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Social interactions, cortisol and reproductive success of domestic goats (Capra hircus) subjected to different animal densities during pregnancy
Applied Animal Behaviour Science 147 (2013) 117–126
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Social interactions, cortisol and reproductive success of domestic goats (Capra hircus) subjected to different animal densities during pregnancy Judit Vas ∗ , Rachel Chojnacki, Marte Flor Kjøren, Charlotte Lyngwa, Inger Lise Andersen Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway
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Article history: Accepted 7 April 2013 Available online 29 May 2013 Keywords: Goat Density Social behaviour Agonistic Cortisol Pregnancy
a b s t r a c t Although goats in many countries are kept indoors in the winter season, during gestation and kidding, recommendations and regulations regarding available space per goat are highly variable. The effects of different housing conditions on the welfare and behaviour are understudied in this species. The aim of the present study was to observe some behavioural, physical and physiological parameters of pregnant dairy goats kept indoors at different animal densities, and their possible influence on reproduction data was also followed. Pregnant Norwegian dairy goats from early pregnancy until parturition were kept constantly at 1, 2 or 3 m2 per animal. Their social behaviour (offensive, defensive, socio-positive), body condition, weight gain and blood cortisol level were monitored throughout pregnancy. Weight and gender of offspring were recorded. We found that goats kept at higher density showed more offensive and defensive behaviours, but there was no difference in socio-positive behaviours between treatments. The increase in agonistic behaviours was not reflected in blood cortisol level, weight gain or production data. We concluded, that higher frequency of agonistic behaviours is present even at 2.0 m2 per animal, and if this is regarded as a sign of social stress recommendations regarding available space per goat should be adjusted. However, keeping goats even at 1 m2 per animal did not have any impact on productivity or weight development, suggesting that they easily habituate to sub-optimal environmental conditions. © 2013 Elsevier B.V. All rights reserved.
1. Introduction High animal densities are reported to increase the frequency of aggression, behavioural problems and reduce performance in a large number of domestic species (reviewed by Estevez et al., 2007) but only a few studies have been conducted in goats and most addressed the effects of feeding space and resting space rather than
∗ Corresponding author. Tel.: +47 64965240; mobile: +47 95104407; fax: +47 64965101. E-mail address: judit banfi[email protected] (J. Vas). 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.04.009
the total amount of space available per animal. Loretz et al. (2004) found that goats rested less with the smallest space allowance but the aggression level remained surprisingly low across densities within a range of 1.0–2.0 m2 per animal. However, the study contained a mixture of breeds, including meat production breeds that might be less aggressive and the goats were in late pregnancy which is a period when they engage in fewer conflicts (Andersen et al., 2008). The increased aggression level with reduced space can largely be explained by the reduction in individual distance, forcing individuals to interact with a limited opportunity to escape from an attacker. Due to the reduced opportunity to escape and communicate in a clear way with
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other group members, more individuals are likely to engage in social conflicts (i.e. fear-induced aggression when escape is no longer an option). Although reduced feeding space increased the amount of agonistic interactions quite substantially in goats (Jørgensen et al., 2007; Loretz et al., 2004), the organization of resting space appears to be more influential than the amount of resting space per se. Sheep, another small ruminant species, are often used as reference in goat studies to generate hypothesis and interpret results because there are fewer studies on goats than sheep (e.g., Ehrlenbruch et al., 2010; Siebert et al., 2011). At the same time, results on behavioural changes to different housing conditions suggest that these two species may respond quite differently to similar environmental conditions and findings in sheep must be treated with caution if extended to goats. For example, in contrast to goats, reduced resting space produced a significant increase in the number of displacements in sheep (Bøe et al., 2006). Sheep and goats both seemed to maximize the individual distance to a large extent with respect to the space available in the pen (Aschwanden et al., 2008; Jørgensen et al., 2009), but sheep were more tolerant towards resting in body contact with other group members than what is shown in dairy goats (Bøe et al., 2006; Andersen and Bøe, 2007). Sheep and goats showed a clear preference for resting against a wall (Andersen and Bøe, 2007; Bøe et al., 2006). Elevated resting platforms in addition to ground floor resting areas increased the individual distance between goats when resting and reduced the level of social conflicts (Andersen and Bøe, 2007) however, providing extra walls in the pens on the same floor level did not affect agonistic interactions at all (Ehrlenbruch et al., 2010). In contrast, sheep showed a reduction in some agonistic behaviour when extra walls were provided in the pen (Jørgensen et al., 2009). Overall, these results show that it is important to be aware that factors such as perimeter length and pen shape (Jørgensen and Bøe, 2009) and how the space is organized may be just as influential as space per se when studying the type and amount of social interactions in a flock. Due to the lack of studies on space requirements in goats, the criterion for high animal density is not clear. Toussaint (1997) recommends 1.5 m2 per goat and this is in accordance with European regulations for organic farming (council regulation (EC) no. 1804/1999). While regulations in Sweden (1.20 m2 /goat) and Switzerland (1.0 m2 /goat) allow lower space requirements, Norwegian regulations have no precise formulations on space allowance neither in sheep nor goats. For social and highly interacting species that show a high degree of behavioural synchrony, such as the goat (e.g., Fournier and Festa-Bianchet, 1995), space is often a prerequisite for well-functioning groups and to secure a high production level. The goal in every loosehousing system is to minimize aggression and social stress while providing the animals as much freedom to move around as possible with a minimum of disturbance during feeding and resting. While the aggression level increases and production declines with reduced space allowance in most other farm animal species (e.g., reviewed by: Estevez et al. (2007)), there is still a need to document the effects of animal density in goats kept in indoor confinement.
The objective of the experiment was to study the effects of three different densities during pregnancy on social interactions, cortisol in plasma and kid production in domestic goats. We predicted a higher number of agonistic interactions and a lower number of affiliative interactions with increased density and that a higher level of social stress with increased density should be manifested in elevated cortisol levels. Previous findings showing that production of goats is only slightly affected by social circumstances (e.g., Andersen et al., 2008; Fernández et al., 2007) can be the result of the goats’ evolutionary and domestication process (Silanikove, 2000) suggesting that goats have a great ability to adapt to social stress situations. Whether animal density would affect kid production most likely depends on the extent to which different animal densities will influence the level of social stress and how well the goats cope with this. 2. Materials and methods 2.1. Experimental design Nine groups of 6 Norwegian dairy goats were housed in three different densities (three replicates/groups for each density): 1.0 m2 per animal; 2.0 m2 per animal or 3.0 m2 per animal. These densities were chosen on the bases that, at present, there are still farms where goats are kept indoors at 0.6–0.8 m2 /animal (Nilssen and Henriksen, 2007) in Norway. Data about the average density of goats kept indoors is not available, neither in Norway nor in other countries. Based on recommendations, it is realistic to assume that, on average, modern farms provide up to 2 m2 space per animal. The lowest density, 3 m2 per animal was chosen to use an extension from a more scientific than applied point of view. All of the pregnant goats were put into their experimental pen on the same day, 3–7 weeks after mating, in the first third of pregnancy. Afterwards, goats were kept in these pens until they started to show signs of labour. Then they were separated to individual kidding pens. Animals were allocated semi-randomly into the 9 groups: each group contained six goats of various weights (group weight means were between 46.1 and 53.8 kg, see later for the entire population) with close expected time of parturition (within 14 days in every group). 2.2. Animals and feeding The experiment was conducted in Norway. Animals were recruited from the experimental goat herd of the Norwegian University of Life Sciences, located in Ås, 35 km south of Oslo. The herd is managed in a comparable way to goat herds at commercial Norwegian farms. In our experiment 54 healthy, pregnant goats were used. All of them were of the Norwegian Dairy Goat breed, living in the same herd, dehorned and multiparous, 18 coloured and 36 white. Their age ranged from 2 to 5 years at the beginning of the experiment (mean ± SE: 2.8 ± 0.0 years), their weight ranged between 36.4 and 68.5 kg (mean ± SE: 50.2 ± 1.0 kg). In another study on animals from the same herd, Eknæs et al. (in preparation) found that
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the height of goats were between 57 and 70 cm (mean ± SE: 63.7 ± 0.2 cm) and lengths of the animals were 61–80 cm (mean ± SE: 71.5 ± 0.2 cm). The goats spent the summer period (until beginning of September) on pasture in the mountains and all of them knew each other to some extent. From the beginning of September, they were housed separately with visual and olfactorical access to other goats. Approximately two weeks before the treatment began (mid of October), they were placed into groups of 15–35 individuals and lactation period was terminated by reducing amount of hay and concentrate provided. In September and October of 2011 more than 60 female goats (>1 year old) were mated or inseminated. After the early stage of pregnancy was confirmed (by not returning to oestrus and/or ultrasound investigation, 3–7 weeks after mating or insemination), 54 goats were chosen for the experiment (choice was made based on close expected time of parturition). At the start of the treatment period (3–7 weeks after conception, beginning of November, 2011), the goats were individually marked with coloured collars, grouped according to the above mentioned criteria and placed in separate, rectangular pens, six animals in each (small density: 3 m2 per goat, pens 276 cm × 650 cm each; medium density: 2 m2 per goat, pens 189 cm × 632 cm, 224 cm × 540 cm, 276 cm × 435 cm; high density: 1 m2 per goat, pens 189 cm × 317 cm, 224 cm × 270 cm, 224 cm × 270 cm). All pens were located in one of two insulated and mechanically ventilated rooms in the same barn with a room temperature of approximately 10 ◦ C. The pens contained expanded metal flooring with 60 cm deep area made of solid wood at the rear end of the pen. The pen walls were made of 1.5 m high solid, 15 mm plywood to avoid physical contact between groups. The pens were cleaned immediately before morning feeding and new bedding of sawdust was added to the solid floor area. In addition to natural light through windows on both sides of the room, artificial light was kept on between 08:00 and 15:00 h. Constant access to fresh water and minerals was provided from two water suppliers and salt blocks with copper in each pen. All of the pens had six openings on the wall at the feeding trough functioning as feeding places for animals. The goats were fed 0.2 kg of concentrate per animal every morning in the beginning of the experimental period and this was gradually increased to 0.5 kg by mid January and was kept at this level until kidding. They had free access to grass silage dispensed every morning and afternoon, which was complemented with hay in the afternoon in the last part of pregnancy (from January). Does gave birth from the beginning of February to the beginning of March. One of the pregnant goats (from the medium density treatment) aborted 16 days before the expected date of parturition. This goat was removed from the experimental pen for eight days for better observation and medication then placed back until the end of treatment to contribute to the social environment of the pregnant goats. Behavioural, body condition, weight and cortisol data of this animal are missing in the last period as this animal was separated at the time of data collection. Behavioural data of the group mates were adjusted to four possible communicational partners instead of five (frequency of observed behaviours were divided by four and
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multiplied by five) to be comparable with other groups’ observations.
2.3. Measurements on adult goats 2.3.1. Observation of social behaviours Social behaviour of goats was observed three times during pregnancy. The first observations were taken one week after the goats were put into the pens as Andersen et al. (2008) found, that in groups with changing social environments, when the group composition is modified the initial increase in social behaviours (mainly offensive) declines and returns to a stable level by one week after the regrouping. The second observation was taken six weeks after the first observation and the last observation another seven weeks later. Social behaviours were registered on the basis of continuous live observation for 1.5 h in the morning (right after the morning feeding, starting between 08:30 and 09:15) and 1.5 h in the afternoon (immediately after the afternoon feeding, starting between 14:00 and 14:45). These times were chosen as feeding was expected to enhance the level of social interactions in goats. The observations were done by three different observers, who were trained to achieve as high inter-observer reliability as possible. Observations each observer were made at the same time and each observer observed one pen during that time. The observation of the social behaviours took 4 days in each observational period and each pen was observed in total for three hours in each period, nine hours during the whole pregnancy. The number, initiator and recipient of the following behaviours were registered based on the ethogram in Andersen et al. (2008): • Frontal clashing: a position where the actor is rearing onto the hind legs with the head and torso twisted followed by descending forcefully onto the front legs delivering a powerful strike forwards and downwards reaching the head of the receiver. • Butting: contact (sudden and forceful movement) with the head towards another goat. • Push: pressing the head to any part of another goat, slowly. • Threatening: pawing or rushing towards, or directing the forehead towards the opponent without physical contact, biting or attempt to bite another goat. • Withdrawing: moving the head and/or body away from another goat (after a social interaction). • Nosing: nose in contact with another goat. • Grooming: grooming by using an-other goat for this activity (the other can be either a passive recipient or take part actively in the mutual grooming). • Displacement from food: making another goat leave its feeding place with or without physical contact. • Displacement from resting: making another goat leave its resting position with or without physical contact. For the statistical analysis the results of the observations in the morning and afternoon were merged in each observational period. From the behaviours registered the
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following behavioural variables were calculated (based on e.g., Andersen et al., 2008): • Offensive behaviours: sum of Frontal clash, Butting, Pushing, Threatening, Displacement for food, Displacement from resting place. • Defensive behaviours: sum of Withdrawal, being recipient of Displacement from food and Displacement from resting place. • Socio-positive behaviours: sum of Grooming and Nosing. 2.3.2. Body condition and weight gain Body condition was assessed before the treatment period and two times during (all together three times during pregnancy: one week before and 6 and 12 weeks after treatment started). The body conditions of the goats was evaluated based on a method described by Villaquiran et al. (2005) where the score can vary between 1.0 (thin) and 5.0 (obese) and higher values refer to more fat repository. However, only the lumbar vertebrae and transverse process were used to evaluate condition as evaluating the sternum and ribs were found to be a stressful procedure and a redundant measurement in the case of goats. Nonetheless, we used a more sensitive scale with increments of 0.25 instead of 0.5. Two trained observers scored body condition on two consecutive days and the average was used in the analyses. The goats were weighed on an electric scale two times: one week before treatment started (before the afternoon feeding, between 12:30 and 14:30) and two days after parturition. Weight gain was calculated as the difference between these two measures. The results of the scoring of body condition and cortisol level in blood measured on two consecutive days were averaged; therefore, the three mean values according to the three data collection periods were used. 2.3.3. Blood cortisol level Blood was taken and processed as described in Andersen et al. (2008), as basal cortisol level in blood has been used in studies to evaluate effect of long-term stress in goats (e.g., Al-Busaidi et al., 2008; Engeland et al., 1999; Romero et al., 1998). Blood was collected for the analysis of the cortisol levels from all of the adult goats three times (before treatment, mid-treatment and at the end of treatment period) on two consecutive days in the morning (before the morning feeding, between 07:00 and 08:30). The days when blood samples were taken were different from the days of both the scoring of body condition and observation of social interactions to avoid possible effect of handling or human presence on the cortisol level in the blood. Samples were taken in the home pen, animals were handled gently and samples were taken in approximately 1.5 min. Blood was collected from the jugular vein into heparinized tubes (Vacutainer, Becton and Dickinson, Leuven, Belgium). Blood samples were stored at −4 ◦ C for two days, then centrifuged at 3000 × g for 15 min and plasma was removed, stored at −20 ◦ C and preserved for the cortisol analysis. The analysis was performed by the Hormon Laboratory of the Oslo University Hospital. Cortisol
was measured by electrochemiluminescence immunoassay (ECLIA, Roche Cobas Cortisol assay) by using Roche Elecsys E immunoanalyzer system (Roche Diagnostics, Mannheim, Germany) the following way: 20 l of the sample was incubated with cortisol-specific biotinylated antibody and rethenium complex labelled cortisol derivate. A second incubation was performed with streptavidincoated microparticles. After capturing of the microparticles on an electrode and applying voltage the induced chemiluminescent, emission was measured by a photomultiplier. This method is reliable between the range of 0.2 and 634.0 ng/ml, and the sensitivity is reported to be lower than 3.08 ng/dl.
2.4. Measurements on kids One female goat (from the medium density treatment) gave birth to one stillborn kid (probably because of complications at birth due to inappropriate position of kid) and the mother could not be saved afterwards. One goat (from the small density treatment) gave birth to two live and two stillborn kids (the latter two were immature). Only data from live born kids are presented later. In our study population we had either singleton or twin litters. Kid weight was measured one day after birth (12–36 h after birth) on an electric scale. The data of twins were averaged so one value represented each litter. The number of live born kids and sex of the offspring were noted.
2.5. Statistical methods All of the statistical models were run in SAS. Most of the variables did not fit a normal distribution; therefore, generalized models were used. The random effect of the pen within treatment was not significant for any of the variables tested; therefore, we used simpler generalized models to test the effect of fixed parameters. We applied a generalized model (genmod) with Poisson distribution and log link to the behavioural variables (offensive, defensive and socio-positive behaviour), body condition and cortisol level using treatment and time as fixed effects which additionally tested the interactions. For weight gain, time was not used as class variable, only treatment. A similar model was used for litter weight and weight of the kid (generalized model with Poisson distribution log link), but here, treatment, weight of mother before treatment started and number of kids in the litter were fixed effects and the possible interaction between treatment and number of kids was tested. To analyze effect of treatment on the sex ratio of kids, only data for litters of twins were used (there were no litters with more than two live born kids). The sex of kids could be one of the following three categories: two males, one male and one female, or two female kids. We applied a generalized model with multinomial distribution and cumulative logit link to test possible effects of treatment and the weight of mother on kid sex ratio and number of kids within the litter.
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Fig. 1. Frequency (with median and interquartile range in the box, outliers shown as dots) of offensive behaviours shown by adult goats of high, medium and small density in the first, second and last third of pregnancy (per animal for sum of the 3 h of observation). (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
3. Results 3.1. Social behaviour, body condition and weight development of adult goats Comparing the three densities in all of the observational periods, the highest frequency of offensive behaviours was recorded in the high density group, medium level in the medium density and the lowest level in the small density (Table 1, Fig. 1a). The amount of offensive behaviours was highest during the first third of pregnancy in all of the treatment groups, and the frequency of these behaviours declined later in the second and last third of pregnancy, except in the smallest density (Table 1, Fig. 1b).
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Fig. 2. Frequency (with median and interquartile range in the box, outliers shown as dots) of defensive behaviours shown by adult goats of high, medium and small density in the first, second and last third of pregnancy (per animal for sum of the 3 h of observation). (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
In the first third of pregnancy, there were fewer defensive behaviours in the small density than in the other densities, in the second third of the pregnancy, there were not differences between treatments; and in the last third of pregnancy, a higher number of defensive behaviours were detected in the high density group than in the small density group (Table 1). The intermediate density did not differ significantly from the two extremes (Fig. 2a). The goats showed more defensive behaviours in the first third of pregnancy than later in the period within the medium and high density treatments, but in the small density group, the last third of pregnancy differed from the two previous time periods (Fig. 2b). In the second period, the goats in the high density groups had a lower level of socio-positive behaviours than
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Table 1 Statistical results of behavioural, physical and physiological data from adult goats. Time
P-value
P-value
2
P-value
628.18 12.50 3.47 0.02 4.13
<0.0001 0.0020 0.1760 0.9910 0.1270
386.33 67.46 249.18 0.06 69.82
<0.0001 <0.0001 <0.0001 0.969 <0.0001
41.67 13.74 26.51 0.00 18.92
<0.0001 0.008 <0.0001 1.0000 0.001
2
Offensive behaviours (frequency) Defensive behaviours (frequency) Socio-positive behaviours (frequency) Body condition (scale score) Cortisol level in blood (ng/ml)
Density × Time
Density
goats in the other densities, but this was not the case in the first and third period of pregnancy (Table 1, Fig. 3a). More socio-positive behaviours were observed in the last third of pregnancy than in the previous two observation
2
periods, and in the high density treatment, the increase of these behaviours were seen between the first and second third of pregnancy (Fig. 3b). Neither density nor the interaction between density and time period had significant effects on body condition scores (mean ± SE in the high density groups in the three periods, respectively: 2.61 ± 0.0; 2.53 ± 0.0; 2.58 ± 0.1; in the medium density groups: 2.58 ± 0.0; 2.51 ± 0.0; 2.57 ± 0.0; in the small density groups: 2.56 ± 0.0; 2.49 ± 0.0; 2.55 ± 0.0). Weight gain throughout pregnancy was not significantly affected by density (mean ± SE: high density 4.9 ± 1.3 kg; medium density 6.0 ± 1.4 kg; small 6.4 ± 0.9 kg; 2 = 0.61; P = 0.737). 3.2. Cortisol measures in adult goats There was no significant effect of density per se on the cortisol level of the goats, but there was a significant interaction between density and time period (Table 1, Fig. 4a, b). In the high and medium density groups, the level of cortisol was highest in the first and second third of pregnancy. In the small density groups, however, a higher level of cortisol was measured in the second third of pregnancy. 3.3. Kid production results
Fig. 3. Frequency (with median and interquartile range in the box, outliers shown as dots, extremes shown as asterisks) of socio-positive behaviours shown by adult goats of high, medium and small density in the first, second and last third of pregnancy (per animal for sum of the 3 h of observation). (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
Neither density nor weight of the mother had an effect on reproductive data such as litter weight (density: 2 = 0.84, P = 0.659; mother weight: 2 = 0.27, P = 0.606; litter weight mean ± SE in small: 5.8 ± 0.4 kg, medium: 6.8 ± 0.4 kg, high: 5.3 ± 0.4 kg), weight of kids (density: 2 = 0.75, P = 0.688; mother weight: 2 = 0.16, P = 0.685; weight of kids mean + SE in small: 3.4 ± 0.1 kg, medium: 3.8 ± 0.2 kg, high: 3.5 ± 0.1 kg) or number of kids (density: 2 = 1.67, P = 0.435; mother weight: 2 = 1.33, P = 0.249, number of singletons vs. twin litters in the small density was 5 vs. 13, respectively, medium density: 4 vs. 13, high density: 8 vs. 10). Number of kids influenced litter weight (2 = 18.58, P < 0.0001), but not the weight of the individual kid (2 = 0.18, P = 0.668). The density and number of kids did not have any interactive effects on litter weight (2 = 0.17, P = 0.917) or kid weight (2 = 0.14, P = 0.930). Within the twin litters, treatment or weight of mother did not have effect on sex ratio of kids (treatment: 2 = 4.18, P = 0.123; weight of mother: 2 = 2.53, P = 0.112). 4. Discussion As predicted and shown in most other farm species (reviewed by Estevez et al., 2007), there was a linear
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Fig. 4. Cortisol level (with median and interquartile range in the box, outliers shown as dots, extremes shown as asterisks) measured in adult goats housed in high, medium or small density groups in the first, second and last third of pregnancy. (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
increase in offensive and defensive agonistic behaviours with increasing density from 3 m2 , via 2 m2 to 1 m2 . Except for the study done by Loretz et al. (2004) focusing on feeding behaviour with a mixture of breeds, there are no other systematic studies on the effects on reduced total space per se in goats. Previous studies show that goats compete more for feeding space than resting space (Andersen and Bøe, 2007; Jørgensen et al., 2007), whereas sheep respond with increased aggression both when resting space is reduced (Bøe et al., 2006) and when feeding space is reduced on a hay diet (Bøe and Andersen, 2010). With respect to the behavioural results, a reduction in total space thus seems to enhance the level of social stress quite substantially and a space recommendation of 1.0–1.5 m2 per goat as indicated in regulations of different European countries (e.g.,
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Toussaint, 1997; council regulation (EC) no. 1804/1999) may not be satisfactory to ensure a high welfare standard in goats housed indoors. The incidence of both offensive and defensive behaviours declined over time and the stage of pregnancy can be one explanation for this result. On the other hand, in contrast to what is suggested previously (Andersen et al., 2008; Fernández et al., 2007), this may indicate that groups of goat need more than one week to get a stable flock with a minimum of aggression. The number of defensive behaviours is somewhat lower than the amount of offensive behaviours, but the reason for this is most likely that not all offensive behaviours are replied with retreat by the receiver. In fact, observations during mixing of the groups in the present study showed that there were much more offensive responses than defensive. Socio-positive behaviours were not affected by density. The present study suggests that these behaviours increase in the final stage of pregnancy when it could be of great functional importance to establish bonds for mutual protection of offspring in maternal groups at least as a risk reducing strategy through synchronized birth and shared vigilance (for review see O’Brien (1988)). This is also supported by the hormonal status which stimulates them to show maternal care (e.g., Capezzuto et al., 2008; Conway et al., 1996; Poindron et al., 2007; Sawada et al., 1995). As stated in recent reviews (Estevez et al., 2007; Miranda-de la Lama and Mattiello, 2010), grooming has the function of maintaining a healthy pelage and reducing the conflict level in a group, but goats seek body contact to a very little extent and overall, the incidence of grooming behaviour is reported to be low (Andersen and Bøe, 2007; Andersen et al., 2011). In contrast to what was predicted, the increased aggression level with increased density was neither reflected in the cortisol measures nor did it affect the productions results of the goats. Also in Andersen et al. (2008), there was no relationship between the amount of agonistic behaviours and the level of blood cortisol in adult goats, suggesting that this might not be a reliable indicator of long-term social stress in goats. Regarding reliability of our blood cortisol measures in discussing negative findings, we can say that the level of cortisol found in this study (average was 9.4 ng/ml) corresponds to the values reported in other papers in different goat breeds mostly ranging from 3 to 15 ng/ml (e.g., Al-Busaidi et al., 2008; Aoyama et al., 2008; Olsson et al., 1995; Ortiz-de-Montellano et al., 2007; Toerien et al., 1999) and the mean is only slightly higher than what was found earlier on the same breed, Norwegian dairy goats (Andersen et al., 2008; Engeland et al., 1999). The method we applied, venipuncture is used frequently and the animals were acclimated to the sampling procedure and frequent handling before the experiment. This sampling procedure may cause acute stress induced by human handling, and the interindividual differences in sensitivity to this procedure may have overshadowed the possible effect of our chronic treatment. Large inter-individual variability in blood cortisol in goats was reported elsewhere having strong impact on group values (e.g., Conway et al., 1996). Another plausible explanation for lack of differences
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between groups can be that the cortisol levels are reported to return to baseline level within 4 h after an acute stressor both in goats and sheep (Aoyama et al., 2008; Nwe et al., 1996; Ortiz-de-Montellano et al., 2007; Roussel et al., 2004; Roussel-Huchette et al., 2008; Shamay et al., 2000; Toerien et al., 1999). If agonistic encounters trigger elevation in cortisol level in an acute way, then the time of sampling chosen (early morning before feeding time) would mirror the agonistic encounters during the late night resting or sleeping period when incidences are rare and independent of group density. It is also possible, that at the time of blood sampling, the animals were in a higher arousal state caused by the nearby feeding time, masking the effects of treatment. The time was chosen based on methods applied by other researchers to get comparable results (e.g., AlBusaidi et al., 2008; Ali et al., 2006; Andersen et al., 2008; Conway et al., 1996; Komara et al., 2010; Olsson et al., 1995, 1996). Additionally, after a rather stable level of blood cortisol in the first and second third of gestation, we found a decrease in blood cortisol level in the third sampling, which was conducted ten days before the first parturition (six weeks before the last). However, Ramadoss et al. (2008) found that cortisol level in sheep is stable during pregnancy when measured on four different days distributed across gestation period, and Romero et al. (1998) found a stable blood cortisol level during pregnancy in goats even during the peripartum period. Andersen et al. (2008) also found a quite stable level of cortisol in the same breed during gestation and a sharp decrease two weeks before the expected date of parturition may be due to the general higher stress tolerance of goats in late pregnancy (in rats: Maestripieri and D’Amato, 1991; Picazo and Fernandez-Guasti, 1993; in humans: Pugh et al., 1963; Hamilton et al., 1988). In conclusion, our blood cortisol measures are comparable to data from other similar studies, but blood cortisol measures are probably not the most suited method to evaluate effects of a chronic treatment such as animal density and behaviour seems to be a more sensitive tool in detecting subtle effects. Indicators of chronic, social stress are scarcely studied and measures such as fur and faecal cortisol may be a more valid and promising physiological indicator than blood cortisol in this respect (faecal cortisol in goats: Nordmann et al., 2011; Patt et al., 2012; fur cortisol in different species e.g., dogs and cats: Accorsi et al., 2008; dogs: Bennett and Hayssen, 2010; cow: Comin et al., 2011; rhesus monkey: Davenport et al., 2006; Dettmer et al., 2012). Surprisingly, the higher level of agonistic behaviour in the small density groups did not lead to more foetal losses or a reduction in number of live born kids, nor did it affect the weight of the newborn. These results were in contrast to those from Duvaux-Ponter et al. (2003), who reported that repeated transportation of mothers during pregnancy resulted in lower kid weight and litter size. Our treatment began well after conception. By this stage of gestation, the foetuses are likely less sensitive to disturbances and are less likely to abort. On the other hand, goats have become adapted to harsh environments (Silanikove, 2000) and several studies did not find any decrease in productivity parameters as effect of treatment aimed at causing an increased level of stress (e.g., Shamay et al.,
2000). For example, in the study of Fernández et al. (2007), researchers regrouped lactating goats three times, and although it coincided with an increase in agonistic interactions, experimenters could observe a decrease in milk production only after the first reestablishment of social structure and the following regroupings did not provoke change in milk composition or milk yield. In some cases, studies even showed positive effect of stress on production, as Andersen et al. (2008) found that mothers from unstable group structure (frequent regrouping during pregnancy) had more kids. Animal density did not affect sex ratio in any significant way in the present study. In regards to the maternal adjustment of offspring sex ratio according to prenatal environment in animals, opposing hypotheses can be argued depending on environmental and social factors like food availability, sexual dimorphism in body parameters, sexual segregation and differential dispersal of sexes (for review see Hewison and Gaillard (1999)). These factors may impact animals in various ways depending on the species, including ungulates (Hewison and Gaillard, 1999) and even within breeds, having an influence on the sex ratio of offspring (Skjervold, 1979). Côté and Festa-Bianchet (2001) observed a herd of mountain goats (Oreamnos americanus) for nine years to investigate whether the assumptions and predictions of the model suggested by Trivers and Willard (1973) or its alternative, the local resource competition model (Clark, 1978), were verified. They concluded that in mountain goats, the assumptions of the models are not always met and experimental results did not confirm the predictions of the models. Andersen et al. (2008) studied effect of sequential regrouping of pregnant goats on the sex of the offspring and found no impact of treatment on ratio of male offspring.
5. Conclusions The reduction of space from 3.0 m2 per goat to 1.0 m2 per animal led to an increase in agonistic interactions but density did not affect the cortisol level of adult goats nor kid production results. If we regard agonistic behaviour as a sign of welfare in goats, space recommendations close to 1.0–1.5 m2 might be questionable.
Acknowledgements This study was conducted in frame of the Animal Welfare Indicators project (AWIN), which was financed by the EU VII Framework programme (FP7-KBBE-2010-4). We are also very grateful for the blood analysis to Peter Torjesen and Kari Julien at the Hormon Laboratory of the Oslo University Hospital. Nonetheless, we would like to thank the staff at the Animal Production Experimental Centre (Norwegian University of Life Sciences), especially Agnes Klouman for their excellent cooperation during the study and Kari Eikanger for the kind technical assistance in collecting the blood samples.
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Social interactions, cortisol and reproductive success of domestic goats (Capra hircus) subjected to different animal densities during pregnancy Judit Vas ∗ , Rachel Chojnacki, Marte Flor Kjøren, Charlotte Lyngwa, Inger Lise Andersen Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway
a r t i c l e
i n f o
Article history: Accepted 7 April 2013 Available online 29 May 2013 Keywords: Goat Density Social behaviour Agonistic Cortisol Pregnancy
a b s t r a c t Although goats in many countries are kept indoors in the winter season, during gestation and kidding, recommendations and regulations regarding available space per goat are highly variable. The effects of different housing conditions on the welfare and behaviour are understudied in this species. The aim of the present study was to observe some behavioural, physical and physiological parameters of pregnant dairy goats kept indoors at different animal densities, and their possible influence on reproduction data was also followed. Pregnant Norwegian dairy goats from early pregnancy until parturition were kept constantly at 1, 2 or 3 m2 per animal. Their social behaviour (offensive, defensive, socio-positive), body condition, weight gain and blood cortisol level were monitored throughout pregnancy. Weight and gender of offspring were recorded. We found that goats kept at higher density showed more offensive and defensive behaviours, but there was no difference in socio-positive behaviours between treatments. The increase in agonistic behaviours was not reflected in blood cortisol level, weight gain or production data. We concluded, that higher frequency of agonistic behaviours is present even at 2.0 m2 per animal, and if this is regarded as a sign of social stress recommendations regarding available space per goat should be adjusted. However, keeping goats even at 1 m2 per animal did not have any impact on productivity or weight development, suggesting that they easily habituate to sub-optimal environmental conditions. © 2013 Elsevier B.V. All rights reserved.
1. Introduction High animal densities are reported to increase the frequency of aggression, behavioural problems and reduce performance in a large number of domestic species (reviewed by Estevez et al., 2007) but only a few studies have been conducted in goats and most addressed the effects of feeding space and resting space rather than
∗ Corresponding author. Tel.: +47 64965240; mobile: +47 95104407; fax: +47 64965101. E-mail address: judit banfi[email protected] (J. Vas). 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.04.009
the total amount of space available per animal. Loretz et al. (2004) found that goats rested less with the smallest space allowance but the aggression level remained surprisingly low across densities within a range of 1.0–2.0 m2 per animal. However, the study contained a mixture of breeds, including meat production breeds that might be less aggressive and the goats were in late pregnancy which is a period when they engage in fewer conflicts (Andersen et al., 2008). The increased aggression level with reduced space can largely be explained by the reduction in individual distance, forcing individuals to interact with a limited opportunity to escape from an attacker. Due to the reduced opportunity to escape and communicate in a clear way with
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other group members, more individuals are likely to engage in social conflicts (i.e. fear-induced aggression when escape is no longer an option). Although reduced feeding space increased the amount of agonistic interactions quite substantially in goats (Jørgensen et al., 2007; Loretz et al., 2004), the organization of resting space appears to be more influential than the amount of resting space per se. Sheep, another small ruminant species, are often used as reference in goat studies to generate hypothesis and interpret results because there are fewer studies on goats than sheep (e.g., Ehrlenbruch et al., 2010; Siebert et al., 2011). At the same time, results on behavioural changes to different housing conditions suggest that these two species may respond quite differently to similar environmental conditions and findings in sheep must be treated with caution if extended to goats. For example, in contrast to goats, reduced resting space produced a significant increase in the number of displacements in sheep (Bøe et al., 2006). Sheep and goats both seemed to maximize the individual distance to a large extent with respect to the space available in the pen (Aschwanden et al., 2008; Jørgensen et al., 2009), but sheep were more tolerant towards resting in body contact with other group members than what is shown in dairy goats (Bøe et al., 2006; Andersen and Bøe, 2007). Sheep and goats showed a clear preference for resting against a wall (Andersen and Bøe, 2007; Bøe et al., 2006). Elevated resting platforms in addition to ground floor resting areas increased the individual distance between goats when resting and reduced the level of social conflicts (Andersen and Bøe, 2007) however, providing extra walls in the pens on the same floor level did not affect agonistic interactions at all (Ehrlenbruch et al., 2010). In contrast, sheep showed a reduction in some agonistic behaviour when extra walls were provided in the pen (Jørgensen et al., 2009). Overall, these results show that it is important to be aware that factors such as perimeter length and pen shape (Jørgensen and Bøe, 2009) and how the space is organized may be just as influential as space per se when studying the type and amount of social interactions in a flock. Due to the lack of studies on space requirements in goats, the criterion for high animal density is not clear. Toussaint (1997) recommends 1.5 m2 per goat and this is in accordance with European regulations for organic farming (council regulation (EC) no. 1804/1999). While regulations in Sweden (1.20 m2 /goat) and Switzerland (1.0 m2 /goat) allow lower space requirements, Norwegian regulations have no precise formulations on space allowance neither in sheep nor goats. For social and highly interacting species that show a high degree of behavioural synchrony, such as the goat (e.g., Fournier and Festa-Bianchet, 1995), space is often a prerequisite for well-functioning groups and to secure a high production level. The goal in every loosehousing system is to minimize aggression and social stress while providing the animals as much freedom to move around as possible with a minimum of disturbance during feeding and resting. While the aggression level increases and production declines with reduced space allowance in most other farm animal species (e.g., reviewed by: Estevez et al. (2007)), there is still a need to document the effects of animal density in goats kept in indoor confinement.
The objective of the experiment was to study the effects of three different densities during pregnancy on social interactions, cortisol in plasma and kid production in domestic goats. We predicted a higher number of agonistic interactions and a lower number of affiliative interactions with increased density and that a higher level of social stress with increased density should be manifested in elevated cortisol levels. Previous findings showing that production of goats is only slightly affected by social circumstances (e.g., Andersen et al., 2008; Fernández et al., 2007) can be the result of the goats’ evolutionary and domestication process (Silanikove, 2000) suggesting that goats have a great ability to adapt to social stress situations. Whether animal density would affect kid production most likely depends on the extent to which different animal densities will influence the level of social stress and how well the goats cope with this. 2. Materials and methods 2.1. Experimental design Nine groups of 6 Norwegian dairy goats were housed in three different densities (three replicates/groups for each density): 1.0 m2 per animal; 2.0 m2 per animal or 3.0 m2 per animal. These densities were chosen on the bases that, at present, there are still farms where goats are kept indoors at 0.6–0.8 m2 /animal (Nilssen and Henriksen, 2007) in Norway. Data about the average density of goats kept indoors is not available, neither in Norway nor in other countries. Based on recommendations, it is realistic to assume that, on average, modern farms provide up to 2 m2 space per animal. The lowest density, 3 m2 per animal was chosen to use an extension from a more scientific than applied point of view. All of the pregnant goats were put into their experimental pen on the same day, 3–7 weeks after mating, in the first third of pregnancy. Afterwards, goats were kept in these pens until they started to show signs of labour. Then they were separated to individual kidding pens. Animals were allocated semi-randomly into the 9 groups: each group contained six goats of various weights (group weight means were between 46.1 and 53.8 kg, see later for the entire population) with close expected time of parturition (within 14 days in every group). 2.2. Animals and feeding The experiment was conducted in Norway. Animals were recruited from the experimental goat herd of the Norwegian University of Life Sciences, located in Ås, 35 km south of Oslo. The herd is managed in a comparable way to goat herds at commercial Norwegian farms. In our experiment 54 healthy, pregnant goats were used. All of them were of the Norwegian Dairy Goat breed, living in the same herd, dehorned and multiparous, 18 coloured and 36 white. Their age ranged from 2 to 5 years at the beginning of the experiment (mean ± SE: 2.8 ± 0.0 years), their weight ranged between 36.4 and 68.5 kg (mean ± SE: 50.2 ± 1.0 kg). In another study on animals from the same herd, Eknæs et al. (in preparation) found that
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the height of goats were between 57 and 70 cm (mean ± SE: 63.7 ± 0.2 cm) and lengths of the animals were 61–80 cm (mean ± SE: 71.5 ± 0.2 cm). The goats spent the summer period (until beginning of September) on pasture in the mountains and all of them knew each other to some extent. From the beginning of September, they were housed separately with visual and olfactorical access to other goats. Approximately two weeks before the treatment began (mid of October), they were placed into groups of 15–35 individuals and lactation period was terminated by reducing amount of hay and concentrate provided. In September and October of 2011 more than 60 female goats (>1 year old) were mated or inseminated. After the early stage of pregnancy was confirmed (by not returning to oestrus and/or ultrasound investigation, 3–7 weeks after mating or insemination), 54 goats were chosen for the experiment (choice was made based on close expected time of parturition). At the start of the treatment period (3–7 weeks after conception, beginning of November, 2011), the goats were individually marked with coloured collars, grouped according to the above mentioned criteria and placed in separate, rectangular pens, six animals in each (small density: 3 m2 per goat, pens 276 cm × 650 cm each; medium density: 2 m2 per goat, pens 189 cm × 632 cm, 224 cm × 540 cm, 276 cm × 435 cm; high density: 1 m2 per goat, pens 189 cm × 317 cm, 224 cm × 270 cm, 224 cm × 270 cm). All pens were located in one of two insulated and mechanically ventilated rooms in the same barn with a room temperature of approximately 10 ◦ C. The pens contained expanded metal flooring with 60 cm deep area made of solid wood at the rear end of the pen. The pen walls were made of 1.5 m high solid, 15 mm plywood to avoid physical contact between groups. The pens were cleaned immediately before morning feeding and new bedding of sawdust was added to the solid floor area. In addition to natural light through windows on both sides of the room, artificial light was kept on between 08:00 and 15:00 h. Constant access to fresh water and minerals was provided from two water suppliers and salt blocks with copper in each pen. All of the pens had six openings on the wall at the feeding trough functioning as feeding places for animals. The goats were fed 0.2 kg of concentrate per animal every morning in the beginning of the experimental period and this was gradually increased to 0.5 kg by mid January and was kept at this level until kidding. They had free access to grass silage dispensed every morning and afternoon, which was complemented with hay in the afternoon in the last part of pregnancy (from January). Does gave birth from the beginning of February to the beginning of March. One of the pregnant goats (from the medium density treatment) aborted 16 days before the expected date of parturition. This goat was removed from the experimental pen for eight days for better observation and medication then placed back until the end of treatment to contribute to the social environment of the pregnant goats. Behavioural, body condition, weight and cortisol data of this animal are missing in the last period as this animal was separated at the time of data collection. Behavioural data of the group mates were adjusted to four possible communicational partners instead of five (frequency of observed behaviours were divided by four and
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multiplied by five) to be comparable with other groups’ observations.
2.3. Measurements on adult goats 2.3.1. Observation of social behaviours Social behaviour of goats was observed three times during pregnancy. The first observations were taken one week after the goats were put into the pens as Andersen et al. (2008) found, that in groups with changing social environments, when the group composition is modified the initial increase in social behaviours (mainly offensive) declines and returns to a stable level by one week after the regrouping. The second observation was taken six weeks after the first observation and the last observation another seven weeks later. Social behaviours were registered on the basis of continuous live observation for 1.5 h in the morning (right after the morning feeding, starting between 08:30 and 09:15) and 1.5 h in the afternoon (immediately after the afternoon feeding, starting between 14:00 and 14:45). These times were chosen as feeding was expected to enhance the level of social interactions in goats. The observations were done by three different observers, who were trained to achieve as high inter-observer reliability as possible. Observations each observer were made at the same time and each observer observed one pen during that time. The observation of the social behaviours took 4 days in each observational period and each pen was observed in total for three hours in each period, nine hours during the whole pregnancy. The number, initiator and recipient of the following behaviours were registered based on the ethogram in Andersen et al. (2008): • Frontal clashing: a position where the actor is rearing onto the hind legs with the head and torso twisted followed by descending forcefully onto the front legs delivering a powerful strike forwards and downwards reaching the head of the receiver. • Butting: contact (sudden and forceful movement) with the head towards another goat. • Push: pressing the head to any part of another goat, slowly. • Threatening: pawing or rushing towards, or directing the forehead towards the opponent without physical contact, biting or attempt to bite another goat. • Withdrawing: moving the head and/or body away from another goat (after a social interaction). • Nosing: nose in contact with another goat. • Grooming: grooming by using an-other goat for this activity (the other can be either a passive recipient or take part actively in the mutual grooming). • Displacement from food: making another goat leave its feeding place with or without physical contact. • Displacement from resting: making another goat leave its resting position with or without physical contact. For the statistical analysis the results of the observations in the morning and afternoon were merged in each observational period. From the behaviours registered the
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following behavioural variables were calculated (based on e.g., Andersen et al., 2008): • Offensive behaviours: sum of Frontal clash, Butting, Pushing, Threatening, Displacement for food, Displacement from resting place. • Defensive behaviours: sum of Withdrawal, being recipient of Displacement from food and Displacement from resting place. • Socio-positive behaviours: sum of Grooming and Nosing. 2.3.2. Body condition and weight gain Body condition was assessed before the treatment period and two times during (all together three times during pregnancy: one week before and 6 and 12 weeks after treatment started). The body conditions of the goats was evaluated based on a method described by Villaquiran et al. (2005) where the score can vary between 1.0 (thin) and 5.0 (obese) and higher values refer to more fat repository. However, only the lumbar vertebrae and transverse process were used to evaluate condition as evaluating the sternum and ribs were found to be a stressful procedure and a redundant measurement in the case of goats. Nonetheless, we used a more sensitive scale with increments of 0.25 instead of 0.5. Two trained observers scored body condition on two consecutive days and the average was used in the analyses. The goats were weighed on an electric scale two times: one week before treatment started (before the afternoon feeding, between 12:30 and 14:30) and two days after parturition. Weight gain was calculated as the difference between these two measures. The results of the scoring of body condition and cortisol level in blood measured on two consecutive days were averaged; therefore, the three mean values according to the three data collection periods were used. 2.3.3. Blood cortisol level Blood was taken and processed as described in Andersen et al. (2008), as basal cortisol level in blood has been used in studies to evaluate effect of long-term stress in goats (e.g., Al-Busaidi et al., 2008; Engeland et al., 1999; Romero et al., 1998). Blood was collected for the analysis of the cortisol levels from all of the adult goats three times (before treatment, mid-treatment and at the end of treatment period) on two consecutive days in the morning (before the morning feeding, between 07:00 and 08:30). The days when blood samples were taken were different from the days of both the scoring of body condition and observation of social interactions to avoid possible effect of handling or human presence on the cortisol level in the blood. Samples were taken in the home pen, animals were handled gently and samples were taken in approximately 1.5 min. Blood was collected from the jugular vein into heparinized tubes (Vacutainer, Becton and Dickinson, Leuven, Belgium). Blood samples were stored at −4 ◦ C for two days, then centrifuged at 3000 × g for 15 min and plasma was removed, stored at −20 ◦ C and preserved for the cortisol analysis. The analysis was performed by the Hormon Laboratory of the Oslo University Hospital. Cortisol
was measured by electrochemiluminescence immunoassay (ECLIA, Roche Cobas Cortisol assay) by using Roche Elecsys E immunoanalyzer system (Roche Diagnostics, Mannheim, Germany) the following way: 20 l of the sample was incubated with cortisol-specific biotinylated antibody and rethenium complex labelled cortisol derivate. A second incubation was performed with streptavidincoated microparticles. After capturing of the microparticles on an electrode and applying voltage the induced chemiluminescent, emission was measured by a photomultiplier. This method is reliable between the range of 0.2 and 634.0 ng/ml, and the sensitivity is reported to be lower than 3.08 ng/dl.
2.4. Measurements on kids One female goat (from the medium density treatment) gave birth to one stillborn kid (probably because of complications at birth due to inappropriate position of kid) and the mother could not be saved afterwards. One goat (from the small density treatment) gave birth to two live and two stillborn kids (the latter two were immature). Only data from live born kids are presented later. In our study population we had either singleton or twin litters. Kid weight was measured one day after birth (12–36 h after birth) on an electric scale. The data of twins were averaged so one value represented each litter. The number of live born kids and sex of the offspring were noted.
2.5. Statistical methods All of the statistical models were run in SAS. Most of the variables did not fit a normal distribution; therefore, generalized models were used. The random effect of the pen within treatment was not significant for any of the variables tested; therefore, we used simpler generalized models to test the effect of fixed parameters. We applied a generalized model (genmod) with Poisson distribution and log link to the behavioural variables (offensive, defensive and socio-positive behaviour), body condition and cortisol level using treatment and time as fixed effects which additionally tested the interactions. For weight gain, time was not used as class variable, only treatment. A similar model was used for litter weight and weight of the kid (generalized model with Poisson distribution log link), but here, treatment, weight of mother before treatment started and number of kids in the litter were fixed effects and the possible interaction between treatment and number of kids was tested. To analyze effect of treatment on the sex ratio of kids, only data for litters of twins were used (there were no litters with more than two live born kids). The sex of kids could be one of the following three categories: two males, one male and one female, or two female kids. We applied a generalized model with multinomial distribution and cumulative logit link to test possible effects of treatment and the weight of mother on kid sex ratio and number of kids within the litter.
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Fig. 1. Frequency (with median and interquartile range in the box, outliers shown as dots) of offensive behaviours shown by adult goats of high, medium and small density in the first, second and last third of pregnancy (per animal for sum of the 3 h of observation). (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
3. Results 3.1. Social behaviour, body condition and weight development of adult goats Comparing the three densities in all of the observational periods, the highest frequency of offensive behaviours was recorded in the high density group, medium level in the medium density and the lowest level in the small density (Table 1, Fig. 1a). The amount of offensive behaviours was highest during the first third of pregnancy in all of the treatment groups, and the frequency of these behaviours declined later in the second and last third of pregnancy, except in the smallest density (Table 1, Fig. 1b).
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Fig. 2. Frequency (with median and interquartile range in the box, outliers shown as dots) of defensive behaviours shown by adult goats of high, medium and small density in the first, second and last third of pregnancy (per animal for sum of the 3 h of observation). (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
In the first third of pregnancy, there were fewer defensive behaviours in the small density than in the other densities, in the second third of the pregnancy, there were not differences between treatments; and in the last third of pregnancy, a higher number of defensive behaviours were detected in the high density group than in the small density group (Table 1). The intermediate density did not differ significantly from the two extremes (Fig. 2a). The goats showed more defensive behaviours in the first third of pregnancy than later in the period within the medium and high density treatments, but in the small density group, the last third of pregnancy differed from the two previous time periods (Fig. 2b). In the second period, the goats in the high density groups had a lower level of socio-positive behaviours than
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Table 1 Statistical results of behavioural, physical and physiological data from adult goats. Time
P-value
P-value
2
P-value
628.18 12.50 3.47 0.02 4.13
<0.0001 0.0020 0.1760 0.9910 0.1270
386.33 67.46 249.18 0.06 69.82
<0.0001 <0.0001 <0.0001 0.969 <0.0001
41.67 13.74 26.51 0.00 18.92
<0.0001 0.008 <0.0001 1.0000 0.001
2
Offensive behaviours (frequency) Defensive behaviours (frequency) Socio-positive behaviours (frequency) Body condition (scale score) Cortisol level in blood (ng/ml)
Density × Time
Density
goats in the other densities, but this was not the case in the first and third period of pregnancy (Table 1, Fig. 3a). More socio-positive behaviours were observed in the last third of pregnancy than in the previous two observation
2
periods, and in the high density treatment, the increase of these behaviours were seen between the first and second third of pregnancy (Fig. 3b). Neither density nor the interaction between density and time period had significant effects on body condition scores (mean ± SE in the high density groups in the three periods, respectively: 2.61 ± 0.0; 2.53 ± 0.0; 2.58 ± 0.1; in the medium density groups: 2.58 ± 0.0; 2.51 ± 0.0; 2.57 ± 0.0; in the small density groups: 2.56 ± 0.0; 2.49 ± 0.0; 2.55 ± 0.0). Weight gain throughout pregnancy was not significantly affected by density (mean ± SE: high density 4.9 ± 1.3 kg; medium density 6.0 ± 1.4 kg; small 6.4 ± 0.9 kg; 2 = 0.61; P = 0.737). 3.2. Cortisol measures in adult goats There was no significant effect of density per se on the cortisol level of the goats, but there was a significant interaction between density and time period (Table 1, Fig. 4a, b). In the high and medium density groups, the level of cortisol was highest in the first and second third of pregnancy. In the small density groups, however, a higher level of cortisol was measured in the second third of pregnancy. 3.3. Kid production results
Fig. 3. Frequency (with median and interquartile range in the box, outliers shown as dots, extremes shown as asterisks) of socio-positive behaviours shown by adult goats of high, medium and small density in the first, second and last third of pregnancy (per animal for sum of the 3 h of observation). (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
Neither density nor weight of the mother had an effect on reproductive data such as litter weight (density: 2 = 0.84, P = 0.659; mother weight: 2 = 0.27, P = 0.606; litter weight mean ± SE in small: 5.8 ± 0.4 kg, medium: 6.8 ± 0.4 kg, high: 5.3 ± 0.4 kg), weight of kids (density: 2 = 0.75, P = 0.688; mother weight: 2 = 0.16, P = 0.685; weight of kids mean + SE in small: 3.4 ± 0.1 kg, medium: 3.8 ± 0.2 kg, high: 3.5 ± 0.1 kg) or number of kids (density: 2 = 1.67, P = 0.435; mother weight: 2 = 1.33, P = 0.249, number of singletons vs. twin litters in the small density was 5 vs. 13, respectively, medium density: 4 vs. 13, high density: 8 vs. 10). Number of kids influenced litter weight (2 = 18.58, P < 0.0001), but not the weight of the individual kid (2 = 0.18, P = 0.668). The density and number of kids did not have any interactive effects on litter weight (2 = 0.17, P = 0.917) or kid weight (2 = 0.14, P = 0.930). Within the twin litters, treatment or weight of mother did not have effect on sex ratio of kids (treatment: 2 = 4.18, P = 0.123; weight of mother: 2 = 2.53, P = 0.112). 4. Discussion As predicted and shown in most other farm species (reviewed by Estevez et al., 2007), there was a linear
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Fig. 4. Cortisol level (with median and interquartile range in the box, outliers shown as dots, extremes shown as asterisks) measured in adult goats housed in high, medium or small density groups in the first, second and last third of pregnancy. (a) Different superscripts indicate significant differences between treatments within definite time periods (P < 0.05). (b) Different superscripts indicate significant differences between time periods within definite treatments (P < 0.05).
increase in offensive and defensive agonistic behaviours with increasing density from 3 m2 , via 2 m2 to 1 m2 . Except for the study done by Loretz et al. (2004) focusing on feeding behaviour with a mixture of breeds, there are no other systematic studies on the effects on reduced total space per se in goats. Previous studies show that goats compete more for feeding space than resting space (Andersen and Bøe, 2007; Jørgensen et al., 2007), whereas sheep respond with increased aggression both when resting space is reduced (Bøe et al., 2006) and when feeding space is reduced on a hay diet (Bøe and Andersen, 2010). With respect to the behavioural results, a reduction in total space thus seems to enhance the level of social stress quite substantially and a space recommendation of 1.0–1.5 m2 per goat as indicated in regulations of different European countries (e.g.,
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Toussaint, 1997; council regulation (EC) no. 1804/1999) may not be satisfactory to ensure a high welfare standard in goats housed indoors. The incidence of both offensive and defensive behaviours declined over time and the stage of pregnancy can be one explanation for this result. On the other hand, in contrast to what is suggested previously (Andersen et al., 2008; Fernández et al., 2007), this may indicate that groups of goat need more than one week to get a stable flock with a minimum of aggression. The number of defensive behaviours is somewhat lower than the amount of offensive behaviours, but the reason for this is most likely that not all offensive behaviours are replied with retreat by the receiver. In fact, observations during mixing of the groups in the present study showed that there were much more offensive responses than defensive. Socio-positive behaviours were not affected by density. The present study suggests that these behaviours increase in the final stage of pregnancy when it could be of great functional importance to establish bonds for mutual protection of offspring in maternal groups at least as a risk reducing strategy through synchronized birth and shared vigilance (for review see O’Brien (1988)). This is also supported by the hormonal status which stimulates them to show maternal care (e.g., Capezzuto et al., 2008; Conway et al., 1996; Poindron et al., 2007; Sawada et al., 1995). As stated in recent reviews (Estevez et al., 2007; Miranda-de la Lama and Mattiello, 2010), grooming has the function of maintaining a healthy pelage and reducing the conflict level in a group, but goats seek body contact to a very little extent and overall, the incidence of grooming behaviour is reported to be low (Andersen and Bøe, 2007; Andersen et al., 2011). In contrast to what was predicted, the increased aggression level with increased density was neither reflected in the cortisol measures nor did it affect the productions results of the goats. Also in Andersen et al. (2008), there was no relationship between the amount of agonistic behaviours and the level of blood cortisol in adult goats, suggesting that this might not be a reliable indicator of long-term social stress in goats. Regarding reliability of our blood cortisol measures in discussing negative findings, we can say that the level of cortisol found in this study (average was 9.4 ng/ml) corresponds to the values reported in other papers in different goat breeds mostly ranging from 3 to 15 ng/ml (e.g., Al-Busaidi et al., 2008; Aoyama et al., 2008; Olsson et al., 1995; Ortiz-de-Montellano et al., 2007; Toerien et al., 1999) and the mean is only slightly higher than what was found earlier on the same breed, Norwegian dairy goats (Andersen et al., 2008; Engeland et al., 1999). The method we applied, venipuncture is used frequently and the animals were acclimated to the sampling procedure and frequent handling before the experiment. This sampling procedure may cause acute stress induced by human handling, and the interindividual differences in sensitivity to this procedure may have overshadowed the possible effect of our chronic treatment. Large inter-individual variability in blood cortisol in goats was reported elsewhere having strong impact on group values (e.g., Conway et al., 1996). Another plausible explanation for lack of differences
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between groups can be that the cortisol levels are reported to return to baseline level within 4 h after an acute stressor both in goats and sheep (Aoyama et al., 2008; Nwe et al., 1996; Ortiz-de-Montellano et al., 2007; Roussel et al., 2004; Roussel-Huchette et al., 2008; Shamay et al., 2000; Toerien et al., 1999). If agonistic encounters trigger elevation in cortisol level in an acute way, then the time of sampling chosen (early morning before feeding time) would mirror the agonistic encounters during the late night resting or sleeping period when incidences are rare and independent of group density. It is also possible, that at the time of blood sampling, the animals were in a higher arousal state caused by the nearby feeding time, masking the effects of treatment. The time was chosen based on methods applied by other researchers to get comparable results (e.g., AlBusaidi et al., 2008; Ali et al., 2006; Andersen et al., 2008; Conway et al., 1996; Komara et al., 2010; Olsson et al., 1995, 1996). Additionally, after a rather stable level of blood cortisol in the first and second third of gestation, we found a decrease in blood cortisol level in the third sampling, which was conducted ten days before the first parturition (six weeks before the last). However, Ramadoss et al. (2008) found that cortisol level in sheep is stable during pregnancy when measured on four different days distributed across gestation period, and Romero et al. (1998) found a stable blood cortisol level during pregnancy in goats even during the peripartum period. Andersen et al. (2008) also found a quite stable level of cortisol in the same breed during gestation and a sharp decrease two weeks before the expected date of parturition may be due to the general higher stress tolerance of goats in late pregnancy (in rats: Maestripieri and D’Amato, 1991; Picazo and Fernandez-Guasti, 1993; in humans: Pugh et al., 1963; Hamilton et al., 1988). In conclusion, our blood cortisol measures are comparable to data from other similar studies, but blood cortisol measures are probably not the most suited method to evaluate effects of a chronic treatment such as animal density and behaviour seems to be a more sensitive tool in detecting subtle effects. Indicators of chronic, social stress are scarcely studied and measures such as fur and faecal cortisol may be a more valid and promising physiological indicator than blood cortisol in this respect (faecal cortisol in goats: Nordmann et al., 2011; Patt et al., 2012; fur cortisol in different species e.g., dogs and cats: Accorsi et al., 2008; dogs: Bennett and Hayssen, 2010; cow: Comin et al., 2011; rhesus monkey: Davenport et al., 2006; Dettmer et al., 2012). Surprisingly, the higher level of agonistic behaviour in the small density groups did not lead to more foetal losses or a reduction in number of live born kids, nor did it affect the weight of the newborn. These results were in contrast to those from Duvaux-Ponter et al. (2003), who reported that repeated transportation of mothers during pregnancy resulted in lower kid weight and litter size. Our treatment began well after conception. By this stage of gestation, the foetuses are likely less sensitive to disturbances and are less likely to abort. On the other hand, goats have become adapted to harsh environments (Silanikove, 2000) and several studies did not find any decrease in productivity parameters as effect of treatment aimed at causing an increased level of stress (e.g., Shamay et al.,
2000). For example, in the study of Fernández et al. (2007), researchers regrouped lactating goats three times, and although it coincided with an increase in agonistic interactions, experimenters could observe a decrease in milk production only after the first reestablishment of social structure and the following regroupings did not provoke change in milk composition or milk yield. In some cases, studies even showed positive effect of stress on production, as Andersen et al. (2008) found that mothers from unstable group structure (frequent regrouping during pregnancy) had more kids. Animal density did not affect sex ratio in any significant way in the present study. In regards to the maternal adjustment of offspring sex ratio according to prenatal environment in animals, opposing hypotheses can be argued depending on environmental and social factors like food availability, sexual dimorphism in body parameters, sexual segregation and differential dispersal of sexes (for review see Hewison and Gaillard (1999)). These factors may impact animals in various ways depending on the species, including ungulates (Hewison and Gaillard, 1999) and even within breeds, having an influence on the sex ratio of offspring (Skjervold, 1979). Côté and Festa-Bianchet (2001) observed a herd of mountain goats (Oreamnos americanus) for nine years to investigate whether the assumptions and predictions of the model suggested by Trivers and Willard (1973) or its alternative, the local resource competition model (Clark, 1978), were verified. They concluded that in mountain goats, the assumptions of the models are not always met and experimental results did not confirm the predictions of the models. Andersen et al. (2008) studied effect of sequential regrouping of pregnant goats on the sex of the offspring and found no impact of treatment on ratio of male offspring.
5. Conclusions The reduction of space from 3.0 m2 per goat to 1.0 m2 per animal led to an increase in agonistic interactions but density did not affect the cortisol level of adult goats nor kid production results. If we regard agonistic behaviour as a sign of welfare in goats, space recommendations close to 1.0–1.5 m2 might be questionable.
Acknowledgements This study was conducted in frame of the Animal Welfare Indicators project (AWIN), which was financed by the EU VII Framework programme (FP7-KBBE-2010-4). We are also very grateful for the blood analysis to Peter Torjesen and Kari Julien at the Hormon Laboratory of the Oslo University Hospital. Nonetheless, we would like to thank the staff at the Animal Production Experimental Centre (Norwegian University of Life Sciences), especially Agnes Klouman for their excellent cooperation during the study and Kari Eikanger for the kind technical assistance in collecting the blood samples.
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