Elsevier

Psychoneuroendocrinology

Volume 97, November 2018, Pages 59-68
Psychoneuroendocrinology

Progressive habituation to separation alleviates the negative effects of weaning in the mother and foal

https://doi.org/10.1016/j.psyneuen.2018.07.005Get rights and content

Highlights

  • Early and definitive separation of an offspring from its mother is detrimental.

  • These negative effects can be alleviated by progressive habituation to separation.

  • Progressive habituation reduced stress to the mothers and their foals.

  • It also favored a less fearful and more curious personality in foals.

  • Expression of 22 genes discriminated the foals based on the weaning method.

Abstract

Early and definitive separation between offspring and their mothers has negative consequences on behavioral and physiological responses. This study compared sudden and definitive weaning (Sudd group, N = 16) and weaning involving progressive habituation to separation using a fence line during the month preceding definitive separation (Prog group, N = 18). The impact of these two methods was assessed in both foals and their mothers through behavioral and biological parameters, including salivary cortisol, telomere length and blood transcriptomes. On the day of definitive separation, Prog foals neighed and trotted less and presented lower cortisol levels than Sudd foals. The weaning type also acted on the foals’ personality development; Prog foals became more curious, less fearful and less gregarious than Sudd foals, and the effects remained visible for at least 3 months. In principal component analysis, the Sudd and Prog groups were well separated along a factor where fear, reactivity and gregariousness correlated with high cortisol levels, but curiosity was associated with an increased telomere length and higher expression of genes involved in mitochondrial functions. Progressive weaning was also beneficial in mares. Principal component analysis showed that most Sudd group mares had higher cortisol levels and displayed more alert postures, neighs and activity on the day of weaning, indicating higher stress levels, while Prog mares had profiles that were characterized by more time spent resting on the day of weaning and longer telomere lengths. In conclusion, this study shows that progressive habituation to separation alleviates the negative effect of definitive weaning on both the mother and her young compared to sudden separation.

Introduction

Most farm animals undergo early weaning. In domestic horses, foals are often separated from their mothers suddenly and definitively between 4 and 6 months of age (Waran et al., 2008). This weaning differs greatly from that observed under feral conditions, in both the age at which the foal is separated and its suddenness. Under natural conditions, foals progressively stop suckling between 11 and 12 months of age, when the mother is about to give birth again, but the bond with the mother remains intact. The young usually stay in contact with their mothers until sexual maturity, although they join new conspecific groups (Tyler, 1972).

Early separation from the mother is known to negatively impact behavioral, neuronal and hormonal responses in the offspring. In the short term, many species express stress encountered in early weaning through various behaviors, such as increased locomotion, vocalization and stereotypies, along with physiological responses such as increased corticosteroid and catecholamine levels, decreased immune system functioning or weight loss (Latham and Mason, 2008; Newberry and Swanson, 2008; Waran et al., 2008; Weary et al., 2008). By disrupting the individual’s development, early weaning can have long term effects by programming changes in gene expression patterns through epigenetic mechanisms in the brain, which in turn lead to long-lasting behavioral and personality modifications (Rubin et al., 2014). Although personality is relatively stable in adults, it is clearly influenced in the young and is thus relatively sensitive to the environment (examples in human, dog or cattle: Goddard and Beilharz, 1986; McDevitt, 1986; Specht et al., 2011; Van Reenen et al., 2004). This phenomenon is also described in horses, whose personalities are comparatively unstable until 8 months of age (Lansade et al., 2008a, 2007).

To limit the distress induced by weaning, different methods have been proposed (Dubcova et al., 2015; Erber et al., 2012; Merkies et al., 2016; Nicol et al., 2005; Waran et al., 2008; Weary et al., 2008). A weaning method that has been tested in several domestic species consists of habituating the young to gradual separation from their mothers during the weeks prior to final weaning. The effects vary by the procedure employed, habituation period length and age at separation. In calves, this method has proven effective since it reduced vocalizations and locomotive activity, while favoring rest and feeding at weaning (Boland et al., 2008; Haley et al., 2005; Loberg et al., 2008; Price et al., 2003).

In horses, one study tested this progressive weaning (Moons et al., 2005). After being habituated to separation from their mothers at 2 to 12 weeks of age, foals were separated completely at 6 months of age. The authors hypothesized that these relatively brief separations early in the nursing period would enhance maternal behavior which subsequently reduce the impact of sudden weaning. However, these very early separations did not beneficially impact the definitive weaning. Nevertheless, it could be hypothesized that if the separations had occurred later, such as in the weeks prior to final weaning as was done in calves, they could have alleviated the detrimental effects of weaning. Furthermore, it could also be hypothesized that a progressive weaning would also likely benefit the mare, but this hypothesis has never been tested before.

The present study compared the sudden and definitive weaning commonly employed in horse rearing with gradual weaning involving a progressive habituation to separation using a fence line during the month preceding weaning. The impact of these two methods was assessed in both foals and their mothers through different parameters. During progressive separations, the mother and young’s behaviors were characterized to determine whether this procedure induced stress comparable to what was experienced at weaning. At weaning, the short-term effects of induced stress were evaluated using behavioral indicators, cortisol and pro-inflammatory cytokine measures. For a more general view of the short-term biological effects of weaning, we used a transcriptomic approach to determine gene expression profiling in blood cells as used previously in another challenging environment analysis (Lansade et al., 2014). Because long-term effects from weaning are suspected, another transcriptomic analysis was performed at 3 months post-weaning. Long-term effects of weaning were also evaluated through blood cell telomere length variation over a 6-month period, starting 3 months before and ending 3 months after weaning, since early-life stress is related to accelerated telomere length attrition in various species (Angelier et al., 2018). The effects of both weaning methods on the foals’ personalities were assessed at two days and three months post-weaning using tests specifically developed to measure horses’ personalities (Lansade and Bouissou, 2008; Lansade et al., 2008a,b,c).

Based on previous literature we made the following assumptions:

  • 1

    On the day of definitive weaning, foals weaned progressively would express less stress related behaviors (neighs, active locomotion, aggressive behaviors), more maintenance behaviors (eating, resting, grooming) and would present lower cortisol level than foals suddenly weaned.

  • 2

    During the progressive separations, animals progressively weaned would express more stress related behaviors and less maintenance behaviors.

  • 3

    After weaning, foals progressively weaned would show a decrease in reactivity towards fearful stimuli, human presence, sensory stimulations and social isolation compared to animals suddenly weaned.

  • 4

    At the physiological levels, the progressive weaning method would induce stronger long-term effects (3 months), with higher telomere lengths and a lower cortisol and a different transcriptomic fingerprints than the sudden weaning method.

Section snippets

Animals

The study involved 34 Welsh pony foals and their dams from the experimental unit of INRA (National Institute for Agricultural Research) Val de Loire Centre, Nouzilly, France. After birth, the foals and their dams lived together at pasture. At five months old, at the beginning of winter, the foals and dams were placed together in a large pen with straw bedding. At seven months old, they were housed in groups of two mothers and their foals in large loose boxes with straw bedding (

Were progressive separations stressful for foals and mares?

For the observations conducted during the separation process in foals, only one variable differed between groups: Prog group foals neighed significantly more than Sudd group foals (U = 8; P = 0.002, Table S2 in Supplementary material). However, this number was dramatically lower than that observed on the day of weaning (Fig. 2). No other behaviors differed between the two groups of foals (Table S2 in Supplementary material). Compared to Sudd mares, Prog mares were seen more frequently in front

Discussion

This study showed that training foals for weaning by habituating them to separation from the mother can alleviate stress induced by definitive weaning. The effects were observed at both behavioral and physiological levels in the foals and their dams. Some of these effects, such as those affecting the foals’ personalities may be long-lasting.

In foals, weaning is a stressful event regardless of method used, as demonstrated by the cortisol level differences before and after weaning. Nevertheless,

Funding

IFCE (Institut Français du Cheval et de l'Equitation – French Horse and Riding Institute) funded this experiment. This funding source had no role in the study design, data collection or analysis, or in preparing or submitting the manuscript.

Competing interests

The authors declare no competing interests.

Author contributions

Conceived and designed the experiments: L.L., A.F., F.R., M.V., E.G., G.B., D.S., F.L., and M.P.M; Performed the experiments: L.L., A.F., F.R., M.V., E.G., C.P., G.B., D.S., and M.P.M; Analyzed the data: L.L., A.F., F.R., M.V., G.B., D.S., and M.P.M; Wrote/reviewed the paper: L.L., A.F., M.V., E.G., C.P., G.B., D.S., A.R., N.M., F.L., and M.P.M.

Acknowledgements

We would like to thank Jean-Marie-Yvon for their assistance during the experiment. English editing was performed by “Springer Nature author services”. We thank Claire Naylies and Yannick Lippi for their contribution to microarray fingerprints acquisition and microarray data analysis carried out at GeT-TRiX Genopole Toulouse Midi-Pyrénées facility.

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