immediately after weaning may be used as a critical indicator to predict the final outcome of weaning pigs [21]. The observed CV of BW in the present study was approximately 10%, and the EE-4 group had the lowest CV of BW compared to the other groups, including the control group. Furthermore, enriched groups had slightly better BW evenness within a group; however, various factors may contribute to this phenomenon. Therefore, further studies are warranted.

As a common condition, post-weaning diarrhea is a well-known disease that is induced by weaning stress in weaned piglets worldwide. Since the start of the weaning process, weaned pigs quickly adapt to various environmental changes, such as different forms of diet and mixing with other pigs. Furthermore, as a result of these changes, weaned pigs exhibit abnormal symptoms, such as lower feed intake and a higher incidence of diarrhea, which are closely associated with the retarded growth of pigs [22–24]. In the present study, pigs raised in the EE-4 group showed the lowest incidence of diarrhea in the early post-weaning period (d 7 post-weaning), although they had a higher incidence of diarrhea than those in the rest of the weaning period. Few studies have examined the incidence of diarrhea in weaned pigs in environments enriched with play objects to demonstrate the precise relationship between environmental enrichment and the incidence of diarrhea. However, few studies have reported that feed intake and CV of BW can be used as indicators to measure the proper growth of weaned pigs [25]. Weaning stress, which is strongly associated with an increase in the inflammatory response in the gastrointestinal tract, is one of the various stressors contributing to the incidence of diarrhea in weaned pigs [26]. In this regard, the results of the present study, which are closely related to previous results showing improved ADG, ADFI, and CV of BW conditions in an enriched environment, may contribute to another positive effect of enriched environments in weaning pigs.

The behavior of animals is considered an essential factor in their growth and welfare, and animals must be exposed to objects that are sufficient to maintain their behavior [27]. It is well known that agonistic behavior during the early post-weaning period, which is common in commercial barren environments, is directly related to poor feed intake and growth in weaning pigs. In the present study, pigs exhibited reduced agonistic behavior, including torso, leg, ear, and tail biting, during the early post-weaning period (d 14). The results of the present study are consistent with previous studies showing that an enriched environment led to elevated play behaviors [28,29] or more proactive and explorative behavior in weaning pigs [28,30,31]. Enriched housed pigs have been shown to spend more time playing before weaning and up to 7 weeks after weaning, and these behaviors are strongly related to less agonistic behavior [28,29]. Moreover, these results were associated with increased weight gain and adaptability to the new environment of weaning pigs, and exposure to enriched housing could impact later life behavior and welfare [32]. Therefore, it can be inferred from these results that positive behavioral changes in weaning pigs in an enriched environment are a better outcome in terms of the growth and welfare of weaning pigs.

The consequences of the weaning process, which is the phased formation of reciprocal dominance relationships through agonistic behavior, are well-known phenomena [33]. Most weaned pigs show this aggressive tendency by fighting or biting other pigs from different groups. This behavior manifests as an accumulation of skin lesions throughout the body, legs, ears, and tail [34,35]. The results of the present study showed that pigs raised under exposure to the enriched environment had reduced skin lesion scores compared to the control group, and there was a trend towards a decrease in the number of skin lesions as exposure time to the enriched environment increased. These results are linked to those of previous studies that observed that over 20% lowered oral activities related to skin lesions in pigs reared in enriched environments [36], and the response to enriched environments is correlated with the age of the pigs [37]. These facts led us to conclude that access to an enriched environment contributed to a reduced skin lesion score, which is consistent with the diminished reciprocal agonistic behavior observed in the present study.

When animals encounter stressful conditions, such as a shortage of environmental enrichment, they can activate the hypothalamic-pituitary-adrenal axis, which is associated with the secretion of glucocorticoid cortisol, an indicator of stress levels measured in blood, urine, saliva, and hair [38]. In the present study, the EE-4 group had lower hair cortisol concentrations during the weaning phase; however, the enriched environment did not affect salivary cortisol concentrations. These results are consistent with previous studies that have shown that barren environments adversely affect the welfare of weaned pigs and that it is connected to the increment of hair cortisol levels in pigs raised in a barren environment [20,39]. Cortisol concentration in hair is a response to chronic stress that is distinct from salivary cortisol levels, which are related to acute stress response in weaning pigs [40]. These responses indicate that they were subjected to sustained stress over weeks while growing in a non-enriched environment, similar to the present study. However, in contrast to the present study, previous studies have demonstrated increased salivary cortisol concentrations in pigs raised in barren environments [41,42]. In this context, the weaning process, including relocation or social mixing, is a stressor that can be characterized by elevated salivary cortisol levels. However, salivary cortisol levels recovered to normal ranges within 8 h, indicating that it is most likely an acute stress response [43,44]. There was a 1.47-fold increase in salivary cortisol concentration after weaning; however, this increase was reduced by 1.26-fold greater two days after weaning. This can be explained as a transient response that progressively decreases concentration [45]. Therefore, environmental enrichment conditions may be consistently more favorable for reducing stress on the growth and welfare of weaning pigs; however, further research is required to refine the appropriate assay that may influence the results.