Natural Behaviour Is Not Enough: Farm Animal Welfare Needs Modern Answers to Tinbergen's Four Questions.

Despite the many scientific objections that have been raise to it, 'natural behaviour' is widely used as an indication of good welfare by the food industry. The supposed link between welfare and natural behaviour derives, however, from a now outdated view of animals becoming frustrated if they cannot perform their natural instinctive behaviour. On the 60th anniversary of its publication, Niko Tinbergens' Four Questions framework is used to show why there is no necessary link between natural behaviour and welfare and why, therefore, reliance on natural behaviour in commercial farming may not result in the claimed improvements in welfare. Used on its own without supporting evidence, 'natural behaviour' lacks the most essential criterion for good welfare-whether it matters to the animals themselves. There are now a number of well-established methods for demonstrating what animals value, including choice tests and, particularly, what animals will work and pay a cost to obtain. Some of the evidence on what animals value is already available in published papers but some will require collaborative research between scientists and commercial farming to find practical and commercially viable ways of providing animals with what they value.

Farm animal welfare: Beyond "natural" behavior.

An animal-centered view guided by what animals value could improve welfare on farms.

Active walking in broiler chickens: a flagship for good welfare, a goal for smart farming and a practical starting point for automated welfare recognition.

Automated assessment of broiler chicken welfare poses particular problems due to the large numbers of birds involved and the variety of different welfare measures that have been proposed. Active (sustained, defect-free) walking is both a universally agreed measure of bird health and a behavior that can be recognized by existing technology. This makes active walking an ideal starting point for automated assessment of chicken welfare at both individual and flock level.

Animal Welfare and Resistance to Disease: Interaction of Affective States and the Immune System.

Good management and improved standards of animal welfare are discussed as important ways of reducing the risk of infection in farm animals without medication. Increasing evidence from both humans and animals suggests that environments that promote wellbeing over stress and positive over negative emotions can reduce susceptibility to disease and/or lead to milder symptoms. We point out, however, that the relationship between welfare, immunity, and disease is highly complex and we caution against claiming more than the current evidence shows. The accumulating but sometimes equivocal evidence of close links between the brain, the gut microbiome, immunity, and welfare are discussed in the context of the known links between mental and physical health in humans. This evidence not only provides empirical support for the importance of good welfare as preventative medicine in animals but also indicates a variety of mechanisms by which good welfare can directly influence disease resistance. Finally, we outline what still needs to be done to explore the potential preventative effects of good welfare.

Can good broiler flock welfare prevent colonization by Campylobacter?

Using data on rearing and welfare metrics of multiple commercial broiler flocks, we investigate how welfare measures such as hock burn, mortality, and pododermatitis, among others, impact the likelihood of a flock becoming colonized by Campylobacter. Using both logistic regression and Bayesian networks, we show that, while some welfare metrics were weakly related to Campylobacter colonization, evidence could not be found to suggest that these metrics directly exacerbated Campylobacter colonization, rather that they were both symptoms of the same parent variable - the managing company. Observed dependency on the management of the flock suggested that yet-undiscovered differences in rearing practice were the principal factor explaining both poor bird welfare and increased risk of Campylobacter, suggesting that action can be taken to improve both these factors simultaneously.

Groups and Individuals: Optical Flow Patterns of Broiler Chicken Flocks Are Correlated with the Behavior of Individual Birds.

Group level measures of welfare flocks have been criticized on the grounds that they give only average measures and overlook the welfare of individual animals. However, we here show that the group-level optical flow patterns made by broiler flocks can be used to deliver information not just about the flock averages but also about the proportion of individuals in different movement categories. Mean optical flow provides information about the average movement of the whole flock while the variance, skew and kurtosis quantify the variation between individuals. We correlated flock optical flow patterns with the behavior and welfare of a sample of 16 birds per flock in two runway tests and a water (latency-to-lie) test. In the runway tests, there was a positive correlation between the average time taken to complete the runway and the skew and kurtosis of optical flow on day 28 of flock life (on average slow individuals came from flocks with a high skew and kurtosis). In the water test, there was a positive correlation between the average length of time the birds remained standing and the mean and variance of flock optical flow (on average, the most mobile individuals came from flocks with the highest mean). Patterns at the flock level thus contain valuable information about the activity of different proportions of the individuals within a flock.

A Mathematical Modeling Approach to Uncover Factors Influencing the Spread of Campylobacter in a Flock of Broiler-Breeder Chickens.

Despite continued efforts to improve biosecurity protocols, Campylobacter continues to be detected in the majority of commercial chicken flocks across Europe. Using an extensive data set of Campylobacter prevalence within a chicken breeder flock for over a year, multiple Bayesian models are presented to explore the dynamics of the spread of Campylobacter in response to seasonal variation, species-specificity, bird health, and total colonization prevalence. These models indicated that birds within the flock varied greatly in their response to bacterial challenge, and that this phenomenon had a large impact on the overall prevalence of different species of Campylobacter. Campylobacter jejuni appeared more frequently in the summer, while Campylobacter coli persisted for a longer duration, amplified by the most susceptible birds in the flock. Our study suggests that strains of Campylobacter that appear most frequently likely possess no demographic advantage, but are instead amplified due to the health of the birds that ingest it.

A Mathematical Model of Campylobacter Dynamics Within a Broiler Flock.

Globally, the bacterial genus Campylobacter is one of the leading causes of human gastroenteritis, with its primary route of infection being through poultry meat. The application of biosecurity measures is currently limited by a lack of understanding of the transmission dynamics within a flock. Our work is the first to undertake a mathematical modeling approach to Campylobacter population dynamics within a flock of broilers (chickens bred specifically for meat). A system of stochastic differential equations is used to model the routes of infection between co-housed birds. The presented model displays the strong correlation between housing density and Campylobacter prevalence, and shows how stochastic variation is the driving factor determining which strains of Campylobacter will emerge first within a flock. The model also shows how the system will rapidly select for phenotypic advantages, to quickly eliminate demographically-weaker strains. A global sensitivity analysis is performed, highlighting that the growth and death rate of other native bacterial species likely contributes the greatest to preventing flock outbreaks, presenting a promising approach to hypothesizing new methods of combatting disease transmission.

A Systematic Review of Precision Livestock Farming in the Poultry Sector: Is Technology Focussed on Improving Bird Welfare?

Precision livestock farming (PLF) systems have the potential to improve animal welfare through providing a continuous picture of welfare states in real time and enabling fast interventions that benefit the current flock. However, it remains unclear whether the goal of PLF development has been to improve welfare or increase production efficiency. The aims of this systematic literature review are to provide an overview of the current state of PLF in poultry farming and investigate whether the focus of PLF research has been to improve bird welfare. The study characteristics extracted from 264 peer-reviewed publications and conference proceedings suggest that poultry PLF has received increasing attention on a global scale, but is yet to become a widespread commercial reality. PLF development has most commonly focussed on broiler farming, followed by laying hens, and mainly involves the use of sensors (environmental and wearable) and cameras. More publications had animal health and welfare than production as either one of or the only goal, suggesting that PLF development so far has focussed on improving animal health and welfare. Future work should prioritise improving the rate of commercialisation of PLF systems, so that their potential to improve bird welfare might be realised.

Monitoring chicken flock behaviour provides early warning of infection by human pathogen Campylobacter.

Campylobacter is the commonest bacterial cause of gastrointestinal infection in humans, and chicken meat is the major source of infection throughout the world. Strict and expensive on-farm biosecurity measures have been largely unsuccessful in controlling infection and are hampered by the time needed to analyse faecal samples, with the result that Campylobacter status is often known only after a flock has been processed. Our data demonstrate an alternative approach that monitors the behaviour of live chickens with cameras and analyses the 'optical flow' patterns made by flock movements. Campylobacter-free chicken flocks have higher mean and lower kurtosis of optical flow than those testing positive for Campylobacter by microbiological methods. We show that by monitoring behaviour in this way, flocks likely to become positive can be identified within the first 7-10 days of life, much earlier than conventional on-farm microbiological methods. This early warning has the potential to lead to a more targeted approach to Campylobacter control and also provides new insights into possible sources of infection that could transform the control of this globally important food-borne pathogen.

Prediction of welfare outcomes for broiler chickens using Bayesian regression on continuous optical flow data.

Currently, assessment of broiler (meat) chicken welfare relies largely on labour-intensive or post-mortem measures of welfare. We here describe a method for continuously and robustly monitoring the welfare of living birds while husbandry changes are still possible. We detail the application of Bayesian modelling to motion data derived from the output of cameras placed in commercial broiler houses. We show that the forecasts produced by the model can be used to accurately assess certain key aspects of the future health and welfare of a flock. The difference between healthy flocks and less-healthy ones becomes predictable days or even weeks before clinical symptoms become apparent. Hockburn (damaged leg skin, usually only seen in birds of two weeks or older) can be well predicted in flocks of only 1-2 days of age, using this approach. Our model combines optical flow descriptors of bird motion with robust multivariate forecasting and provides a sparse, efficient model with sparsity-inducing priors to achieve maximum predictive power with the minimum number of key variables.

Commercial scale research and assessment of poultry welfare.

1. Commercial level research on poultry welfare is increasingly important because of the insight it gives into what improves welfare in the context of other important drivers such as human health, environmental impact and cost. 2. There are, however, a number of problems with conducting commercial level research - such as conflicts over aims, financial compensation and legal issues - that need to be addressed if the gains from commercial research are to be optimized. Cooperation between all parties and mutual understanding of the different priorities that may exist between industry and academia are essential. 3. Three important developments for the future are: the setting up of a 'data bank', the application of new statistical methods for analyzing data and new technology for assessing welfare automatically.

Prediction of feather damage in laying hens using optical flows and Markov models.

Feather pecking in laying hens is a major welfare and production problem for commercial egg producers, resulting in mortality, loss of production as well as welfare issues for the damaged birds. Damaging outbreaks of feather pecking are currently impossible to control, despite a number of proposed interventions. However, the ability to predict feather damage in advance would be a valuable research tool for identifying which management or environmental factors could be the most effective interventions at different ages. This paper proposes a framework for forecasting the damage caused by injurious pecking based on automated image processing and statistical analysis. By frame-by-frame analysis of video recordings of laying hen flocks, optical flow measures are calculated as indicators of the movement of the birds. From the optical flow datasets, measures of disturbance are extracted using hidden Markov models. Based on these disturbance measures and age-related variables, the levels of feather damage in flocks in future weeks is predicted. Applying the proposed method to real-world datasets, it is shown that the disturbance measures offer improved predictive values for feather damage thus enabling an identification of flocks with probable prevalence of damage and injury later in lay.

A user's guide to animal welfare science.

Here, I provide a guide for those new to the burgeoning field of animal welfare science as to what this comprehensive, relatively young discipline is all about. Drawing on all branches of biology, including behavioural ecology and neuroscience, the science of animal welfare asks three big questions: Are animals conscious? How can we assess good and bad welfare in animals? How can we use science to improve animal welfare in practice? I also provide guidelines for an evidence-based approach to welfare issues for policy makers and other users of animal welfare research.

Chicken welfare is influenced more by housing conditions than by stocking density.

Intensive broiler (meat) chicken production now exceeds 800 million birds each year in the United Kingdom and 2 x 10(10) birds worldwide, but it attracts accusations of poor welfare. The European Union is currently adopting standards for broilers aimed at a chief welfare concern--namely, overcrowding--by limiting maximum 'stocking density' (bird weight per unit area). It is not clear, however, whether this will genuinely improve bird welfare because evidence is contradictory. Here we report on broiler welfare in relation to the European Union proposals through a large-scale study (2.7 million birds) with the unprecedented cooperation of ten major broiler producers in an experimental manipulation of stocking density under a range of commercial conditions. Producer companies stocked birds to five different final densities, but otherwise followed company practice, which we recorded in addition to temperature, humidity, litter and air quality. We assessed welfare through mortality, physiology, behaviour and health, with an emphasis on leg health and walking ability. Our results show that differences among producers in the environment that they provide for chickens have more impact on welfare than has stocking density itself.

Behaviour as a tool in the assessment of animal welfare.

A central issue in animal welfare research is how to assess the welfare state of animals objectively and scientifically. I argue that this issue can be approached by asking two key questions: 1) is the animal physically healthy and 2) does the animal have what it wants? Behaviour is used to answer both of these questions. In the assessment of physical health, it can be used for clinical and pre-clinical diagnosis. In the assessment of what animals want, it has a major role through choice and preference testing. It is particularly important that applied ethologists develop methods for assessing welfare in situ--in the places where concern for animal welfare is greatest such as on farms and in zoos.

ARE WARNING COLORS HANDICAPS?

The handicap theory, in which the cost of waste guarantees honest advertising, is being used increasingly in solutions to the problems of biological signal evolution. However, it is usually applied to systems which are insufficiently understood to allow testing against alternative theories. In particular, the ability of the handicap theory to explain the design of signals has never been properly tested. We test its ability to explain signal design features in an unusually well studied area of biological signalling: warning coloration and mimicry. Since a full handicap model proves immediately unrealistic, we modify the model to incorporate realistic assumptions about predator learning. Using this model we explicitly compare the handicap theory with a purely "conventional" signalling model and with a null model. Predictions relating to three key design features (conspicuousness, pattern similarity, and Batesian mimicry) are compared, and tested against available data. Although many predictions remain to be tested adequately, we conclude that: (i) conspicuousness is most plausibly explained by the conventional signalling theory that ascribes the function of conspicuous coloration to signal efficacy rather than waste; (ii) pattern similarity, within and between species, is unlikely to be the result of the need to produce similar degrees of conspicuousness, as predicted by the handicap theory, but is plausibly explained as the result of pattern generalization amongst discriminating predators, as predicted by the conventional signalling theory; and (iii) Batesian mimicry is predicted by the conventional signalling theory, but not the handicap theory. Therefore the handicap theory fails to provide an adequate explanation of the main design features of at least one major signalling system.