Prolonged nest building increase the reproductive outcome in American female mink

Highlights

• Mink females are motivated for non-maternal nest building during winter/spring.

• Provision of nesting material only on the wired nest box lid limits nest building.

• Non-maternal nest building prior to mating tends to reduce stress hormone levels.

• Maternal nest building steadily increases through the gestation period.

• Prolonged easy access to nesting material increases reproductive output markedly.

Abstract

The timing of the onset of maternal-related nest building in American mink is unknown, and it is expected that farmed mink are highly motivated to perform nest building during times with restricted access to nesting material on mink farms. Not fulfilled motivations due to thwarting can lead to stress response with increased HPA-axis output and performance of abnormal behaviour. We aimed to investigate when maternal nest building have onset and to test how prolonged access to nesting material influences dams stress response and reproductive outcome. We set up two groups that differed in timing of allocation of nesting material in the cage: group ALWAYS from 15 January and group REGULAR from 23 March. On 16 January after allocation of nesting material to ALWAYS, the mink built advanced nests, and their nest scores (P < 0.001) and nest temperature (P < 0.001) stayed significantly higher through to 23 March. When both groups had access to nesting material, from 23 March through birth, no difference was found in nest score (P = 0.28) and temperature (P = 0.27). ALWAYS mink females had better reproduction outcome: offspring survival (P = 0.007) and litter size (in average +1.2 young) Day 7 after birth (P = 0.021). Additionally, access to nesting material during winter/early spring (group ALWAYS) tended to reduce females’ faecal cortisol metabolite concentrations (FCM; P  = 0.075) and the performance of active behaviour including stereotypic behaviour (P = 0.008). After mating, maternal nest building was documented as the nest scores increased through the period 24 March to Day 2 after birth. During this period, when both groups had equal access to nesting material, no differences was found in FCM, stereotypic and active behaviour, nest score and nest climate. In conclusion, the current study demonstrated for the first time that adult mink females are motivated for nest building prior to mating, during winter/early spring, thus it is not only a maternal behaviour. Further, prolonged access to nesting material in the cage had a stress-reducing effect and a positive long-term effect on the reproductive outcome in farmed mink.

Introduction

In captivity, farm mink (Neovison vison) may experience periods where they cannot perform behavioural patterns they are motivated for. Such periods can elicit acute and chronic stress (Jensen and Toates, 1997) and thus decrease welfare. In the current study, we investigated the period where the mink females are expected to develop motivation for performing maternal-related nest building. It is well-known that mated mink females are highly motivated to perform nest building behaviour during most of the gestation period from shortly after second mating through to after birth (Day -36 to Day 7; Day of birth = 0; Malmkvist and Palme, 2008, 2015). However, the timing of the onset of maternal-related nest building is unknown, as pregnant mink females in previous studies built nests within one day after the first allocation of nesting material during the gestation period, i.e. straw into the cage (studied after mating, from March 23; Malmkvist and Palme, 2015). The instant nest building upon access to straw made us suspect that these mink could be highly motivated for nest building even earlier, due to either thermoregulation or early onset of maternal nest building post-mating as seen in golden hamsters and mice (Richards, 1969; Lynch and Possidente, 1978; Broida and Svare, 1982). Until now, provision of straw or other nesting materials for female mink selected for breeding has only been studied in the reproductive season, more specifically from after second mating until after delivery. The authors concluded that access to nesting material in the cage reduces the mink dams’ level of stress hormone (measured as FCM: faecal cortisol metabolites) during the gestation period (Malmkvist and Palme, 2015). The reduction in FCM could be due to either 1) performing highly motivated behavioural patterns regarding nest building, 2) having access to a proper nest or 3) a combination of the two factors. Access to straw, an artificial nest or a combination of both reduced postpartum FCM and had a positive effect on the reproduction outcome compared to a group with less nest building possibility and barren nests (Malmkvist and Palme, 2008).

Preventing animals from performing highly motivated behaviour can results in stress responses and/inclusive abnormal behaviour (Reviewed in, Jensen and Pedersen, 2008). Development of abnormal behaviours due to prevention from performing of highly motivated behaviours is seen in e.g. pigs prior to parturition, when prevented from nesting material and mobilization they start to bar bites (Cronin et al., 1994) and mink prevented from oral manipulation of feed performed more stereotypy and fur-chewing when fed finely ground feed compared to chunky feed (Malmkvist et al., 2013). That the abnormal behaviours was due to frustration stress was supported by both immobilisation in pigs and finely ground feed shown increases HPA-axis output (Cronin et al., 1991; Jarvis et al., 1997, 2002; Oliviero et al., 2008; Malmkvist et al., 2013). These results support the hypothesis that lack of access to nesting material for nest building or lack of having access to a proper nest may acts as a stressor for farm mink females shortly after mating.

Prevention of nest building can negatively influence not only pregnant mink females’ welfare, by inducing stress and frustration due to not performing motivated behaviour, but also their reproductive success. Generally, mink females with a high level of FCM give birth to litters with fewer young (Malmkvist and Palme, 2008). Further, pregnant mink females not provided with material suited for nest building behaviour had more variable parturitions, i.e. with an increased standard deviation of the inter-birth interval (Malmkvist and Palme, 2008). Higher S.D. of the inter-birth interval is considered indicative of birthing problems and correlates with higher early offspring mortality, including stillbirths in mink as well as pigs (Pedersen et al., 2006; Malmkvist et al., 2007). Likewise, dams awareness towards offspring in need correlated with offspring survival, indicative of the importance of maternal care (Malmkvist and Houbak, 2000). How treatments affect maternal care is tested by difference in offspring retrieval test in current study.

Total offspring mortality on mink farms is hard to estimate in practice; percentages (including stillborn and liveborn offspring) are reported to be 20% (over 6 weeks; Schneider and Hunter, 1993), 28.7% (over 4 weeks; Martino and Villar, 1990) and 28.3% (over 1 week in a study with no man-made intervention; Schou and Malmkvist, 2017). Stillbirths account for around half of the early offspring mortality (proportion of stillborn 37–53%; Schou and Malmkvist, 2017; Malmkvist et al., 2007; Schneider and Hunter, 1993). Stillborn and liveborn mortality seem to be two sides of the same coin as litters with stillborn offspring are in greater risk of experiencing mortalities among the liveborn (Schou and Malmkvist, 2017), which could indicate that the reason for offspring mortality is a dam trait, maybe due to the dams stress response. Stillborn offspring are generally found fully developed (Malmkvist et al., 2007), which indicates that the mortality is occurring close to or during the parturition. Liveborn offspring mortality mainly occurs in the first week after birth (62%; Martino and Villar, 1990) with the first three days accounting for above 90% of the first week mortality (Malmkvist et al., 2007; Schou and Malmkvist, 2017). A majority of the dead offspring have no signs of physical lesions, congenital defects or infection (Martino and Villar, 1990; Schneider and Hunter, 1993). Thus, a relatively high number of apparently vigorous offspring die during the first week after birth. The correlation between stillborn and liveborn offspring mortality indicates that some factors or traits occurring before birth cause offspring mortality. Therefore, we suggest that mink females’ behaviour and stress experienced prior to mating and during the gestation period could play a role in determining early offspring survival for both liveborn and stillborn offspring.

We aimed to enhance the understanding of influences on early offspring survival in farm mink by conducting a study focussing how prolonged access to nesting material affect dams I) nest building (nest score and in-nest climate), II) stress (FCM, abnormal behaviour, offspring-retrieval) and III) reproductive outcome inclusive offspring growth. We hypothesised that female mink are motivated for maternal nest building earlier than 23 March (the earliest time for straw provision in previous studies). Further, we expected that prolonged access to nest building material would reduce mink females’ stress response and improve their reproductive outcome.