Trending terms but what do they mean and how do we measure them?
By Andrea M. Luttman, Janice M. Siegford and Catherine W. Ernst
To put it simply, a robust animal is one that is able to meet its production potential despite any stressors or disturbances it may experience in its lifetime (Knap, 2005).
Resilience is a key component to robustness and is described as an animal’s capacity to quickly recover from a stressor and return to its pre-stress state (Colditz and Hine, 2016). Resilience characterizes a response to a single event, such as a specific disease challenge, transportation, a very hot day, or getting introduced to a new social cohort.
Robustness can be thought of as cumulative resilience enabling the animal to not have compromised production, reproduction, health or welfare regardless of environment. Breeding robust animals is the ultimate goal and developing a better understanding of resilience to various stressors is the first step in achieving that goal.
Researchers have begun examining resilience to various types of stress including heat stress and disease. Our research team is focusing on resilience to social stress. Because pigs are routinely mixed into new social cohorts during the production process, social stress is an interesting issue in pigs and is increasingly important with the transition to gestational group-housing.
The pork industry has developed many ways for producers to better manage nutritional stress, heat stress, etc. but social stress is dependent on the individual animal as well as its specific social context, and therefore is very difficult to manage.
Identifying pigs that are resilient (or not) to social stress could provide a means to select resilient pigs for future breeding and to efficiently manage pigs that are classified as vulnerable to enhance their ability to achieve their production potential.
First steps in characterizing resilience to social stressOur team at Michigan State University has recently completed a study using weaning as a model to investigate if there was enough variation in stress response of cross-bred gilts to identify distinct populations of resilient and vulnerable pigs at weaning, and if so, determine if long-term differences persist in these two populations.
This study, funded by the Michigan Alliance for Animal Agriculture (MAAA), has been the starting point for our examination of the underlying molecular mechanisms of stress regulation and resilience to social stress; our continued work planned to begin in 2023 is funded by the USDA NIFA.
We were able to identify distinct stress resilient and stress vulnerable populations by measuring serum cortisol concentrations at three timepoints: 1d pre-weaning, the day of weaning and 4d post-weaning. Assessing cortisol at three timepoints was crucial to not only assess a pig’s acute stress response but also its ability to recover and return to baseline.
It’s important to note that we were not influencing stress response with any experimental treatment. We were observing and measuring a response to a stressor (weaning) that commonly occurs in swine production under conditions approximating a commercial setting.
We enrolled 26 litters with an average of seven gilts/litter (range 5-12 gilts/litter) in the study. Gilt piglets that were cross-fostered or had an extremely different weaning weight from their littermates were not eligible for focal pig selection.
We then ranked the eligible gilt piglets within litter and designated the one with the greatest recovery as stress resilient (SR, n=26) and the one with the least recovery as stress vulnerable (SV, n=26).
These two populations of focal gilts were confirmed to have distinct stress response patterns as demonstrated in Figure 1.
Not only did we find enough variation in stress response to identify distinct populations of resilient and vulnerable pigs, but we have also started to identify behavioral differences between these two groups. At approximately eight weeks of age, gilts were moved from nursery rooms to grow-finish rooms and mixed into new social cohorts.
We found that gilts designated as stress resilient engaged in more fights than stress vulnerable gilts as demonstrated by greater number of skin wounds (Table 1).
SR
SV
Stage
LSM
95% CI
p-value
1d Pre-Mixing
27
(22-33)
26
(21-32)
0.771
1d Post-Mixing
62
(49-77)
47
(38-59)
0.042*
4d Post-Mixing
15
(12-20)
14
(10-19)
0.548
Table 1. Skin wound counts surrounding movement into grow-finish rooms*
*Least square means (LSM) and 95% confidence interval (CI) for skin wound counts of stress resilient (SR) and stress vulnerable (SV) pigs at each stage surrounding mixing into new social cohorts when pigs were moved into grow-finish rooms.
There were no differences in skin wound counts 1d pre-mixing or 4d post mixing, but SR gilts exhibited significantly more (approx. 30% more, p=0.04) skin wounds at 1d post-mixing compared to SV gilts.
For this study we did not include video observations and therefore cannot make conclusions of whether SR gilts are truly more aggressive and SV gilts less aggressive or whether SR gilts are more likely to engage with other pigs while SV pigs withdraw from contact as much as possible.
Additionally, we conducted a novel object test on all focal gilts to investigate if there were differences in how they handled a new situation. To do this, we walked each individual pig from their home pen to a test pen located in a different area of the farm (Figure 2).
Pigs were given one minute to acclimate to the pen before we lowered a novel object (in this case, a basketball) at a fixed location in the test pen and pigs were observed for five minutes.
Behavioral results of the novel object test are provided in Table 2. There were no differences in how quickly SR or SV gilts approached the novel object, but we did find that SR gilts touched the novel object significantly more (approx. 40% more, p=0.03) and vocalized significantly less (approx. 35% less, p=0.04) than SV gilts.
Increased object touches despite no differences in latency may suggest that SR gilts engage in more exploratory behavior but are not necessarily bolder than SV gilts when faced with novelty.
Vocalizations come in a range of types and can vary depending on the context and emotional state of the pig, making them difficult to interpret. However, in general, vocalizations correlate to a pig’s level of arousal or excitement, and low-pitch vocalizations are used to maintain social contact.
Researchers are still trying to understand the role of high-pitch vocalizations as they have been observed in both positive and negative emotional states.
Thus, while we cannot use vocalizations to make any straightforward inferences about differences in emotional state during the novel object test, we can hypothesize that SV gilts are perhaps more excitable based on their increased number of total vocalizations.
As we plan our upcoming project, our team plans to develop more robust behavioral measures to better characterize differences in fearfulness, reactivity, and coping styles.
SR SVLatency(seconds) LSM 95% CI LSM 95% CI p-value
Cross 1m Line
15.4
(7.2-31.9(
16.1
(7.5-33.1)
0.878
Cross 0.5m Line
24.8
(13.2-45.5)
27.4
(14.8-50.0)
0.729
Touch Object
49.3
(28.5-84.5)
38.0
(22.1-64.7)
0.445
Event Frequency (Count)
4.5
(3.6-5.4)
5.1
(4.2-6.0)
0.310
Cross 0.5 Line
3.7
(2.9-4.5)
(3.0-4.5)
0.936
5.7
(4.4-7.0)
4.0
(2.8-5.3)
0.029*
Vocalizations (count)
High-pitch
5.2
(2.7-9.5)
3.2
(1.5-6.1)
0.180
Total
76.7
(55.9-104.9)
104.2
(76.4-142.0)
0.037*
Table 2. Behavioral results of the novel object test*.
*Least square means (LSM) and 95% confidence interval (CI) of stress resilient (SR) and stress vulnerable (SV) pigs for each measurement. Measurements included latency time (in seconds) to approach and/or touch the novel object, frequency counts for approaching and/or touching the novel object, and frequency counts of vocalizations.
Why should pork producers care about resilience to social stress?Our recent study used weaning as a model to initially study resilience to social stress, but our group is primarily interested in sow resilience to social stress during gestational group-housing. For the gestating sow, social stress has implications beyond the aggression they themselves experience when they are first mixed.
The stress experienced by the gestating sow can also be transmitted to the in-utero offspring, a phenomenon called prenatal stress, and prenatal stress can impact the offspring’s lifelong performance and health.
Previous research has found that stress during gestation, whether induced by giving exogenous corticosteroids or occurring naturally from intentional mixing, does impact the offspring.
There have been observed differences in birth weight, weaning weight, maternal behavior, stress response and reproductive fitness in the offspring of socially stressed sows (Jarvis et al., 2006; Kranendonk et al. 2006a,b; Ashworth et al., 2011).
The bottom line is social stress during gestation is not only a welfare concern but potentially detrimental to production viability, whether the goal is raising feeder pigs or maintaining a maternal line. Since social stress is difficult to manage once pigs are in the barn, the best option is to select pigs that are resilient to social stress.
Despite this, little research has been done to understand the genetics behind stress resilience.
Next stepsOur team’s long-term goals are to characterize the life-long and intergenerational effects of early life social stress as well as prenatal social stress on resilience in the pig, and to identify molecular mechanisms underlying those effects.
Our first study has confirmed that there is enough phenotypic variation in pigs’ physiological stress responses to identify distinct populations of resilient or vulnerable pigs and that those two populations exhibit behavioral differences.
In the coming year, we are going to start identifying the genetic mechanisms that control this variation in stress response. We will be working with litters of purebred Yorkshire gilts to repeat our weaning study, but this time collecting samples to look at epigenetic regulation of gene expression, specifically examining DNA methylation and transcriptomic profiles of resilient and vulnerable pigs.
Later we will also be transitioning our SR/SV selection process to group-housed gestating sows. We will then follow the offspring of SR/SV sows to identify phenotypic differences and examine their DNA methylation and transcriptomic profiles.
Whole-genome DNA methylation data integrated with transcriptomic data is a new avenue to determine the genetic control of stress resilience that can be developed into new breeding selection criteria to ultimately improve performance in group-housing environments.
While we are still in the early stages, we believe that findings from this project could lead to powerful, positive change in the pork industry.
AcknowledgementsThe authors wish to thank the other members of our research team, Bora Lee (graduate student), Nancy Raney (laboratory technician), Dr. J.P. Steibel (Iowa State University), and numerous undergraduate student assistants.
We also thank Kevin Turner and Chris Rozeboom from the MSU Swine Teaching & Research Center for their expertise and assistance.
This project was funded by the Michigan Alliance for Animal Agriculture (award number AA-21-160).
Our continuing work is funded by Agriculture and Food Research Initiative award number 2022-67015-36865 from the USDA National Institute of Food and Agriculture. AML is supported by a pre-doctoral fellowship from USDA NIFA (award number 2022-67011-36562)
ReferencesColditz, I. G., & Hine, B. C. (2016). Resilience in farm animals: Biology, management, breeding and implications for animal welfare. Animal Production Science, 56(12), 1961–1983. https://doi.org/10.1071/AN15297
Knap, P. W. (2005). Breeding robust pigs. Australian Journal of Experimental Agriculture, 45(7–8), 763–773. https://doi.org/10.1071/EA05041
Jarvis, S., Moinard, C., Robson, S. K., Baxter, E., Ormandy, E., Douglas, A. J., Seckl, J. R., Russell, J. A., & Lawrence, A. B. (2006). Programming the offspring of the pig by prenatal social stress: Neuroendocrine activity and behaviour. Hormones and Behavior, 49(1), 68–80. https://doi.org/10.1016/j.yhbeh.2005.05.004
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. H., & Taverne, M. A. M. (2006). Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Hormones and Behavior, 49(5), 663–672. https://doi.org/10.1016/j.yhbeh.2005.12.008
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. H., Wiegant, V. M., & Taverne, M. A. M. (2006). Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation. Domestic Animal Endocrinology, 30(3), 218–238. https://doi.org/10.1016/j.domaniend.2005.07.001
Ashworth, C. J., Hogg, C. O., Hoeks, C. W. F., Donald, R. D., Duncan, W. C., Lawrence, A. B., & Rutherford, K. M. D. (2011). Pre-natal social stress and post-natal pain affect the developing pig reproductive axis. Reproduction, 142(6), 907–914. https://doi.org/10.1530/REP-11-0280
Luttman is a PhD candidate majoring in genetics and genome sciences, and Siegford and Ernst are professors of animal science, all at Michigan State University.