Schild Et Al. 2020 Accepted Unformatted Manuscript

1 A review of neonatal mortality in outdoor organic production and possibilities to
2 increase piglet survival
3 Sarah-Lina Aa. Schild1*, Emma M. Baxter2, Lene J. Pedersen3
5 1
Department of Biosystems and Technology, Swedish University of Agricultural Sciences,
6 Sundsvägen 16, 23053 Alnarp, Sweden
7 2
Department of Animal & Veterinary Sciences, Scotland’s Rural College, King’s Buildings,
8 West Mains Road, Edinburgh, EH9 3JG, United Kingdom
9 3
Department of Animal Science, Aarhus University, Blichers Allé 20, 8830 Tjele, Denmark
10
11 *Corresponding author: Sarah-Lina Aa. Schild. Email: sarah.lina.schild@slu.se
12
13 Highlights
14  High piglet mortality in outdoor production conflicts with the organic principles
15  A consistent problem related to mortality appears to be large litter sizes
16  Optimise breeding strategies by using less prolific genetics
17  Select for improved maternal behaviour and piglet robustness
18
19 Keywords: Piglet mortality, outdoor parturition, piglet viability, farrowing and lactating sows,
20 animal welfare, sow genetics

21
22 Abstract
23 The current level of piglet mortality in production systems with outdoor farrowing is high and
24 conflicts with the ethical principles of organic farming. Over the last decade, there has been a
25 rise in scientific studies addressing the level of piglet mortality in outdoor pig production and
26 the causes for mortality. Therefore, the aim of this paper was to review current literature on
27 risk factors for piglet mortality in outdoor pig production, to identify causes of mortality and
28 possibilities for improving piglet survival. A consistent problem related to outdoor piglet
29 mortality appears to be the use of highly prolific sow hybrids. Large litter sizes are
30 accompanied by long parturitions and the birth of piglets displaying signs of lowered
31 viability. Management interventions such as use of birth assistance and caretaking of less
32 viable piglets, as is common in indoor systems, is more difficult to apply in outdoor
33 production. Therefore, based on the present review, we suggest that use of less prolific sow
34 genetics, in systems with outdoor farrowing, may be one way to increase piglet survival.
35 Sows used in outdoor systems should give birth to piglets displaying signs of high vitality
36 and the sows should be able to nurse their own litter. This solution also conforms to the
37 organic mind-set of operating a system with the least possible human intervention.
38
39 1. Introduction
40 Concurrent with the rising public concern for animal welfare (Kristiansen and Merfield,
41 2006; Fraser, 2008), across Europe, organic pig production is growing (Früh et al., 2014). In
42 the EU, the countries with the highest share of organic pigs in all livestock are Denmark
43 (~3.9%), Austria (~2.6%), Sweden (~2.4%) and France (~2.3%) (eurostat, 2020). Like
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44 organic farming in general, organic pig production is based on the four ethical principles put
45 forward by the International Federation of Organic Agriculture Movements. These are the
46 principles of health, ecology, fairness and care (IFOAM, 2005). The first principle refers to
47 health as “the maintenance of physical, mental, social and ecological well-being” (IFOAM,
48 2005). Generally, piglet mortality appears higher in European outdoor pig production
49 (Prunier et al., 2014a; Prunier et al., 2014b) than in conventional indoor production. A recent
50 study conducted at nine large, organic, pig-producing herds (size 85-910 sows) revealed that
51 close to one in three piglets die before weaning at seven weeks of age in Danish pig
52 production with outdoor farrowing. The majority of piglet death was due to stillbirth,
53 crushing, starvation and infection (Rangstrup-Christensen et al., 2018b). As discussed by
54 Pedersen et al. (2010), death due to crushing, starvation or infection is associated with pain,
55 hunger, fear and/or stress. Thus, the mortality reported in organic pig production conflicts
56 with the ethical principle of health. Furthermore, the high mortality provides a basis for
57 questioning whether the production complies with the principle of fairness, which “insists
58 that animals should be provided with the conditions and opportunities of life that accord with
59 their physiology, natural behavior and well-being“ (IFOAM, 2005).
60 In accordance with the principle of fairness, the outdoor conditions in organic production
61 allow animals increased opportunity to express species-specific behaviour. Both outdoor
62 access and possibility of performing species-specific behaviour are qualities, which
63 consumers stress as important for animal welfare (reviewed by Thorslund et al., 2017) and
64 nine in ten Europeans value the animal welfare friendliness of animal production (94% of
65 27,672 survey respondents, Eurobaromenter, 2016). However, the extensive housing
66 conditions and limited possibility for management intervention during, for instance, long
67 parturitions and extreme weather conditions may challenge animal welfare and the ethical
68 principles of organic farming. This paper therefore aims to review current literature on risk
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69 factors for piglet mortality in outdoor pig production, to identify causes of mortality and
70 possibilities for improving piglet survival.
71
72 2. Sow risk factors for piglet mortality
73 2.1 The course of parturition and the sow´s physical condition
74 Studies, both on sows giving birth outdoors in huts (Baxter et al., 2009; Thorsen et al., 2017;
75 Schild et al., 2019b) and indoors in farrowing crates without outdoor access (e.g. Borges et
76 al., 2005; Canario et al., 2006; Mainau et al., 2010), have documented increased stillbirth risk
77 when parturition is prolonged and a recent study indicated that postnatal mortality may also
78 be affected (Schild et al., 2019b). Although others have not found such a trend (Baxter et al.,
79 2009; Thorsen et al., 2017), van Dijk et al. (2006) and Alonso-Spilsbury et al. (2005)
80 suggested a greater risk of the umbilical cord rupturing or prolonged cord compression during
81 prolonged parturitions, which can result in piglet death or postnatal complications due to
82 hypoxia during the birthing process. Accordingly, hypoxia has been related to increased
83 stillbirth risk (Pedersen et al., 2011) and lowered postnatal viability (Herpin et al., 1996;
84 Alonso-Spilsbury et al., 2005). Several factors affect parturition duration and e.g. Baxter et
85 al. (2009) and Schild et al. (2019b) found positive correlations between parturition duration
86 and litter size in systems with outdoor farrowing. Increasing parity has also been associated
87 with longer parturitions in outdoor pig herds, Wülbers-Mindermann et al. (2002) saw longer
88 parturitions in multiparous (235.4±104.6 minutes) compared to primiparous (157±81.8
89 minutes) sows. Sows of higher parity give birth to larger litter sizes (Koketsu et al., 1999;
90 Quesnel et al., 2008; Hales et al., 2014), which may be part of the reason for the longer
91 parturition in older sows. A reduced physical condition resulting from a life of production
92 may also add to a long parturition duration in high parity sows. Constipation can also prolong
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93 parturition (Oliviero et al., 2010). Contrarily, access to nesting material prior to parturition is
94 related to increased oxytocin levels (Yun et al., 2013; Yun et al., 2014) and the possibility to
95 express nest building behaviour decreases parturition duration (Westin et al., 2015). In
96 outdoor farrowing systems, sows are loose-housed and in the EU, organic sows must have
97 access to roughage (REGULATION (EU) 2018/848, 2018), which will lower constipation
98 risk (Peltoniemi and Oliviero, 2015). In addition, sows giving birth outdoors are provided
99 with plenty of nesting material and freedom to perform nest building behaviour. Thus, several
100 prerequisites to achieve a complication free parturition are satisfied. Despite these housing
101 conditions, recent studies on sows giving birth outdoors, report long parturitions (e.g. 450
102 min in Thorsen et al. (2017); 258 min in Schild et al. (2019b), Table 1). The durations
103 reported in Thorsen et al. (2017) and Schild et al. (2019b), may be considered in the upper
104 range of what might constitute a “typical” or standard parturition duration (durations >5h are
105 considered longer than average, Oliviero et al., 2010) or even longer than “normal” (normal
106 duration 3h; Borges et al., 2005). The sow hybrids in both aforementioned studies were
107 highly prolific as reflected by their birth litter sizes (18.4 totalborn, 1-6 parity Danbred sows,
108 Thorsen et al., 2017; 17.0 totalborn, 1-2 parity Danbred or Topigs Norsvin sows, Schild et
109 al., 2019b). Since long parturitions are correlated with a large litter size (in outdoor herds e.g.
110 Baxter et al., 2009; Schild et al., 2019b) differences between sow hybrids with different
111 prolificacy may be expected. In several European countries (e.g. Denmark, France and
112 Germany) the same hyper prolific sow hybrids are used in organic production as in
113 conventional indoor production (Früh et al., 2014). This choice of genetics could be one of
114 the reasons for the long parturitions and high risk of piglet mortality in organic pig
115 production.
116 Oliviero et al. (2010) found longer parturitions in sows with higher average back fat
117 thickness, which may explain the relationship between sow body weight and piglet mortality.
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118 Rangstrup-Christensen et al. (2018a), studying sows giving birth on pasture in huts, reported
119 a greater risk of early live born death when piglets were born to fat sows (i.e. “ribs, backbone
120 and hip bones cannot be seen or felt when firm pressure is applied, or fat deposits are clearly
121 visible”) compared to piglets born to normal (i.e. “ribs, backbone and hip bones are barely
122 visible or are barely felt with firm pressure”) or skinny (i.e. “ribs, backbone and hip bones
123 are obvious or easily detected with pressure”) sows. Also, Wülbers-Mindermann et al.
124 (2002), studying sows housed outdoors in huts or indoors in pens, showed that a 10 kg
125 increase in sow body weight prior to parturition was accompanied by ~12% increase in early
126 piglet mortality, while the risk of late mortality was increased by ~8%.
127 Several studies report higher piglet mortality amongst litters from first parity (indoor and
128 outdoor; Berger et al., 1997; indoor and outdoor; Wülbers-Mindermann et al., 2002; various
129 indoor farrowing systems and outdoor; KilBride et al., 2012) and from high parity sows
130 (access to outdoor run; Wientjes et al., 2012; outdoor parturition; Rangstrup-Christensen et
131 al., 2018a). Young sows still allocate resources for their own growth (Eissen et al., 2000) and
132 they have a lower feed consumption than older sows (Eissen et al., 2000; Ocepek et al.,
133 2016). This can result in less nutrients being available for the developing foetuses, resulting
134 in stillbirth or the birth of less viable piglets that later die. Furthermore, sows in first parity
135 may react more strongly to the presence of piglets and studies show more savaging in gilts
136 (Harris et al., 2003; Chen et al., 2008), which could also increase live born death.
137 Since high parity sows are more prone to have long parturitions, a higher piglet mortality is
138 expected. Furthermore, due to the risk of long parturitions these sows may be in greater risk
139 of suffering exhaustion postpartum (pp), which increases the risk of flopping (defined as “the
140 hindquarter drops quickly to the floor” Damm et al. (2005)), a behaviour related to piglet
141 crushing (Damm et al., 2005). A long production life may also result in lowered muscular
142 control, which could also increase the risk of flopping. Although, in outdoor systems sows
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143 have the possibility to exercise, so increased stamina and muscular control may be expected;
144 Krogh et al. (2018) showed that highly prolific sows housed on pasture may walk between
145 1.1 km (in early lactation) and 3.4 km (in mid gestation) daily.
146 Being a live born piglet in a litter with stillborn piglets has also been related to increased risk
147 of dying (indoors, Leenhouwers et al. (1999); indoor and outdoor production systems,
148 KilBride et al. (2012); organic farms with outdoor farrowing, Rangstrup-Christensen et al.
149 (2018a)). Birth of stillborn piglets could be a sign of dystocia, which would result in reduced
150 viability of their live born littermates.
151
152 2.2 Sow health and nutrition
153 Not many studies have focused on the health condition of sows kept under outdoor
154 conditions. The focus has been on disease prevention through management as some of the
155 risks for outdoor herds include exposure to parasites and contact with wildlife, which may
156 increase zoonotic infection risk (Bonde and Sørensen, 2004; Edwards, 2005; Sutherland et
157 al., 2013).
158 In their description of organic pig production in Europe (Austria, Denmark, France,
159 Germany, Italy, Sweden, Switzerland and the UK) Früh et al. (2014) report the main health
160 issues in outdoor systems as MMA (metritis, mastitis, agalactia) (or one of the three) and leg
161 problems/lameness. Both these conditions can affect piglet mortality. Sows suffering MMA
162 may have insufficient colostrum production and lactation performance in the first day’s pp,
163 which increases the risk of piglet death due to e.g. starvation. Leg problems can result in
164 lowered sow mobility (including abnormal lying down behaviour). For instance under indoor
165 conditions sows suffering overgrown hooves have been reported to display abnormal lying
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166 down behaviour (crated sows, Bonde et al., 2004) and as suggested by Anil et al. (2009)
167 impaired lying down behaviour, as seen in lame sows, may increase the risk of piglet
168 crushing. However, whether overgrown hooves constitute a problem under outdoor
169 conditions and whether this condition affects the lying down behaviour of sows housed in
170 huts has yet to be studied. Furthermore, when sows are housed outdoors good locomotion is
171 required as sows need to be able to walk the distances between their feed, water, hut and (in
172 the summer) wallow. If sows e.g. due to lameness are unable to walk to their feed and/or
173 water trough it may result in an insufficient feed and water intake. Lowered energy during
174 parturition has negative consequences for the course of parturition (Feyera et al., 2018). A
175 high feed intake is also required for a high lactation performance (Vadmand et al., 2015;
176 Strathe et al., 2017) and water constitutes the main component of milk (Hurley, 2014), thus
177 this stresses the importance of sows reaching both feed and water.
178 Disease is characterized by a lowered feed intake and lowered activity (Weary et al., 2009).
179 Under outdoor conditions, this reduction in feed intake may be even more pronounced due to
180 the larger distances between the resources. In practise, some farmers will move the feed and
181 water troughs nearer to the hut, when diseased animals are identified, to try to encourage feed
182 and water intake.
183
184 2.3 Maternal behaviour
185 The main cause of early postnatal mortality in both outdoor (Edwards et al., 1994; Baxter et
186 al., 2009; KilBride et al., 2012; Rangstrup-Christensen et al., 2018b; Schild et al., 2019b) and
187 indoor (e.g. Marchant et al., 2000; Pedersen et al., 2006) production is crushing by the sow.
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188 Piglet death due to crushing is, among other factors, related to the behaviour of the sow.
189 Sows displaying a higher frequency of posture changes crush more piglets. High risk posture
190 changes include changes from standing to lying and rolling (Weary et al., 1996; Wechsler and
191 Hegglin, 1997; Marchant et al., 2001; Nicolaisen et al., 2019). Larger amounts of nest
192 building behaviour prior to parturition have been associated with a lower frequency of
193 posture changes during parturition (Ocepek and Andersen, 2017; Bolhuis et al., 2018). In
194 addition, an increased display of pre-lying behaviour (e.g. sniffing, rooting, scraping) is
195 related to a lower risk of piglet crushing (Marchant et al., 2001; Andersen et al., 2005;
196 Wischner et al., 2010). Furthermore, sow behaviour during parturition was shown to be
197 related to sow responsiveness during a Piglet Scream Test, with more responsive sows
198 displaying less risky behaviour (Wechsler and Hegglin, 1997; Grandinson et al., 2003;
199 Andersen et al., 2005). Some studies have found indications of a relationship between sow
200 responsiveness in the Piglet Scream Test and piglet death (Wechsler and Hegglin, 1997;
201 Grandinson et al., 2003) although others could not confirm this (Špinka et al., 2000; Held et
202 al., 2002). Since sow responsiveness in this test differs between individual sows (e.g. Špinka
203 et al., 2000; Grandinson et al., 2003; Held et al., 2006), selection of more reactive sows may
204 potentially benefit piglet survival (Grandinson et al., 2003). However, not only behavioural
205 factors but also physical factors may impact sows’ lying down behaviour and their
206 responsiveness. For instance, sows suffering pp exhaustion and sows that could be described
207 as “unfit” (i.e. high body condition score and/or high parity) may have reduced muscular
208 control and may therefore be more prone to flop down during the lying down movement and
209 be less responsive to piglet screams. Such relationships have been confirmed mainly in
210 indoor systems where sows are less agile and where space may further limit their possibilities
211 to manoeuvre. However, it cannot be excluded that outdoor kept sows may also suffer from
212 fatigue, especially the older animals.
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213 Piglet vigilance or mobility may be lower in the first hours after birth (English and Smith,
214 1975) and so the greatest risk of crushing is expected during or immediately following
215 parturition. Accordingly, Vieuille et al. (2003) found higher risk of crushing in the first 12h
216 pp when sows gave birth outdoors in huts (recordings from the first 40h pp). Also, in indoor
217 loose-housed and crated sows, Weary et al. (1996) saw a greater risk of crushing and near
218 crushing (defined as: a piglet being trapped under the sow and surviving the event) during as
219 compared to after parturition. In contrast, Schild et al. (2019b) found no relationship between
220 the frequency of posture changes during parturition and early postnatal mortality, when sows
221 gave birth in huts, despite crushing being the main cause of death. The discrepancy between
222 the studies by Weary et al. (1996) (crates or pens 6.5m2; ~10 total born) and Schild et al.
223 (2019b) (4.4-6.0m2 hut and 450m2 paddock; 17 total born) may be due to differences in
224 housing conditions and/or in litter sizes. Weary et al. (1996) highlighted sow rolling
225 behaviour as particularly risky. Pens in their studies were simple with guard rails for piglet
226 protection. Most outdoor huts have sloped sides that prevent the sow from crushing piglets
227 against the walls. Sloped walls have been shown to be protective and preferable to rails
228 (Damm et al., 2006) and researchers working on pen design for loose housed sows have
229 highlighted the importance of design detail, including these protective elements, to reduce
230 piglet mortality (Baxter et al., 2011; Pedersen et al., 2013; Baxter et al., 2015). In addition
231 there are other protective elements in outdoor huts, namely the deep-straw bedding, that
232 Baxter et al. (2009) discussed, could be cushioning and protecting the piglets even when there
233 were crush incidents. Furthermore, the results by Schild et al. (2019b) suggest that crushing
234 in an outdoor system is more related to piglet vitality than to sow body movements and/or
235 that crushing mainly occurs after parturition is completed.
236
237 3 Piglet and litter characteristics influencing neonatal mortality
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238 A number of piglet characteristics are associated with piglet survival chances both in indoor
239 and outdoor systems. Traits such as: low birth weight (e.g. in outdoor Baxter et al. (2009);
240 Schild et al. (2020) and indoor systems Tuchscherer et al. (2000); Quiniou et al. (2002);
241 Baxter et al. (2008)), low rectal temperature (outdoors Baxter et al. (2009); Schild et al.
242 (2020) and indoors Tuchscherer et al. (2000); Baxter et al. (2008)) and signs of intrauterine
243 growth restriction (IUGR) (indoors Hales et al., 2013) have been related to an increased risk
244 of piglet death during lactation. Also a larger birth litter size increases the risk of both pre
245 (e.g. in systems with outdoor parturition Baxter et al., 2009; KilBride et al., 2012; Rangstrup-
246 Christensen et al., 2017; Schild et al., 2019a) and postnatal mortality (outdoor parturition;
247 Baxter et al. (2009); Schild et al. (2019a), parturition indoors but with access to an outdoor
248 run; Wientjes et al. (2012)), although KilBride et al. (2012) found no relationship between
249 litter size and risk of postnatal death. However, KilBride et al. (2012) conducted an
250 epidemiological study on outdoor production in the UK. Outdoor herds in the UK have
251 traditionally used less prolific hybrid genetics than those being used in outdoor production in
252 Denmark, France and Germany. The average total born in UK outdoor production was 11.6
253 piglets in 2012 and whilst current figures have added an extra piglet (12.6 - AHDB Pork,
254 2019), Danish herds are averaging 19.0 total born (national average for indoor production
255 (Hansen, 2019) but the same hybrid genetics as used outdoors). As increased litter size
256 reduces birth weight, increases within litter weight variation and increases the incidence of
257 IUGR (Baxter et al., 2013) it is likely that piglets in UK outdoor production are more robust
258 than those born to hyper prolific hybrid sows, which could account for the discrepancies
259 discussed.
260 A large litter size also increases piglet competition at the udder (Andersen et al., 2011).
261 Studies from indoor production suggest that increased piglet competition may result in piglets
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262 missing milk ejection (Andersen et al., 2011; Bozděchová et al., 2014; Illmann et al., 2018)
263 thereby increasing the risk of starving piglets.
264
265 4 Housing environment and neonatal mortality
266 4.1 Thermal conditions
267 When animals are housed outdoors, they are exposed to more extreme and fluctuating
268 thermal conditions than what is seen indoors. This can have negative consequences for both
269 sows and piglets in systems with outdoor farrowing. At high temperatures, there is a risk of
270 sows experiencing hyperthermia. This condition may influence the course of parturition and
271 sow milk production. Several studies have demonstrated a lowered lactation performance in
272 sows housed above their upper critical temperature (Prunier et al., 1997; Quiniou and Noblet,
273 1999; Renaudeau et al., 2001). Muns et al. (2016) found indications (P<0.1) of longer
274 parturitions in crated sows housed at 25°C compared to sows housed at 20°C. Others have
275 not been able to confirm this for loose-housed sows (housed at 15, 20 or 25°C) most likely
276 because loose sows are better able to thermoregulate by altering their behaviour e.g. by
277 choosing to lie on the cooler slatted floor rather than the warmer solid floor (Malmkvist et al.,
278 2012). From March-November, Schild et al. (2019a) found higher risk of stillbirth (30%
279 increase) when outdoor-housed sows gave birth at high (T≥27°C) compared to medium-to-
280 high (22°C<T <27°C) hut temperatures. However, the authors showed no effect of hut
281 temperature on early live born mortality. During winter, hut insulation may benefit early
282 piglet survival, Randolph et al. (2005) found no effect of hut temperature on early mortality
283 (including stillborn piglets) when sows gave birth in insulated huts (typical diurnal
284 temperature: winter insulated ~11 to ~14°C/uninsulated ~9 to ~22°C; summer insulated ~12
285 to ~30°C/uninsulated ~12 to ~45°C). Only few studies have investigated how the thermal
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286 conditions affect parturition and signs of hyperthermia when sows give birth outdoors. In the
287 first three days pp Schild et al. (2018) found a higher sow surface temperature (recorded
288 using a thermal imaging camera directed at the cornea of the eye when sows were lying
289 inside their insulated A-frame hut) when hut temperature increased (5°C increase was
290 accompanied by ~1°C increase in maximum sow surface temperature).
291 Free-range and organic pig producers use management initiatives in an attempt to improve
292 the thermal conditions inside the farrowing hut and to provide the animals opportunity for
293 performing thermoregulatory behaviour. For instance, in Denmark specifications are
294 provided in the legislation stating that farrowing huts “must be insulated or arranged so that
295 the temperature requirement of the pig can be met under all weather conditions… the
296 temperature requirements of the sow, gilt and piglets must be taken into account” (LBK nr 51
297 af 11/01/2017, 2017). Similarly, in the UK there are specific welfare codes for pigs stating
298 that “farrowing accommodation should be able to manage higher or lower temperature
299 variations through various options, which may include extra ventilation, insulation or
300 bedding” (Defra, 2019). During summer, Randolph et al. (2005) (study from southern
301 England) found a lower hut temperature in insulated (temperature rarely exceeded 25°C)
302 compared to uninsulated huts (temperature exceeded 25°C for an average of 5h/day and
303 reached levels above 45°C). Hut insulation may also reduce the temperature fluctuations
304 inside the hut (Edwards et al., 1995; Randolph et al., 2005). Although, Johnson and McGlone
305 (2003) (study from Texas) found no difference in average daily temperature (or humidity)
306 between insulated and uninsulated huts.
307 In e.g. Denmark (LBK nr 51 af 11/01/2017, 2017) and Sweden (KRAV, 2019) it is required
308 that organic/free-range sows be provided with access to wallows (or the like) during warm
309 weather (in Denmark defined as temperature exceeding 15°C in the shade). In the UK, the
310 Defra Code of Recommendations for Pig Welfare has wording in relation to hyperthermia
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311 stating that “adequate shelter must…be provided to protect against sunburn, for example,
312 through the provision of shade and or wallows. The accommodation should have shutters at
313 the opposite end to the door to provide through ventilation” (Defra, 2019).
314 The pig has a very limited ability to sweat (Ingram, 1967) and so to utilize evaporative
315 cooling across the body surface, pigs rely on the behaviour termed wallowing (Ingram, 1965;
316 Fraser, 1970; Steinbach, 1970; Fialho et al., 2004; Bracke, 2011). Several studies document
317 increased wallowing in pigs at increasing temperatures (Heitman et al., 1962; Fraser, 1970;
318 Huynh et al., 2005; Huynh et al., 2007). In addition to provision of wallows, in Denmark,
319 according to the updated code of practise, organic sows must be provided with access to
320 shade (besides that provided by the hut) in the farrowing field during summer (Anonymous,
321 2017), and studies suggest pigs may use shade seeking for thermoregulation (Blackshaw and
322 Blackshaw, 1994; Schild et al., 2018). During warm weather, sows need access to a wallow
323 in order to thermoregulate sufficiently. If the sows have difficulties to walk to the wallow e.g.
324 due to lameness, they risk becoming hyperthermic, which may compromise piglet survival by
325 leading to prolonged parturitions (Muns et al., 2016) and lowered lactation performance
326 (Black et al., 1993; Prunier et al., 1997; Quiniou and Noblet, 1999; Renaudeau et al., 2001).
327 In contrast to high temperatures, which may indirectly influence piglet mortality by causing
328 hyperthermia in parturient and lactating sows, low hut temperature can result in piglets
329 experiencing hypothermia, which increases the risk of piglet death (Tuchscherer et al., 2000;
330 Baxter et al., 2008). When sows gave birth in uninsulated huts, Randolph et al. (2005)
331 showed an increased risk of early mortality at low hut temperatures, whereas this relationship
332 was not found when sows gave birth in insulated huts (typical diurnal temperature: winter
333 insulated ~11 to ~14°C/uninsulated ~9 to ~22°C; summer insulated ~12 to ~30°C/uninsulated
334 ~12 to ~45°C). Accordingly, Schild et al. (2019a) saw no effect of hut temperature on early
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335 live born mortality when sows gave birth in insulated huts (the daily average of the 10%
336 highest/lowest farrowing hut temperatures on day 1 pp for summer, autumn, winter and
337 spring, respectively, 24.2/13.7, 16.5/9.1, 9.0/2.7, 16.6/6.1°C). Whilst well-designed huts and
338 good paddock management can reduce the potential for heat or cold stress in outdoor
339 production, certain genetics are likely to be at greater risk of these conditions. Sows
340 producing large litters not only produce piglets that are likely to be at greater risk of
341 hypothermia (because of their smaller size they have higher heat loss due to a high surface-
342 to-volume ratio, Herpin et al., 2002), but the high lactational output to feed larger litters and
343 the associated elevation in metabolism (Feyera and Theil, 2017) make sows more susceptible
344 to heat stress. Thus, a large litter size may be accompanied by increased vulnerability to
345 temperature for both sows and piglets.
346 In their study, Schild et al. (2019a) recorded hut temperatures (in winter the lower 10% =
347 2.7±0.5°C) far below the lower critical temperature of the neonatal piglet (34-35°C Mount,
348 1959; likely higher in the first hours pp Kammersgaard, 2013) yet showed no effect of hut
349 temperature on early live born mortality. This may be due to a sufficient nest microclimate
350 preventing piglets from becoming hypothermic. Recordings of farrowing nest temperature in
351 the first week pp revealed a considerably higher temperature (average 23.4°C) in the nest
352 (recorded ~1 cm into the straw between the resting piglets) compared to the ambient hut
353 temperature (11.7°C; recorded ~50 cm above the huddling piglets) and outdoor temperature
354 (3.9°C) (Schild, 2018). When sows gave birth in semi-natural conditions Algers and Jensen
355 (1990) also recorded higher nest (average 20.3°C, recorded in the straw in 5 cm distance to
356 the piglets) compared to ambient (-1.5°C) temperature.
357
358 4.3 Space allowance and farrowing hut design
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359 In order to perform pre-lying behaviour and display controlled lying down movements
360 (calm/slow movements and not sudden movements/falls) sows need space. There is limited
361 work on sow lying behaviour with the majority restricted to describing sows moving from
362 standing to lying with some pre-lying behaviours described (Baxter and Schwaller, 1983;
363 Blackshaw and Hagelsø, 1990; Wischner et al., 2010). Where sows have been observed in
364 loose systems it is evident that pre-lying behaviour involves some clustering or grouping
365 behaviours to collect the piglets (Blackshaw and Hagelsø, 1990; Schmid, 1991) and this
366 requires space for the sows to turn around (Weber et al., 2009). The optimum amount of
367 space to allow this whilst continuing to protect the piglets from “risky” posture changes
368 (Weary et al., 1996; Damm et al., 2005) has been an important aspect of system design.
369 Cronin et al. (1998) showed that sow behaviour is influenced by the width and the size of the
370 nesting area when lactating sows are housed in loose-housed farrowing pens. In their study in
371 the pens with a narrow nesting area sows spent more time standing, displayed a higher
372 frequency of posture changes and less grunting (during nursing) compared to sows kept in
373 wide pens. However, sows in wide pens were less likely to lean against the sloping walls
374 when lying down and higher mortality was seen in the larger pens. In addition, piglets in
375 narrow nests spent less time near the udder of the sows compared to piglets kept in wider
376 nests. Whilst Cronin et al. (1998) had reservations about the wider pen because of
377 performance they also concluded that having too narrow farrowing nests could negatively
378 affect the pre- and postpartum behaviour and reduced piglet survival. Accordingly, in
379 pregnant sows, Bøe et al. (2011) saw changes in behaviour when pens were narrowed, with
380 less turning around when the pen width was below 80% of the sow length and more lying
381 behaviour when it was below 50% of the sow length. Baxter et al. (2015), when looking at
382 the relationship between space and performance in a loose-housing system (PigSAFE), found
383 that the larger space afforded to the sow and her litter resulted in higher piglet mortality.
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384 They compared “large” and “small” versions of the same design (large = 9.7 m 2 in total with
385 a nest area of 4.0 m2, and a small =7.9 m2 in total with a nest area of 3.3 m2) and concluded
386 that although there were protective features in the nest area of both the pens (sloped walls),
387 the sow was afforded greater unobstructed floor space in the larger nest and could lie down
388 unsupported if she chose. In addition, she could roll without contacting the supportive
389 structures, which, as already discussed, is a risky behaviour for crushing (Weary et al., 1996).
390 The other risk with a larger nest space is that piglets have a greater area in which to wander
391 and become chilled when distant from heat sources. Chilled piglets are more vulnerable and
392 thus at greater risk of being crushed. Therefore, an optimum space is required to facilitate
393 freedom of movement and protect piglets. It is worth noting that both Cronin et al. (1998) and
394 Baxter et al. (2015) had pen designs incorporating areas in addition to the nest and these areas
395 allowed the sows to perform other behaviours away from the piglets. This is the case in
396 outdoor production, where most of the sow’s activity will be performed away from the hut
397 and therefore posing less risk to the piglets.
398 Two of the most widely used hut designs in outdoor pig production are the A-frame hut and
399 the arc hut (Figure 1). The A-frame hut measures ~4 m 2 and the arch hut ~4.8 m2. Because
400 both hut designs are smaller at the top, the space available for the sow is less. Therefore, the
401 A-frame hut and the arch hut (when provided with straw), resemble the narrow pens studied
402 in Cronin et al. (1998). It is therefore possible that sows kept in such huts also display the
403 previously mentioned behavioural changes. Due to the large provision of straw in outdoor
404 herds during winter, the behavioural changes may be more pronounced in this season.
405 In accordance with Cronin et al. (1998), studies on farrowing huts indicate that larger huts are
406 often characterized as the better huts compared to small huts (e.g. Berger et al., 1997;
407 McGlone and Hicks, 2000; Honeyman and Roush, 2002). This could be due to the sows
408 being better able to display pre-lying behaviour and controlled lying down movements
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409 resulting in less piglet crushing. In addition to sufficient space, providing sows with the
410 possibility to lean against something when they attempt to lie down may also lower crushing
411 risk. Marchant et al. (2001) showed that when sows had nothing to lean against, 36 % of the
412 lying down cases resulted in dangerous situations, and 15 % resulted in crushing of piglets,
413 compared to 4 % dangerous situations and 0.5 % crushing when sows had something to lean
414 against. In both the A-frame and the arch hut the sides slope inwards (at the top). Studies on
415 indoor loose housed sows have focused on walls, which slope the opposite way (Damm et al.,
416 2006; Baxter et al., 2015). It is possible that the sides in the A-frame and arch huts are less
417 suited as support for sows than the sloping walls known from the indoor production. One
418 could expect the sloping walls in the aforementioned farrowing huts to provide no support
419 during the part of the lying down movement where support is actually most needed (when
420 muscular control in the hind quarters is required), because the sides of the hut slope in the
421 “wrong” direction. Thereby, it is likely that the sow in the last stage of the lying down
422 movement loses contact with the hut wall. Whether the sides of these farrowing huts provide
423 enough support for the sows when they lie down has not yet been studied.
424
425 5 Possible means to reduce piglet mortality
426 5.1 Early-life interventions and piglet management
427 Several studies show that the majority of stillborn piglets die during parturition (Leenhouwers
428 et al., 1999; Marchant et al., 2000; Rangstrup-Christensen et al., 2018b). The use of birth
429 assistance could therefore provide an opportunity for saving viable piglets, which suffer
430 hypoxia during prolonged parturitions, in outdoor systems. Indoors, it is often part of normal
431 farm routines to perform birth assistance during long parturitions and studies have
432 documented the effectiveness of this management practise in reducing stillbirth risk. For
Page 18 of 35
433 instance, studies report that total mortality can be lowered by as much as 50 % (indoor
434 systems; White et al., 1996; Christison et al., 1997; Andersen et al., 2009) by implementing
435 systematic birth supervision and caretaking of less viable piglets. Furthermore, White et al.
436 (1996) showed that the proportion of stillborn piglets (not specified how these were
437 identified) was 15.6 % and 32.1 % of the total piglet mortality for sows subjected to or not
438 subjected to birth assistance, respectively. Berger et al. (1997) compared outdoor pig
439 producers with either high or low piglet mortality. They found that herds, which provided
440 birth assistance and supervised parturitions actually had higher piglet mortality. Whether this
441 increased mortality was caused by the birth assistance as such is not known. There is a
442 possibility that the presence of humans at the time of parturition constitutes a disturbance for
443 the sows (which is a known stressor around parturition - Lawrence et al., 1997) and thus
444 could actually be counterproductive in some cases. Studies investigating systematic use of
445 birth supervision and assistance outdoors are needed to establish whether this management
446 practise is beneficial for piglet survival in outdoor production where animals are not as
447 habituated to the presence of humans as sows housed indoors (Schild et al., 2019b).
448 Due to the design of the current farrowing huts (e.g. A-frame and arch huts) it is difficult, and
449 may be dangerous for the caretaker, to supervise the parturitions and provide birth assistance
450 effectively. Schild et al. (2019b) compared sow behaviour during the first three hours of
451 parturition when sows gave birth in two hut designs, the traditional A-frame hut and a
452 communal hut (housing four sows individually but under the same roof) with better
453 possibilities for supervision and access to the animals. The study showed that hut design had
454 only a minor impact on sow behaviour. Sows in communal huts spent more time standing but
455 no effect of hut design was found on the duration of lying or the frequency of posture
456 changes. The authors proposed that use of communal huts (with individual housing) could
Page 19 of 35
457 hold potential for implementing systematic birth supervision and assistance in outdoor
458 production.
459 Huts with increased supervision and intervention possibilities would also make it easier to
460 conduct cross-fostering outdoors. Cross-fostering in outdoor pig production systems has only
461 received little scientific attention. In the study by Prunier et al. (2014a) factors such as “lack
462 of batch farrowing, few sows per batch, difficulty to transfer piglets from one sow to the
463 other one, especially outdoors and lack of the farmer’s willingness to perform cross fostering
464 in order to respect the natural behaviour of the sow” were listed as reasons for not
465 implementing cross-fostering. Due to the use of highly prolific sows in outdoor production
466 and consequently large birth litter sizes, use of cross-fostering may be used to even out litters
467 thereby limiting piglet competition at the udder, which would benefit piglet survival.
468
469 5.2 Use of other genetics
470 There is a positive correlation between birth litter size and parturition duration (e.g. Baxter et
471 al., 2009; Schild et al., 2019b). Therefore, another way to reduce the occurrence of long
472 parturitions could be the use of less prolific sows. Schild et al. (2019b) compared the
473 parturition duration of DanBred Landrace Yorkshire hybrid crosses (DanBred) to that of
474 Topigs Norsvin Landrace Z-line (Yorkshire) hybrids (TN70). Numerically, DanBred sows
475 had longer parturitions in their second parity (Figure 2), but no significant difference could be
476 shown between the two hybrids. The authors suggested that greater differences in parturition
477 duration may be expected in the later parities as litter size increases with sow parity (Koketsu
478 et al., 1999; Quesnel et al., 2008; Hales et al., 2014) and litter size and parturition duration
479 are correlated (Baxter et al., 2009; Schild et al., 2019b).
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480 Aside from the benefit for reducing stillbirth, use of less prolific sow genetics could also
481 affect the viability of the piglets born alive. Schild et al. (2020) compared piglet
482 characteristics in piglets born to DanBred sows to those of piglets born to TN70 sows. The
483 TN70 sows gave birth to fewer piglets than the DanBred sows, their piglets were heavier at
484 day 1 and 3 pp and had a higher rectal temperature on day 1 pp. Furthermore, piglets born to
485 sows in first parity (irrespective of sow hybrid) and of the DanBred hybrid genetics had
486 greater odds of displaying signs of IUGR, also TN70 sows had more functional teats when
487 compared to DanBred sows (Schild et al., 2020). High vitality is required of piglets in a
488 system with outdoor farrowing where management initiatives such as drying of the neonates,
489 provision of heat and confinement of the sow are not used. Therefore, sows giving birth to
490 piglets displaying traits of increased viability may be beneficial in outdoor systems. Studies
491 suggest that the body composition and physical maturity at birth could have been altered by
492 the intense selection in conventional pig breeds (Herpin et al., 1993; Canario et al., 2007;
493 Miles et al., 2012) resulting in piglets being less mature at birth. Pig breed also affects the
494 thermal tolerance of piglets (Foley et al., 1971; Herpin et al., 2004) and Foley et al. (1971)
495 found wild boar piglets to be more cold-resistant than domestic piglets. Use of other pig
496 breeds could be another means for securing birth of more viable piglets in outdoor systems.
497 Wild boar piglets also have the additional protection of being born with pelage which offers
498 additional thermal protection that typical domestic piglets do not have (Foley et al., 1971).
499
500 5.3 Climate and grass cover around parturition
501 Provision of means, allowing e.g. farrowing and lactating sows to perform thermoregulatory
502 behaviour during summer, such as access to shade and a wallow, as is required in Denmark,
503 may benefit sows prior to parturition and during lactation. In Denmark, inclusion of trees
Page 21 of 35
504 (e.g. poplars and willows) in outdoor pig production is gaining ever more interest. One way
505 to bring down hut temperature could therefore be to move the farrowing huts into the tree
506 area in order to shade the hut (Jakobsen, 2018; Schild, 2018). Sows provided with access to
507 shade (constituted by an area with poplar trees) in their farrowing field were lying less inside
508 their hut at high compared to low hut temperatures (Schild et al., 2018). Furthermore, once
509 inside the area with poplar trees, sows were more often observed lying at high compared to
510 low hut temperatures, indicating sows may have used the shaded area for thermoregulation
511 (Schild et al., 2018). Blackshaw and Blackshaw (1994) also found increased shade seeking
512 and saw more pigs lying in the shade when temperature increased. However, due to the sow’s
513 motivation to stay in the nest during parturition and in the first week pp (sows remained in or
514 close to the nest the first 9 days pp; Jensen, 1986) sows may not benefit from access to shade
515 and wallow during these periods. Measures to bring down hut temperature, during periods
516 where sows are motivated to remain in the hut, may be needed e.g. to lower stillbirth risk
517 (Schild et al., 2019a). Global temperature is rising and the “warming has resulted in an
518 increased frequency, intensity and duration of heat-related events, including heatwaves in
519 most land regions” (IPCC, 2019). Furthermore, these heat-related events are projected to
520 continue to increase through the 21st century (IPCC, 2019). This development in global
521 temperature calls for more attention to the problem of hyperthermia in sows.
522 Painting the huts with solar reflective paint is customary in e.g. Australia. In a pilot study the
523 temperature was recorded inside an A-frame hut, which was painted metal grey (average
524 32.2°C, range 20.1-46.0°C) and inside a hut painted with white solar reflective paint (average
525 30.1°C, range 19.6-41.6°C) (Schild, 2018). There was a numeric reduction in mean and max
526 hut temperature in the white-painted hut compared to the grey-painted hut. Thus, there may
527 be potential benefits of painting farrowing huts with solar reflective paint as a means to bring
Page 22 of 35
528 down hut temperature, this could be relevant in systems where shading e.g. under trees is not
529 possible.
530 Producers may vary the amount of straw provided to the farrowing huts depending on
531 weather conditions and season (e.g. Schild et al., 2019a). In a survey of outdoor pig breeding
532 herds, Berger et al. (1997), found a negative correlation between piglet loss and the amount
533 of straw provision. Although it is hard to tell the cause-effect relationship in such a study,
534 their results suggested 22 kg of straw as a minimum requirement to reduce piglet loss. Straw
535 has high insulating capabilities as indicated by Mount (1967) who found lower heat loss to
536 the floor (reduced by 41%) in pigs (age 0-6 days of age) having 2.5 cm bedding compared to
537 pigs housed directly on concrete. Furthermore, Pedersen et al. (2016) found a reduction in the
538 immediate pp drop in rectal temperature in piglets placed on a 30-cm layer of dry straw
539 compared to piglets placed on a solid concrete floor (minimum rectal temperature for piglets
540 on straw 35.9°C vs concrete 34.0°C).
541 Berger et al., (1997) found a relationship between grass-cover in the paddock and piglet
542 mortality. The authors suggested that sows housed on poor grass cover may have dragged
543 mud into the hut whereby humidity in the nest was increased. This emphasizes that a proper
544 nest microclimate may be key in avoiding hypothermia among the neonatal piglets during
545 low ambient temperatures in systems with outdoor farrowing. In addition, Berger et al. (1997)
546 proposed that the bacterial load in the nest could be increased when more mud was dragged
547 in by the sow. It is also possible that good grass cover provides sows with access to nutrients,
548 which may improve their nutritional balance in energy and protein (e.g. pregnant sows
549 housed on pasture obtained both energy and protein e.g. SID lysine from grazing (Eskildsen
550 et al., Accepted)) and also in micronutrients.
551
Page 23 of 35
552 6 Perspectives and conclusions
553 There are various causes for mortality in pig production systems with outdoor farrowing,
554 many of which appear related to the use of highly prolific sows and increased birth litter
555 sizes. The large litters are related to prolonged parturitions and the birth of less viable piglets
556 both of which are hard to manage under outdoor conditions. Initiatives are needed to increase
557 piglet survival and several are proposed based on this review. Some solutions can readily be
558 adopted with the current production systems whereas other are suggestions for future
559 development and implementation. When considering the solutions, which may be adopted in
560 today’s housing systems, firstly, producers should focus on managing the body condition of
561 their sows as fat sows and increasing body weight is related to increased piglet mortality.
562 Secondly, assuring proper ventilation in the huts and/or adopting other means to lower hut
563 temperature during warm weather (e.g. shading the huts) is also proposed as a means to lower
564 piglet mortality. Lastly, systematic use of cross fostering and nurse sows (specifically in
565 countries with large litter sizes) are suggested as a way to lower piglet competition at the
566 udder and to lower the need for systematic euthanasia or starvation of surplus piglets. To
567 achieve long-term improvements in piglet survival in outdoor pig production, three strategies
568 are suggested; one is to use less prolific sow genetics and/or focus breeding goals for organic
569 sows on piglet survival and robustness towards thermal changes rather than on the number of
570 piglets per litter. A second suggestion is to change the farrowing hut design to allow easier
571 interventions by animal caretakers e.g. to perform birth assistance and caretaking of the
572 neonates (Schild, 2018; Schild et al., 2019b). A third suggestion, in need of further research,
573 is to develop automated surveillance systems (i.e. Precision Livestock Farming tools) to assist
574 the caretaker to identify animals at risk, e.g. identify sows with postpartum dysgalactia
575 syndrome (PDS) or with signs of heat stress. Implementing all these initiatives would be ideal
576 and would likely improve animal welfare and benefit piglet survival. Use of less prolific sows
Page 24 of 35
577 may have several benefits, as a smaller litter size would reduce the risk of: 1) hypothermic
578 piglets by decreasing the percentage of small piglets, 2) the sow having more piglets than
579 functional teats, and 3) sows suffering from hyperthermia by lowering the lactation output
580 required to feed the piglets. Due to the rising global temperature and expected increase in the
581 frequency, intensity and duration of heat-waves (IPCC, 2019), lowering the risk of
582 hyperthermia among outdoor sows appears essential if the welfare of the sow and her litter is
583 to be secured in the future.
584
585 Acknowledgements, Funding
586 The writing of this review was partly supported by the funding by the Green Development
587 and Demonstration Programme under the Ministry of Food, Agriculture and Fisheries,
588 Denmark projects VIPiglets J.nr. 34009-13-0679 and PorganiX J.nr. 34009-17-1297.
589
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934
935
Page 33 of 35
936 Figure 1 Examples of the common hut types used in organic and free-range pig production
937 with outdoor farrowing. To the left a picture of an arch hut and to the right a picture of an A-
938 frame hut.
939
Page 34 of 35
940 Figure 2. The parturition duration in 1st and 2nd parity Danbred (raw mean±standard error;
941 16.8±0.8 and 20.2±1.1 total born, respectively) and Topigs Norsvin (15.1±0.6 and 16.8±0.6
942 total born, respectively) crossbred sows (reproduced after Schild et al., 2019b).
943
944
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1 A review of neonatal mortality in outdoor organic production and possibilities to

2 increase piglet survival

3 Sarah-Lina Aa. Schild1*, Emma M. Baxter2, Lene J. Pedersen3

6 Sundsvägen 16, 23053 Alnarp, Sweden

8 West Mains Road, Edinburgh, EH9 3JG, United Kingdom

11 *Corresponding author: Sarah-Lina Aa. Schild. Email: sarah.lina.schild@slu.se

15  A consistent problem related to mortality appears to be large litter sizes

16  Optimise breeding strategies by using less prolific genetics

17  Select for improved maternal behaviour and piglet robustness

20 animal welfare, sow genetics

32 viable piglets, as is common in indoor systems, is more difficult to apply in outdoor

53 crushing, starvation and infection (Rangstrup-Christensen et al., 2018b). As discussed by

59 their physiology, natural behavior and well-being“ (IFOAM, 2005).

61 allow animals increased opportunity to express species-specific behaviour. Both outdoor

62 access and possibility of performing species-specific behaviour are qualities, which

65 27,672 survey respondents, Eurobaromenter, 2016). However, the extensive housing

70 possibilities for improving piglet survival.

72 2. Sow risk factors for piglet mortality

73 2.1 The course of parturition and the sow´s physical condition

88 parturitions in multiparous (235.4±104.6 minutes) compared to primiparous (157±81.8

150 viability of their live born littermates.

152 2.2 Sow health and nutrition

157 al., 2013).

182 and water intake.

184 2.3 Maternal behaviour

212 fatigue, especially the older animals.

235 that crushing mainly occurs after parturition is completed.

237 3 Piglet and litter characteristics influencing neonatal mortality

263 thereby increasing the risk of starving piglets.

265 4 Housing environment and neonatal mortality

266 4.1 Thermal conditions

290 accompanied by ~1°C increase in maximum sow surface temperature).

293 performing thermoregulatory behaviour. For instance, in Denmark specifications are

306 between insulated and uninsulated huts.

333 insulated ~11 to ~14°C/uninsulated ~9 to ~22°C; summer insulated ~12 to ~30°C/uninsulated

345 temperature for both sows and piglets.

356 the piglets) compared to ambient (-1.5°C) temperature.

358 4.3 Space allowance and farrowing hut design

397 and therefore posing less risk to the piglets.

425 5 Possible means to reduce piglet mortality

426 5.1 Early-life interventions and piglet management

469 5.2 Use of other genetics

479 are correlated (Baxter et al., 2009; Schild et al., 2019b).

500 5.3 Climate and grass cover around parturition

540 on straw 35.9°C vs concrete 34.0°C).

550 et al., Accepted)) and also in micronutrients.

583 to be secured in the future.

585 Acknowledgements, Funding

591 AHDB Pork, 2019. Outdoor Breeding Herd. Available: https://pork.ahdb.org.uk/prices-stats/costings-

746 IFOAM, 2005. Principles of organic agriculture: Available: https://www.ifoam.bio/en/organic-

783 LBK nr 51 af 11/01/2017, 2017. Announcement of legislation on outdoor housing of pigs

938 frame hut.

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