Behavior and physiology of two different sow breeds in a farrowing environment during late 35-day lactation
Behavior and physiology of two different sow breeds in a farrowing environment during late 35-day lactation
Honggui Liu 1 2 3
Ran Yi 1 2 3
Chao Wang 1 2 3
Peng Zhao 1 2 3
Mingyue Zhang 1 2 3
Shiwen Xu 0 1 3
Jun Bao 1 2 3
0 College of Veterinary Medicine, Northeast Agricultural University , Harbin, P. R. , China
1 Funding: This study was supported by the Earmarked Fund for China Agriculture Research System (grant no. CARS-35) to JB, the Province Science Foundation of Hei Longjiang in China (project nos. C2016016 and 2017RAQXJ062) to HGL and National Nature Science Foundation of China (31472131) to JB
2 College of Animal Science and Technology, Northeast Agricultural University , Harbin, P. R., China , 2 Key Laboratory of Swine Facilities Engineering, Ministry of Agriculture , Harbin, Hei Longjiang Province , China
3 Editor: Cheryl S. Rosenfeld, University of Missouri Columbia , UNITED STATES
To improve the overall welfare levels of sows and to reduce stress levels at late 35-day lactation, we selected targeted behavioral indicators that might be associated with stress. Therefore, we monitored and evaluated the adaptive capability of two different breeds of sows to the farrowing environment. In this study, Damin sows (Large White × Min pig sows, n = 20) and Large White sows (n = 20) were farrowed in individual pens. Saliva was collected and tested for cortisol density at ±15 min, and then at +15, 30, 60, 90, 120, 180 and 240 min after an adrenocorticotropic hormone (ACTH) stimulation test conducted at 20, 27 and 34 d post-partum. The postures, including ventral and lateral recumbency to other postures, defecating, urinating, sham-chewing and bar-biting behavior, were observed by video from 07:00 to 09:00 and from 13:00 to 15:00 on the 7th day of each week from the 3rd to the 5th week post-parturition. In addition, the concentrations of salivary interleukin (IL)-6, tumor necrosis factor (TNF)-α and secretory immunoglobulin (SIgA) were assayed after the observed behaviors. The results showed no significant difference between Damin sows and Large White sows in terms of behaviors at the 3rd week. Additionally, there were no significant differences between Damin and Large White sows in terms of the behaviors of ventral recumbency and bar-biting with the exception of lateral recumbency to other postures, sham-chewing, defecation and urination in the fifth week. Meanwhlie, there was significant difference between two breeds in term of ventral recumbency at the 4th week. The result of the ACTH test showed a significant difference between the Damin and Large White sows by the 27th and 34th days postpartum (P<0.01). In addition, the serological concentrations of IL-6 and TNF-α were not significantly different between the two breeds at the 3rd week postpartum. However, these indicators were significantly different at the 5th week postpartum (P = 0.000, and P = 0.003, respectively). The SIgA concentrations in saliva were significantly different between breeds at the 3rd week postpartum (P<0.01). In conclusion, both breeds of sows maybe in a state of stress after the 4th week postpartum. However, the Damin sows may be better than the Large White sows in terms of adapting to this farrowing environment.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
At present, in response to the concern of animal welfare advocates, there has been a strong
interest in the loose farrowing environment of lactating sows [
]. However, in such an
environment, the sows might gradually increase the stress experienced by piglets and the
environment, especially during long lactation periods [
]. Therefore, selecting adaptable
breeds with the intention of reducing stress might further improve the welfare of lactating
sows in late lactation, and could be an effective means of reducing the harm caused by a
stressful environment. Therefore, we attempted to explore the behaviors of different breeds
of sows to improve their adaptability and to decrease stress experienced over the course of
35 days by late lactating sows. For example, the Min pig is a local breed found in
north-eastern China, and displays good maternal instincts. This is an outstanding characteristic of the
Min pig and the Min pig hybrid breeds, which show resistance to stress [4±6]. Thus, by
utilizing the above advantages, we selected primiparous Damin sows (Large White × Min pig
sows) in an attempt to improve the adaptability of pigs in a farrowing environment during
The behavior of a pig can reflect the interaction between its own biological requirements
and its response to environmental conditions. Therefore, we can use behaviors to judge the
adaptability of the animals to their environment. Some reports showed the behaviors of the
sows, such as sham-chewing [
], bar-biting [
], excessive excretion [9±11] and other behaviors,
might be related to a lack of adaptability to the environment [
]. To avoid the stress caused
by the sow not being able to avoid the piglets attempt to stimulate milk let down by massaging
the udder in late lactation, sows often show long standing and prone postures [
here we used behavioral indicators, including ventral recumbency[
], lateral recumbency to
] and bar-biting[
evaluate an enriched environment during lactational stress, and also determined the degrees of
adaptation and adjustment to the environment.
Changes in behaviors might be associated with changes in peripheral and central nervous
system physiological processes [
]. Therefore, we needed to monitor the endocrine
secretions of sows. However, if one uses methods to determine urinary or fecal corticoid levels,
these can be affected by social rank and experience during an environmental event (i.e., by
stress or its duration). Therefore, these measured end-points will clearly cannot accurately
reflect the state of chronic stress in any individual animal [2, 15±19]. In addition, due to the
presence of glucocorticoid secretion and changes in the circadian rhythm, the hypothalamic±
pituitary±adrenal axis can adapt to long-term stress durations. Thus, combining these
measurements with assays of adrenocorticotropic hormone (ACTH) and the results of cortisol
stimulation tests can be used to evaluate the chronic stress state of different breeds of sows
The response of the immune system to stress is an adaptive mechanism showing how
organisms have evolved to cope with challenging situations [
]. An insufficient adaptation
can lead to reduced immune competence and increased disease susceptibility [
exploring the adaptability of the sows of two different breeds in the later period of lactation, we
aimed to determine the concentration of secretory immunoglobulin (SIgA) in saliva [
and the levels of interleukin (IL)-6 and tumor necrosis factor (TNF)-α in serum . This was
necessary to expand our knowledge of the complex relationship between stressful events and
immune functioning during late lactation. Moreover, there is growing interest in assessing
psychosocial stress in farm animals to improve our understanding of their overall welfare and
2 / 13
Materials and methods
All procedures used in the present study were approved by the Institutional Animal Care and
Use Committee of Northeast Agricultural University (Approval No. IACECNEAU20121013).
Forty sows were selected (20 Damin, and 20 Large White) that were mated with Duroc
(Canadian) boars. Backfat values and weights of the two different breeds had no significant
difference when mating at the age of 7±8 months (backfat:18.99 ± 1.22 vs 19.06 ± 0.91; weights:
113.39 ± 6.10 vs 115.99 ± 5.01 kg, respectively). They were fed in the same pens (5.7 m wide,
and 4.5 m long, each containing 10 pregnant sows). The ground, of concrete, was covered with
straw. There were three water sources and natural ventilation supplied for sows during
pregnancy. Sows were randomly transferred to the parturition pen on the 7th day before the
expected due date.
Housing and management
The design of the parturition pens is shown in Fig 1. The inside was 480 cm long, and 160 cm
wide. The door of the parturition pen was 80 cm wide and 120 cm high. There was terrestrial
heat in the piglet activity and rest region. It had access to the parturition area and only meet
the piglet's access freely. Meanwhile, the parturition area was also the activity and rest region
for piglets. There was a low barrier in the door to prevent the piglets from leaving the rest areas
during the first three days after birth. The sows could active freely. The feeding trough for
piglets was 20 cm high and 60 cm wide. The ground inside the farrowing pens was of concrete,
covered with straw (3.50 ± 0.25 kg). All of the straw was provided weekly. The sows were fed
twice daily (at 07:30 and 16:00) in the farrowing pens. The health of the piglets was checked;
the number of piglets experiencing diarrhea and swelling were recorded, and any sick piglets
were removed at 06:30 each morning. Approximately 2 cm of bedding was added to the floor
of the farrowing pens at 07:30 each weekend. These sows were fed 3 kg/day pre-parturition
and were reduced by 0.5 kg/day 1 week before farrowing. On the first day after farrowing, the
sows were fed 0.5 kg. Then, the ration on following days was increased by 0.5 kg/day until the
sows could be fed ad libitum. After weaning, the rations of the primiparous sows were
decreased to 3 kg/day until mating. All the sows were fed with complete feed containing the
following constituents per kg: ME 12.9 MJ, crude protein 185.0 g, crude fat 50.0 g, crude ash
80.0 g, and lysine 12.0 g. During the study period, the temperature and relative humidity (both
interior and exterior) of the farrowing pens were measured daily with a hygrothermograph
(Kestrel 4000 Pocket Weather Tracker; Kestrel, Santa Cruz, CA, USA). The daily temperature
and relative humidity inside the farrowing pens were measured at 08:00 (16.5ÊC; 90.0%), 14:00
(30.5ÊC; 30.4%) and 20:00 (21.6ÊC; 58.7%), in August and at 08:00 (8.7ÊC; 85.5%), 14:00
(33.0ÊC; 20.3%) and 20:00 (14.7ÊC; 51.3%) in September.
Behavioral observations. The behaviors of the sows were recorded automatically by a
video surveillance system (DS-IT5, Hangzhou Hikvision Digital Technology Co., Ltd.,
Hangzhou, P. R. China) for data acquisition to prevent artificially delimited observation times from
impacting on the test results. From the 2nd to the 4th week and on the 3rd and 6th day each
week post-parturition, all behaviors were recorded on video with sampling and continuous
recording from 07:00 to 09:00, and 13:00 to 15:00. Data for continuous behaviors were
3 / 13
Fig 1. The design of the farrowing pens.
recorded in numbers and converted into aggregate data over the total observation time. The
parameters and their definitions are outlined in Table 1.
ACTH stimulation test. Synthetic ACTH (Ser±Tyr±Ser±Met±Glu±His±Phe±Arg±Trp±
Gly±Lys±Pro±Val±Gly±Lys±Lys±Arg±Arg±Pro±Val±Lys±Val±Tyr±Pro), was diluted with
0.9% sterile saline, and injected into a marginal ear vein (dose of 10 pg/kg;[
Some behavioral parameters and their definitions are from Hurnik et al., (1995) [
a These behaviors are presented as percentages of time.
b These behaviors are presented as the hourly number of occurrences.
4 / 13
]). Saliva was collected and tested for the levels of cortisol at ±15 min, and
at 15, 30, 60, 90, 120, 180 and 240 min after the ACTH stimulation test at 20, 27 and 34 days
Physiological measurements. Plasma concentrations of IL6 and TNF-α from 3rd to 5th
week after parturition were measured using a commercial porcine enzyme-linked
immunosorbent assay (ELISA) kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, P. R. China)
(Physiological measurements test[
]). Salivary concentrations of SIgA were assayed using a
commercial porcine ELISA kit (Nanjing Jiancheng Bioengineering Institute).
The study is a two-way crossed classification. All breed-dependent data was statistically
analyzed with SPSS18.0. Normality test and homogeneity test were performed first. Data which
were not normally distributed were log transformed using Transform (SPSS18.0). They were
examined for normal distribution, considering skewness, kurtosis, the Shapiro±Wilks test for
normality, and a normal probability plot. Statistical analysis method of LSD, SNK, Duncan
and Bonferroni in Post-Hoc Teats in a GLM procedure of the SPSS statistical software (v.
18.0,) was used to test the behavioral differences between the two breeds in time-dependent
observations, which found the following effects:
Yijk m Breedi Timej Breedi
where Yijk = value observed for characteristics analyzed; μ indicates the overall average; Breedi
indicates the effect of the breeds on behavior data; Timej indicates the effect of observation
weeks (W3, W4, W5) after parturition on behavior data; Breedi × Timej indicates the
interaction between the breeds and the observed time; eijk = random errors associated with
observation. All data are presented as the mean ± standard deviation.
There was no significant difference in ventral recumbency behavior of the two breeds of sows
at 3rd week postpartum (Table 2). However, at the 4th and 5th week, the rate of ventral
recumbency was significantly different between breeds (F0.05(1,38) = 4.781; P = 0.035 and F0.05(1,38)
= 6.551; P = 0.015, respectively). With extending the period of lactation, the two breeds of sows
showed increasing ventral recumbency times, and that in Large White sows were significantly
higher than that in Damin sows (F0.05(1,114) = 12,716; P = 0.001). There was no significant
difference between the two breeds of sows from 3rd to 5th postpartum in terms of the behavior of
lateral recumbency to other postures (F0.05(2,114) = 0.101; P = 0.101). With an extended period
of lactation, both breeds gradually increased their frequency of the behavior of lateral
recumbency to other postures, and that in Large White sows were significantly lower than that in
Damin sows (F0.05(1,114) = 5.801; P = 0.018). In addition, with extending the period of
lactation, the two breeds of sows showed increasing frequency of defecation, and that in Large
White sows were significantly higher than that in Damin sows (F0.05(1,114) = 6.085; P = 0.015),
and there were no significant differences in the frequency of urination or defecation between
the breeds (P>0.05). Further, there were no significant differences between breeds in terms of
sham-chewing (F0.05(1,114) = 1.086; P = 0.300). However, there was significant difference
between the two breeds of sows from 3rd to 5th postpartum in terms of sham-chewing
(F0.05(2,114) = 4.343; P = 0.015). With extending the period of lactation, the two breeds of
sows showed increasing frequency of bar-biting, and that in Large White sows were
5 / 13
Lateral recumbency to other postures
Note: Different superscript letters in a row indicate significant differences between observation weeks (a vs. b vs. c P<0.05).
Different superscript letters in a column indicate significant differences between breeds (x vs. y P<0.05).
Means and standard deviation are shown.
significantly higher than that in Damin sows (P<0.01), and there was also significant
difference between the two breeds of sows from 3rd to 5th postpartum in terms of bar-biting
(P<0.01). All the detail data of behavioral parameters are respectively shown in Table 2.
ACTH stimulation test
An ACTH stimulation test was conducted in both breeds of sows at the 20th, 27th and 34th
days postpartum. There were no significant changes in the concentration of cortisol on the
20th day after farrowing. However, at 27th and 34th days postpartum, before the level of
cortisol returned to a normal level, the salivary levels increased rapidly after the injection of ACTH.
Cortisol concentrations in saliva were significantly higher in Large White sows than in Damin
sows at each time point (P<0.05). In addition, there were similar results of testing at 34th day
postpartum. A tend of the changes in cortisol concentrations in saliva following the ACTH
stimulation test at the 34th day postpartum is shown in Fig 2.
The serum levels of IL-6 in both breeds of sows were not significantly different at the 3rd
week postpartum; however, the levels were significantly different at the 4th and 5th weeks
(F0.05(1,38) = 5.045; P = 0.031 and F0.05(1,38) = 543.253; P = 0.000, respectively). The levels of
TNFα in serum in the two breeds of sows were not significantly different at the 3rd and 4th week
postpartum. However, they were significantly different at week 5 (F0.05(1,38) = 10.055; P = 0.003). The
SIgA concentrations in saliva in the two breeds of sows were significantly different at the 3rd and
5th weeks postpartum(F0.05(1,38) = 40.411; P = 0.000). With extension of the testing time, the
TNF6 / 13
Fig 2. A tend of the changes in cortisol concentrations in saliva following the ACTH stimulation test at the 34th day postpartum. All data are
presented as the mean ± standard deviation.
α concentrations in serum decreased gradually in both breeds of sows. By contrast, the levels of
IL6 in serum in Damin sows tended to increase, while they increased first and then decreased in
Large White sows. In addition, the SIgA concentration in saliva in two breeds of sows tended to
decrease first, and then increase. The results are shown in Table 3.
The behaviors of ventral recumbency and lateral recumbency to other postures were two
important signals indicating that sows refused to allow piglets to suckle [
]. In this study,
Note: Different superscripts in a column indicate significant differences between observation weeks (x vs. y P<0.05).
Different superscripts in a row indicate significant differences between breeds. (a vs. b vs. c P<0.05).
Means and standard deviations are shown.
7 / 13
from the trend of ventral recumbency at 3±5 weeks postpartum, both breeds of sows gradually
prevented piglets from stimulating the udder. Thus, an enriched environment for
farrowing might not necessarily eliminate this effect, because of the influence of both breeds of sows
caused by extension of the time for breastfeeding piglets. However, the incidence of ventral
recumbency was significantly lower in Damin sows than in Large White sows, instead, more
behavior of lateral recumbency to other postures were shown in Damin sows. It may show that
they may indicate more willingness to nurse, indicating that the former had certain genetic
and biological advantages in response to late lactational stress as shown by the Min pig,
including good motherhood[
Some authors believe that excessive excretion is linked with the animal's negative emotions
and stress . Yet, in this experiment, there was no such excessive urination in the two breeds
of sow and the result might be related to the enriched environment for the farrowing of piglets,
given that both breeds of sows received reduced stress. However, such behaviors might be
induced by the stress of serious environmental restraint; for example, sows in a limited space
will exhibit excessive urination behavior [
]. In this study, we found the behavior of
defecation was influenced by breeds all the time. We speculated that the result may be related to the
feed intakes and excretion law of different breeds in the late lactation, and that was no
correlation with stress conditions. It was required to do further specific research to determine the
value of defecation behavior for evaluating the adaptation of sows in the late lactation.
From the perspective of adaptability, when the animals were in a poor environment, they
would try to counteract adverse effects in various ways such as behavioral and physiological
]. Some scholars believed that sham-chewing was one of the most common
stereotypic behaviors of sows reared in the crate environment [
]. The occurrence of sham-chewing
was caused by restricted feeding, and eating motivation caused by starvation increases to the
shift of behavioral direction [
]. In this study, the main reason why there was no difference of
sham-chewing between two breeds may be the loose farrowing environment and sufficient
feeding in lactation condition could not lead to sham-chewing. The mentioned point above of
view was in conformity with the actual result. The behaviors of and bar-biting at the 5th week
postpartum were more prevalent in Large White sows than in Damin sows. This showed that
the former breed may exhibit a more obvious maladjustment in response to late lactation
stress. This was similar to the conclusions made by others [
]. At the same time, we also
believe that there is important value in studying abnormal behaviors such as and bar-biting in
measuring the adaptability of lactating sows to a late lactating environment.
The adrenal gland response to a challenge with ACTH is a measure of chronic physiological
]. Adaptation of HPA axis to chronic stress involves increased adrenocortical
response to ACTH, which increases the level of cortisol during acute stress stimulation. In this
study, the level of salivary cortisol before ACTH stimulation test was used as the control to
compare the changes of the level of salivary cortisol at different time points after ACTH
stimulation test. ACTH stimulation test on the 20th day postpartum showed that there were no
significant changes in the level of salivary cortisol, which might be due to the high stress of sows
from the factors of both the environment and piglets. The results of ACTH stimulation test on
day27 showed that the sows showed a response of stress at this time. And the stress response of
ACTH stimulation test still showed on day34. The results showed that chronic stress was still
evident in both breeds of sows, despite them living in enriched environmental farrowing pens
at the 5th week postpartum. Compared with day20, the ability of resisting the stress of sows
obviously decreased on day27 and day34, and they were at the level of low stress. We speculate
8 / 13
that the sows were in the chronic stress. Cronin et al. (1991) [
]and Jarvis et al. (2006) [
suggest that during longer lactation, when sows begin to show signs of chronic stress, it may
be harmful to sows. This was the farm manager's set time for weaning of piglets and provided
a theoretical basis for enhancing the welfare levels of the sows. In addition, ACTH stimulation
test results showed that salivary cortisol concentrations were higher in Large White sows than
in Damin sows, and the main reason for this difference might be breed-related.
It is a natural tendency to spend time away from their piglets as lactation progresses and
gradually reduce suckling frequency, effectively creating a gradual weaning process [
When the frequency of lactation cannot be reduced, the external environment and piglets are
likely to produce stress on sows, which is not conducive to the welfare of sows. Some
researchers speculate that sows may adapt to the chronic effects produced by environment and piglets
during lactation, and the response of the stress system may be reduced to a level
indistinguishable from that of non-stressed individuals [
]. The Damin and Large White sows showed
significant differences in the levels of IL-6 in serum at the 4th and 5th weeks postpartum, and
Damin sows showed higher levels than Large White sows at the 5th week postpartum. We
believe a major reason for this difference might arise from the pro- and anti-inflammatory
properties of IL-6 [
]. In addition, the insensitivity of plasma IL-6 levels to stress was reduced,
and this might be associated with the anti-inflammatory action of this cytokine. At the 5th
week, Damin sows adapted better to the late lactation environment by increasing a
compensatory and mediating immunoregulation with beneficial cytokine secretion [
the adaptability to the stress of late lactation of Large White sows decreased in the 5th week,
and decreases in the levels of IL-6 were observed. The reluctance for lactation that was shown
at the 5th week of the stress environment and experienced by Large White sows might pose a
threat to their health. Thus, in the current study, the changed levels of IL-6 showed that the
adaptability of Damin sows during late lactation was stronger than that of Large White sows.
Also, with prolonged lactation, levels of IL-6 in serum in the Damin sows increased
significantly. Moreover, the levels of IL-6 in serum in Large White sows increased first, and then
decreased. Our observation showed that the levels of IL-6 in serum decreased or remained
unchanged, but that finding is inconsistent with other studies [
]. The reasons might have
been related to the different breeds of sows employed in the studies. In addition, changes in
cell distribution might reflect psychological effects of the stressor, which would be
characterized by an uncontrolled and unpredictable response to environmental conditions with a
display of anxiety [44±46].
Experiments conducted with Damin sows during lactation at the 5th week showed that
TNF-α concentrations in serum were higher than those found in Large White sows. We
believe that the main reasons for the observed differences in behavior might be due to the
action of this cytokine. This anti-inflammatory factor played a key role in the response of
Damin sows to the late lactation environment and a marked participation in Large White
sows. However, with an extended duration of lactation, the serum TNF-α levels decreased
gradually in both breeds of sows under stress conditions, similar to previous reports [43, 47±
49]. A possible explanation for the stress-induced modulation of TNF-α production might be
due to an adaptive response that can initiate enhanced immune surveillance capable of
preparing the animal for potential mediators of danger [
]. Thus, our findings emphasize the
particular importance of TNF-α in mediating the adaptive response to short-term psychosocial
stress in sows.
We found that the levels of SIgA in saliva increased with the duration of lactation, and this
was discordant with previously published work [
]. We believe that the levels of SIgA in saliva
may represent a transient index of the emotional state at the time that the test pigs were
9 / 13
Min pig hybrids in late lactation remained susceptible to chronic stress. However, in response
to chronic stress behavior and immune responses, the Large White sows adapted better to the
environment of late lactation, and clearly this adaptive capacity differed between the two
breeds of sows. At the same time, the results of actual production might improve the welfare of
sows and determine the weaning age of piglets. There might be benefits from additional
research and field studies in this field.
S1 Dataset. The Data of behavior and physiological indexes.
S2 Dataset. The data of ACTH test.
The authors would like to thank Jian Han for technical assistance, Zhipeng Wang for help in
statistical analyses and all the staff at the Swine Complex for care of the animals. We thank
James Cummins, PhD, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for
editing the English text of a draft of this manuscript. This study was supported by the
Earmarked Fund for China Agriculture Research System (grant no. CARS-35), the Province
Science Foundation of Hei Longjiang in China (project nos. C2016016 and 2017RAQXJ062) and
National Nature Science Foundation of China (31472131).
Conceptualization: Honggui Liu, Jun Bao.
Data curation: Ran Yi, Chao Wang, Peng Zhao, Mingyue Zhang.
Formal analysis: Ran Yi, Chao Wang, Peng Zhao, Mingyue Zhang.
Funding acquisition: Honggui Liu, Jun Bao.
Investigation: Ran Yi, Chao Wang, Peng Zhao, Mingyue Zhang.
Methodology: Ran Yi, Chao Wang, Mingyue Zhang.
Project administration: Honggui Liu.
Resources: Honggui Liu.
Supervision: Honggui Liu.
Writing ± original draft: Honggui Liu, Ran Yi, Chao Wang.
Writing ± review & editing: Honggui Liu, Ran Yi, Chao Wang, Shiwen Xu, Jun Bao.
10 / 13
Weerd HAVD, Day JEL. A review of environmental enrichment for pigs housed in intensive housing
systems. Applied Animal Behaviour Science. 2009; 116(1):1±20.
11 / 13
31. Levi L. THE URINARY OUTPUT OF ADRENALIN AND NORADRENALIN DURING PLEASANT AND
UNPLEASANT EMOTIONAL STATES. A PRELIMINARY REPORT. Psychosomatic Medicine. 1965;
12 / 13
1. Damm BI , Forkman B , Pedersen LJ . Lying down and rolling behaviour in sows in relation to piglet crushing . Applied Animal Behaviour Science . 2005 ; 90 ( 1 ):3± 20 .
2. Jarvis S , D'Eath RB , Robson SK , Lawrence AB . The effect of confinement during lactation on the hypothalamic-pituitary-adrenal axis and behaviour of primiparous sows . Physiology & Behavior . 2006 ; 87 ( 2 ): 345 .
4. Cui S , Chen D , Li J , Li X , Yin G , Bao J. comparison of postural changes and maternal responsiveness during early lactation in Landrace and Minpig sows . Applied Animal Behaviour Science . 2011 ; 131 ( 1 ): 40 ± 7 .
5. Liu HG , Wang C , Lv J , Yu YQ , Zhang JL , Bao J. Behavior and performance in primiparous sows of two Min pig hybrid breeds in outdoor housing systems . Applied Animal Behaviour Science . 2013 ; 146 ( 1 ± 4): 37 ± 44 .
Wang X , Zhang B . Comparison of reproduction performance in Minpig sows and Minpig hybrid sows Heilongjiang . J Anim Sci Vet Sci . 2002 ; 1 : 12 ± 4 .
7. Mason GJ . Forms of stereotypic behaviour, Stereotypic animal behaviour: fundamentals and applications to welfare . 1993 .
8. Lawrence AB , Terlouw EM . A review of behavioral factors involved in the development and continued performance of stereotypic behaviors in pigs . Journal of Animal Science . 1993 ; 71 ( 10 ): 2815 . PMID: 8226385
9. Fraser D. The vocalizations and other behaviour of growing pigs in an "open field" test . Applied Animal Ethology. 1974 ; 1 ( 1 ):3± 16 .
10. Mendl M , Paul E. Consciousness, emotion and animal welfare: insights from cognitive science . Animal Welfare . 2004 ; 13 ( 1 ): 17 ± 25 ( 9 ).
11. Wemelsfelder F. Experience in Substrate-Enriched and Substrate-Impoverished Environments Affects Behaviour of Pigs in a T-Maze Task . Behaviour . 1997 ; 134 ( 9 /10): 643 ± 59 .
12. Hurnik JF , Webster AB , Siegel PB . Dictionary of farm animal behavior . 1995 .
13. Axelrod J , Reisine TD . Stress hormones: their interaction and regulation . Science . 1984 ; 224 ( 4648 ): 452 ± 9 . PMID: 6143403
14. Johnson EO , Kamilaris TC , Chrousos GP , Gold PW . Mechanisms of stress: A dynamic overview of hormonal and behavioral homeostasis . Neuroscience & Biobehavioral Reviews . 1992 ; 16 ( 2 ): 115 .
15. Aguilera G . Regulation of pituitary ACTH secretion during chronic stress . Frontiers in Neuroendocrinology . 1994 ; 15 ( 4 ): 321 . https://doi.org/10.1006/frne. 1994 .1013 PMID: 7895891
16. Boonstra R . Equipped for life: The adaptive role of the stress axis in male mammals . Journal of Mammalogy . 2005 ; 86 ( 2 ): 236 ± 47 .
17. Harbuz MS , Lightman SL . Stress and the hypothalamo-pituitary-adrenal axis: acute, chronic and immunological activation . Journal of Endocrinology . 1992 ; 134 ( 3 ): 327 ± 39 . PMID: 1402543
18. Pignatelli D , Maia M , Castro AR , Da CMM , Vivier J , Defaye G . Chronic stress effects on the rat adrenal cortex . Endocrine Research . 2000 ; 26 ( 4 ): 537 ± 44 . PMID: 11196426
19. Schrader L , Ladewig J . Temporal differences in the responses of the pituitary adrenocortical axis, the sympathoadrenomedullar axis, heart rate, and behaviour to a daily repeated stressor in domestic pigs . Physiology & Behavior . 1999 ; 66 ( 5 ): 775 ± 83 .
20. Janssens CJ , Helmond FA , Wiegant VM . Chronic stress and pituitary-adrenocortical responses to corticotropin-releasing hormone and vasopressin in female pigs . European Journal of Endocrinology . 1995 ; 132 ( 4 ): 479 ± 86 . PMID: 7711887
21. Tuchscherer M , Kanitz E , Puppe B , Tuchscherer A , Viergutz T. Changes in endocrine and immune responses of neonatal pigs exposed to a psychosocial stressor . Research in Veterinary Science . 2009 ; 87 ( 3 ): 380 ±8. https://doi.org/10.1016/j.rvsc. 2009 . 04 .010 PMID: 19433330
22. Watanuki S , Kim YK . Physiological responses induced by pleasant stimuli . Journal of Physiological Anthropology & Applied Human Science . 2005 ; 24 ( 1 ): 135 ± 8 .
23. Dillon KM , Minchoff B , Baker KH . Positive emotional states and enhancement of the immune system . International Journal of Psychiatry in Medicine . 1986 ; 15 ( 1 ): 13 ± 8 .
24. Cantorna MT , Humpalwinter J , Deluca HF . In vivo upregulation of interleukin-4 is one mechanism underlying the immunoregulatory effects of 1,25-dihydroxyvitamin D(3 ). Archives of Biochemistry & Biophysics . 2000 ; 377 ( 1 ): 135 .
25. Reefmann N , Kaszàs FB , Wechsler B , Gygax L , WuÈrbel H . Ear and tail postures as indicators of emotional valence in sheep . Applied Animal Behaviour Science . 2009 ; 118 ( 4 ): 199 ± 207 .
26. Cook NJ , Schaefer AL , Lepage P , Morgan JS . Salivary vs. serum cortisol for the assessment of adrenal activity in swine . Canadian Journal of Animal Science . 1996 ; 76 ( 3 ): 329 ± 35 .
27. Franczak A , Zmijewska A , Kurowicka B , Wojciechowicz B , Petroff BK , Kotwica G. The effect of tumor necrosis factor α (TNFα), interleukin 1β (IL1β) and interleukin 6 (IL6) on endometrial PGF2α synthesis, metabolism and release in early-pregnant pigs . Theriogenology . 2012 ; 77 ( 1 ): 155 . https://doi.org/10. 1016/j.theriogenology. 2011 . 07 .029 PMID: 21924479
28. Gonyou HW , Beltranena E , Whittington DL , Patience JF . The behaviour of pigs weaned at 12 and 21 days of age from weaning to market . Canadian Journal of Animal Science . 1998 ; 78 ( 4 ): 517 ± 23 .
29. Valros A , Rundgren M , SÏpinka M , Saloniemi H , Rydhmer L , HulteÂn F , et al. Metabolic state of the sow, nursing behaviour and milk production . Livestock Production Science . 2003 ; 79 ( 2 ±3): 155 ± 67 .
30. Douglas C , Bateson M , Walsh C , BeÂdueÂ A , Edwards SA . Environmental enrichment induces optimistic cognitive biases in pigs . Applied Animal Behaviour Science . 2012 ; 139 ( 1 ±2): 65 ± 73 .
32. Chapinal N , Torre JLRDL , Cerisuelo A , Gasa J , Baucells MD , Coma J , et al. Evaluation of welfare and productivity in pregnant sows kept in stalls or in 2 different group housing systems . Journal of Veterinary Behavior Clinical Applications & Research . 2010 ; 5 ( 2 ): 82 ± 93 . https://doi.org/10.1371/journal.pone. 0125911
33. Broom DM . Indicators of poor welfare . British Veterinary Journal . 1986 ; 142 ( 6 ): 524 ±6. https://doi.org/ 10.1016/ 0007 - 1935 ( 86 ) 90109 - 0 PMID: 3594185
34. Arellano PE , Pijoan C , Jacobson LD , Algers B . Stereotyped behaviour, social interactions and suckling pattern of pigs housed in groups or in single crates . Applied Animal Behaviour Science . 1992 ; 35 ( 2 ): 157 ± 66 .
35. Spoolder HAM , Burbidge JA , Edwards SA , Simmins PH , Lawrence AB . Effects of food level and straw bedding during pregnancy on sow performance and responses to an ACTH challenge . Livestock Production Science . 1997 ; 47 ( 1 ): 51 ± 7 .
36. Cronin GM , Barnett JL , Hodge FM , Smith JA , Mccallum TH . The welfare of pigs in two farrowing/lactation environments: cortisol responses of sows . Applied Animal Behaviour Science . 1991 ; 32 ( 2 ±3): 117 ± 27 .
37. Jarvis S , D'Eath RB , Robson SK , Lawrence AB . The effect of confinement during lactation on the hypothalamic±pituitary±adrenal axis and behaviour of primiparous sows . Physiology & Behavior . 2006 ; 87 ( 2 ): 345 ± 52 .
38. Pajor EA , Weary DM , Fraser D , Kramer DL . Alternative housing for sows and litters: 1. Effects of sowcontrolled housing on responses to weaning . Applied Animal Behaviour Science . 1999 ; 65 ( 2 ): 105 ± 21 .
39. Borell EHV . The biology of stress and its application to livestock housing and transportation assessment . 2001 .
40. Zaldivar F , Wangrodriguez J , Nemet D , Schwindt C , Galassetti P , Mills PJ , et al. Constitutive pro- and anti-inflammatory cytokine and growth factor response to exercise in leukocytes . Journal of applied physiology (Bethesda , Md: 1985 ). 2006 ; 100 ( 4 ): 1124 ± 33 .
41. Chrousos GP . Stress, chronic inflammation, and emotional and physical well-being: Concurrent effects and chronic sequelae . Journal of Allergy & Clinical Immunology . 2000 ; 106 ( 5 ): 275 ± 91 .
42. Jr MG , Agarwal SK . Stress, immune regulation, and immunity: applications for asthma . Allergy & Asthma Proceedings . 2000 ; 21 ( 4 ): 241 .
43. DeRijk R , Michelson D , Karp B , Petrides J , Galliven E , Deuster P , et al. Exercise and circadian rhythminduced variations in plasma cortisol differentially regulate interleukin-1β (IL-1β), IL-6, and tumor necrosis factor-α (TNFα) production in humans: high sensitivity of TNFα and resistance of IL-6 . The Journal of Clinical Endocrinology & Metabolism . 1997 ; 82 ( 7 ): 2182 ± 91 .
44. Brosschot JF , Godaert GL , Benschop RJ , Olff M , Ballieux RE , Heijnen CJ . Experimental stress and immunological reactivity: a closer look at perceived uncontrollability . Psychosomatic Medicine . 1998 ; 60 ( 3 ): 359 ± 61 . PMID: 9625225
45. Mormede P , Dantzer R , Michaud B , Kelley KW , Le MM . Influence of stressor predictability and behavioral control on lymphocyte reactivity, antibody responses and neuroendocrine activation in rats . Physiology & Behavior . 1988 ; 43 ( 5 ): 577 .
46. Peters ML , Godaert GL , Ballieux RE , Brosschot JF , Sweep FC , Swinkels LM , et al. Immune responses to experimental stress: effects of mental effort and uncontrollability . Psychosomatic Medicine . 1999 ; 61 ( 4 ): 513 ± 24 . PMID: 10443760
47. Besedovsky HO , Del RA. The cytokine-HPA axis feed-back circuit . Zeitschrift FuÈr Rheumatologie . 2000 ; 59 ( 2 ):II26± II30 .
48. Chandrashekara S , Jayashree K , Veeranna HB , Vadiraj HS , Ramesh MN , Shobha A , et al. Effects of anxiety on TNF-alpha levels during psychological stress . Journal of Psychosomatic Research . 2007 ; 63 ( 1 ): 65 ±9. https://doi.org/10.1016/j.jpsychores. 2007 . 03 .001 PMID: 17586339
49. Sapolsky RM , Romero LM , Munck AU . How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions . Endocrine Reviews . 2000 ; 21 ( 1 ): 55 ± 89 . https://doi.org/10.1210/edrv.21.1.0389 PMID: 10696570
50. Dhabhar FS . Stress-induced augmentation of immune functionÐthe role of stress hormones, leukocyte trafficking, and cytokines . Brain Behavior & Immunity . 2002 ; 16 ( 6 ): 785 ± 98 .
51. Maes M , Van Bockstaele DR , Gastel A , Song C , Schotte C , Neels H , et al. The effects of psychological stress on leukocyte subset distribution in humans: evidence of immune activation . Neuropsychobiology . 1999 ; 39 ( 1 ):1. https://doi.org/10.1159/000026552 PMID: 9892853