Allowing sows to farrow unconfined has positive implications for sow and piglet welfare

Applied Animal Behaviour Science 221 (2019) 104872

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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim

Allowing sows to farrow unconfined has positive implications for sow and piglet welfare

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Tanya Louise Nowlanda, , William Hendrik Ernest John van Wettereb, Kate Joanna Plushc a

South Australian Research and Development Institute, Animal Welfare Science Centre, JS Davies Building, University of Adelaide, Roseworthy, SA, 5400, Australia School of Animal and Veterinary Sciences, The University of Adelaide, Animal Welfare Science Centre, Roseworthy, SA, 5400, Australia c SunPork Group, Shea-oak Log SA, 5371, Australia b

A R T I C LE I N FO

A B S T R A C T

Keywords: Behaviour Confinement Piglet mortality Sow Farrowing

To reduce piglet mortality from overlay, farrowing crates confine the sow, restricting nest building activities. The aim of this study was to investigate the impact of confinement in the lead up to and during parturition on sow and litter characteristics. Sows (parity 1.6 ± 0.1) were housed in pens the size of a traditional crate with bars that allowed for temporary confinement. Two treatments were applied; OPEN (n = 36): pen was open until the sow stood following parturition, at which point they were closed, and CLOSED (n = 34): pen was closed through parturition. At d 10 of lactation the pens were opened for both treatments. A subset of sows (n = 12 CLOSED, n = 14 OPEN) were observed remotely during parturition and 18 h after parturition for behavioural analyses. Blood samples were collected hourly from −24 h until farrowing completion, and again at 24 h post farrowing. Piglet weights were collected at birth, 24 h and at weaning. OPEN sows displayed a reduced incidence of pain-related behaviours including tail flicks (8.4 ± 0.7 vs 27.6 ± 1.5; P < 0.001), movement of back leg forward (122.0 ± 3.0 vs 163.4 ± 3.7; P < 0.001) and strains (146.1 ± 3.2 vs 182.9 ± 3.9; P < 0.001) during farrowing. OPEN sows also nosed crate fixtures less frequently (4.1 ± 0.4 vs CLOSED 7.3 ± 0.8; P < 0.001) and performed more posture changes (23.2 ± 1.3 vs CLOSED 14.3 ± 1.1; P < 0.001) during farrowing. Confinement of sows did not impact plasma cortisol concentration at any point (P > 0.05). Sows from OPEN pens gave birth to fewer stillborn piglets than CLOSED (0.2 ± 0.1 vs 0.4 ± 0.1 piglets/litter respectively; P < 0.05). Colostrum ingestion was higher in piglets from OPEN sows (332.8 ± 7.8 g) than CLOSED (310.8 ± 7.0 g; P < 0.01). Individual weight at weaning was increased in piglets from OPEN sows (5.9 ± 0.2 kg) when compared with CLOSED (5.7 ± 0.2 kg; P < 0.01). Postnatal mortality did not differ between treatments (P < 0.05). Allowing the sow a greater freedom of movement exclusively in the lead up to and during parturition changes sow behaviour during this time and improves piglet growth whilst maintaining survival rates.

1. Introduction In the hours leading up to parturition sows are highly motivated to perform nest-building activities. This process involves physical isolation, sourcing suitable material, nest construction and the farrowing process itself (Van Beirendonck et al., 2014; Yun and Valros, 2015). This behavioural repertoire is primarily driven by endocrine changes within the sow that prepare her for parturition (Jarvis et al., 2006). As a result of the increased piglet mortality from sow crushing commonly seen within open farrowing systems (approx. 6–18% higher than closed crates) (Burri et al., 2009; Rootwelt et al., 2014; Condous et al., 2016), farrowing crates were developed in an effort to reduce piglet mortality. They act by confining the sow from before farrowing through lactation

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to weaning. Confinement within a farrowing crate prevents the adequate performance of almost all of these intrinsic sow pre-farrowing behaviours, and as a result is thought to cause frustration and stress (hypothalamicpituitary-adrenal (HPA) axis activation) (Jarvis et al., 2006; Bulens et al., 2014). Particularly, research suggests that confined sows exhibit an increased level of cortisol prior to farrowing (Lawrence et al., 1994) which, through effects on opioid secretion (Lawrence et al., 1997), cause a decrease in post-expulsion oxytocin pulse (Oliviero et al., 2008, 2010) resulting in an extended farrowing duration and inter-piglet birth intervals. Subsequently stillbirth rates are increased (Oliviero et al., 2008). While the farrowing process itself is affected by the restriction of nestbuilding prior to parturition, a large body of indirect evidence

Corresponding author. E-mail address: [email protected] (T.L. Nowland).

https://doi.org/10.1016/j.applanim.2019.104872 Received 12 December 2018; Received in revised form 6 September 2019; Accepted 9 September 2019 Available online 12 September 2019 0168-1591/ © 2019 Elsevier B.V. All rights reserved.

Applied Animal Behaviour Science 221 (2019) 104872

T.L. Nowland, et al.

(n = 34) entered in to closed crates where they remained until day 10 of lactation, at which point they were opened.

suggests that this physiological stress may also have a direct influence on sow behaviour at farrowing such as risky posture changes resulting from changes in pain sensitivity (Ison et al., 2016) and colostrum production and quality (Chen et al., 1998; Dewey, 2001; Yun et al., 2014b; Yun and Valros, 2015). All of which are important drivers of piglet survival in the peri-natal period. So, in addition to compromised sow welfare, there is evidence to suggest that confinement prior to and during farrowing my impair piglet vitality and early survival. In an effort to reduce sow confinement a number of studies have investigated the use of alternative farrowing systems that offer temporary confinement of the sow (Chidgey et al., 2015; Hales et al., 2015; Chidgey et al., 2016; Condous et al., 2016). With the majority of preweaning death occurring within the first week of a piglet’s life, many studies have now demonstrated that if the sow is kept confined for the first five days there will be no negative effect on piglet pre-weaning mortality (Moustsen et al., 2013; Hales et al., 2015; Singh et al., 2017). Although this type of system is suitable for ensuring minimal sow confinement and reducing piglet mortality, it is still not ideal as it involves the confinement of the sow in the lead up to and during farrowing. Therefore, the aim of this study was to determine the impact of confinement in the lead up to and during parturition on sow behaviour, colostrum production and quality, physiological indicators of stress and piglet growth and survival. We hypothesized that allowing the sow greater freedom of movement exclusively during the period leading up to and during parturition would reduce distress in the sow, improve the farrowing process, facilitate adequate maternal behaviours consequently improving piglet vigour, survival and growth.

2.3. Sow measures The day following entry to the farrowing house, each sow had an indwelling ear vein catheter placed to facilitate hourly blood sampling. Each sow was given topical anaesthesia (Xylocaine Jelly 2% Gel, Astrazeneca Pty Ltd, NSW) on both ears at least 20 min prior to ear vein catheter insertion attempt. The sow was restrained by a nose snare and a catheter placement unit (Jelco OPTIVA® I.V. Catheter, Smiths Medical, United States) was used to guide a vinyl tube (Microtube Extrusions Pty Ltd, NSW) in to the ear and held in place using veterinary adhesive (Tensoplast® Vet, BSN Medical Pty Ltd, Mount Waverley, VIC). Patency was maintained by daily flushing with heparinised saline until sample collection. On the day prior to the expected farrowing date, blood samples were collected hourly via syringe and immediately transferred into a 5 ml heparin-lithium coated collection tube. The sampling was continued from −24 h until the birth of the last piglet. One final sample was collected 24 h after the completion of farrowing. Blood samples were maintained on ice and were centrifuged at 1000g for 10 min and plasma stored at −20 °C. Cortisol samples were analysed in duplicate with a commercial radioimmunoassay kit (ImmuChemTM CT cortisol kit, MP Biomedicals, Orangeburg, NY, USA) according to manufacturer’s instructions by The University of Adelaide’s Research Assay Facility. The average inter-assay coefficient of variation (CV) was 9.2% and intra-assay CV was 8.2%. Farrowing duration (birth of the first piglet until birth of the last piglet) and piglet birth intervals were recorded for all sows. A 20 mL colostrum sample was collected from the anterior teats during parturition for a subset of sows (n = 21 CLOSED and n = 20 OPEN) and frozen immediately at -20 °C. The weight gain calculated from individual piglet weights at birth and 24 h was then used to calculate colostrum acquisition of the piglet (Devillers et al., 2007) and summed to give a total colostrum output of the sow. Total colostrum protein percentage was estimated by Brix optical refractometry (STARR DBR-1; STARR Instruments, Dandenong South, Victoria, Australia), and a radial immunodiffusion assay was performed for immunoglobulin G (IgG) concentration of the thawed colostrum sample, using a method modified from Bernard (1974).

2. Methods This experiment was conducted in accordance with the Australian Code of Practice for the Care and use of Animals for Scientific Purposes (NHMRC, 2013) and was approved by the University of Adelaide’s Animal Ethics Committee (AEC # S-2014-198). 2.1. Animals and management A total of 70 Large White x Landrace sows (parities 1–3; 1.6 ± 0.1) and their litters from The University of Adelaide’s research piggery, South Australia, were included in this experiment, which consisted of seven replicates conducted between October 2015 and May 2016. Sows were group housed during gestation from mating to farrowing shed entry and had no previous experience with reduced confinement systems during farrowing and lactation prior to the experiment. Sows were moved into the farrowing accommodation at d 110 of gestation. Once in the farrowing accommodation, sows were fed a commercial lactation diet (14.2 MJ DE/kg) twice daily and had ad libitum access to water. Prior to farrowing, sows were fed 2.5 kg/d after farrowing the feeding level was gradually increased to a maximum of 7–8 kg by day seven of lactation. No nesting materials were supplied. Sows farrowed naturally and were monitored 24 h a day until farrowing completion. Litters were fostered within treatment to teat capacity approximately 24 h after birth. Daily routine management practices were performed by piggery staff and this included an iron injection and oral coccidiostat given to the piglets at d 1 of age. Piglets were weaned on d 21.

2.4. Piglet measures Individual piglets were identified at birth by unique ear tag and the following measures were recorded; time of birth, vitality and meconium staining at birth (Table 1), rectal temperature at birth and d 1, weight at birth and d 1 and blood glucose concentration on d 1 (Accu-Chek® Performa Meter Kit, Roche Diagnostics, GmbH, Germany). All measures collected on d 1 were performed exactly 24 h following birth. In addition, piglets were weighed at weaning (d 21) and all pre-weaning mortality was recorded. The cause of mortality was noted using the following definitions. If a piglet was born dead, with that death occurring either immediately prior to or during farrowing it was recorded as a stillborn piglet. Any live born piglet deaths that occurred within the first 24 h were classified as pre-foster mortality and any that occurred after 24 h and prior to weaning were classified as post-foster mortality.

2.2. Experimental design and housing 2.5. Behavioural observations The farrowing pens were located within two identical farrowing rooms that housed six pens in each. The rooms were climate controlled, with fully slatted plastic flooring. Two treatment groups were applied using a ‘360 farrower crate’ (Midlands Pig Producers Ltd, UK) in either an OPEN or CLOSED position. Sows allocated to OPEN pens (n = 36) were open at farrowing house entry until the sow stood for the firsttime following placenta expulsion, at which point they were closed and re-opened on day 10 of lactation. Sows allocated to CLOSED crates

Sow behaviour was monitored using closed-circuit television (CCTV) cameras (3-megapixel fixed lens IP dome cameras, Hikvision HDTVI Cameras, China) which were mounted directly above each farrowing crate and were connected to a 16 channel NVR system, with infrared capabilities to allow for visual recording at night. Footage from each sow from the birth of the first piglet to birth of the last piglet (farrowing) and from birth of last piglet to 18 h (post-farrow) was 2

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Table 1 Vitality and meconium staining scoring method (Baxter et al., 2008; Orozco-Gregorio et al., 2010). Piglet variables

Vitality First inhalation of breath Constant movement Meconium Staining

Grading Scale 0

1

2

3

Stillborn

In > 11 s In > 21 s Small amounts (usually only around the nose/ face area)

Within 6–10 s Within 11–20 s Meconium covering up to half the body

In < 5 s In < 10 s. All body surfaces covered in meconium

No staining present

Table 2 Ethogram of behaviours observed during farrowing and 18 h after the birth of the last piglet. Behaviours were recorded as duration in seconds (state) or frequencies (event). Behaviour

Definition

State

Event

Posture Sitting Standing Lying Posture change

Front legs straight and back end on the floor Upright, with all feet on the floor Lying laterally or ventrally Sow changes position in a way that is risky to piglets

✓ ✓ ✓ ✓

Nesting/stereotypies Nosing crate fixture Bar biting Champing

Back and forth movements with nose or face on ground, bars, drinker and feeder but not drinking or feeding Biting bars with mouth Animal opens and closes mouth in air, often has foamy mouth

✓ ✓ ✓

Social Negative piglet interaction Positive piglet interaction Reaction to overlay

Sow lunges for or tries to snap at or intentionally bite piglet/s or lays on piglet/s. Results in piglet death or fatal injury. Sow noses piglet or nuzzles and/or eats piglet’s umbilical cord or the piglet approaches sows face and nuzzles or nudges it. Reacts quickly, slowly or does not react

✓ ✓ ✓

Pain related behaviour Tail flick Back leg forward Straining

Tail moved rapidly up and down In lateral lying position, the back leg is pulled forward and/or in towards the body Laying on either side, all four legs lifting and pushing away or straining by muscle clenching

✓ ✓ ✓

Nursing events Active time

When greater then 50% of the litter are actively seeking a teat or massaging the udder

✓

farrowed in a CLOSED crate nosed crate fixtures more during farrowing than those housed in an OPEN pen (CLOSED: 7.3 ± 0.8, OPEN: 4.1 ± 0.4, X21 = 12.406, P < 0.001). Sows housed within an OPEN pen in the lead up to and during farrowing performed less tail flicking (X21 = 126.890, P < 0.001; Fig. 3), back leg forward (X21 = 74.357, P < 0.001; Fig. 3) and straining (X21 = 53.240, P < 0.001; Fig. 3) during farrowing when compared with those housed in a CLOSED crate.

downloaded from the NVR system and stored on a hard drive. Behaviours were analysed using Observer XT v11 (Noldus Information Technology, Wageningen, The Netherlands) for a subset of sows (n = 12 CLOSED, n = 14 OPEN). An ethogram of the behaviours observed is presented in Table 2. 2.6. Statistical methods All analyses were performed using SPSS, version 21 (IBM, Armonk, NY) and data expressed as means ± SEM. A detailed outline of each analyses can be found in Table 3. Data were considered significant if the P-value was less than 0.05.

3.2. Sow performance Total litter size, the number of live born piglets and the number of piglets weaned did not differ between treatments (P > 0.05; Table 4). The average number of stillbirths per sow was greater for CLOSED sows compared with OPEN sows (X21 = 4.894, P = 0.027; Table 4). Farrowing duration and inter-piglet birth interval did not differ between treatment groups (P > 0.05; Table 4). There was no impact of treatment on total volume of colostrum produced, percentage protein or IgG concentration of the colostrum sample (P > 0.05; Table 4).

3. Results 3.1. Farrowing behaviour Treatment did not affect the total time sows spent lying (OPEN: 145.0 ± 26.7 min, CLOSED: 184.5 ± 22.7 min, F1,18 = 1.742, P = 0.203), the number of sitting events (OPEN: 4.4 ± 0.6, CLOSED: 3.7 ± 0.6, X21 = 0.781, P = 0.377) or the duration of posture changes (F1,18 = 1.530, P = 0.232; Fig. 1). The number of posture changes was significantly higher in the sows housed in the OPEN pens (X21 = 28.108, P < 0.001; Fig. 1). Sows in the OPEN treatment recorded a higher number of sow initiated and piglet initiated positive interactions (F1,18 = 6.216, P = 0.023 and F1,18 = 4.233, P = 0.050 respectively; Fig. 2), while no difference in the number of negative interactions was observed (F1,18 = 2.213, P = 0.154; Fig. 2). Treatment did not affect the number of bar biting and champing events (OPEN: 2.8 ± 0.5, CLOSED: 2.8 ± 0.5, X21 = 0.000, P = 0.999), however sows that

3.3. Post farrow behaviour Treatment did not affect the amount of time sows spent standing (OPEN: 9.3 ± 2.4 min, CLOSED: 9.2 ± 2.4 min; F1,17.91 = 0.000, P = 0.991) and lying laterally (OPEN: 71.6 ± 13.3 min, CLOSED: 83.2 ± 13.4 min; F1,17.27 = 0.765, P = 0.394). Sows housed in a CLOSED crate tended to spend more time lying ventrally than those housed in an OPEN pen (F1,21 = 3.003, P = 0.098; Fig. 4), however the number of ventral lying events performed was not affected by treatment (F1,21 = 3.128, P = 0.091; Fig. 4). Sows housed within a CLOSED crate performed a greater number of sitting events (F1,22 = 5.753, P = 0.026; 3

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Table 3 Type of model and terms within each model for all variables presented. Data were analysed in SPSS v21. Transformation

Sow behaviour Frequency Duration Sow traits Plasma cortisol concentration Total born and born alive Born dead Farrowing duration Colostrum quantity and quality Pre-weaning mortality

Repeated measure

GLMM w poisson GLMM GLMM

Log10

Litter weight at weaning Number of pigs weaned Piglet traits Piglet interval Meconium score Vitality score

Model

Hour

Random effect

Parity, Treatment, Parity*Treatment

Batch

Parity, Treatment, Time, Parity*Time, Treatment*Time, Parity*Treatment*Time Parity, Treatment, Parity*Treatment

Batch Batch Batch Batch

GLMM w poisson

Batch

GLMM GLMM

Batch Batch

Log10

Rectal temperature Blood glucose concentration Piglet weight and weight gain

Piglet number

Fixed effect

Batch Batch

GLMM GLMM w poisson GLMM GLMM

GLMM w poisson GLMM w negative binomial GLMM GLMM GLMM

Covariate

Batch

Born alive Total born and litter size fostered Litter size fostered

Birth weight Total born, birth weight

Sex, Parity, Treatment, Parity*Treatment, Sex*Treatment

Birth weight, litter size fostered

3.5. Piglet performance

Fig. 5), however the mean time they spent sitting did not differ between treatments (F1,21 = 0.508, P > 0.05; Fig. 5). There was no significant difference between treatment groups for the total number of positive piglet interactions (sow and piglet initiated: F1,21 = 2.070, P = 0.165; Fig. 6), however sows housed within the OPEN treatment group tended to perform more negative piglet interactions within the 24 h following farrowing (F1,21 = 3.640, P = 0.070; Fig. 6). No treatment differences were visible for the number of posture changes performed (OPEN: 45.5 ± 5.7, CLOSED: 45.5 ± 5.9, F1,21 = 0.000, P = 0.999), the amount of time piglets spent active at the udder (OPEN: 9.02 ± 1.1 min, CLOSED: 9.7 ± 1.1 min; F1,19.81 = 0.276, P = 0.605) and the sows reaction time to a piglet overlay (OPEN: 0.9 ± 0.3 min, CLOSED: 0.3 ± 0.3 min, F1,21 = 2.241, P = 0.149).

There was no significant difference between treatment groups for meconium and vitality score given to the piglets at birth (P < 0.05; Table 5). Rectal temperature was higher in piglets at birth but not at d 1 of age (P = 0.002 and P = 0.916 respectively; Table 5) within the CLOSED treatment group. Blood glucose concentration was higher in piglets born to a sow in the OPEN treatment at d 1 (P = 0.010; Table 5). Piglets born to a sow in the OPEN treatment had a significantly higher individual piglet weight gain to d 1 (F1,221 = 7.491, P = 0.007; Fig. 8) and a significantly higher individual weaning weight (F1,259 = 7.173, P = 0.008; Fig. 8) than those born to sows within the CLOSED treatment. There was no significant difference between treatment groups for pre and post foster mortality, liveborn mortality (sum of both pre and post foster mortality) and total piglet mortality (sum of both stillborn and liveborn mortality) (P > 0.05; Table 6).

3.4. Sow plasma cortisol concentrations No significant difference between treatment groups was observed for plasma cortisol concentration (nmol/l) at any time point in the lead up to and during farrowing (F32, 415 = 0.736, P = 0.854; Fig. 7). Those animals whose farrowing process exceeded 5 h displayed levels greater than 100 nmol/l.

4. Discussion In the present study sows housed within CLOSED crates spent a greater amount of time nosing crate fixtures during parturition, when compared with those housed in OPEN pens. This is somewhat different to previous studies who demonstrated that this behaviour primarily

Fig. 1. Mean ± SEM for (a) sow posture change number and (b) sow posture change duration observed during farrowing for sows housed in an OPEN or CLOSED ‘360 farrower’ (n = 12 CLOSED, n = 14 OPEN). Subscripts indicate a significant difference of P < 0.05. 4

Applied Animal Behaviour Science 221 (2019) 104872

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Fig. 2. Mean ± SEM for (a) positive maternal interactions and (b) negative maternal interactions observed during farrowing for sows housed in an OPEN or CLOSED ‘360 farrower’ during the farrowing event (n = 12 CLOSED, n = 14 OPEN). Subscripts indicate a significant difference of P < 0.05.

the birth process. Previous studies have demonstrated that this social interaction with the sow can be beneficial for piglet survival. Specifically, Thodberg et al. (2002) and Andersen et al. (2005) demonstrated that those sows who demonstrated higher levels of activity towards piglets were more responsive to piglet distress calls. Additionally, Illmann et al. (2015) demonstrated that sows who performed more posture changes after the birth of the first piglet were more likely to react to a piglets screams and had higher piglet body weight gain during lactation. Our finding that there was no difference in sow response time to piglet overlay would seem to contrast these findings as posture changes during farrowing were increased for this group, but no specific maternal response tests were carried out. The finding that posture changes were significantly higher for sows housed within an OPEN pen was somewhat expected as sows in OPEN pens interacted with their piglets more so would have had to get up more during farrowing to do so. Hales et al. (2016) supports this observation, demonstrating an increase in posture changes within loose housed sows when compared to those that were confined, however these observations were made from day 1–3 not during farrowing. Posture changes during farrowing are often seen as being risky as the probability of piglet crushing is increased. However, under the intensive supervision conditions of our investigation, this increased sow movement did not impact on piglet mortality during the farrowing event. Pain related behaviours are spontaneous and are only performed in response to a pain stimulus (Ison et al., 2016). We have demonstrated for the first time that sows housed within an OPEN pen perform fewer of these behaviours supposed to indicate a more painful farrowing, namely straining, tail flicking and back leg forward. Little research currently exists surrounding the impact of confinement on the mechanisms present within the sow that enable her to cope with farrowing. One idea that has been explored is parturition-induced hypoalgesia. This is the process whereby an animal’s tolerance to pain is increased, to the point that immediately prior to and during parturition,

occurs in the lead up to farrowing (Wischner et al., 2009; Yun et al., 2014a; Yun and Valros, 2015). Additionally, as no nest building material was given to either treatment group, it would be assumed that both treatments would direct this behaviour towards the crate fixtures regardless of space. There could be two possible reasons for this observation. The behaviours we observed during farrowing may not have been not nesting behaviours but rather stereotypies that resulted as the sow was unable to construct a nest leading up to farrowing. Interestingly however, no differences between treatment groups existed for the stereotypies bar biting and champing. A more logical explanation would be that sows housed within CLOSED crates may have performed this behaviour more during farrowing as they could not adequately express this behaviour prior to the farrowing event (Jarvis et al., 2001). However, as we did not measure any pre-farrow behavior, we cannot make any conclusions as to whether the amount of pre-farrow nest building behaviour impacted the amount performed during farrowing. In this experiment those animals that were housed within an OPEN pen had an increased ability to interact with their piglets during farrowing. As a result of this, sows housed within OPEN pens exhibited a significantly higher number of positive piglet interactions during farrowing. This was expected as previous studies have identified that sows within an open pen maintain contact with their litter through sniffing, grunting and nose to nose contact (Blackshaw and Hagelso, 1990). Additionally, a study conducted by Castrén et al. (1993) suggested that there is a correlation with the cessation of nest building and a rise in oxytocin levels in sows. Oxytocin is a social hormone (Chen and Sato, 2016) and as OPEN penned sows performed reduced nestbuilding behaviours during farrowing then sows within a CLOSED pen there is a possibility that it was elevated in the brain of OPEN sows, which may explain the increased piglet contact observed. Interestingly, interactions where the piglet initiated the contact were significantly higher within the OPEN treatment group also, with piglets born to OPEN sows approaching the sows face and or nose more frequently. This is likely due to the sow’s ability to re-position herself towards her litter during

Fig. 3. Mean ± SEM for pain related behaviours observed during farrowing for sows housed in an OPEN or CLOSED ‘360 farrower’ during the farrowing event. (a) tail flicking, (b) leg lifting and (c) straining (P < 0.001) (n = 12 CLOSED, n = 14 OPEN). Subscripts indicate a significant difference of P < 0.05. 5

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Table 4 Effect of an OPEN or CLOSED ‘360 farrower’ on sow performance measures.

Total litter size Born alive Still born piglets Number piglets weaned Farrowing duration, min Average birth interval, min Calculated colostrum production, kg Brix refractometry protein, % Colostrum IgG, g/mL

OPEN

CLOSED

Test statistics

P-value

11.9 ± 0.6 11.6 ± 0.6 0.2 ± 0.1 10.2 ± 0.4 2.4 ± 0.1 (230.7) 1.3 ± 0.1 (20.4) 2.7 ± 0.1 24.4 ± 0.8 108.6 ± 8.2

11.8 ± 0.6 11.3 ± 0.6 0.4 ± 0.1 9.6 ± 0.3 2.3 ± 0.1 (212.8) 1.3 ± 0.1 (18.8) 2.7 ± 0.2 24.6 ± 1.0 109.5 ± 9.2

F1,62 = 0.010 F1,62 = 0.197 X21 = 4.894 F1,59 = 1.490 F1,53 = 0.093 F1,53 = 0.099 F1,52 = 0.014 F1,31 = 0.019 F1,32 = 0.006

0.920 0.659 0.027 0.227 0.762 0.754 0.907 0.890 0.938

All data presented as mean ± SEM. Where parentheses are present, transformations have occurred, and back-transformed means are given.

(Oliviero et al., 2008; Hales et al., 2016). New research suggests that cortisol may not be the most adequate tool to assess stress as it can be elevated in response to pleasure, excitement and arousal as well as fear, anxiety and pain (Ralph and Tilbrook, 2016). Additionally, plasma cortisol concentration naturally elevates in the lead up to farrowing to enable the final development of offspring before birth, creating a great deal of ‘noise’ in which it becomes difficult to detect any treatment effects (Sangild et al., 1993; Fowden et al., 2007; Keller-Wood et al., 2014). Interestingly however, our results demonstrate that those animals that had farrowing durations that exceeded five hours had elevated plasma cortisol concentrations of 100 nmol/l. Arguably, these extreme cortisol levels would suggest that sows with extended farrowing durations are suffering with regards to welfare. This notion should be confirmed and interventions that reduce length of farrowing should be tested to improve sow welfare during this time. Interestingly, those piglets born to OPEN pen sows exhibited increased colostrum intake. As no treatment differences existed for the quality (i.e. % protein and colostrum IgG) and quantity of milk produced, this finding would suggest that the weight gain observed in piglets was not due to differences in sow colostrum but rather the piglet’s ability to acquire it. This can be achieved in two ways; either the piglet is born more vigorous and so performs more sucking behaviour during the colostrum phase of lactation, or there were behavioural changes in the sow during this time that gave piglets better access to the colostrum. Quesnel (2011) identified a negative relationship between stillbirths and sow colostrum production, hinting that birth trauma and piglet viability may impact colostrum intake. However, there was no treatment influence on the piglet vigour traits measured at birth (staining and vitality score) and so this would suggest that it was indeed improved udder access driven by shifts in sow behaviour. We were able to demonstrate that sows in OPEN pens spent less time sitting, and lying ventrally, but we could not demonstrate any changes in lateral lying in the 18 h following farrowing. We also attempted to measure letdown events however the positioning of the cameras did not enable for the ability to distinguish between the exact phases of a letdown event, i.e. pre-letdown massage, letdown and post letdown massage. Whilst no difference in the amount of time piglet

they are almost non-responsive to adverse stimuli (Jarvis et al., 1997). The finding that pain related behaviours were influenced by confinement was intriguing and may simply be the result of the increased ability to move around and become comfortable in the lead up to and during farrowing for the sows housed within OPEN pens. Alternately, it has been demonstrated that allowing the sow to perform highly motivated, intrinsic nest building behaviours result in increased concentrations of circulating oxytocin levels (Oliviero et al., 2008). There is evidence that central oxytocin has analgesic properties (Han et al., 2018), and so it may be true that confining sows predisposes them to a greater level of visceral pain associated with dilation, distention and initial contractions in the hours leading up to, and during parturition. For these two reasons, housing sows in farrowing crates may result in amplified pain for sows. Nevertheless, in order to determine if this was the cause for the differences in pain related behaviour observed in the present study, further investigation is needed as no quantitative measure of pain was included in this experiment. The current finding that confinement during farrowing resulted in more piglet death immediately prior to or during farrowing is consistent with previous studies (Oliviero et al., 2010; Condous et al., 2016). However, given we observed no treatment effects on inter piglet birth intervals, or confinement induced elevations in cortisol levels, alterations in oxytocin release suggested by Oliviero et al. (2008) does not appear responsible for the reduced stillbirths observed in this study. Perhaps an alternate explanation is related to blood flow differences that may be apparent between the two treatments. During times of high distress, blood is diverted away from uterine tissue towards key organs and skeletal muscle (Levine et al., 2016) as part of the ‘fight or flight’ response. Given our findings that sow display a greater incidence of pain related behaviours when confined, a decrease in blood flow to the uterus, placenta, umbilical cord and so piglet, may be sufficient to cause intra-partum death. The increased straining behaviour observed in the CLOSED sows would give rise to this argument, but future work should investigate the interaction between stress, parturition and uterine blood flow in sows. Plasma cortisol concentration was unaffected by the housing conditions investigated presently, and this contrasts previous findings

Fig. 4. Mean ± SEM for (a) the number of ventral lying events and (b) the mean time spent lying ventrally, 18 h post farrowing for sows housed in an OPEN or CLOSED ‘360 farrower’ (n = 12 CLOSED, n = 14 OPEN). 6

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Fig. 5. Mean ± SEM for (a) the number of sitting events and (b) the mean time spent sitting, observed 18 h post farrowing for sows housed in an OPEN or CLOSED ‘360 farrower’ (n = 12 CLOSED, n = 14 OPEN). Subscripts indicate a significant difference of P < 0.05.

Fig. 6. Mean ± SEM for (a) the number of positive piglet interactions and (b) the number of negative piglet interaction observed 18 h post farrowing for sows housed in an OPEN or CLOSED ‘360 farrower’ (n = 12 CLOSED, n = 14 OPEN).

Fig. 7. Mean ± SEM for hourly plasma cortisol levels commencing 24 h prior to farrowing through until the last piglet was born for sows that farrowed in OPEN (n = 19) and CLOSED (n = 19) farrowing pens.

Table 5 Piglet measures at birth and d 1 for piglets born to sows housed in OPEN ‘360 farrower’ pens (n = 265) and CLOSED ‘360 farrower’ crates (n = 313). Data presented as mean ± SEM. OPEN Meconium stain score Vitality score Birth rectal temperature, ºC Day 1 rectal temperature, ºC Day 1 blood glucose concentration, mmol/L

0.64 ± 0.12 1.82 ± 0.47 36.8 ± 0.40 38.3 ± 0.03 5.3 ± 0.10

CLOSED

Test statistic

P-value

0.58 ± 0.10 1.81 ± 0.46 37.1 ± 0.40 38.4 ± 0.04 5.1 ± 0.10

X21 X21

0.477 0.938 0.002 0.916 0.010

= 0.507 = 0.006 F1,226 = 9.868 F1,251 = 0.011 F1,182 = 6.804

farrowing accommodation in this study. Namely, piglets born to OPEN sows had increase blood glucose concentrations at d 1, indicating increased energy intake, further supporting the outcome of improved colostrum ingestion. Interestingly, this was achieved with lower core body temperature at birth but not day 1 within the OPEN penned

spent active at the udder was observed, we cannot conclude that this activity was directly associated with a milk letdown event. More intensive behavioural observations are thus required to determine why piglets born to sows in OPEN pens ingest more colostrum. Other factors important for piglet survival were also affected by 7

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Fig. 8. Mean ± SEM for (a) individual piglet weight gain from birth to day 1 and (b) individual piglet weaning weight for piglets born to sows housed in OPEN ‘360 farrower’ pens (n = 243) and CLOSED ‘360 farrower’ crates (n = 284). Subscripts indicate a significant difference of P < 0.05.

Consent for publication

Table 6 Liveborn piglet mortality for sows and their litters housed in an OPEN or CLOSED ‘360 farrower’. Data are displayed as means ± SEM. OPEN Pre-foster mortality Post-foster mortality Total liveborn mortality1 Total piglet mortality2 1 2

0.8 0.4 1.2 1.5

± ± ± ±

0.2 0.1 0.2 0.2

CLOSED

Test statistic

P-value

0.6 0.7 1.4 1.8

X21 X21 X21 X21

0.421 0.128 0.462 0.211

± ± ± ±

0.2 0.2 0.2 0.3

= = = =

0.647 2.318 0.535 1.562

Consent for publication was received by the funding body the Pork CRC, the document can be presented if required. Availability of data and materials All data generated or analysed during this study are included in this published article [and its supplementary information files].

The sum of both pre and post-foster mortality. The sum of both stillborn and liveborn mortality.

Author’s contributions

piglets. Furthermore, those piglets born and raised on OPEN pen sows also demonstrated increased weight at weaning. This likely being the result of the improved colostrum intake observed within the first 24 h of life, however improvements in sow behaviour within the OPEN penned sows could also be likely. As sow behaviour was not measured beyond 18 h this cannot be confirmed. Taken collectively, it is evident that farrowing environment not only impacts sow behaviour, but also traits important for piglet survival.

TN had substantial contribution in the collection and interpretation of data and was heavily involved in writing the manuscript. TN received final approval of the version to be published and has agreed to be accountable for all aspects of the work. KP contributed to the initial conception, experimental design, data collection and analysis. WvW contributed to the initial conception and design. All authors have read and approved the final manuscript. Declaration of Competing Interest

4.1. Conclusion

None.

Allowing sows to farrow unconfined reduced pain related behaviours, increased the number of posture changes performed and increased maternal behaviour as seen through positive piglet interactions during farrowing. Sows housed within a CLOSED crate spent significantly more time sitting and tended to spend more time lying ventrally in the 18 h following farrowing. The number of piglets born dead was reduced in sows housed in an OPEN pen prior to and during farrowing, and colostrum intake and weaning weight was increased with no impact on pre-weaning mortality. These data suggest that allowing the sow a greater freedom of movement exclusively in the lead up to and during the parturition process exerts beneficial impacts on factors important for survival and improves piglet growth, with little influence on postnatal mortality. Further work into the physiological processes that may be responsible for the improvement in piglet health and growth should be carried out.

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