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The provision of toys to pigs can improve the human-animal relationship

Porcine Health Management volume 6, Article number: 29 (2020) Cite this article

Abstract

It is now widely recognised that a positive human-animal relationship is beneficial not only for farm animals’ welfare but also for productivity and the quality of products. A better understanding of animal emotions is an important goal in disciplines ranging from neuroscience to animal welfare science, but few reliable tools exist for measuring these emotions. In this study, whether the provision of toys to solicit play behaviour in pigs is associated with a change in the human-animal relationship and the emotional state of pigs was investigated. We involved a group of sixteen mini-pigs housed in an experimental setting and the use of a preliminary test called the ‘strange person’ test. After a Control and a Play session (with medium-sized dog toys, balls with ropes), the strange person test was performed. During the test, a person wearing a colourful overall, a hood, a mask, gloves and boots (unknown person with an odd appearance) entered the pen, where 2 mini-pigs were housed, for a 2-min video recording. The strange person test results after the Play and Control sessions were compared. The results showed that the latency to approach the person (duration in seconds) and the duration for which the pig was distant from the strange person (duration in seconds) were significantly lower after the Play session than after the Control session (Degrees of Freedom =30; Statistic of the F test =39.1; p < 0.0001 and Degrees of Freedom =15; Statistic of the F test =54.3; p < 0.0001, respectively). The duration of direct contact (duration in seconds) (Degrees of Freedom =15; Statistic of the F test =14.8; p = 0.002), the need to separate the pig from the strange person (frequency) (Degrees of Freedom =30; Statistic of the F test =9.3; p = 0.005) and the duration of tail movement (duration in seconds) (Degrees of Freedom =15; Statistic of the F test =12.6; p = 0.003) were all significantly higher after the Play sessions than after the Control sessions. Overall, the results suggest a change in the human-animal relationship after the Play sessions: the pigs seemed to be less fearful and more inclined to interact with the strange person, showing a more positive emotional state. This preliminary study suggests that the provision of toys, and more precisely, the opportunity to perform object play behaviour, and sometimes, spontaneously, social play behaviour, can improve the human-animal relationship. Additional research to explore this topic thoroughly may yield interesting results because a positive emotional state of the animals and a good human-animal relationship are essential to ensure good quality of life of farm animals.

Introduction

A human-animal relationship can be defined as the degree of relatedness or distance between animals and humans [12]. It is widely recognised since many years now that a positive human-animal relationship is beneficial not only for the welfare of farm animals but also for productivity and the quality of animal products [58]. On the one hand, a negative human-animal relationship occurs when negative handling is performed by stockpeople or any other person in contact with farm animals, such as a veterinarian. These negative interactions, like aversive interactions or perceived as threatening (e.g. moving abruptly the animals from one pen to another, tagging or weighting brusquely), can lead to many undesirable repercussions, not only for the animals but also for the industry and the consumers. One important repercussion is the fear of humans, which represents one of the factors for depressed growth and reproductive performance in commercial pigs [24]. In addition, pigs who are fearful of humans are generally the most difficult pigs to handle [22]. According to Waiblinger et al. [58], several studies showed that negative handling increases adrenal weight (indicative of chronic stress), impairs growth and reproductive performance and induces a high fear of humans, both in the laboratory [16, 24, 51] and on commercial farms [20, 21, 25]. For example, one study by Hemsworth et al. [28] with 90 commercial pigs examined the relationships between handling prior to slaughter and some measures of meat quality, and the results showed a negative correlation between the negative interactions received and the plasma glucose concentrations post-slaughter and a positive correlation between both post-slaughter plasma lactate concentrations and the light reflectance of the ham (a high reflectance indicates a pH drop during post-mortem glycolysis, which is linked to PSE meat: pale, soft, exudative) and other factors. Other studies have shown that there is a progressive increase in the potential incidence of pale, soft, exudative (PSE) and dark, firm, dry (DFD) meat in the slaughterhouse plants using more stressful handling systems (e.g. [59]). These results suggested that the behaviour of stockpeople prior to slaughter can influence meat quality.

On the other hand, regular pleasant contact with humans, which fosters a positive human-animal relationship, may result in desirable effects to the physiology, behaviour, health and productivity of farm animals [63]. Several studies showed many positive aspects, such as the reduction of stress reactions of cows during rectal palpation/insemination due to previous positive handling as well as positive, gentle interactions from the person during the procedure [57] and the improved possibility to detect oestrus behaviour in fearful sows after gentle handling [43]. In addition, gentle handling and stroking of dairy cows and heifers showed to decrease their fear of humans [5], reduce cortisol levels [19], and lower their heart rate [50] during different procedures [44]. Rault [45] showed that positive human contact led to sustained cerebrospinal fluid oxytocin elevation in pigs for 120 min, which outlasted the 15-min interaction. Additionally, Rault [45] showed that the frequency of positive interactions was correlated with an increase in cerebrospinal fluid oxytocin, providing a neurophysiological basis for a positive human-animal relationship.

Nevertheless, the question of how human contact can have a positive impact on responses to stressors and productivity is not well understood [63]. In addition, the literature on the ability of farm animals to recognise individual people is inconsistent [63]. Some studies suggested that farm animals respond the same way to different people. Hemsworth [23] compared the response of pigs to two different stockpersons who differed markedly in their nature of contact with pigs. The results suggested that pigs are unable to differentiate between different people and that aversive handling by one person makes the animals fearful of all people. In contrast, other studies [32, 54] suggested that pigs are able to recognise individual people. Thus, further research on this topic may be very useful.

The assessment of human-animal valence is essential to obtain more information about the welfare of farm animals. Many different methods and tests exist to assess the valence of the human-animal relationship and the emotional state of animals, as they are generally linked, such as the human approach test in sows [18], the qualitative behaviour assessment in sows and other species [61], the avoidance distance test in cows and other species [60], tests measuring the approach or avoidance of people (e.g., [27]), visual attention in horses [48], the presence of a stationary human test and the presence of a moving human test in sheep [8], and an adaptation of the methods of behavioural assessment in zoo animals [6].

A better understanding of animal emotions is an important goal in disciplines ranging from neuroscience to animal welfare science, but few reliable tools exist for measuring these emotions [4, 10]. Play behaviour is generally recognised as a trigger of positive emotions in mammals [30, 39], and previous studies consistently suggested that a high tail movement duration (a behaviour often seen during play) indicates positive emotions in pigs [33,34,35, 46, 47].

In this study, whether the provision of toys to solicit play behaviour in pigs was associated with a change in the human-animal relationship was investigated in an experimental setting with the use of a preliminary test called the ‘strange person’ test with minipigs, a model of domestic industrial pigs [11, 36]. Our hypothesis was that the pigs could be in a more positive affective state after playing and then the valence of the human-animal relationship could be improved.

Material and methods

The housing, husbandry and care for the animals involved in this experiment were carried out according to French and European legislation and the principles of replacement, reduction and refinement. The project, including this experimental procedure, was approved by the IRSEA’s (Research Institute in Semiochemistry and Applied Ethology) Ethics Committee (C2EA125) and the French Ministry of Research (AFCE_201609_01).

Animals and housing

The mini-pigs (Sus scrofa domesticus) (n = 16: castrated males = 8; females = 8) involved in the study were part of a new strain resulting from the cross-breeding of miniature breeds (Asian potbelly breeds: Vietnamese and Chinese) with conventional white-hair breeds (Landrace and Large White), and they were born at the Specipig (centre for breeding and biomedical research) in Barcelona, Spain. The pigs were enrolled in this study at the age of one year. The pigs were socialised to humans since the beginning of their lives: the animal-keepers fed them every day and performed the regular cares; the veterinarians and researchers visited them regularly. They were housed in an experimental and controlled system in two identical rooms (30 m2) with monitored environmental parameters: a mean ambient temperature of 22 °C, the same ventilation provided by 2 artificial ventilators in each room and 60% humidity. Two pigs of the same sex and age were housed in each pen, which had the following features: an area of 2.5 m2 (1.85 m × 1.35 m), walls and doors with a height of 0.90 m, slatted floors, a feeder and a drinker. The mini-pigs were separated into pairs after weaning to prevent fighting, so the pigs were used to being together. The pens were cleaned daily. The lights were on from 8.00 a.m. until 6.00 p.m. The pigs were fed twice a day with a special diet for mini-pigs maintained in restricted conditions for long-term trials (Special Diets Services, Paris, France) and had continuous access to drinking water.

Procedure

The study took place over four consecutive days; the animals were divided into two identical rooms with eight pigs in each room, and each day, only the animals in one room participated in the study. Thus, each animal participated in the study for a total of two days in two different situations: one Control session and one Play session. The tests were performed always at the same time, from 9:30 a.m. to 12:00 a.m. The pigs were not moved to other rooms or pens to participate in the study; they stayed in their own rooms and pens with their mates (in pairs) to avoid any stress that may occur from changing locations. During the Play sessions, the pigs stayed in their own pens (2.5 m2 of slatted floors), where two medium-sized dog toys (balls with ropes attached, Denta Fun, 7 cm/50 cm, 132 g, MonAnimalerie.net, Saint-Alexandre, France) were introduced. This type of toy was previously tested with these mini-pigs, and the toy yielded a high motivation to play when it was provided for a 10 min’ period [33]. One operator put the toys on the floor in the centre of the pen and then exited the pen, while the pigs were present in the same pen. In each pen, two toys were provided to reduce conflict due to competition. Video recordings were used to confirm that the pigs played during the Play sessions, according to previous literature [33, 34], measuring object and social play duration (Table 1). During the Control sessions, the animals were again placed in their own pens, and no toy was provided to them; this setting represented their typical housing situation, which did not have any additional stimuli. After the Control or Play session, the strange person test was performed immediately. During the test, a person wearing a colourful overall, a hood, a mask, gloves and boots (unknown person with an odd appearance) entered the pen, where 2 mini-pigs were housed, for a 2-min video recording. The person’s eyes were also covered with a dark film to prevent the pigs from seeing them. In each test, the person was dressed differently, with different colours and masks, to create novelty [26, 53]. The person was completely covered with an overall, a hood, a mask (covering also the eyes), gloves and boots, to prevent the pigs from smelling the skin or body. A tall screen was installed between the pens (the pigs were habituated to the screen) to prevent the neighbouring pigs from seeing the strange person when the test was being performed near them. Thus, the person could only be seen by the two pigs being tested. The strange person entered the pen and sat down with his or her back against the wall of the pen; the person always moved to the same position and did not move, touch or interact with the pigs in any possible way. The behaviours of each pig were recorded during the test: object play, social play, latency to approach the person, duration for which the pig was distant from the person, direct contact with the person, need to move the pig away and tail movement. All the behaviours were scored based on the continuous video recordings by two independent observers who had access to the description of each behaviour (Table 2) and an Excel matrix.

Table 1 Descriptive data of 600 s of the Play and Control sessions
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Table 2 Description of the behaviours observed in the video analysis of the strange person test (120 s)
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Statistical analysis

Data analysis was carried out using SAS 9.4 software (Copyright (c) 2002–2012 by SAS Institute Inc., Cary, NC, USA). The significance threshold was fixed at 5%, which is a standard threshold.

The reliability between the two observers who assessed the video recordings was calculated using the CORR procedure and Spearman’s or Pearson’s correlation coefficients, depending on the normality of data (normality was verified using the UNIVARIATE procedure): Spearman’s correlation coefficient was used when normality was not verified for at least one variable, and Pearson’s correlation coefficient, when normality was verified for both variables. This methodology was selected according to a study by Martin and Bateson [38].

Comparisons of the strange person test results after the Play and Control sessions were performed using mixed models, and the pen was considered a random effect. The following parameters were studied: latency to approach the person (duration in seconds), duration for which the pig was distant from the person (duration in seconds), duration of direct contact (duration in seconds), the need to separate the pig (in frequency) and duration of tail movement (duration in seconds).

For the continuous variables (latency to approach the person, duration for which the pig was distant from the person, duration of direct contact and duration of tail movement), the distribution of the variable and the model residuals were analysed using the UNIVARIATE procedure to determine whether the assumption of normality was met. If normality was verified, the raw data were used for the model using a general linear mixed model with the MIXED procedure. If the data for the variable did not follow a normal distribution, other continuous distributions were tested with the UNIVARIATE procedure. When a distribution was identified, the data were modelled with the corresponding generalised linear mixed model using the GLIMMIX procedure. When no distribution was identified, a Box-Cox transformation was applied with the TRANSREG procedure to reach normality. Whether a general linear mixed model or generalised linear mixed model was used, the best structure of the covariance matrix was selected by minimising the AICC and BIC criteria.

For the discrete variable (the need to separate the pig, in frequency), the distribution of the data was analysed to identify the best discrete distribution for modelling the data. Because the data distribution corresponded to a Poisson distribution, a Poisson mixed model was generated using the GLIMMIX procedure and the LAPLACE method for estimating parameters. When the Poisson model showed overdispersion, a negative binomial mixed model was preferred.

Results

Inter-observer reliability

The reliability between the two observers who performed the video analysis was calculated using Spearman’s or Pearson correlation coefficients (Table 3). The reliability (inter-observer agreement) was high for all the parameters.

Table 3 Inter-observer reliability between the two observers carrying out the video analysis
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Comparisons between the strange person test results after the play and control sessions

Comparisons between the strange person test results after the Play and Control sessions were analysed for all parameters. The video recordings confirmed that the pigs performed play behaviour during all Play sessions and that they did not perform play behaviour (neither object play nor social play) during Control sessions (Table 1).

Latency to approach the person (duration in seconds)

A significant difference was found between the strange person test results after the Play and Control sessions (Degrees of Freedom = 30; Statistic of the F test = 39.1; p < 0.0001; generalised linear mixed model for a lognormal distribution). More precisely, the latency to approach the person was significantly lower after the Play sessions than after the Control sessions (Table 4).

Table 4 Parameters (behaviours) analysed during the strange person test (total of 120 s): comparison between the test results after the Play sessions and after the Control sessions
Full size table

Duration for which the pig was distant from the person (duration in seconds)

A significant difference was observed between the strange person test results after the Play and Control sessions (Degrees of Freedom = 15; Statistic of the F test =54.3; p < 0.0001; general linear mixed model). The duration for which the pig was distant from the person was significantly lower after the Play sessions than after the Control sessions (Table 4).

Direct contact (duration in seconds)

A significant difference was found between the strange person test results after the Play and Control sessions (Degrees of Freedom = 15; Statistic of the F test = 14.8; p = 0.002; general linear mixed model). The duration of direct contact was significantly higher after the Play sessions than after the Control sessions (Table 4).

Need to move the pig away (frequency)

A significant difference was found between the strange person test results after the Play and Control sessions (Degrees of Freedom = 30; Statistic of the F test = 9.3; p = 0.005; generalised linear mixed model for a Poisson distribution). The need to move the pig away was significantly higher after the Play sessions than after the Control sessions (Table 4).

Tail movement (duration in seconds)

A significant difference was found between the strange person test results after the Play and Control sessions (Degrees of Freedom = 15; Statistic of the F test = 12.6; p = 0.003; general linear mixed model). The tail movement was significantly more frequent after the Play sessions than after the Control sessions (Table 4).

Discussion

This exploratory study aimed to investigate whether the provision of toys adapted to pigs to allow them to perform play behaviour was associated with a change in the human-animal relationship and their emotional state. This association was tested with a preliminary and simple test named the ‘strange person’ test, which was adapted to the present conditions.

Overall, the results suggest an improvement in the human-animal relationship after Play sessions: the pigs seemed to be less fearful, more curious and more inclined to interact with the strange person, showing a more positive emotional state based on an increase in tail movement duration (e.g., [34]). This result suggests that the provision of toys, and more precisely, the opportunity to perform object play behaviour, and sometimes, spontaneously, social play behaviour, can improve the human-animal relationship and the positive emotions of pigs.

The latency to approach the person and the duration for which the pig was distant from the person reflected the fearfulness of the animals [27] towards the strange person as well as their emotional state [3] because of two factors: the person was unfamiliar and the situation was strange for the pigs, as the person was dressed up and did not interact at all with them, which were both strange aspects for the pigs. The results showed that the latency to approach the strange person and the time the pigs spent distant from the person were shorter after playing than after the Control situation, suggesting that the animals were less fearful and in a more positive emotional state, as they were more inclined to approach the person. The results may even suggest that the animals were in a more optimistic state [41], as it can be interpreted that they preferred to approach something new rather than remain in a safe place far from it. Some studies have shown that the provision of environmental enrichment can improve the human-animal relationship and thus their approach towards humans and the ease of working with and handling them (e.g., [49]). Nevertheless, other studies suggested that enrichment objects do not affect the ease of handling pigs [7, 29]. Thus, van de Weerd and Day [56] suggested that the type of enrichment and quantity of stimuli provided influences the extent of the effect on their behaviour towards humans. This preliminary study provides more information about this topic.

The duration of direct contact with the person, which is also related to the absence or presence of fearfulness, is also linked to exploratory behaviour, as we defined it as the duration of time that the pig spent touching the strange person with the snout. By watching the video recordings thoroughly (data not shown), we observed that the most common behaviour performed by the pigs during direct contact with the person was explorative behaviour, or more precisely, the following behavioural elements: rooting, chewing and sniffing [52]. When pigs explore their surroundings, they do it with different purposes, such as to find food or a place to lie (appetitive behaviour, also named extrinsic exploration) or to obtain general information on their surroundings (intrinsic exploration) [2, 62], as in the case of the present study. Intrinsic exploration is motivated by curiosity, and it serves to keep the pig informed about the environment and the resources available in it [52]. Curiosity has been considered a positive feeling for the animals by several authors [17, 40,41,42], and according to the affective state orientation, an animal’s welfare is positive when it adapts with positive emotional experiences and/or without negative experiences during its interactions with other animals, people and the environment [14]. Thus, this result suggests that pigs were more inclined to interact with the person after playing (improvement of the human-animal relationship) and that they seemed to be in a more positive emotional state.

The need to move the pig away was significantly more frequent after the Play sessions than after the Control sessions. This parameter may be linked to the confidence of the pig and thus to their emotional state, as well as to the motivation to explore and to interact with the person. The need to move the pig was more frequent after playing, and this result supports previous findings; thus, the pigs seemed to be in a more positive emotional state and more motivated to interact with the person, even when the person was strange and unfamiliar. Nevertheless, in this case, it was a ‘negative’ aspect for the human, as it suggests that the pig was too confident and then it may be dangerous when interacting with humans, as suggested with other species like horses [9, 13]. Of course, it is a preliminary test, the results of which should be interpreted with caution, but the results seem to be in agreement with those of other studies in different species.

Finally, regarding tail movement duration, we found that the duration was significantly longer after play than after the control conditions. Some studies showed a link between an increase in tail movement duration in pigs and play behaviour or the interaction with some types of enrichment material [33, 34, 37]. In the present study, this behaviour was significantly higher after playing, not during it, which is a new finding. It has also been suggested to be an indicator of positive emotions (or an indicator of emotions with a positive valence or outcome) by several studies conducted in different conditions [33,34,35, 37, 46, 47]. The present significant difference supports the previous results about the other parameters, suggesting that the pigs were in a more positive state after playing during the strange person test than after a control situation based on the increase in tail movement duration.

Many authors have highlighted the need for more research to identify indicators of emotional states [3, 10, 39], particularly of emotional valence, to better assess animal welfare [15]. The present study also provides more information about some indicators of positive emotions, which may be useful to improve animal welfare assessments in a feasible way, as well as some preliminary tools to assess the human-animal relationship.

Some limitations of the study would be the sample size and the use of mini-pigs instead of domestic commercial pigs. Nevertheless, these controlled and experimental conditions allowed us to obtain significant results, which open some doors for future studies.

Finally, this preliminary study suggests that the provision of toys to pigs can improve the human-animal relationship, which, in combination with other methods, such as being nice to the pigs, may be a feasible and simple method of improving this relationship. Additional research to explore this concept thoroughly may yield interesting results because a positive emotional state of the animals and a good human-animal relationship are essential to ensure the quality of life of farm animals as well as the quality of the final product. Other factors may be of interest to study, like the potential sex and/or hormonal differences in some behaviours, like in fear reactions, as already shown in other species like sheep [1, 55]. Future studies with domestic commercial pigs in farm conditions may be of interest, with an adaptation of the ‘strange person’ test, in order to investigate if the results would be the same than in the experimental setting with mini-pigs.

Conclusions

In conclusion, this exploratory study suggests that play behaviour due to the provision of toys seems to improve the human-animal relationship and the emotional state of pigs. More research in farm conditions, with this method and other methods, should be performed to provide more information about this potentially interesting and feasible method of improving the human-animal relationship and emotional state of pigs.

Availability of data and materials

The datasets during and/or analysed during the current study available from the corresponding author on reasonable request.

References

  1. Acevedo-Rodriguez A, Mani SK, Handa RJ. Oxytocin and estrogen receptor β in the brain: an overview. Front Endocrinol. 2015;6:160.

    Google Scholar 

  2. Berlyne DE. Conflict, arousal and curiosity. New York: McCraw-Hill Book Company; 1960.

    Google Scholar 

  3. Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, Bakken M, Veissier I, Aubert A. Assessment of positive emotions in animals to improve their welfare. Physiol Behav. 2007;92(3):375–97.

    CAS  PubMed  Google Scholar 

  4. Boissy A, Lee C. How assessing relationships between emotions and cognition can improve farm animal welfare. Rev Sci Tech Off Int Epiz. 2014;33(1):103–10.

    CAS  Google Scholar 

  5. Breuer K, Hemsworth P, Coleman G. The effect of positive or negative handling on the behavioural and physiological responses of nonlactating heifers. Appl Anim Behav Sci. 2003;84:3–22.

    Google Scholar 

  6. Claxton AM. The potential of the human–animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Appl Anim Behav Sci. 2011;133(1–2):1–10.

    Google Scholar 

  7. Day JEL, Spoolder HAM, Burfoot A, Chamberlain HL, Edwards SA. The separate and interactive effects of handling and environmental enrichment on the behaviour and welfare of growing pigs. Appl Anim Behav Sci. 2002;75:177–92.

    Google Scholar 

  8. Destrez A, Coulon M, Deiss V, Delval E, Boissy A, Boivin X. The valence of the long-lasting emotional experiences with various handlers modulates discrimination and generalization of individual humans in sheep. J Anim Sci. 2013;91(11):5418–26.

    CAS  PubMed  Google Scholar 

  9. Doherty O, McGreevy PD, Pearson G. The importance of learning theory and equitation science to the veterinarian. Appl Anim Behav Sci. 2017;190:111–22.

    Google Scholar 

  10. Duncan IJH. Science-based assessment of animal welfare: farm animals. Rev Sci Tech Off Int Epiz. 2005;24(2):483–92.

    CAS  Google Scholar 

  11. Ellegaard L, Cunningham A, Edwards S, Grand N, Nevalainen T, Prescott M, Schuurman T. Welfare of minipig with special reference to use in regulatory toxicology studies. J Pharmacol Tox Met. 2010;62(3):167–83.

    CAS  Google Scholar 

  12. Estep DQ, Hetts S. Interactions, relationships and bonds: the conceptual basis for scientist-animal relations. In: Davis H, Balfour AD, editors. The inevitable bond-examining scientist-animal interactions. Cambridge: CAB International; 1992. p. 6–26.

    Google Scholar 

  13. Fiedler J, McGreevy P. Reconciling horse welfare, worker safety, and public expectations: horse event incident management systems in Australia. Animals. 2016;6(3):16.

    Google Scholar 

  14. Fraser D. Assessing animal welfare at the farm and group level: the interplay of science and values. Anim Welf. 2003;12:433–43.

    CAS  Google Scholar 

  15. Freymond SB, Briefer EF, Zollinger A, Gindrat-von Allmen Y, Wyss C, Bachmann I. Behaviour of horses in a judgment bias test associated with positive or negative reinforcement. Appl Anim Behav Sci. 2014;158:34–45.

    Google Scholar 

  16. Gonyou HW, Hemsworth PH, Barnett JL. Effects of frequent interactions with humans on growing pigs. Appl Anim Behav Sci. 1986;16:269–78.

    Google Scholar 

  17. Green TC, Mellor DJ. Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts. N Z Vet J. 2011;59(6):263–71.

    CAS  PubMed  Google Scholar 

  18. Hemsworth PH, Brand A, Willems P. The behavioural response of sows to the presence of human beings and its relation to productivity. Livest Prod Sci. 1981;8:67–74.

    Google Scholar 

  19. Hemsworth P, Barnett J. The effects of handling by humans at calving and during milking on the behaviour and milk cortisol concentrations of primiparous dairy cows. Appl Anim Behav Sci. 1989;22:313–26.

    Google Scholar 

  20. Hemsworth PH, Barnett JL, Coleman GL, Hansen C. A study of the relationships between the attitudinal and behavioural profiles of stockpersons and the level of fear of humans and reproductive performance of commercial pigs. Appl Anim Behav Sci. 1989;23:301–14.

    Google Scholar 

  21. Hemsworth PH, Barnett JL, Coleman GJ. The human–animal relationship in agriculture and its consequences for the animal. Anim Welf. 1993;2:33–51.

    Google Scholar 

  22. Hemsworth PH, Coleman GJ, Barnett JL. Improving the attitude and behaviour of stockpersons towards pigs and the consequences on the behaviour and reproductive performance of commercial pigs. Appl Anim Behav Sci. 1994a;39(3–4):349–62.

    Google Scholar 

  23. Hemsworth PH, Coleman GJ, Cox M, Barnett JL. Stimulus generalization: the inability of pigs to discriminate between humans on the basis of their previous handling experience. Appl Anim Behav Sci. 1994b;40:129–42.

    Google Scholar 

  24. Hemsworth PH, Coleman GJ. Human–livestock interactions: the stockperson and the productivity of intensively farmed animals. Wallingford: CAB International; 1998.

    Google Scholar 

  25. Hemsworth PH, Pedersen V, Cox M, Cronin GM, Coleman GJ. A note on the relationship between the behavioural response of lactating sows to humans and the survival of their piglets. Appl Anim Behav Sci. 1999;65:43–52.

    Google Scholar 

  26. Hemsworth PH. Ethical stockmanship. Aust Vet J. 2007;85(5):194–200.

    CAS  PubMed  Google Scholar 

  27. Hemsworth PH, Coleman GJ, Barnett JL, Borg S. Relationships between human–animal interactions and productivity of commercial dairy cows. J Anim Sci. 2000;78:2821–31.

    CAS  PubMed  Google Scholar 

  28. Hemsworth PH, Barnett JL, Hofmeyr C, Coleman GJ, Dowling S, Boyce J. The effects of fear of humans and pre-slaughter handling on the meat quality of pigs. Aust J Agric Res. 2002;53(4):493–501.

    Google Scholar 

  29. Hill J, McGlone JJ, Fullwood S, Miller M. Environmental enrichment influences on pig behavior, performance, and meat quality. Appl Anim Behav Sci. 1998;57(1):51–68.

    Google Scholar 

  30. Horback K. Nosing around: play in pigs. Anim Behav Cogn. 2014;2:186.

    Google Scholar 

  31. Kiley-Worthington M. The tail movements of ungulates, canids and felids with particular reference to their causation and function as displays. Behaviour. 1975;56(1-2):69–114.

  32. Koba Y, Tanida H. How do miniature pigs discriminate between people? The effect of exchanging cues between a non-handler and their familiar handler on discrimination. Appl Anim Behav Sci. 1999;61(3):239–52.

    Google Scholar 

  33. Marcet-Rius M, Cozzi A, Bienboire-Frosini C, Teruel E, Chabaud C, Monneret P, Leclercq J, Lafont-Lecuelle C, Pageat P. Selection of putative indicators of positive emotions triggered by object and social play in mini-pigs. Appl Anim Behav Sci. 2018a;202:13–5.

    Google Scholar 

  34. Marcet-Rius M, Pageat P, Bienboire-Frosini C, Teruel E, Monneret P, Leclercq J, Lafont-Lecuelle C, Cozzi A. Tail and ear movements as possible indicators of emotions in pigs. Appl Anim Behav Sci. 2018b;205:14–8.

    Google Scholar 

  35. Marcet-Rius M, Fàbrega E, Cozzi A, Bienboire-Frosini C, Descout E, Velarde A, Pageat P. Are tail and ear movements indicators of emotions in tail-docked pigs in response to environmental enrichment? Animals. 2019a;9(7):449.

    Google Scholar 

  36. Marcet-Rius M. Physiological and behavioural indicators of positive animal welfare in pigs (PhD thesis, Pathologie, Toxicologie, Génétique et Nutrition, Institut National Polytechnique de Toulouse); 2019.

    Google Scholar 

  37. Marcet-Rius M, Kalonji G, Cozzi A, Bienboire-Frosini C, Monneret P, Kowalczyk I, Teruel E, Codecasa E, Pageat P. Effects of straw provision, as environmental enrichment, on behavioural indicators of welfare and emotions in pigs reared in an experimental system. Livest Sci. 2019c;221:89–94.

    Google Scholar 

  38. Martin P, Bateson P. Measuring behaviour, An Introductory Guide. 3rd ed. Cambridge: Cambridge University Press; 2007. p. 76–8.

    Google Scholar 

  39. Mellor DJ, Patterson-Kane E, Stafford KJ. The sciences of animal welfare (UFAW animal welfare). Palmerston North: Wiley; 2009. p. 72–93.

    Google Scholar 

  40. Mellor DJ. Animal emotions, behaviour and the promotion of positive welfare states. N Z Vet J. 2012;60(1):1–8.

    CAS  PubMed  Google Scholar 

  41. Mendl M, Burman OHP, Paul ES. An integrative and functional framework to the study of animal emotion and mood. Proc R Soc B. 2010;277:2895–904.

    PubMed  Google Scholar 

  42. Panksepp J. Affective neuroscience: the foundations of human and animal emotions. Oxford: Oxford University Press; 2004. p. 149–63.

    Google Scholar 

  43. Pedersen LJ, Damm BI, Kongsted AG. The influence of adverse or gentle handling procedures on sexual behaviour in fearful and confident sows. Appl Anim Behav Sci. 2003;83(4):277–90.

    Google Scholar 

  44. Proctor HS, Carder G. Can ear postures reliably measure the positive emotional state of cows? Appl Anim Behav Sci. 2014;161:20–7.

    Google Scholar 

  45. Rault J-L. Effects of positive and negative human contacts and intranasal oxytocin on cerebrospinal fluid oxytocin. Psychoneuroendocrinology. 2016;69:60–6.

    CAS  PubMed  Google Scholar 

  46. Reimert I, Bolhuis JE, Kemp B, Rodenburg TB. Indicators of positive and negative emotions and emotional contagion in pigs. Physiol Behav. 2013;109:42–50.

    CAS  PubMed  Google Scholar 

  47. Reimert I, Fong S, Rodenburg TB, Bolhuis JE. Emotional states and emotional contagion in pigs after exposure to a positive and negative treatment. Appl Anim Behav Sci. 2017;193:37–42.

    Google Scholar 

  48. Rochais C, Henry S, Sankey C, Nassur F, Gorecka-Bruzda A, Hausberger M. Visual attention, an indicator of human-animal relationships? A study of domestic horses (Equus caballus). Front Psychol. 2014;5:108.

    CAS  PubMed  Google Scholar 

  49. Rodarte Covarrubias LF, Trujillo Ortega ME, Doporto Díaz JM, Galindo Maldonado FA. Effect of environmental manipulation on social behavior, reactivity to humans and production of piglets weaned at 14 days of age. Vet Méx. 2005;36(4):375–80.

    Google Scholar 

  50. Schmied C, Boivin X, Scala S, Waiblinger S. Effect of previous stroking on reactions to a veterinary procedure. Behaviour and heartrate of dairy cows. Interact Stud. 2010;11:467–81.

    Google Scholar 

  51. Seabrook MF, Bartle NC. Human factors. In: Phillips C, Piggins D, editors. Farm animals and the environment. Wallingford, UK.: CAB International; 1992.

    Google Scholar 

  52. Studnitz M, Jensen MB, Pedersen LJ. Why do pigs root and in what will they root? A review on the exploratory behaviour of pigs in relation to environmental enrichment. Appl Anim Behav Sci. 2007;107:183–97.

    Google Scholar 

  53. Tanida H, Senda K, Suzuki S, Tanaka YT. Color discrimination in weanling pigs. Anim Feed Sci Tech. 1991;62:1029–34.

    Google Scholar 

  54. Tanida H, Nagano Y. The ability of miniature pigs to discriminate stimuli between a stranger and their familiar handler. Appl Anim Behav Sci. 1998;56:149–59.

    Google Scholar 

  55. Vandenheede M, Bouissou MF. Sex differences in fear reactions in sheep. Appl Anim Behav Sci. 1993;37(1):39–55.

    Google Scholar 

  56. van de Weerd HA, Day JEL. A review of environmental enrichment for pigs housed in intensive housing systems. Appl Anim Behav Sci. 2009;116:1–20.

    Google Scholar 

  57. Waiblinger S, Menke C, Korff J, Bucher A. Previous handling and gentle interactions affect behaviour and heart rate of dairy cows during a veterinary procedure. Appl Anim Behav Sci. 2004;85(1–2):31–42.

    Google Scholar 

  58. Waiblinger S, Boivin X, Pedersen V, Tosi MV, Janczak AM, Visser EK, Jones RB. Assessing the human–animal relationship in farmed species: a critical review. Appl Anim Behav Sci. 2006;101(3–4):185–242.

    Google Scholar 

  59. Warriss PD, Brown SN, Adams SJM, Corlett IK. Relationships between subjective and objective assessments of stress at slaughter and meat quality in pigs. Meat Sci. 1994;38(2):329–40.

    CAS  PubMed  Google Scholar 

  60. Welfare Quality. Welfare Quality ® assessment protocol for cattle. 2009.

    Google Scholar 

  61. Wemelsfelder F, Hunter EA, Lawrence AB, Mendl MT. Assessing the ‘whole-animal’: a free-choice profiling approach. Anim Behav. 2001;62:209–20.

    Google Scholar 

  62. Wood-Gush DGM, Vestergaard KS. Exploratory behavior and the welfare of intensively kept animals. J Agric Ethics. 1989;2:161–9.

    Google Scholar 

  63. Zulkifli I. Review of human-animal interactions and their impact on animal productivity and welfare. J Anim Sci Biotechno. 2013;4(1):25.

    Google Scholar 

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Acknowledgements

We would like to extend our sincere thanks to all the members of the IRSEA team who collaborated on this project. Additionally, we thank our mini-pigs for participating in this work and for making it possible. Finally, we acknowledge the official English language editing company AJE (American Journal Experts) for reviewing the language in our manuscript.

Funding

This work was supported by the ‘Convention Industrielle de Formation par la Recherche’ (CIFRE) fellowship from the ‘Association Nationale de la Recherche et de la Technologie’ (ANRT).

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Authors and Affiliations

  1. Physiological and Behavioural Mechanisms of Adaptation Department, IRSEA (Research Institute in Semiochemistry and Applied Ethology), Quartier Salignan, 84400, Apt, France

    Míriam Marcet-Rius & Cécile Bienboire-Frosini

  2. Semiochemicals’ Identification and Analogs’ Design Department, IRSEA (Research Institute in Semiochemistry and Applied Ethology), Quartier Salignan, 84400, Apt, France

    Patrick Pageat

  3. Statistical Analysis Service, IRSEA (Research Institute in Semiochemistry and Applied Ethology), Quartier Salignan, 84400, Apt, France

    Eva Teruel

  4. Animal Experimentation Service, IRSEA (Research Institute in Semiochemistry and Applied Ethology), Quartier Salignan, 84400, Apt, France

    Philippe Monneret & Julien Leclercq

  5. Research and Education Board, IRSEA (Research Institute in Semiochemistry and Applied Ethology), Quartier Salignan, 84400, Apt, France

    Alessandro Cozzi

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  1. Míriam Marcet-Rius
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Contributions

Conceptualization, M.M.-R., P.P., A.C. and C.B.-F.; methodology, M.M.-R., P.M. and J.L.; validation, P.P., A.C. and C.B.-F.; formal analysis, M.M.-R., P.M. and E.T.; data curation, M.M.-R., P.M. and E.T.; writing—original draft preparation, M.M.-R; writing—review and editing, P.P., A.C. and C.B.-F.; supervision, P.P., A.C. and C.B.-F.; funding acquisition, M.M.-R. The author(s) read and approved the final manuscript.

Corresponding author

Correspondence to Míriam Marcet-Rius.

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Ethics approval and consent to participate

The project, including this experimental procedure, was approved by the IRSEA’s (Research Institute in Semiochemistry and Applied Ethology) Ethics Committee (C2EA125) and the French Ministry of Research (AFCE_201609_01).

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Not applicable.

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The authors declare that they have no competing interests.

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Marcet-Rius, M., Pageat, P., Bienboire-Frosini, C. et al. The provision of toys to pigs can improve the human-animal relationship. Porc Health Manag 6, 29 (2020). https://doi.org/10.1186/s40813-020-00167-x

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Keywords

Porcine Health Management

ISSN: 2055-5660

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