ORIGINAL RESEARCH published: 03 December 2020 doi: 10.3389/fvets.2020.600259 Sex Differences in Group Composition and Habitat Use of Iberian Free-Range Pigs Antoni Dalmau 1*, Míriam Martínez-Macipe 1 , Xavier Manteca 2 and Eva Mainau 2 1 Institute of Agrifood Research and Technology (IRTA), Animal Welfare Program, Girona, Spain, 2 Universitat Autònoma de Barcelona (UAB), Veterinary School, Campus Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain The aim of the present work was to study group size, group composition and habitat use of Iberian pigs along the year when reared outdoor. This consists of a regimen in which animals are reared free range from 2 months of age until at least 14 months of age. In a first stage, animals are supplemented with concentrates, and in a second, called montanera, pigs eat just natural resources in areas with no more than two pigs per hectare. In these systems, males are castrated to avoid boar taint and females spayed to avoid the attraction and mounting by wild boars. The study was carried out in five different farms allocated in the south-west of Spain during 2 consecutive years, from March 2012 to February 2014, under the montanera regimen, and with a total of 995 animals observed (498 males and 497 females). The data were analyzed with SAS by Edited by: means of general models and proc mixed. Mean group size along the year was of 17 ± Janice M. Siegford, 12.9 individuals, but this was significantly lower (P < 0.05) during the montanera (12 ± Michigan State University, United States 0.8) and at midday (13 ± 0.8). Groups were bigger (P < 0.05) when they were more than Reviewed by: 50 m from a tree (23 ± 1.8), or <10 m from the shelter (25 ± 1.5), the feeding area (31 ± Nicolas Devillers, 3.1) and the water-bath area (25 ± 1.5). Nine percent of the groups were solitary animals, Agriculture and Agri-Food Canada (AAFC), Canada being higher (P = 0.0286) during the montanera (11%) than the rest of the year (8%) and Irene Camerlink, being formed in 68% by males. Males were less involved in mixed groups than were Polish Academy of Sciences, Poland females (75% vs. 91%), especially in spring, where the largest (P < 0.0001) male groups *Correspondence: were found. Female groups were less frequent and smaller (P < 0.0001) than were male Antoni Dalmau antoni.dalmau@irta.es and mixed groups. In conclusion, although males were castrated at a very young age, they showed a different behavior than females, forming in bachelor groups during the Specialty section: spring and being less involved in mixed groups and with more solitary animals. During the This article was submitted to Animal Behavior and Welfare, montanera, when animals were feeding on acorns and other natural resources, groups a section of the journal were smaller and closer to the trees, solitary males reaching a maximum percent. Frontiers in Veterinary Science Keywords: behavior, habitat, Iberian, outdoor, pig, population structure, sex differences Received: 29 August 2020 Accepted: 11 November 2020 Published: 03 December 2020 INTRODUCTION Citation: Dalmau A, Martínez-Macipe M, The Iberian Pig is a native breed of the Iberian Peninsula that originates from Sus scrofa Manteca X and Mainau E (2020) Sex Differences in Group Composition and mediterraneous and is reared in the south-west of the Iberian Peninsula (1). The Iberian Pig is Habitat Use of Iberian Free-Range characterized by its fat-production ability (2) and high rusticity. This enables the animals to cope Pigs. Front. Vet. Sci. 7:600259. better with climatic hazards. The Iberian Pig has been raised for centuries to produce dry-cured doi: 10.3389/fvets.2020.600259 meat. Currently, the meat is considered “Iberian” when it comes from a pig with a minimum of 50% Frontiers in Veterinary Science | www.frontiersin.org 1 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs of Iberian genetics, where the mother must be 100% Iberian the reproductive status. Although there is limited information (RD 4/2014). In the most traditional production system, Iberian available on the precise time of sexual maturity in Iberian pigs, piglets are weaned to at least 2 months old, and then they are it has been described that the Iberian female pig begins puberty mixed in large pastures. In these areas, they are given concentrate at an average age of 6 to 7 months (3, 19), and for boars it has been at the same time as having natural resources for several months, described to be from 7 to 9 months of age (20). Therefore, males until reaching around 90 kg−115 kg of body weight (2). The and females are reared for several months after sexual maturity. whole reproductive cycle of the animal is planned to provide As a result, in males, castration is required to avoid boar taint an adequate physiological status capable of taking advantage in their final product (21), and females are spayed. The negative of La Dehesa during the late fattening phase. La Dehesa effect on growth due to oestrous behavior in Iberian females is a Mediterranean ecosystem based on oak forest (Quercus (22, 23) or in other breeds slaughtered at heavy weights (24) has rotundifolia and Quercus suber) with herbaceous species, mainly been suggested to justify the need for spaying, but according to grasses and legumes, where animals can graze (3). In fact, in Dalmau et al. (25), the main reason to justify spaying in these late autumn, when the acorns from the oaks (Quercus ilex) and females is the presence of wild boars in La Dehesa. In fact, the cork oaks (Quercus suber) fall, pigs eat only the acorns and other cohabiting of wild boars with entire females can produce a high natural products like tubers, grasses, legumes, fungi or roots from percentage of pregnancies, which disturb the production cycle the dehesa pastures (4). This late fattening phase at La Dehesa is and could have sanitary and ethical problems. called “montanera” and the pigs must gain their last 50 kg−60 kg Rodríguez-Estévez et al. (1), studied group size and resting based only on that type of food source (5). In fact, pigs feeding locations of free-range pigs during the montanera and concluded freely during the montanera season are regarded as a distinctive that pigs split into small groups during daytime to forage but then mark of the best quality Iberian pig products (6). Rodríguez- rest together in a larger group to spend the nights in a common Estévez et al. (7) measured a daily consumption of 7.1 kg−8.4 kg area. Nevertheless, no studies exist regarding the group size or of acorns and 2.0 kg−2.7 kg of fresh grass during this phase. composition (male, female, and mixed groups) in these animals Iberian pigs should be slaughtered at least at 14 months of age along the year. This should include the two types of feeding and a body weight of 150 kg−160 kg (RD 4/2014). The regulation schedules: first, when they are fed with concentrate given by the requires <2 pigs/ha during the montanera; however, the stocking farmer, and later, during the montanera, when they need to search rate used is lower in practice, because pigs are not allowed to for food available only from natural resources. This changes the receive any kind of feed or alimentary supplement during this activity budgets (26), so it is expected to produce changes in phase. Hence, the stocking rate is typically <1 pig/ha (8). the group size and composition. Finally, in swine species the Pigs are social animals and usually live in groups (9, 10), dominance order is resource-related (27), so it is hypothesized performing a wide repertoire of sexual, feeding and social that different kinds of resources in free-range situations, such as behaviors (11, 12). Living in groups is regarded as an anti- trees, shelter, water bath area, drinking or feeding area and fences predator tool for many ungulates: it reduces the predation risk, could interact with group size and composition in Iberian pigs on the one hand, by the numerical dilution and, on the other, reared outdoors. by having more vigilant animals able to warn the others about Accordingly, the aim of the present study was to study the a coming danger. This anti-predator adaptation is especially group size and composition (males, females and mixed groups) in common in species living in open habitats (11) and it is part of relation to their feeding regimen (animals fed with concentrates a cooperative behavior in which some individuals may benefit or maintained at montanera with no supplementation), and from having others entering potentially dangerous areas first (13). distance to different resources (trees, shelter, feeding area, However, pigs could find more protection in areas covered by drinker, fences and water bath area) along the year in Iberian trees, where group sizes could be smaller. It is assumed that pigs reared in outdoor conditions in five different farms in the domestic pigs, if given the chance, show the same behavior south-west of Spain. repertoire as do wild boars (9, 14). In fact, Stolba and Wood-Gush (1989) described wild boars as gregarious animals that typically live in groups, mainly composed of females with their offspring, MATERIALS AND METHODS in matriarchal hierarchies, and Copado et al. (15) observed in free-ranging domestic pigs of different ages that adult females Data were collected at five different farms dedicated to Iberian were the group leaders with strong cohesion and stable social pig production in Extremadura, Spain. The study was performed hierarchies. This sexual segregation has been observed in other during two consecutive production cycles (from spring, at 3 to ungulates and determines different group sizes and habitat uses 6 months of age, until slaughter the following winter, at 14 to in males and females (16). In fact, space preferences for different 17 months age), from 2012 to 2014. In consequence, each pig activities have been described in pigs (17, 18). was studied for around 12 months. Pigs were in all cases pure The traditional Iberian pig production system provides an Iberian breed or crossed to 50% with duroc (male duroc x female opportunity to study the flexibility of social organization of a Iberian pig). Animals 100% Iberian were born around September large group of pigs at an extremely low stocking rate. However, the previous year, and animals 50% Iberian were born around two considerations should be considered. The first one is that in December the previous year. A farm contained only one type of contrast to natural wild boar or even feral pigs, in these groups genetics. The quantity of animals studied varied with the farm all animals have a similar age. The second one is related with and production cycle (Table 1). In all farms, males and females Frontiers in Veterinary Science | www.frontiersin.org 2 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs were neutered according to the commercial practices in the area. of the visits), summer (June, July and August; with 38% of the In the case of males, this means that surgical castration was visits), autumn (September, October, November; with 23% of the performed before 1 week of age, and in the case of females that visits) and winter (December, January and February, with 21% spaying was performed at around 2 months of age. Sex ratios of of the visits). The montanera could be slightly different among female:male ranged from 0.8 to 1.3. After weaning, at around 2 different farms, but it covered mainly the late autumn and all months of age, pigs were allocated in the study areas, between 1 winter (Table 1). Three periods of the day were considered for the and 3 months before beginning the observations in March, and analysis, morning (from 7:00 to 11:59 h), midday (from 12:00 to they were never mixed again with unknown animals. From this 14:59 h) and afternoon (from 15:00 to 21:00 h). Therefore, in the moment, pigs were reared in a free-range area where a zone to present study, the term montanera includes a specific period of receive food (feeding area), drinkers, a shelter and a pond (water the year (late autumn and winter), when the animals were older, bath area) were provided within a total space allowance from 7 to had more space (at least one hectare per two pigs) and were fed 67 pigs per hectare. The free-range area included oaks and other just with natural resources (with a high presence of acorns). In normal dehesa vegetation, and pigs were fed with concentrates addition, the season/age effect was linked to an age effect, was (3,000 Kcal EM/kg) once a day, in the morning, in a restricted animals were younger in spring and older in winter. regimen that ranged from 2 kg per animal during the spring and early summer to 1 kg per animal in the most restricted period Statistical Analysis at the late summer and early autumn. When the acorns started Analyses were carried out with the Statistical Analysis System to fall in early winter, the montanera period started (Table 1), (SAS software, SAS Institute Inc.; Cary, NC, USA). The size and pigs (1) were moved to a bigger landscape or (2) another of the observed groups (1,247 in total) were studied according part of the free-range area was open to provide more space and to the fixed effects: montanera (yes or no), time of the day resources, in all cases ensuring a density of less than two pigs (morning, midday and afternoon), season/age (spring, summer, per hectare, with a maximum study area of 180 ha. During this autumn and winter), and distances to fences, trees, water bath period, animals were not fed by farmers. areas, shelter, feeding area and drinkers (<10, 10–50, and >50 Each farm was visited once every 1 or 2 weeks, from 7:30 meters) and interactions. Space allowance was as well-included to 21:00 h. Eight percent of the observations were carried out as covariable. For those groups in which all males and females from 07:30 to 09:30 h, 56% from 09:30 to 11:30 h, 27% from were identified (579 in total), the models considered as a fixed 11:30 to 13:30 h, 2% from 13:30 to 15:00 h and 7% from 17:00 effect the same as that described previously, considering as well to 21:00 h, avoiding the times when animals were fed during the type of group (only females, only males and mixed groups) the non-montanera period. To observe the animals, the same and interactions between type of groups and the rest of fixed observer traveled every day to different farms (allocated a mean effects. The observation day and the farm∗ year effect (1 to 8 herds time of 1 to 2 h from each other). The animals were approached taking into account the five and three farms assessed the first on foot and observed from a distance, trying not to be noticed by and second year, respectively) were also included in the models using binoculars. During a pilot study for the selection of farms, as a repeated measure. As residuals were normally distributed, the different resources found in the study area were defined and mixed models by means of Proc Mixed were used. The least- described, such as trees, water bath area, shelter, feeding area and square means of fixed effects (LSMEANS) was used when the fences, which are common elements in this type of farms. The analysis of variance indicated differences. For the analysis of feeding area consisted in a concrete zone with 0.5 to 1.0 m2 per solitary animals or presence of males and females in mixed animal where pigs were fed all at the same time by leaving the groups a proc Glimmix with a binomial distribution was used. concentrate on the floor. This area was just besides the entry For the incidence of different group types (male, female and to the landscape for facilitating the storage and disposal of feed. mixed groups) a proc Glimmix with a multinomial distribution Drinkers were in all cases allocated besides the feeding area too. was used. In addition, spearman correlations were studied for the Only in farm 4 the shelter was at < 300 m to the feeding area distances to different resources in relation to the season/age of the (around 220 to 260 m) and in all the rest of cases it was at more animals (from spring to winter), montanera and moment of the than 300 m of distance. The water bath area was as well in all cases day (from morning to afternoon). In all cases, significance was allocated to more than 300 m from the feeding and shelter areas, fixed at P < 0.05. except in farm 4 that it was at 250 m from the shelter. During the visits, the observer indicated, for each group of animals, RESULTS how far the group was from each element (<10 m, between 10 and 50 m or >50 m); how many animals and, when possible, Group Size what gender (male or female), formed the group. A group was The five herds studied the first year and the three studied the considered any animal or animals located at more than 50 meters second, accounting for a total of 647 and 348 Iberian pigs, from any other animal (9, 28). A Leica Disto (Barcelona, Spain) respectively, were found to have formed a total of 1,247 groups. distance-meter was used for the distance measurements. For each This represents five groups per observation period, with a mean visit, two observation blocks were made 2 h apart. A total of 260 ± SD size of 17 ± 12.9 individuals per group. Solitary animals, observations were performed. The assessments were performed those found more than 50 meters apart from any other individual, from a distance to ensure that animals were followed when represented 9% of the groups. A group containing all the animals walking, foraging or lying. The four seasons of the year were of a herd was only seen in seven observations: in Farm 2 four considered as well: spring (March, April and May, with 18% times, with 127 individuals; in Farm 4 just once, with 200 Frontiers in Veterinary Science | www.frontiersin.org 3 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs TABLE 1 | Number of visits to each farm, percentage of purebred, quantity of pigs in the 1st and 2nd year, available area during the year and during montanera, dates of montanera start for the 1st and 2nd year of study. Farm 1 Farm 2 Farm 3 Farm 4 Farm 5 Visits 28 44 15 26 17 % Purebreed 50% 100% 100% 100% 50% Pigs at first year 94 127 145 140 141 Sex ratio (females/males) 0.9 1.1 1.3 1.1 0.8 Space allowance during the no montanera 13 pigs/hectare 11 pigs/hectare 18 pigs/hectare 47 pigs/hectare 14 pigs/hectare Pigs at second year 61 87 0 200 0 Sex ratio (females/males) 1.3 0.9 0 0.9 0 Space allowance during the no montanera 8 pigs/hectare 7 pigs/hectare 0 67 pigs/hectare 0 Date to the first montanera 13/11/2012 21/11/2012 23/11/2012 14/12/2012 12/11/2012 Space allowance during the montanera 1.8 pigs/hectare 0.7 pigs/hectare 1.8 pigs/hectare 1.2 pigs/hectare 1.8 pigs/hectare Date to the second montanera 14/11/2013 19/11/2013 0 6/11/2013 0 Space allowance during the montanera 1.2 pigs/hectare 0.5 pigs/hectare 0 1.6 pigs/hectare 0 Landscape characteristics Mountainous area (slopes >30◦ ) Plain Plain Small hills Small hills individuals, and in Farm 5 twice, with 141 individuals. In all of (Table 2). The second structure with more groups situated to these cases, this occurred during the non-montanera period. The <10 meters away was fences, with 38% of the groups seen at this most typical size of groups was from two to 25 animals (two to distance. On the other hand, most of the groups were seen to four animals accounting for 23% of the total; five to 10 animals, be more than 50 meters from shelters, drinkers, water bath and 24% of the total, and 11 to 25 animals, 25% of the total). Finally, feeding area (90, 89, 83, and 76%, respectively). To be closer to a groups larger than 26 animals accounted for a total of 19% of the tree was positively correlated with the montanera (r = 0.40) and total observations. Considering all groups observed, those found season/age of the animals (r = 0.50, Table 2). Groups of solitary in Farm 1 represented 20% of all groups observed, those from animals represented 7% of the total in spring, 8% in summer, 12% Farm 2, 31%, those from Farm 3, 10%, those from Farm 4, 27%, in autumn and 10% in winter. However, no significant differences and those from Farm 5, 12% (Figure 1). were found among seasons for this type of group. In contrast, the Group size was affected by the montanera (P = 0.0008), by the percentage that groups of solitary animals represented of the total time of the day (P = 0.0044), distance to the trees (P = 0.0264), was higher (P = 0.0286) during the montanera period (11%) than distance to the feeder (P < 0.0001), distance to the water bath the rest of the year (8%). area (P = 0.0199), and distance to the shelter (P = 0.0084), with just a trend for season (P = 0.0974). Twenty-nine percent of Type and Composition of the Groups the groups were observed during the montanera period, being Considering the 579 groups where all the animals could smaller (12 ± 0.8 individuals per group) than the other 71% be identified by sex (male or female), 14% were formed of the groups found the rest of the year (19 ± 0.8 individuals only by females, 26% only by males and 60% were mixed per group; Figure 2). Groups were smaller at midday (mean size groups (with at least one male or one female). An effect of ± SE; 13 ± 0.8 individuals per group), as compared with the season/age (P = 0.0147) was found for group composition, morning (19 ± 1.0 individuals per group) or the afternoon (19 autumn, with the lowest percentage of mixed groups (15, 33, ± 2.4 individuals per group). Group size at more than 50 m from and 52% of female, male and mixed groups, respectively), a tree was bigger (23 ± 1.8 individuals per group) than at 10 to being statistically different from summer (12, 23, and 50 m (16 ± 1.4 individuals per group) or <10 m from a tree (18 65% of female, male and mixed groups, respectively) and ± 1.4 individuals per group). Group size at <10 m from a feeder winter (16, 21, and 63% of female, male and mixed groups, was bigger (31 ± 3.1 individuals per group) than at 10 to 50 m (13 respectively). In addition, spring (15, 25, and 61% of ± 2.8 individuals per group) or more than 50 m from the feeder female, male and mixed groups, respectively) was different (14 ± 1.7 individuals per group). Group size at <10 m from the from summer. water bath area was bigger (25 ± 2.9 individuals per group) than An effect of group type was found on group size (P < at more than 50 m from a water bath area (19 ± 2.3 individuals 0.0001), female groups being smaller (mean 5 ± 0.9 animals per group). Finally, group size at <10 m from a shelter was bigger per group) than male and mixed groups (9 ± 0.8 and 11 ± (25 ± 1.5 individuals per group) than at 10 to 50 m (15 ± 1.2 1.3 animals per group, respectively). In addition, a montanera individuals per group) or more than 50 m from the shelter (18 ± effect (P = 0.0020), an interaction montanera∗ group type (P 1.4 individuals per group). = 0.0004), and an interaction season∗ group type (P < 0.0001), Globally, the 1,247 groups were closer to the trees (66% of but not an effect of season (P = 0.1833) were found for group the groups being at a distance of <10 meters from a tree) than size. While female and mixed group sizes were not different to the feeding area, drinker, water bath area, shelter and fences between montanera and no montanera periods, male group Frontiers in Veterinary Science | www.frontiersin.org 4 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs FIGURE 1 | Percentage of groups of different sizes (one; two to four; five to 10; 11 to 25; and more than 25 animals per group) per each farm (1 to 5) for Iberian pigs reared free-range from a total of 1,247 groups observed. FIGURE 2 | Percentage of groups of different sizes (one; two to four; five to 10; 11 to 25; 26 to 60; and more than 60 animals per group) in Iberian pigs reared free-range when being fed with concentrates (Fed) and when feeding just with natural resources [Not fed (montanera)] from a total of 1,247 groups observed. Frontiers in Veterinary Science | www.frontiersin.org 5 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs TABLE 2 | Spearman correlation results for the effects montanera (being fed just with natural resources, with a maximum density of 2 pigs per hectare in the late autumn and winter) in comparison to no montanera (being fed with natural resources and concentrate, with a maximum density of 67 pigs per hectare in spring to early autumn), later during the day (defined in base to observations during the afternoon and midday in comparison to the observations in the morning), and older (related with the age of the animals along the year, being the oldest in winter and the youngest in spring) according to distances to trees, drinker, feeder, water bath area, fences, and shelter areas (positive correlation showing a shorter distance to these resources and negative correlation a longer distance). Montanera Moment of the day Season Yes (%) No (%) r Morning (%) Midday (%) Afternoon (%) r Spring (%) Summer (%) Autumn (%) Winter (%) r Distance to trees <20 m 95 53 0.40 63 74 41 0.06 27 59 84 94 0.50 20–50 m 3 9 6 8 14 10 10 2 4 >100 m 2 38 31 18 45 63 31 14 2 Distance to Feeder <20 m 4 16 −0.21 15 7 16 −0.12 13 16 17 2 −0.13 20–50 m 6 13 13 8 11 9 15 13 4 >100 m 90 71 72 85 73 78 69 70 94 Distance to drinker <20 m 2 8 −0.14 7 4 13 NS* 7 9 6 2 −0.08 20–50 m 2 5 4 3 13 4 5 7 2 >100 m 96 87 89 93 74 89 86 17 96 Distance to water bath <20 m 4 11 −0.14 8 9 20 NS 5 14 10 4 NS 20–50 m 5 9 8 9 4 6 10 9 5 >100 m 91 80 84 82 76 89 76 81 91 Distance to fences <20 m 31 40 −0.09 42 30 39 −0.10 34 41 39 32 NS 20–50 m 16 15 15 15 13 18 12 15 17 >100 m 53 45 43 55 48 48 47 46 51 Distance to shelter <20 m 2 9 −0.14 7 6 11 NS 18 5 5 2 −0.17 20–50 m 1 3 3 2 9 2 4 3 1 >100 m 97 88 90 92 80 80 91 92 97 *NS, not significant correlation at P < 0.05. size was higher (P < 0.0001) during the no montanera (4 ± proportion of mixed groups with more males than females being 1.3 individuals per group) than during the montanera (2 ± lower in the montanera (25% out of the total) than in the non- 0.2 individuals per group). Actually, male groups were bigger montanera (39% out of the total). The number of females in in spring to any other group type in this season and to the mixed groups was lower (P = 0.0036) during the non-montanera male group size at any other season (Figure 3), while mixed (4.1 ± 0.32) than during the montanera (5.0 ± 0.47). For males, groups at spring were smaller than at any other season/age although no significant differences were found, the number of (Figure 3). males in mixed groups was 4.3 ± 0.44 and 3.7 ± 0.31, during Females were more present (P = 0.0005) in mixed groups the non-montanera and the montanera, respectively. Overall, than males. Overall, 91% of the females were found in mixed two percent of males and females were found being solitary. groups, while this was the case only for 75% of the males. However, in males, this percentage was higher (P < 0.0001) However, these figures were different along the year (P < 0.0001; during the montanera (3.7%) than in the rest of the year (1.9%). Figure 4). Males were less present in mixed groups in spring Overall, 68% of all solitary animals were males and the rest, 32%, than in the rest of the year. Overall, the number of males and were females. females in mixed groups was of 4 ± 0.3 in both cases, but a An interaction distance to the feeder∗ group type (P = seasonal effect was found for males (P = 0.0059) and females 0.0082) and distance to the shelter∗ group type (P = 0.0253) (P = 0.0125), in both cases being lower in spring, with 2 ± was found for group size, in both cases the male groups 0.3 males and 3 ± 0.4 females per mixed group, respectively. found at <10 m from these resources being in bigger groups Forty-nine percent of the groups had a sex ratio weighted in than female and mixed groups at the same distance, or male favor of the females (the maximum proportion being found groups at other distances. However, more mixed groups were of 9 females for one male) and another 17% had a sex ratio found at <10 m from the feeding area (P < 0.0001) than exactly of one. Therefore, only 34% of the mixed groups had in other positions, while the contrary was found for shelter more males than females (the maximum being a proportion of (P = 0.0138) and fences (P = 0.0290), where more mixed 8.5 males for one female). No effect of season was observed, groups were found to >50 m from these resources than at but an effect of montanera (P = 0.0430) was found, with the other distances. Frontiers in Veterinary Science | www.frontiersin.org 6 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs FIGURE 3 | In the left axis and with bars, mean number of animals per group (female, male, and mixed groups). In the right axis and with lines, percentage of solitary females and males out of the total females and males observed for the different seasons (spring: March to May; summer: June to August; autumn: September to November and winter: December to February) in free-range Iberian pigs, being the youngest in spring and the oldest in winter. FIGURE 4 | In the left axis and with bars, percentage of males and females out of the total of males and females observed found in mixed groups (groups with at least one male and female). In the right axis and with lines, percentage of mixed groups where more males than females are present and percentage of mixed groups where more females than males are present, observed for the different seasons (spring: March to May; summer: June to August; autumn: September to November and winter: December to February) in free-range Iberian pigs. Frontiers in Veterinary Science | www.frontiersin.org 7 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs DISCUSSION animals of at least 13 months of age during the montanera, found a group mean size of 9 animals, closer to the 12 animals found In the present study, only 2% of males and females were found during the montanera than the 17 during the non-montanera in to be solitary along the year. While the benefits of group living the present study. have been fully described (11), and being alone can be risky The fact of a reduced number of animals per group during the for the individual, it has some advantages as well, such as less montanera could be explained because of the age of the animal, competition for resources. Gabor et al. (29) found that 41% of because more space was available or because they needed to be the feral pigs studied were solitary, and Gabor and Hellgren more focused on feeding strategies in forest areas and less on (30) described 27% of the observations as solitary peccaries. forming big groups in more open areas as in an anti-predator In our study, solitary animals accounted for only 9% of the strategy (40). In fact, Martínez-Macipe et al. (34) found a clear groups, achieving a maximum during the montanera of 11% of increase in exploratory/foraging behavior in Iberian pigs during the groups (when the animals were older and more space was montanera, in comparison to previous seasons where animals available), with 3.7% of the males being solitary. In addition, were fed, and in the present study, being in the montanera was 68% of the solitary animals were males. Therefore, although the positively correlated with being closer to trees and negatively percentages are far from those found in feral pigs or peccaries, with being closer to any other structure (fences, feeding area, some sexual divergence in pig behavior during the montanera drinker, water bath area and fences). Accordingly, Rodríguez- was found, with males seen more frequently alone. Estévez et al. (1) determined that pigs grazing together accounted Mature males are the most seen solitary type of animal in wild for four or fewer individuals, but when they were seen eating boar and warthog (31). Puberty arrives at an average age of 6 to 7 acorns there were only one or two animals together. Another months for females and 7 to 9 months for males (3, 19, 20), and effect found during the montanera was an increase in the number pigs in the present study were studied until 14 to 17 months of of mixed groups that contained more females than males. In age (montanera beginning at 10 to 13 months old). Nevertheless, fact, the presence of females in mixed groups increased during the males of the present study were castrated, and according this period, in comparison to the rest of the year. In males, to Reiland (32) and Sipos (33) they were just adolescents, as only a numerical difference was found (not significant), but the adulthood arrives later than 17 months of age. In consequence, combination of both factors is what could explain that during it was not expected to have an important part of the population the montanera, only 25% of the mixed groups contained more behaving as mature animals. Accordingly, there is just a minority males than females, being 39% for the rest of the year. As of the animals being alone, as most of the pigs studied, males mentioned previously, during the montanera, the number of and females, formed into groups. Although the risk for predation solitary males increased significantly, and in comparison to other is low for these Iberian pigs in the areas where they are reared, seasons, male group size was lower. Therefore, while females Martínez-Macipe et al. (34) described in the same farms how maintained a similar gregariousness in all seasons, males showed animals at the periphery of the groups were more vigilant than more differences along the year, while they were growing and were animals in the center, so some anti-predator instinct is becoming older. During the spring, for instance, these younger maintained in these animals and, accordingly, a high percentage males reduced dramatically their presence in mixed groups and of gregariousness would be expected. very clearly increased the male group size. The consequences It has been described that pigs in natural environments form of that was a reduction in the mixed group size instead of a matriarchal social groups consisting of 2–4 closely related sows reduction in the incidence of these types of groups. In general, and their offspring of different sizes and ages. As the offspring females formed smaller groups along the year than did males, mature, some of the females split off to form their own group explaining this reduced size in mixed group size when males were and the males split off to form adolescent bachelor groups, less interested in staying with females (at the youngest ages). becoming solitary as mature boars (9, 35, 36). Battocchio et al. The figure of little presence of young males in mixed groups (37), described a group size of 8–9 animals for wild boars, but just forming big groups without females is typical of several Focardi et al. (38) found quite variable group sizes. In fact, species, such as Przewalsky horses (Equus przewalskii), (41), Focardi et al. (13) described that group size and the frequency Pyrenean chamois (Rupicapara pyrenaica) (16) or guanacos of mixed-sex groups are typically larger in autumn-winter after (Lama guancioe) (42), and they are called bachelor groups, weaning and during the rut. In production systems, the herds are described too in wild boar (9, 35, 36). However, it should be biased in age (all have the same age) and numbers (it is decided expected that this social structure would be maintained longer, by the farmers and not by the availability of ancestors), so groups and in the present study in summer this changed to another are artificially equal in age and big in size. However, in the present social structure. Actually, summer was the season with more study, all of the herd were rarely seen in a single group, and mixed groups found (65%), and males and females reached this never happened during the montanera, when the animals the maximum involvement in mixed groups (90% of the total were older and more space was available. In contrast, 81% of the of males and 93% of the total of females; Figure 4), and this groups found in this study had from 1 to 25 individuals, which meant an important change, in comparison to the previous is in accordance with Romero et al. (39) in peccaries (1–6, 8– season, again, especially for males. The dehesa is described as an 14, 16–21) and Gabor et al. (29) in feral pigs (5–27 animals). ecosystem in which species of herbs, bushes and trees coexist in Rodríguez-Estévez et al. (1), studying an Iberian pig herd with a semi-desert regime (43), and summer, when temperatures of Frontiers in Veterinary Science | www.frontiersin.org 8 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs 40◦ C with very low humidity can be reached, is the maximum the feeding regimen are three items associated to the Iberian pig exponent of this desert-like environment. Iberian pigs can eat finalized in the montanera, and it is not possible to determine the ad libitum during the montanera (considered the fattening- weight of each one of these factors separately in the results found finishing phase), when several natural resources are available, in the present study. but during the time before this last phase, restricted feeding is used. In the traditional rearing systems this was due to CONCLUSIONS the scarce feeding resources during the summertime, which is hot and dry. Nowadays, that these animals are supplemented The Iberian pigs observed along the year in the present study with concentrates, a restricted feeding is deliberately used showed a gregarious behavior, with only 2% of the males and before fattening to increase fat deposition in the finishing (44). females found as being solitary animals. Although males and Therefore, although the animals are fed, they are maintained, in females were castrated and spayed, respectively, some divergence most cases, below their needs, and the natural resources in this in the behavior of both sexes was found. The aggregation season are extremely scarce, so this could explain the important structure of females was more stable along the year, with females changes seen in the group composition and sizes from spring to forming in smaller groups and having a higher presence in mixed summer. In fact, during the first year of the present study, the groups than did males. Males formed in bachelor groups in total rainfall registered in the area was of 365 mm (with 60, 0.3, spring, when they were the youngest, with a very low presence in and 240 mm in spring, summer and autumn, respectively) and mixed groups, but this changed in summer, when the maximum during the second year of 646 mm (with 266, 6, and 165 mm group size and presence of mixed groups was found, which in spring, summer and autumn, respectively). Therefore, both coincides with the hardest season for pigs in terms of availability summers were extremely dry. of food. During the montanera, when the animals were older and In the study area, especially in rainy years, autumn offers more space was available, the presence of males in mixed groups another important change in the natural resources available was reduced again and the incidence of solitary males increased. for pigs. In the years when these animals were studied, the Solitary males represented two-thirds of the solitary animals, temperature ranged from 9 to 32◦ C and rainfall represented males showing less affinity for other males than did females for from 25 to 65% of the annual precipitation during autumn. other females. During the montanera, when the animals were Therefore, although the montanera began approximately at mid- feeding on just natural resources, groups were smaller and were November in most cases (Table 1), autumn, in which pigs are found closer to trees than the rest of the year. still fed with concentrates for around 80% of the days, should be considered a pre-montanera season. Actually, it is clearly a transitional phase between the hard summer, where animals DATA AVAILABILITY STATEMENT extremely depend on concentrates that are provided under a The raw data supporting the conclusions of this article will be restricted regimen to the winter, when a great quantity of acorns made available by the authors, without undue reservation. will be available and pigs will survive just from natural resources. Accordingly, the groups at <10 m from a tree increased from 59% in summer to the 84% found in autumn (even being under ETHICS STATEMENT the same landscape conditions, including space allowance). This percentage was then of 94% in winter, but in this case with a clear The animal study was reviewed and approved by The increase in space allowance (from 7–67 to 0.5–1.8 pigs/hectare). Institutional Animal Care and Use Committee (IACUC) of In addition, autumn was the season with the minimum incidence IRTA with the comment No intervention on the animals. of mixed groups (54%), and an increase in the presence of solitary Observational study. males and females was observed (Figure 3). In addition, an important reduction from summer to autumn, and maintained AUTHOR CONTRIBUTIONS in winter, was observed in the number of mixed groups with more males than females (Figure 4), confirming that autumn is AD was responsible for the development of the study, supervision really a transitional phase from summer to winter. Later, the main of the analysis, collection of the data, and writing the paper. difference found in winter was a slight, but significant, increase MM-M was responsible for collecting and analyzing the data of mixed groups in relation to autumn. Therefore, instead of an and writing a first draft of the paper. XM performed advisory increase in sexual aggregation, according to the figures found functions and collaborated in the development of the study. in percentage of males and females in mixed groups (Figure 4), EM was responsible for training MM-M and collaborated this could be the effect of more mixed groups with a slight in the supervision of the data analysis and writing of the reduction in group size. As discussed previously, the differences paper. All authors contributed to the article and approved the in group sizes could be associated with the age of the animals, submitted version. the feeding regimen or space allowance, so animals with a greater presence close to the trees and eating acorns, which happened FUNDING more frequently in autumn and winter (especially during the montanera) formed smaller groups than in previous periods. This research was funded by the Spanish National Institute of Unfortunately, the space allowance, the age of the animals and Agricultural Research (INIA-RTA2010-00062-CO2). Frontiers in Veterinary Science | www.frontiersin.org 9 December 2020 | Volume 7 | Article 600259 Dalmau et al. Group Composition in Iberian Pigs ACKNOWLEDGMENTS the Government of Extremadura. We are extremely thankful to them and the staff who helped us to find the animals The study was conducted within commercial farms whose and gave us vital information. Aeceriber is acknowledged as owners voluntarily allowed us access to the pigs’ enclosures well for their help in selecting the farms and contacting and also inside the experimental farm of Valdesequera, of the farmers. REFERENCES 19. Gonzalez-Añover P, Encinas T, Gomez-Izquierdo E, Sanz E, Letelier CA, Torres-Rovira L, et al. Advanced onset of puberty in gilts of 1. 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Buddies and bullies: social original publication in this journal is cited, in accordance with accepted academic structure of a bachelor group of Przewalski horses. Appl Anim Behav Sci. practice. No use, distribution or reproduction is permitted which does not comply (1988) 21:169–85. doi: 10.1016/0168-1591(88)90106-2 with these terms. Frontiers in Veterinary Science | www.frontiersin.org 11 December 2020 | Volume 7 | Article 600259