Anxiety is an affective state that is beneficial for the survival of an animal. However, if the animal’s anxiety response is inappropriate, then the animal will suffer from negative affect 49. We investigated anxiety in fast- and slow-growing broilers as they gained weight and aged, while housed in a simple or complex environment. Both strain and environmental complexity impacted anxiety in broilers, with effects in some cases dependent on body weight. Slow-growing birds were less anxious than fast-growing birds (likelihood to feed; vigilance in simple environments), although they seemed more restless (latency to first step). Light birds were less anxious than heavier birds (likelihood to feed; vigilance) in complex environments and less anxious than light birds in simple environments (likelihood to feed). Complexity reduced anxiety (vigilance).
Fast-growing broilers at 2-kg body weights were tested using a similar test protocol while housed in complex or simple environments 26. Aligned with our findings, they reported that fast-growing broilers were less anxious when housed in complex environments compared to simple environments. Although our results indicate a similar benefit of complexity on anxiety, the proportion of birds feeding did differ between studies, with 64% of birds feeding 26, compared to 35% of fast-growing birds in the current study at the same weight point. Our response rate of 32% at 1-kg body weight was higher than reported in a pharmacological validation study, where 2% of fast-growing broilers (1.3 kg body weight) treated with an anxiogenic substance began feeding, and 10% of the saline-treated broilers began feeding 50. The handling and injection procedure may have reduced response rates in their study compared to ours, as rough handling can increase fear in broilers 51,52.
Slow-growing broilers that were part of the current study, underwent an ABT (at 3 kg body weight) and showed a response rate of 91% in the high-complexity treatment and 80% in the low-complexity treatment 53. These birds were naïve to the ABT, but did undergo repeated handling and judgement bias training and testing, which may explain the increased response rate compared to the 47% of 3-kg slow-growing broilers feeding, as reported here. This suggest that repeated exposure to novel experiences, perhaps especially experiences that stimulate cognition, can contribute to either how birds respond in an ABT, or can reduce bird anxiety.
Slow-growing broilers were overall more likely to begin feeding than fast-growing broilers, indicating they experienced less anxiety. Slow-growing broilers may experience a greater sense of self-efficacy when faced with the threat of a predator. Self-efficacy is defined as an individual’s confidence about their capability to perform a specific task 54. For broilers in the ABT, this could be translated to their sense of ability to escape a potential predator. Lack of self-efficacy and anxious thoughts and behavior are positively associated in humans 55–60. This may be similar in other species, including chickens. Due to the genetic selection for meat yield, fast-growing broilers have different body conformation than slow-growing broilers. Breast meat accounts for a greater proportion (35%61 27% 62) of the carcass yield in fast-growing broilers than slow-growing broilers (25%61 18% 62). Fast-growing broilers also have a shorter body length (24 cm) compared to slow-growing broilers (30 cm) while having similar breast muscle length (fast-growing 18 cm vs slow-growing 19 cm) 62. These body composition differences result in more exertion required for locomotion and other physical activities, thus making locomoting require more energy63 compared to a chicken with smaller breast muscles and larger body length. We theorize that fast-growing broilers would experience a lack of self-efficacy because they consider their own difficulty escaping an actual predator based on their physical abilities, and therefore experience more anxiety when posed with a threat of a predator, compared to a slower-growing strain with a greater sense of self-efficacy. Since they are less likely to successfully escape, they may feel more anxious when faced by this situation.
Further impacting their sense of self-efficacy could be the birds’ gait. In the ABT, broilers were required to move towards the feed in order to eat. Fast-growing broilers experience worse gait 7,64 and expend more energy to locomote than slow-growing broilers 63, potentially impacting their willingness to eat during the test. However, only non-lame broilers were selected for testing and broilers only needed to take a maximum of three steps to access the feed. Thus, differences in gait should not have impacted eating behavior during the test.
Fast-growing broilers were less likely to be highly vigilant when raised in a complex environment compared to fast-growing broilers in a simple environment. Similarly, anxiety was reduced in fast-growing broilers raised with enrichments 26 and in starlings offered water baths 65 compared to a barren control. Access to resources can improve health and affect, improving leg strength 19,66, walking ability 20–23, and increasing optimism 29 in fast-growing broilers. These physical and psychological benefits of environmental complexity may have contributed to the fast-growing broilers’ sense of self-efficacy, resulting in their reduced vigilance, thus decreased anxiety during the test. This is similar to how increased self-efficacy reduced anxiety in humans 60. Fast-growing broilers from complex pens may have expected a more positive outcome than fast-growing birds from simple pens, thus leading the former to be less vigilant. When broilers are placed into the ABT arena, they are faced with a novel environment and novel feed, which can induce a fear response. Complexity can reduce fearfulness 25,26,28. As such, birds from the complex environment may have been less fearful in the novel ABT environment and more willing to interact with a novel food item than birds from the simple environment. However, other studies have not found an effect of complexity on fearfulness 25,26,67,68. The ABT likely induces both fear and anxiety, and fast-growing broilers from complex pens seemed to be better equipped to cope with these conditions compared to those from simple pens.
Anxiety was mitigated by complexity at lower weights, but increased and became similar in birds from simple and complex environments at later weight points. Lighter broilers in a complex environment were more likely to begin feeding compared to heavier broilers in a complex environment, with no difference in the simple environment. This indicates less anxiety for light compared to heavy broilers when raised in a complex environment only. This suggest that the environmental resources were beneficial in reducing anxiety for all broilers, but only at low body weights. The resources may not have been suitable for heavier birds even if motivation to use the resources remained. The fast-growing broilers may not have been able to benefit from the resources as they gained weight due to their reduced ability to interact with them 69. Yet, slow-growing broilers do not experience such a reduction in ability 7,64, while the same effects of weight gain were observed. Rather, the reduced benefit with increasing weight may be related to their age when gaining weight, as they begin to mature and develop social hierarchies. Male chickens may begin aggressive pecking as early as two weeks of age, which is behavior associated with social hierarchy development, while females show aggressive pecking in week 5 onwards, reaching adult frequencies between 8 and 10 weeks of age 70. The slow-growing broilers were 8 weeks old at 3 kg live weight, thus it is likely that a similar behavioral development took place. This may have increased agonistic behavior related to available resources, compared to the fast-growing broilers that were less than 6 weeks old at 3 kg live weight. The increased social pressures may have contributed to anxiety at later ages, especially in complex environments where resources were limitedly available, in contrast with simple environments where no resources were available besides feed, water, and litter. This could imply that slow-growing broilers may need more resources as they grow older in order to avoid potential negative social interactions and subsequent negative affect. This argumentation is not supported by previous work. Slow-growing broilers did not show increased conspecific aggression with age, although the authors mention methodological limitations to determine this conclusively 71. It would be valuable to determine if complexity induces negative social interactions as birds mature, and if a greater availability of resources would limit this potential impact.
Fast-growing broilers were less vigilant when housed in a complex environment than in a simple environment, but this effect was not seen in the slow-growing broilers. A complex environment may have benefitted the fast-growing broilers more than slow-growing broilers. Since the pen design was standardized across both strains, and intended for fast-growing broilers, slow-growing broilers’ needs may not have been met. Both strains were offered a low, flat perch which was intended to be accessible for fast-growing broilers even if they experience gait issues 4–6. However, slow-growing broilers seem to prefer higher platforms. Platforms at 20, 30, 40, 50 cm heights were used by 9% 72, 18% 73, 16–30% 71, and 26–29% 74 of the flock. These studies suggest that height is positively associated with number of birds using the platforms, although this was not directly compared. Since our perches were low, few slow-growing broilers may have used them, therefore, motivation to perch might not have been met. This motivation is strong in domestic chickens, similar to their ancestor, the Red Jungle Fowl 75,76 and the behavior serves to avoid predators 77. Slow-growing broilers have not been selected for increased production as rigorously as fast-growing broilers. Thus, their motivations and abilities may be closer to their ancestors compared to the fast-growing strain. In line, this stronger motivation and ability to use perches in slow-growers compared to fast-growers is reported previously 71–73. Fast-growing broilers may have a similar preference for higher elevations, as one study reported more prevalent use of elevated structures of 10, 13, and 18cm height, compared to one of 7cm height 78. Without an adequately high location to avoid predation, slow-growing broilers may especially experience a lacking sense of safety from predation while using low perches. This could have contributed to the lack of contrast in behavioral responses between slow-growing broilers in complex or simple pens. The potential benefits from other resources in the complex pens for slow-growing broilers is unknown. We recommend further investigation into the resource preferences of slow-growing broiler chicken strains.
Slow-growing broilers had a shorter latency to step in complex environments compared to fast-growing broilers in simple environments only. Anxiety in animals is characterized by restless behavior 79,80. A short latency to step was interpreted as greater restlessness and anxiety in broilers 81. This would suggest that slow-growing broilers in complex environments are more restless, thus more anxious, which is opposite of what other behavioral indicators suggest. However, others reported no differences between treatments (hens 37; broilers 26) or applied an opposite interpretation 38. This suggests that the measure is difficult to interpret. Activity and number of steps are recorded in other species, rather than latencies to step (pigs, 82; sheep, 83). Based on these prior studies, and the conflicting interpretations and results, we have determined that latency to first step may not be the optimal measure for anxiety.
Many birds did not eat during the ABT; therefore, we could not statistically analyze the latency to feed. Novelty of the test environment may have limited their behavioral responses due to fear and anxiety, which could be mitigated by habituation prior to testing. Broilers spent 79% of the time performing vigilance behaviors during the ABT, indicating a high level of anxiety. Habituation may reduce fear and anxiety caused by other stimuli than the conspecific alarm call. Previous experiments allowed birds to habituate to the arena 37,38, although others did not habituate chickens to the arena and still found differences in latency to feed 26,36. It may be beneficial to habituate the broilers to the arena and the novel feed, depending on genetic strains used or treatments provided. The large proportion of time spent performing vigilance behaviors in this experiment may indicate the high levels of anxiety experienced, explaining why they did not begin eating within the test.
The test duration of 5 minutes may not be long enough to detect a difference in latency to feed between treatment groups. A prior study used 10 minutes for the ABT 37, while others successfully used a 7-minute 81 or 5-minute approach 26,36. A longer testing period could increase participation from anxious broilers.
Our bird selection procedure for good gait may have biased our results to more positive affect. We selected birds because walking ability may confound the results of the ABT, since birds needed to walk to the feeder. Lameness may reduce their willingness to move to eat, appearing more anxious 84. Gait disorders cause pain in fast-growing broilers 85–88 and increase fear 89. Birds with better gait may actually be less anxious than birds with worse gait, as pain is a negative experience with affective components 90. Experiencing chronic pain can increase anxiety, as reported in humans 91–93 and rats 94–96. Therefore, broilers with impaired walking ability were likely experiencing more negative affect. However, our design excluded these animals in the assessment.
The broiler chicken industry is showing a move towards the production of slower-growing strains. Consumers show concern about the treatment of production animals and their welfare status, and report a willingness to pay for welfare improvements 97,98. For instance, when consumers are provided news articles with professionals stating the improved health of slow-growing broilers, they report a willingness to pay a premium for products from slow-growing broilers compared to products from fast-growing broilers 99. Voluntary animal welfare certification programs in the United States will require slow-growing strains for their suppliers 100,101. Slower-growing broiler strains comprise almost 40% of Dutch broiler production, 24% of French broiler production, and 11% of production in the United Kingdom 102.
This experiment is the first to assess differences in affective state, specifically anxiety, between fast- and slow-growing strains housed with or without additional resources. The improved affect (reduced anxiety) in the slow-growing strain used here was not consistent as birds gained weight (anxiety increased), suggesting that a move to slow-growing strains may require more adjustments to commercial practices besides just choosing a broiler strain with different genetic potential for growth. Thus, replacing Ross 708 with Redbro Mini broilers will not necessarily guarantee less anxiety, even when housed in complex environments. Future studies should focus on testing the same and other genetic strains to confirm whether our results are representative of the same and other fast- and slow-growing strains.