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In this video it shows the process a boar takes before mounting a sow.

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Ultra Aggressive Pig Mating ★ Life of Pigs P19✔

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Uploaded by Todd S. Lokken on 2017-03-23.

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After the female becomes pregnant there is a monitoring period to make sure nothing goes wrong.

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Artificial Insemination is used as well instead of natural mounting so farmers can pick the genetic makeup of the animal which also lowers the risk of transmission of diseases.

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Sows and gilts have an average 21 day heat cycle, although this can range from 17 to 25 days. After cycle the animal can go to back into another heat cycle within three weeks.

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In this video it just showed certain ways to detect If the sow is in estrus or not.

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This short video shows a female pig in standing heat. Heat detection, or estrus detection, is very important for people who are involved in the production of pork. Hog farmers watch sows and gilts (young females) for estrus, or sexual receptiveness.

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When a female is in heat she will show sings by going out of her way to find a boar. Also one way to check is by applying pressure to her back, if she stands stiffed with no movement she is most likely in estrus.

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The male sniffs the female, noses sides, flanks and vulva, and emits a ‘mating song’ of soft guttural grunts (6–8 seconds). He foams at the mouth and moves his jaw from side to side as the female poses and bites the male’s ears gently. When the female stands still the male will then mount (Gonyou)".

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Behaviors of ovulations and sexual receptivity

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Behaviors of ovulations and sexual receptivity

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"Female-female mounting is one of the more obvious visual displays advertising sexual readiness in cattle, goats, and swine. (Principles and applications of domestic animal behavior)".

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The goal was to estimate the relationship between behaviour, physiology, and spatial integration in pigs. There were 64 groups of pigs involved. Pairs of familiar pigs were grouped with 2 unfamiliar pairs. The pigs that did not interact with the unfamiliar pigs had many skin lesions and high body weight. The pigs that showed more aggression showed a stronger increase in haptoglobin. which is protein showed in the blood stream.

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Irene Camerlink,

Simon P. Turner,

Winanda W. Ursinus,

Inonge Reimert,

J. Elizabeth Bolhuis

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Abstract

Social conflict is mostly studied in relation to aggression. A more integral approach, including aggressive and affiliative behaviour as well as physiology, may however give a better understanding of the animals' experience during social conflict. The experience of social conflict may also be reflected in the spatial distribution between conspecifics. The objective was to assess the relationship between behaviour, physiology, and spatial integration in pigs ( Sus scrofa) during social conflict. Hereto, 64 groups of pigs (9 wk of age) were studied in a 24 h regrouping test whereby pairs of familiar pigs were grouped with 2 unfamiliar pairs, in either barren or straw-enriched housing. Data on aggressive and affiliative behaviour, skin lesions, body weight, and haptoglobin could be summarized into three principal component analysis factors. These three factors were analysed in relation to spatial integration, i.e. inter-individual distances and lying in body contact. Pigs stayed up to 24 h after encounter in closer proximity to the familiar pig than to unfamiliar pigs. Pigs with a high factor 1 score were more inactive, gave little social nosing, had many skin lesions and a high body weight. They tended to space further away from the familiar pig ( b = 1.9 cm; P = 0.08) and unfamiliar ones ( b = 0.7 cm; P = 0.05). Pigs that were involved in much aggression (factor 2), and that had a strong increase in haptoglobin (factor 3), tended to be relatively most far away from unfamiliar pigs ( b = 0.03 times further; P = 0.08). Results on lying in body contact were coherent with results on distances. Pigs in enriched housing spaced further apart than pigs in barren housing ( P<0.001). The combined analysis of measures revealed animals that may either promote or slow down group cohesion, which may not have become clear from single parameters. This emphasizes the importance of an integral approach to social conflict.

Citation: Camerlink I, Turner SP, Ursinus WW, Reimert I, Bolhuis JE (2014) Aggression and Affiliation during Social Conflict in Pigs. PLoS ONE 9(11): e113502. https://doi.org/10.1371/journal.pone.0113502

Editor: Cheryl McCormick, Brock University, Canada

Received: May 2, 2014; Accepted: October 24, 2014; Published: November 26, 2014

Copyright: © 2014 Camerlink et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the Supporting Information files.

Funding: This study is part of the project, "Seeking sociable swine? Incorporating social genetic effects into pig breeding programs to achieve balanced improvement in productivity and welfare," which is financially supported by the program "The Value of Animal Welfare" of the Netherlands Organization for Scientific Research (NWO) and the Dutch Ministry of Economic Affairs. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

When unfamiliar animals first meet this may result in social conflict. Social conflict may involve excessive aggression, and efforts have been made to reduce aggression in captive animals [1] [2]. Aggression, however, only resembles part of the behavioural repertoire that animals may express to solve social conflicts. Alongside aggression there may be subtle affiliative behaviours, such as social grooming and body contact, that may promote reconciliation and group cohesion [3], [4]. These behaviours are well studied in primates [5], but largely ignored in most other species [6], [7], [8]. Assessing animals, for example for breeding purposes or welfare classification, should not only require assessment of aggression, but might also require taking into account cognitive processes and social skills that may promote social cohesion (pigs [2], crested macaque [9]).

In gregarious animals, social cohesion may be measured by the distance between group members (i.e. their spatial integration) and their affiliative interactions such as allogrooming ([10], marmots [11], pigs [12]). These measures may reflect social acceptance, and have been suggested to reflect the animals' experience of a stressful situation [5], [12]. Animals may show clear preferences for whom they allow in close proximity and will move away or show aggression when disliked animals approach too closely [13], [14]. This is especially relevant in livestock farming, where animals may be introduced to unfamiliar conspecifics several times during the production cycle and are commonly kept under minimal space requirements, allowing little room to move away from each other (pigs [15], poultry [16]).

In commercially kept pigs, regrouping aggression is considered to be a major welfare issue [17]. Regrouping, whereby unfamiliar animals encounter each other, is a common management strategy in commercial pig farming to obtain groups of equal body weight or gender. Regrouping results in aggressive interactions, which amongst others causes (skin) injuries [18], [19], and alters stress physiology, e.g. [20]. Aggression in pigs has been studied for decades [1], [21], but up to now remains a persistent problem, which may emphasize the need for a different approach. Insight into pigs' experience of social conflict might contribute to a solution, but this has hardly been studied [12], [22].

To solve complex behavioural issues, and to achieve sustainable welfare improvement, an integral approach might be required [23]. We aimed to take such an approach in pigs by assessing behavioural and physiological characteristics that may be related to the spatial integration between pigs during social conflict. We hypothesized that the spatial integration of regrouped pigs would depend on aggressive interactions as well as on positive social contact. The objective was to investigate if specific characteristics in behaviour and physiology would contribute most to small inter-individual distances, indicative of social cohesion.

Materials and Methods

This study was part of a larger trial in which animals were selected for diverging indirect genetic effects for growth (IGEg) and either housed in barren or enriched pens (described in Animals and housing). Because these factors may influence the social interactions between animals, they were taken into account in the current study.

Ethics

This study was carried out in strict accordance with the recommendations in the European Guidelines for accommodation and care of animals. The protocol was approved by the Institutional Animal Care and Use Committee of Wageningen University (Protocol Number: 2010055).

Animals and housing

A total of 384 pigs of 9 weeks of age, housed in 64 pens, were studied over four batches. These animals were offspring from 64 TOPIGS-20 sows (sow line of Great Yorkshire × Dutch Landrace) and 24 Tempo boars (commercial synthetic boar line with Great Yorkshire genetic background), which were selected on either 'high' or 'low' indirect genetic effects for growth (IGEg). IGEg is a breeding value that accounts for the genetic effect that a pig may have on the growth rate of its group members [24], [25], [26]. Details of the selection on IGEg are previously described [27]. Piglets were housed in conventional farrowing crates until weaning (at 26 days of age).

From weaning until slaughter, pigs were housed in groups of six (three females and three castrated male pigs) of the same IGEg classification. Each group contained at least one pig from both sexes that had an active response in the backtest, with a minimum of two pigs from the same backtest classification [27]. The backtest is a behavioural test whereby the response of piglets may be indicative of a piglet's coping style or behavioural strategy [28], and may relate to its aggressive behaviour as well as to other traits [29].

In the 2×2 experimental arrangement that was applied from weaning, half of each IGEg group (high vs. low) was housed in barren pens and the other half was housed in enriched pens. The barren conventional pens had a 60% solid concrete and 40% slatted floor. Enriched pens had a solid floor with a deep litter bedding of straw and wood shavings. Space allowance in both housing conditions was between 1.0-1.2 m ² per pig, depending on the barn. Pen dimensions were 1.90 m×3.20 m in two batches, whereas in the other two batches pens measured 2.25×3.25 m. Each pen contained a single space feeder, a nipple drinker, and a metal chain with a ball. Pigs were fed ad libitum with dry pelleted feed. The thermostat was set at 20°C, and minimum and maximum ambient temperature were recorded daily. Lights were on between 07:00 and 19:00 h.

Regrouping test and skin lesion score

At nine weeks of age, pigs were regrouped for 24 h (∼12:00 h to ∼12:00 h the following day) within their IGEg group and housing condition. From each pen, one male and one female pig were relocated into an unfamiliar pen where they were joined with two pairs of pigs originating from two different pens. None of the pigs in the new pen were full-sibs, and pen composition was balanced for backtest response. Pigs received a number sprayed on their back for recognition, and a coloured dot on their neck (stock marker spray) to identify the pig pair. Video cameras were mounted above the pens to enable video recordings. After 24 h, pigs were returned to their initial pen, and the number of fresh skin lesions was counted for the anterior, middle, and rear regions for both sides of the body immediately upon return [18]. For each pig, body weight was recorded at 9 weeks of age.

Spatial distribution

Data on spatial distribution of pigs were obtained from the video footage that was available from the regrouping test. For each pen there were video recordings from 11:00-19:00 h on the day of regrouping, and from 07:00-12:00 h the following day. Every hour, from the moment that all six pigs had entered the new pen, a screenshot was made from the video footage. The screenshot was made when at least 4 of the 6 pigs were lying. In case more than 2 pigs were standing, the video was forwarded until the moment that at least 4 pigs were lying. In this way, 13 to 14 images were obtained per pen. For each pen, a grid with corresponding x and y coordinates was made at an appropriate scale to be overlaid on the video playback. Hereto, the screenshot was focussed on one pen and rulers were placed along the sides of the pen. Rulers were adapted for scale to fit the true pen dimensions and depth, whereby each cm on the ruler represented 20 cm in reality. From the rulers, the x and y coordinate at the height of the neck of each pig was noted. When the neck of a pig could not be located due to objects in front of the lens (e.g. feeder), the middle of the pig was taken as a reference point. When the distances were calculated, a distinction was made between the familiar pig of the pair and the 4 unfamiliar pigs. It was also noted whether a pig was lying with at least 50% of its body in direct contact with a familiar or unfamiliar pig, whereby the middle of the pig was used as a reference point.

Live behavioural observations

Behaviour of the pigs was observed live during the regrouping test by 2-min instantaneous scan sampling for six hours. The Observer 5.0 software package (Noldus Information Technology B.V., Wageningen, The Netherlands) installed on a hand-held computer was used for behaviour recordings. Observations were divided into 1 h blocks (with 15 min breaks between each block) from 14:00-17:30 h on the day of regrouping and from 08:00-11:30 h the following day. This procedure resulted in 180 observations per pig. Behaviours that were analysed were inactivity (lying with the eyes closed or eyes open), aggression (reciprocal fighting, head knocks, and unilateral biting), and social nosing (nosing the body of a pen mate without performing oral manipulation and nose-nose contact with a pen mate). For aggressive behaviour and social nosing both the giver and receiver of the behaviour were recorded as either a familiar pig or an unfamiliar one.

Data preparation

The distance between two spatial coordinates was calculated using a ²+b ² = c ², in which a = x pig1-x pig2, where x pig1 is the x-coordinate of one pig and x pig2 the x-coordinate of another pig. The same procedure was used for b, which is the difference between the y-coordinates of two pigs. The square root of the resulting c ² was the distance between two pigs.

The distances to the four unfamiliar pigs were averaged, resulting in one value for the distance to the familiar pig and one value for the average distance to the unfamiliar pigs. Due to the lying positions of the pigs, whereby the back of the pig was not always visible from the cameras' perspective, the individual markings on the back of the pigs could not always be identified. The specific colour marking for pig pairs (marking in the neck) could, however, always be identified and therefore the average distance to unfamiliar pigs was only available per pig pair. Pig pairs where one of the pigs was removed from the experiment (due to health reasons prior to the regrouping test) were excluded from analysis ( n  = 5). A relative distance between familiar and unfamiliar pigs was calculated by dividing the average distance to the unfamiliar pigs by the distance to the familiar pig. The original data from all observations on distances (S1) and by pig (S2) are available in the supplementary files.

Residuals of the variables were obtained from a general linear model (Proc GLM) with housing condition, IGEg group, and batch as fixed effects. For Δhaptoglobin one outlier was removed (3.2 mg/ml), which was 4.4 SD higher than the mean (0.14 mg/ml) and 1.3 SD higher than the second highest value. The skin lesion scores were square root transformed, and the behavioural observations were transformed by arcsine square root. After transformation, all residuals followed a normal distribution.

Principal component analysis (PCA)

The behavioural and physiological data were correlated with Pearson correlations on the residuals of the GLM. Four out of the 10 variables showed at least one significant correlation above 0.30. Data were therefore analysed in a principal component analysis (PCA) with orthogonal rotation. The skin lesions on the anterior, middle, and rear of the body were strongly correlated (r p 0.45-0.73; all P<0.001). To prevent creating a PCA factor that would only resemble skin lesions due to the high correlations, we included the total number of skin lesions in the PCA rather than the numbers by body region. The PCA resulted in three factors with an Eigenvalue above 1. The loadings on the factors are given in Table 1 ( Results section) with the corresponding factor maps ( Figure 1).

Data analysis

Data preparation, the PCA, and data analysis were carried out in SAS 9.2. The effect of familiarity on the spatial integration between pigs was analysed in a mixed model (Proc MIXED) with repeated measures per pair (1).

(1) Spatial integration pair  =  familiarity + IGEg group + housing condition + batch + pig pair (pen + IGEg group + housing condition + batch) + pen + e, where 'spatial integration' denotes distance and body contact on pair level. 'Familiarity' was a class effect (unfamiliar/familiar) resulting in two repeated values per pair. Pig pair was included as a random effect to account for the repeated measures per pair, and was nested within pen, IGEg group, housing condition, and batch. Pen was included as second random effect.

The difference in distance between familiar and unfamiliar pigs over time was analysed in a mixed model (2) with 14 repeated observations over time per pair.

(2) Difference in distance pair  =  observation + IGEg group + housing condition + batch + pig pair (pen + IGEg group + housing condition + batch) + pen + e, where 'difference in distance' was the distance to unfamiliar pigs minus the distance to the familiar pig. 'Observation' (∼14 observations over 24 h) was included as fixed class effect, while pig pair was included as random effect nested within pen, IGEg group, housing condition, and batch, along with the random pen effect. Two- and three way interactions were tested, but omitted from the model due to non-significance.

The effect of behaviour and physiology on the spatial integration between pigs was analysed using a mixed model (3), with the response variables separate for familiar and unfamiliar pigs.

(3) Spatial integration pair  =  factor 1 pig + factor 2 pig + factor 3 pig + IGEg group + housing condition + batch + pig pair (pen + IGEg group + housing condition + batch) + pen + e, where 'spatial integration' denotes the measures on pair level for the distance to the familiar pig, the average distance of a pig pair to unfamiliar pigs, the relative distance between the two, and the proportion of observations that pigs spent in body contact with a familiar or an unfamiliar pig. The three PCA factors were on individual pig level and were included as explanatory variables. Interactions between these variables were explored and significant interactions were retained. The effect of IGEg group, housing condition, and batch on the spatial integration was explored, along with the relevant interactions between these variables. The pig pair and pen were included as random effects, whereby pig pair was nested within pen, IGEg group, housing condition, and batch. The residuals of model 1 and 3 were normally distributed for all spatial integration variables.

The difference in haptoglobin concentration was tested in a mixed model with the sample moment (pre-test/post-test) as repeated observation. The haptoglobin concentration was the response variable whereas 'sample moment', IGEg group, housing condition, and batch were explanatory variables, with the pig pair and pen as random statements as described above.

Values presented are (untransformed) LSmeans ± SEM.

Results

Familiarity

Pigs stayed in close proximity to the pig they were familiar to, whereas they spaced away from unfamiliar pigs ( Figure 2). On average, familiar pigs lay 125±2 cm apart, whereas their average distance to unfamiliar pigs was 158±2 cm ( F 1,187 = 205; P<0.001). Pigs stayed in closer proximity to the familiar pig than to the unfamiliar pigs until night time ( Figure 3; all P<0.001). On the following morning, the distance between unfamiliar pigs was smaller, but remained significantly larger than the distance between familiar pigs (all P<0.05), except at 07:00 h ( P = 0.39), which was the first hour after the dark period, and at 10:00 h ( P  = 0.07).

The closer proximity between familiar pigs was also reflected in the amount of body contact. Familiar pigs lay with at least half of their body in direct contact with each other on an average of 14±0.7% of the observations (range 0-71%), but in contact with one or more of the unfamiliar pigs on 21±0.7% of observations (range 0-54%). If pigs did not differentiate between familiar and unfamiliar pigs when resting, the chance that a pig would lie next to the familiar pig would be four times smaller ( ¹/ ₅) than to one of the unfamiliar pigs ( ⁴/ ₅). When corrected for chance, the frequency of lying in body contact with an unfamiliar pig would equate 5±0.7%. Therefore, pigs lay in contact with the familiar pig more often than with unfamiliar pigs as would be expected by chance ( P<0.001).

Principal component analysis

The principal component analysis revealed three factors, which together explained 55.6% of the variation ( Table 1). A high score on factor 1 related to inactivity, a low amount of giving social nosing towards others, a high number of skin lesions, and a high body weight. This combination of variables might describe sociality. A high score on factor 2 was mainly explained by a high amount of aggressive behaviour given and received, as well as a high number of skin lesions. Factor 2 described involvement in aggression (not 'aggressive' in itself, because it also includes pigs that received much aggression and are therefore not necessarily aggressive themselves). Factor 3 explained the increase in the level of haptoglobin, i.e. Δhaptoglobin. The increase in haptoglobin was unrelated to the amount of skin lesions (r p 0.07; P = 0.21), which was also reflected in the loadings in factor 3 ( Table 1). The receipt of social nosing was the only variable that did not clearly associate with one of the factors ( Table 1). Separate analysis of this variable in the mixed models indeed did not reveal a relationship with measures on the distances or body contact.

Inter-individual distances

Pigs with a high factor 1 score tended to space further away from the familiar pig ( b = 1.9±1.1 cm; P = 0.08), as well as from unfamiliar pigs ( b = 0.7±0.4 cm; P  = 0.05). Opposite, animals that were active, involved little in aggression, and gave much social nosing, i.e. the animals with a low factor 1 score, were closely situated to other pigs. Pigs spent 1.8±1.3% of the behavioural scans giving social nosing, of which on average 20% was directed towards the familiar conspecific.

Pigs with a high factor 2 score gave and received high amounts of aggressive behaviour. Aggressive behaviour, which occurred on average on 1.1±1.4% of the behavioural scans observed after the first peak of aggression, was directed towards unfamiliar pigs on 90% of occasions. Involvement in aggression (factor 2) did not significantly affect distances toward the familiar pig ( b = −0.9±1.1 cm; P = 0.46) or toward unfamiliar pigs ( b = 0.1±0.4 cm; P  = 0.87).

Increased haptoglobin (factor 3) did not affect the distance toward the familiar pig ( b = −1.1±1.1 cm; P = 0.31) or unfamiliar pigs ( b = −0.4±0.4 cm; P = 0.24). The haptoglobin concentration significantly increased after regrouping ( P<0.001). Before the test the haptoglobin concentration was on average 0.55±0.03 mg/ml (0.04-2.55), and at 3 d after the test it was on average 0.70±0.03 mg/ml (range 0.04-3.5), resulting in a difference (Δ) of 0.14±0.03 mg/ml (range −2.0-2.3). These values are within a normal range for healthy animals.

Relative distance

Pigs were on average 1.3±0.02 times further away (range 0.8-3.3) from unfamiliar pigs than from the pig they were familiar to, which is here referred to as the relative distance. Although pigs with a high factor 1 score (sociality) spaced further away from the unfamiliar pigs as well as from the familiar pig, this was only in absolute distance, and not relative to each other ( P = 0.47). Since both absolute distances were increased, the relative distance to unfamiliar pigs as compared to the distance to the familiar pig remained the same. The relative distance tended to be greatest, i.e. pigs were relatively most far away from unfamiliar pigs, in pigs with a high factor 2 score (much involvement in aggression) and a high factor 3 score (high increase in haptoglobin) ( b = 0.03±0.01 times further; P = 0.09). The relative distance to unfamiliar pigs was not affected by the separate contribution of factor 2 ( b = 0.02±0.02 times further; P = 0.29) or factor 3 ( b = 0.01±0.01 times further; P  = 0.41).

Lying in body contact

Pigs with a high factor 2 (much involvement in aggression) and a high factor 3 score (high increase in haptoglobin) tended to lay most in body contact with the familiar pig ( b = 0.8±0.4% of observations; P = 0.09), but less with unfamiliar pigs ( b = −0.4±0.3% of observations; P = 0.10). Lying in body contact with the familiar pig or with unfamiliar pigs was unaffected by factor 1 ( P = 0.94; P = 0.48, respectively), or the separate contribution of factor 2 (fam: P = 0.99; unfam: P = 0.86) or factor 3 (fam: P = 0.69; unfam: P  = 0.82).

Enriched housing conditions

Pigs in pens that were enriched with a deep litter layer of straw and wood shavings kept a larger distance to familiar and unfamiliar pigs than those in barren pens ( Table 2). However, pigs in enriched pens only spaced further away from each other than pigs in barren pens during the batches with a maximum ambient temperature around 21.5°C ( Figure 4: Jan, Mar, Oct), whereas in the batch with a maximum ambient temperatures of 29.7°C (Jun) there was no significant difference between housing conditions ( Figure 4). This interaction between housing condition and batch, which is confounded with temperature, was apparent for the distance to the familiar pig ( P = 0.08) and to unfamiliar pigs ( P<0.01). The relative distance to unfamiliar pigs was smaller, which means that pigs in enriched pens were relatively closer to unfamiliar pigs than to the familiar pig as compared to pigs in barren pens ( Table 2). Pigs in barren pens lay twice as much in body contact with familiar or unfamiliar pigs than pigs in enriched pens ( Table 2).

Indirect genetic effects

There were no significant effects of selection on 'indirect genetic effect for growth' (IGEg) on any of the measures on spatial integration (all P >0.10). The genotype by environment set-up, however, tended to interact for lying in body contact with the familiar pig ( F 1,126 = 2.99; P = 0.09). Pigs which were genetically selected to have a positive effect on the growth rate of their group members (high IGEg pigs) were lying most frequently in body contact with their familiar pig when they were housed in barren pens. In contrast, of the four treatment groups (IGEg × housing condition), high IGEg pigs were lying least frequently in body contact with the familiar pig when they were housed in enriched pens ( Figure 5).

Discussion

We aimed to assess the relationship between behaviour, skin lesions, and plasma haptoglobin of pigs and their spatial integration during social conflict. Pigs clearly distinguished between familiar and unfamiliar pigs over the 24 h period after mixing, whereby they remained closer to the familiar pig. The results highlight that reduced aggression does not necessarily equate to reduced social tension, which may be reflected by large spatial distances. It is therefore important to consider a spectrum of parameters before conclusions are drawn upon the contribution of an animal to the functioning of a group.

Characteristics of pigs with a large inter-individual distance

Factor 1 in the principal component analysis described sociality, whereby pigs with high factor 1 scores were inactive pigs with a high number of skin lesions, high body weight, and little social nosing behaviour. These pigs tended to space further away from all other pigs irrespective of familiarity. It seems plausible that these pigs were exhausted of fighting and were therefore less active. As a result of fighting and higher body weight, they may have had an increased body temperature [40], which might make them space further away from others. This withdrawn position may have led to less social interactions in the form of social nosing. These pigs might also have been unsuccessful in their fights and consequently might not have been allowed in close proximity [41]. If aggressiveness is the underlying cause of large inter-individual distances than selection against aggressiveness [42] might change inter-individual distances. It could also be that these pigs were dominant. Dominant pigs may keep a larger portable (personal) space than subordinates [43] which may reflect their own choices or the unwillingness of other animals to closely approach them [13]. This high dominance status would be in line with the high body weight [44], and high amounts of aggression as reflected in the skin lesions [18]. If dominance is underlying the differences in distances, than a more rapid establishment of dominance relationships might lead sooner to social cohesion. Irrespective of the underlying cause, the response of the 'antisocial' pigs seemed to hamper the social cohesion of the group of pigs. For future studies it would be worthwhile to include tests on aggressiveness and dominance status.

The role of aggression

Factor 2 described involvement in aggressive behaviour given and received. Factor 2 did not have any significant effect on the measures of spatial integration, which indicates that studying aggression alone may miss important aspects of social conflict. A potential reason why factor 2 did not relate to any of the measures of spatial integration might be the simultaneous inclusion of given and received aggression in the PCA. The amounts of aggressive behaviours that are given and received are correlated [18]. Giving aggression may provoke a different behavioural repertoire than receiving aggression, and this may be reflected in the inter-individual distances measured at other time points than the aggressive act. That these different types of involvement in aggression loaded equally on factor 2 may have caused that factor 2 did not reveal any significant effects on the spatial integration. More detailed observation of aggressive behaviour, including the time frame directly after regrouping, might give more clarity on the relationship between aggression and spatial distances.

Indirect genetic effects

Pigs that were selected on high IGEg, which is a positive genetic effect on the growth of pen mates, spent almost twice as many observations in body contact with the familiar pig than pigs from other treatment groups. The inter-individual distance between animals may decrease with genetic selection for social traits, as has been observed in Japanese quail ( Coturnix japonica) selected for social reinstatement behaviour [71]. The distance may decrease further in novel and potentially stressful environments [71]. Stress is likely to be greater in barren housed animals as compared to enriched housed animals [72], [73]. As argued above, being in close contact with a familiar conspecific may reduce stress. Previous studies suggested that high IGEg pigs cope better with stressful situations [27], [61], [74], [75]. It might be that this capacity to cope with stress relates to a higher tendency to give or seek social support.

An integral approach to social conflict

The combination of behavioural and physiological data suggests that spatial integration depends mostly on aggression, sociability, and stress vulnerability. The distances and amount of body contact between unfamiliar pigs could only be observed on pair level, which was a restriction to the study design. The familiar pig pairs, however, commonly stayed in close proximity to each other, and thus their average distance to the other pigs is a reasonable approximation of their individual distance to unfamiliar pigs. Aggression as a single parameter failed to indicate spatial integration between pigs, but in combination with haptoglobin it revealed pigs that spent more time in body contact with the familiar pig and spaced relatively further away from unfamiliar pigs. The social cohesion was hampered by animals with a high factor 1 score, indicating much skin lesions, high body weight, little social nosing, and inactivity. It is unclear whether these pigs spaced away from others due to dominance status, exhaustion, or high body temperature. Contrary, pigs that showed much social nosing were low in body weight, had few skin lesions, were more active, and were more prone to approach familiar and unfamiliar pigs. Genetics and housing conditions may affect inter-individual distances between pigs, whereby straw housing may lead to a larger portable space. If we would like to improve spatial integration between unfamiliar animals upon encounter, this would not necessarily require animals with little aggression per se, but would rather require animals that cope well in a group, for example by rapid establishment of dominance relationships. Absence of fighting is not the same as being free of social tension, and therefore an integral approach may be necessary when assessing animal welfare.

Acknowledgments

This study was financed by the Netherlands Organization for Scientific Research (NWO) and the Dutch Ministry of Economic Affairs. We are grateful to Monique Suer for her contribution to the data and analysis, Rosalie van Emous, Suzanne Hendrikx, and David Jansen for their work on obtaining the data, and Bas Kemp for his advice on the analysis. We would like to acknowledge the colleagues from the Adaptation Physiology Group of Wageningen University and animal care takers of experimental farm 'De Haar' that helped with the animal work during the trial.

Author Contributions

Conceived and designed the experiments: IC SPT WWU IR JEB. Performed the experiments: IC WWU IR. Analyzed the data: IC SPT WWU IR JEB. Wrote the paper: IC SPT WWU IR JEB.

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3. 38. Heegaard PM, Klausen J, Nielsen JP, González-Ramón N, Piñeiro M, et al. The porcine acute phase response to infection with Actinobacillus pleuropneumoniae, haptoglobin, C-reactive protein, major acute phase protein and serum amyloid A protein are sensitive indicators of infection. Comp Biochem Physiol B. 1998;119:365-373.

4. 40. De Jong IC, Lambooij E, Korte SM, Blokhuis HJ, Koolhaas JM. Mixing induces long-term hyperthermia in growing pigs. In: De Jong IC. Chronic stress parameters in pigs. PhD Dissertation, University Groningen, The Netherlands. 1999.

5. 71. François N, Mills AD, Faure JM. Inter-individual distances during open-field tests in Japanese quail (Coturnix japonica) selected for high or low levels of social reinstatement behaviour. Behav Processes. 1999;47:73-80.

# data[].attributes.attachment_link.title
Aggression and Affiliation during Social Conflict in Pigs

# data[].attributes.attachment_link.description
Social conflict is mostly studied in relation to aggression. A more integral approach, including aggressive and affiliative behaviour as well as physiology, may however give a better understanding of the animals' experience during social conflict. The experience of social conflict may also be reflected in the spatial distribution between conspecifics.

# data[].attributes.body
Trial 1 evaluated the effects on how frequent the availability of environmental enrichment.  The animals were used with four different treatments. The first one had no equipment the second one had objects provided for six days that were not interrupted. The third one had objects provided every other day. The fourth had objects every six days. Providing environmental objects with rewards showed big behaviors of pigs. But was hard to keep it up.

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Simone Pereira Machado,

Fabiana Ribeiro Caldara,

Luciana Foppa,

Rafael de Moura,

Liliane Maria Piano Gonçalves,

Rodrigo Garófallo Garcia,

Irenilza de Alencar Nääs,

Viviane Maria Oliveira dos Santos Nieto,

Geyssane Farias de Oliveira

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Abstract

Three trials were carried out in a completely randomized design aiming to assess the behavior of pigs in growth phase in enriched environments. Trial 1 evaluated the effects of frequency of availability of environmental enrichment. The animals were assigned to four treatments: 1) control with no enrichment object; 2) objects provided for six consecutive days uninterruptedly; 3) objects provided on alternate days, and 4) objects provided for six consecutive days taken away by the end of the afternoon and replaced at dawn. Trial 2 assessed the effects of scent on animals' acceptance and maintenance of interest in objects. Animals were assigned to four treatments: 1) unscented object; 2) object with banana scent; 3) object with rum scent; 4) object with scents alternated every other day. Trial 3 aimed to assess the influence of environmental enrichment based on providing rewards at different difficulty levels. Animals were assigned to three treatments: 1) object with no reward; 2) object with a reward at an easy level; 3) object with a reward at a difficult level. Each trial had six days of behavioral observations every ten minutes for eight hours each day using images from video cameras. Enrichment objects stimulated the animals' natural behavior of nuzzling and exploring the environment. The way the objects were available did not impact the success of their use. Offering enrichment on alternate days or removing the objects by the end of the day was not an effective strategy to extend the animals' interest. The olfactory stimulus in environmental enrichment objects had no positive effect on extending the animals' interest on them, nor did alternating the aromas. The tactile stimulus was a key factor for object attractiveness. Providing environmental enrichment objects with rewards stimulated the exploratory behavior of pigs. The level of difficulty to obtain the reward may discourage the animals.

Citation: Machado SP, Caldara FR, Foppa L, de Moura R, Gonçalves LMP, Garcia RG, et al. (2017) Behavior of Pigs Reared in Enriched Environment: Alternatives to Extend Pigs Attention. PLoS ONE 12(1): e0168427. https://doi.org/10.1371/journal.pone.0168427

Editor: Elisabetta Palagi, Universita degli Studi di Pisa, ITALY

Received: July 6, 2016; Accepted: December 1, 2016; Published: January 6, 2017

Copyright: © 2017 Machado et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: The authors received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Brazilian pig farming has a predominance of intensive production systems in confinement featuring facilities with cement floors and high animal density. However, this type of system has been questioned due to the volume and difficulties in properly managing waste, which entails serious environmental pollution issues, and due to reduced animal well-being [ 1]. Abnormal behaviors are commonly observed in animals reared in confinement since the inability of exercising the species natural behaviors significantly impacts their well-being.

One of the most relevant subjects in welfare guidelines is the issues related to intensive confinement. In this context, Machado Filho and Hötzel [ 2] suggest two approaches to improving animal well-being: alternative production systems and the environmental enrichment.

Environmental enrichment is a principle of animal management that seeks to enhance the quality of life of animals in captivity by identifying and providing environmental stimuli required for them to reach psychological and physiological well-being. This strategy stimulates the behaviors typical of the species, thus lowering stress and making the captive environment more complex and diverse by meeting their ethological needs [ 1]. According to Campos [ 3], environmental enrichment is a way of providing better living conditions to the animals. Pigs reared in enriched environments typically show behavioral evidence of better well-being compared to those in confinement [ 1] and, when the strategies are well planned and applied, they may significantly reduce the frequency of abnormal behaviors [ 4].

One way of enriching the environment is by including objects designed to attract interest and allow the animals to express species-specific behaviors. Current literature suggests the environmental enrichment objects must be attractive, chewable, consumable, deformable, destructible, and have a stimulating scent or flavor, and yet create novelty [ 5]. Those objects must motivate the species and prove effective in their goal throughout the production process since studies indicate that the animals quickly lose interest in them [ 6, 7]. Studies have shown the reduction in pig interaction with the objects within five to six days [ 8, 5].

Thus, the current challenge for the scientific community is to develop environmental enrichment techniques that meet their goals of improving animal well-being, and that might maintain continued interest in the objects while being easily implemented and economically viable.

The current study was developed aiming to assess the behavior of pigs in the growth phase in enriched environments, as well as to evaluate alternatives that aim to extend animal interest in the objects used as enrichment.

Material and Methods

Three trials were carried out between September and October 2015 on a commercial pig farm in the city of Dourados, MS, Brazil. The city's coordinates are 22°13'18.54" S and 54°48'23.09" W and its main altitude is 430 m. The climate in the region is humid mesothermal (Cwa) according to the Köppen classification featuring rainy summers and dry winters with an average annual rainfall of 1,500 mm and average annual temperature of 22°C. The study was done during the day in a way not to interfere with the general farm management.

The research complied with ethical standards and was approved by the Ethics Committee on Animal Use (permit 06/2015) of the Federal University of Grande Dourados.

The study used 506 commercial hybrid grower pigs (161 females and 345 males) all of the same genetic lineage. The trials were carried out before the immunocastration of the male grower pigs. The animals were housed in a masonry barn (100 m long x 8.0 m wide) with collective 60 m ² pens featuring a running water pool at the end of the pen, automated feeding troughs, and nipple drinker. Each pen housed around 46 animals whose mean initial weight was 25 ± 2 kg. The animals remained 21 days adapting to the facilities and establishing social hierarchy and the experimental evaluations began when they were 86 days old. The pigs were fed and had access to water at libitum.

Trial 1

The trial was carried out aiming to assess the behavior of pigs in an environment enriched with objects and the effects of the frequency of availability of those objects on the maintenance of interest by the animals. A total of 184 animals (92 females and 92 non-castrated males) were assigned to the four treatments in a completely randomized design with 46 animals per treatment:

1. T1- control treatment with no enrichment object;

2. T2-objects provided uninterruptedly for six consecutive days;

3. T3- objects provided on alternate days over six days;

4. T4- objects provided in the morning and taken away by the end of the afternoon for six consecutive days.

The objects tested in T4 were removed immediately after the video recording from the pen every day at 3:15 PM and added again in the next day at 6:30 AM. The video recording only started 40 minutes after the tested objects were added to the pen to avoid the change in the behavior of the pigs due to the presence of the researcher inside the pen.

The environmental enrichment objects were made with PVC pipes 25 cm long and 20 cm in diameter attached to four 65 cm-long pieces of non-toxic clear plastic tubing, which allows the pigs to exercise the exploratory activity of chewing. Each length of pipe was filled with sisal ropes to absorb the impact of the animals' bites, thus keeping them from breaking. Two objects were hung in each pen at the pigs' eye height to facilitate visual contact, except in the control treatment ( Fig 1).

Trial 2

The trial was carried out aiming to assess the animals' acceptance of scented enrichment objects, as well as the effects of alternating scents on the extension of the pigs' interest in the objects. A total of 184 animals (non-castrated males) were assigned to four treatments in a completely randomized design with 46 animals per treatment:

1. T1- unscented enrichment object (control);

2. T2- banana-scented enrichment object;

3. T3- rum-scented enrichment object;

4. T4- banana- and rum-scented enrichment object alternated every other day.

Two objects were hung per pen in the same way as in trial I. Holes were drilled in the plastic pipe attached to the PVC structure. The aromatic essences (Arcolor®; Composition: artificial aromatic basis diluted in water and neutral ethylic alcohol) were stored inside the PVC pipe and were absorbed by the sisal ropes and exhaled through the holes in the plastic tube ( Fig 2). The essences inside the PVC structure were refilled daily to keep the scent durable. The essences were diluted in water at 0.1:1 ratio (100 mL essence for 1.0 L water). The scents presented were based on the human perception of odor believing their stimulus value to a pig, since these animals have a very good sense of smell [ 9]. The authors indicate pigs present an olfactory acuity approximately 2000 times more sensitive than human; therefore, the dilution proposed in the present study aimed to be easily detected by the pigs. The objects were hung at the pigs' eye height to enable visual contact. The essence was alternate (banana- and rum-scented) every day during T4 in the attempt to keep each odor as a novelty for the pigs.

Trial 3

The trial aimed to assess the pigs' behavior in the presence of environmental enrichment objects based on providing rewards (tasty snacks) at different difficulty levels. The animals (n = 138-69 females and 69 non-castrated males) were assigned to three treatments in a completely randomized design with 46 animals per treatment in the same pen. The treatments were:

1. Providing an enrichment object with no reward;

2. Providing an enrichment object with reward at an effortless level;

3. Providing an enrichment object with reward at a challenging level;

The enrichment objects were made using empty 10 L water jugs, and steel stands 1.15 m tall x 1.45 m wide. A steel rod was placed across the jugs and attached to the stand. Two jugs were placed in each rod, forming a spinning structure ( Fig 3).

The structures were fixed to the floor of the pens in a way that the jugs were at the height of the animals' heads not to be touched. The interaction of the pigs with the toy should make the jugs spin 360° to release the reward inside. Different holes were drilled in the jugs to customize the levels of difficulty to turn them so the reward could be obtained. Therefore, the animals in the treatment with difficult level had to try harder to be able to turn the jug and get the reward.

The reward consisted of popcorn, which was shown to be very attractive to the pigs in a previous pilot experiment. The snack was also a regular part of the animals' diet (corn), so they would pose no risk. The popcorn was made and replaced every morning before the behavioral observations.

Behavior Analyses

All observations were performed for a total of 8 h daily, between 7:10 AM and 3:10 PM, during six consecutive days during the experimental period. The pig behavior was analyzed using video images recorded by video cameras installed at the top of the pens and directly connected to a device with an image capture card and LCD monitor. One video camera was installed for each treatment, with independent adjustments, targeting the objects and focusing the whole pen. The video images were stored in the monitoring apparatus's internal memory for later evaluation.

The video images were watched using the video software CyberLink and the recording was paused every 10-min completing 48 events per day (480 minutes of video recording per day).

The video image instantaneous scan samples were taken using the print screen function on the computer. The instantaneous scan samples were opened in the software Paint (Microsoft Windows ® operational system) and then marked with colors ( Fig 4) that represented each animal behavior listed in the ethogram ( Table 1). All animals in each pen were evaluated individually, and the number of the animals performing each behavior was registered and transposed to a spreadsheet.

Since the trials were carried out on a commercial farm, the experiments were done with the minimum interference in the general management generating a limitation to perform the tests during the day. The trials were carried out during the Southern hemisphere winter with short photoperiod when the pigs have their peak of activities close to the time chosen to the monitored.

The behavioral assessment used an ethogram adapted from the methodology proposed in the literature [ 3, 10] ( Table 1).

Statistical Analysis

Activity behavior parameters measured the number of pigs per pen performing a particular activity in each event (48 events per day) registered every 10 minutes. A histogram of the frequency of behavioral activities was built. Activity behaviors were recorded as the percentage of pigs performing a particular behavior at each scan sampling occasion and were analyzed as a percent of the time [ 11]. For each day of observation, there were 48 events, and for each event, it was considered that the pig exerted that particular behavior until the next event (10 minutes) [ 11].

The mean values concerning each behavior present in the ethogram were determined in minutes and as percentages of the total time. The time in minutes the animals spent in each assessed behavior was calculated based on the average of 46 animals per treatment. The frequency was considered as a percent of the total evaluated time. The values presented were the average number of a given behavior in six days.

Data normality was verified using Lilliefors test, analysis of variance was applied, and the means were compared by Tukey's test using the software Assistat [ 12].

Results and Discussion

Trial 1

The different methods of providing the environmental enrichment objects did not impact (p>0.05) the time the animals spent in agonistic behaviors, nuzzling and exploring the environment, interacting with the enrichment object or with other pigs, or moving around or sitting ( Table 2) ( Fig 5).

The animals spent on average over 60% of the time sleeping or lying. The result is similar to those from a previous study [ 13] that states that pigs spent on average 61% of the time sleeping in an environment with no enrichment. Compared to all other farm animals, pigs spend the most time idle and sleeping [ 14]. However, the pigs maintained in environments with no environmental enrichment (control) spent more time resting (p<0.05) compared to those that had the objects constantly in the pen (T2) or yet with objects on alternate days (T3).

The animals in the treatments with no objects and with objects constantly in the pen for six consecutive days spent more time eating and drinking than the others. In a study where the performance of pigs reared in the enriched and not enriched environment, it was found that high daily intake in the group in the barren environment had no positive impact on the finishing animals' performance [ 15]. The authors credited this result to the waste of feed by the pigs that used the food as a playing source.

The pigs in the treatment in which the object was provided on alternate days had a higher frequency of sexual behavior (p<0.05). Sexual behaviors, such as mount, are part of the natural behavior repertoire of pigs [ 16]. However, some factors may change the natural frequency of those behaviors, and that may become a problem for the animals' well-being. There is no apparent explanation for only the animals in that group showing a greater expression of sexual behavior. Nonetheless, the expression did not reach high levels that could compromise the animal welfare. This behavior was found in the range of 1.2 to 2.0% in a previous study that evaluated the effectiveness of an immunocastration vaccine to suppress aggressive and sexual behaviors of entire male pigs [ 11].

Agonistic behaviors are also part of the standard behavior of pigs. It is known that pigs are animals that fight over the control of resources or space and perform shows of force. The frequencies observed for agonistic behavior were relatively low at 0.49% on average of the total period assessed. Neither the enrichment objects nor the strategies of providing them were able to reduce this behavior compared to the control treatment. Other investigations also found no effect of environmental enrichment on the reduction of aggressive behaviors [ 17, 18].

Environmental enrichment did not impact (p>0.05) the expression of investigative behavior in the animals. Pigs have the natural habit of nuzzling and exploring the environment. In natural conditions, these animals spend much of their time searching for food and exploring the environment and this type of behavior is considered crucial for the species [ 19, 20]. In the present study, the animals spent around 10% to 15% of their time exploring the environment. That shows that the confinement environment, even when enriched, limits the expression of the natural animal behavior and that the objects in the pen may have diverted part of the animals investigative behavior.

The time the animals spent interacting with the enrichment objects showed that they were attractive and well accepted by the animals, which may be related to the characteristics of the materials employed. The flexibility and destructibility of the object used as environmental enrichment positively contribute to the success of the technique [ 21]. However, the different frequencies of providing the objects did not impact (p>0.05) the time the animals spent interacting with the object. An important property of an enrichment object is to generate the feeling of novelty involved in exploration [ 22]. However, little is known about the time pigs take to forget a particular object. It was expected that providing the objects on alternate days or taking them away at dusk and replacing them at dawn might stimulate greater interest by the animals in them and become an effective strategy to extend the benefits of enrichment. However, that was not observed and the time the animals spent interacting with the objects was similar among the treatments, as well as the frequency over the experimental period ( Fig 6).

Trial 2

The different treatments did not impact (p>0.05) the time the animals spent with the behavioral activities: sleeping or lying, sexual and agonistic behavior, nuzzling or exploring the environment, moving around or sitting, and interacting with the other pigs ( Table 3) ( Fig 7).

The incidence of agonistic and sexual behaviors was low at 0.19 and 0.11% of the total time on average, respectively. Agonistic behaviors are part of the normal behavioral repertoire of pigs. However, some factors such as sex and environment may increase their incidence. Since the trial was carried out with grower pigs, the frequency of either behavior can be considered small compared to another study [ 23]. However, the agonistic behaviors observed did not represent destructive behaviors among the animals. Destructive behaviors can be described as those in which the pigs suffer some injury or trauma, such as biting the tail, ear, flank, and vulva [ 24].

Entire males are more likely to have aggressive, and sexual behavior than castrated males [ 25]. In an earlier study [ 26] it was observed that, before the second dose of the immunocastration vaccine, sensitized pigs had testosterone levels comparable to that of boars. Males that show the mounting behavior more often have lower growth rates [ 27]. This negative relation may reflect a harmful effect on pig well-being. Thus, the use of enrichment objects may have contributed to keeping the low incidence of both behaviors, regardless of the use of scents. Synthetic maternal pheromone and non-maternal pheromones decreased aggressive behavior and improved weight gain and the feed efficiency in groups of pigs at weaning [ 28, 29]. However, non-pheromonal compounds or odor-masking agents were not as efficient at reducing aggressive behavior as pheromones and did not affect the performance [ 30]. The use of scents was successful in reducing aggressiveness when mixing pig batches or including new individuals in the group [ 31].

Animals in the treatments with objects containing banana or rum scents alone spent a lower percentage of the time eating and drinking compared to the control treatments or with other scents (p<0.05). This behavior may be related to the time those animals spent sleeping (approximately 72% of the time), which was 13% above the mean of the other treatments.

The presence of scents in the enrichment objects impacted (p<0.05) the time the animals spent interacting with them. The animals in the control treatment interacted with the objects more often, with a significant difference, compared to the treatment with banana scent. Such result shows that banana smell can be considered unattractive or repellent to the animal and, thus, inhibited the access to the objects. In a research where weaned, piglets subjected to transportation stress were exposed to banana scent, and maternal pheromone, it was observed that the animals spent more time resting compared to those in the control treatment [ 32]. However, exposing the piglets to scents may have caused fear since those animals showed lower latency time for the flight behavior. Rum scent was better accepted, and it is likely that the lower average observed for the treatment with other scents was due to the days in which banana essence was used. Pigs are omnivorous, and scavengers and odors related to feed are usually attractive. However, the scents used did not have the attractive effect expected.

The enrichment objects were attractive and stimulated the animals' interest in them, which was evidenced by an average of 9.6% of the total time spent interacting with the objects. This percentage becomes relevant when it is compared with the mean time the animals spent with other necessary activities such as eating or drinking (9.1% of the time) and nuzzling or exploring the environment (11.5% of the time). An environmental enrichment to be considered useful, it must be able to reduce abnormal behaviors and increase the behavior patterns considered normal for the species such as exploring, social interaction, and playing [ 5].

From these results, it is inferred that the scents did not play a stimulus role, neither they impact the animals' interest over the days ( Fig 8), while the physical characteristics of the object were responsible for its attractiveness. This result matches with that reported in a previous study [ 8] when assessing enriched environments for pigs, the authors concluded that objects scented garlic drew less interest from the animals compared to unscented objects.

Some studies have been conducted using a wide variety of flavors to identify those most preferred by pigs. Most studies reported a preference for a sweet taste like fruity flavors [ 33, 34]. In previous research [ 5, 35], scented objects draw high initial interest that, however, in not kept over time, while unscented objects were more efficient in keeping the pig's attention. On the other hand, in another study [ 36] when assessing natural and synthetic scents, the author reported that weaned piglets showed a keen interest in the objects and that strawberry scent was the preferred odor. However, it is recommended a refill of the essence every 14 days to maintain a proper attractiveness.

Another study related to environmental enrichment for pigs using straw or objects like toys found that it positively impacted neural development and behavioral traits [ 37].

Likewise, environmental enrichment with scented elements was found to promote behavioral changes [ 1]. The rearing environment enriched with objects is likely to instigate pig curiosity [ 31]. Likewise, it is recommended the straw or any other substrate being regularly replaced as a way of increasing the animals' interest in the enrichment factor. Cleaning the enrichment objects may also work as a strategy to stimulate the animals' interest [ 38].

However, the results of the present research suggest that the attractive effect of the enriching object was caused by the object's physical characteristics and not by the scents assessed. The hypothesis that exploring the pigs' olfaction as a form of enrichment and that alternating scents might extend their interest could not be confirmed in this study.

Trial 3

The environmental enrichment objects did not impact (p>0.05) the frequency of agonistic behaviors, interaction with the object, interaction with other pigs, or moving around or sitting ( Table 4) ( Fig 9).

Regardless of the treatment, the animals spent over 65% of the time sleeping or lying. However, the animals in the treatment which offered no reward for interacting with the enrichment object spent more time idle compared to those in the treatment with effortless reward. The group dealing with difficult level (pigs had to try harder to obtain the compensation) showed intermediate frequency of interaction with the object, not differing from the others. The rates of eating or drinking behavior varied, with the animals in the treatment with no reward spending less time eating and drinking than the others, whereas they spent more time sleeping.

The presence of the reward, as well as the level of difficulty, did not impact the time the animals spent interacting with the object (p>0.05). However, the animals in the treatment with effortless reward level spent more time exploring the environment (p>0.05) compared to those that had an object with no reward (14.52% vs. 4.06%) which shows that providing objects with an effortless reward may have encouraged the pigs' exploratory nature.

The exploratory behavior keeps the pigs abreast of the availability of resources, which is essential for their survival when they are dependent on exhaustible and seasonal sources of food. Although the species has been domesticated and fed by humans for several generations, the rooting appears to be a high-priority behavior. Pigs explore their surroundings by rooting, sniffing, biting, and chewing various food items as well as indigestible articles and become familiar with their environment and the different resources within it [ 19, 39].

The successful use of environmental enrichment is not based only on the activities targeted at the object, but also on how it may impact the pig's behavioral repertoire. The findings suggest that environmental enrichment objects with rewards enhance the pigs' curiosity and makes them more active during the day, thus contributing to reducing the stress generated by confinement. Pigs are opportunistic feeders and are attracted by readily available food sources, and the easy obtention of reward (popcorn) might have stimulated the exploratory behavior. However, in the current study, the increase in the difficulty in getting the compensation might have discouraged the pig's exploratory behavior (5.97%) since the animals were fed at libitum. Several studies show that restrictive feeding increases the occurrence of rooting behavior, i. e., appetitive foraging [ 40, 41] which implies that a greater motivation for exploratory behavior is to be expected in growing pigs when they are reared in feed restriction.

Although no difference was found between the frequency of interaction with the objects in the different treatments, the time the animals spent in this activity is significant at 4.18% of the total time. That makes it the fourth most exerted activity by the pigs over the assessment periods, however, it is less time than those observed in trials 1 and 2, whose objects had distinct characteristics and could be chewed by the animals.

Some authors [ 42- 44] reported that environmental enrichment measures decrease undesirable behaviors such as aggressiveness and increase specific natural behaviors of pigs, such as investigative conduct. Environmental enrichment increases brain neurotrophin levels, which are associated with better spatial learning, memory, and manifestation of the exploratory behavior [ 45].

Animals in the treatment with effortless reward dedicated less time to sexual behaviors compared to those that had objects with no reward (p<0.05). The ones in the group with difficult reward showed intermediate frequency of this type of behavior. Nonetheless, irrespective of the treatment, the incidence of this behavior was low, likely because they were all female.

The relationship between the number pigs and objects used in environmental enrichment might be a limiting factor in the success of the procedure since the low ratio can lead to competition and increase of aggressivity and frustration in the reared group. A study regarding this issue [ 46] indicates that there was not limitation in the access to the objects by the pigs up to the ratio 1: 32 (object: pig). In the present study, there was a ratio of 1:24. The absence of agonistic behaviors in all trials of the current study indicates that the number of objects in the pen was sufficient for all pigs.

In the present study, the objects in trials 1 and 2 were placed at the height of the animals eyes, as the literature suggests that when objects offered to pigs became dirty, the pigs lost interest in them [ 47]. In all trials, it was noted a trend of the pigs to remain resting during the day. Confined pigs tend to sleep mostly during the day when there is no motivation for exploring [ 14]. Comparing the pig behavior in indoor and free-range systems [ 48] found that pigs in an outdoor system are more active and perform more natural behaviors (foraging and rooting) than pigs in an indoor system. In the present study using several sources of environmental enrichment, the pig behaved more similarly to those reared indoors than that in the outdoor systems. In trials 1 and 2 the pigs interacted with the objects practically the same time as feeding, indicating high importance of the enrichment presence in the pen.

Environmental enrichment devices and different strategies of exploring opportunities should be further investigated in pig production, as it appears to amend welfare conditions during rearing.

Conclusion

The way the environmental enrichment objects were made available did not impact the success of their use. Offering enrichment on alternate days or removing the objects by the end of the day was not an effective strategy to extend the animals' interest.

The olfactory stimulus in environmental enrichment objects had no positive effect on extending the animals' interest on them, nor did alternating the aromas. The tactile stimulus was the key factor for object attractiveness.

Providing environmental enrichment objects with rewards stimulated the exploratory behavior of pigs. The level of difficulty to obtain the reward may discourage the animals.

Author Contributions

1. Conceptualization: FRC SPM.

2. Data curation: SPM LF RM VMOSN GFO.

3. Formal analysis: SPM LF RM LMPG.

4. Funding acquisition: FRC RGG.

5. Investigation: SPM LF RM.

6. Methodology: FRC SPM LF RM.

7. Project administration: FRC LF SPM RM.

8. Resources: FRC RGG IAN.

9. Supervision: FRC LF SPM.

10. Visualization: FRC LF.

11. Writing - original draft: FRC LF SPM.

12. Writing - review & editing: FRC LF LMPG.

# data[].attributes.attachment_link.title
Behavior of Pigs Reared in Enriched Environment: Alternatives to Extend Pigs Attention

# data[].attributes.attachment_link.description
Three trials were carried out in a completely randomized design aiming to assess the behavior of pigs in growth phase in enriched environments. Trial 1 evaluated the effects of frequency of availability of environmental enrichment.

# data[].attributes.body
The most frequently shown behavior was from “head to head” to “nosing”, and “nosing”. This is what they will get when getting ready to mount (H.Tanida)".

# data[].attributes.body
Swine experiences their different sexual behaviors around one month of age.

# data[].attributes.body
Sexual behavior is showing during this time for boars. They will not only mount females but males as well.

# data[].attributes.body
The courtship that was observed showed boars behaviors were broken down into seven categories: sniffing, head to head, nosing, following, chin resting, mounting and copulation (H.Tanida)".