Understanding functional performance in bird skulls: advanced computational modelling to investigate cranial biomechanics and kinesis

Birds are well known for having a huge variety of beak shapes and sizes; a feature that is widely believed to be responsible for their evolutionary success. What is less well known is that bird beaks are incredibly mobile: when opening their mouths, birds don't just lower their jaws, but raise the upper beak as well using a flexible hinge region just behind the nostrils. This hinge presents something of a conundrum, because a flexible skull should be less good at turning muscle force into biting force. Our research aims to test several ideas based on mechanics about why the hinge evolved. Perhaps a hinged skull allows the beak to open wider, without over-stretching birds' jaw muscles? Or allows dangerously high forces generated in the beak to be absorbed before they can reach the brain? Perhaps movement in the skull changes the leverage of the jaw muscles to make them more efficient? Or maybe the hinge is simply a side-effect of thinning down the bones to reduce weight as birds evolved away from their heavy, dinosaur ancestors?
These ideas are rarely explored because the moving parts are difficult to see without harming the birds. Our research aims to change this by building advanced computer models of the movement in the skull during bird feeding, and using them to test ideas that would be impossible or unethical to test on living animals; for example, in the computer we can "turn off" certain muscles, or "lock" the hinge so that it can't move. We will use 3D x-rays ("CT scans") of bird specimens donated by museums to rebuild the skull and muscles inside a computer, and analyse them using engineering methods ("finite element analysis" and "multibody dynamics analysis") designed for testing the performance of man-made structures like bridges and cars. We will also produce a database of properties of bird bones, muscles, and hinge anatomy, which will be shared online along with the models for other researchers, museums, and teachers to use.
A critical step in this process is validating the computer models, to make sure that they are producing numbers that are realistic and reliable. Inside the CT scanner, we will apply forces to the beaks of our museum-donated specimens to mimic biting. By taking a scan before and after the force is applied, we will be able to calculate how much deformation has occurred in the bones and compare this to our computer models to verify their accuracy. Using the CT scanner to measure this deformation represents a major advancement, because for the first time we will be able to measure the motion and deformation in 3D through the whole structure, instead of just on the surface over small areas. We will also measure the bite force of the same species of living birds by having them bite on a small pressure sensor. At the same time, we will film the birds biting to track the motion and deformation of the beak. These motion and bite force measurements will be used to validate the multibody dynamics models, which will then feed back into the finite element models to simulate skull deformation during actual feeding. Not only will the validated models allow us to test the evolutionary ideas outlined above, but they will give us vital information about how to best model several anatomical features that are characteristic of, but not exclusive to birds, including: ultra-thin bones; complicated bone shapes; skulls made from multiple materials; and moving joints within the skull.
With this knowledge, we will not only gain insight into the evolutionary story of bird beaks, but we be able to advise others on best practices for computer models that can reduce, and hopefully ultimately replace, the need for invasive animal testing.

Recent years have seen an explosion of data on the ecomorphological evolution of bird feeding, however, functional data has lagged behind. This is largely because of the practical difficulties of in vivo study: bird skulls are highly kinetic, with internal moving parts that are impossible to observe directly. Computational models (finite element [FEA] and multibody dynamics [MDA] analysis) are now widely used tools in biomechanics, especially when direct observation is problematic; however, such modelling is of limited use when it has not been experimentally validated. Birds present several traits with little to no validation data: ultra-thin bones; keratinous coverings; synovial joints; bending zones; and more. Our research aims to validate FEA and MDA models of bird feeding using a combination of anatomical study (dissection, diceCT, strain gauging, and materials testing), and novel in vivo (digital image correlation from high-speed cameras) and ex vivo (digital volume correlation in the CT scanner chamber) strain and motion data, thus establishing best practices for birds and other animals presenting similar modelling challenges.
We will then use our validated models to address several questions about cranial kinesis from an evolutionary perspective. We will test hypotheses exploring the roles of muscle anatomy; gape; joint mobility; and material and structural stiffness, in the generation of bite force and the dissipation of stress around the skull, with particular attention on the role of the craniofacial hinge (a bending zone between the beak and cranium).
This study will significantly advance our understanding of the mechanics and evolution of cranial kinesis in birds. Along the way, we will produce and experimentally appraise the most complex cranial biomechanical models ever constructed, laying the foundations for future studies of bird feeding and making a major progression towards Replacement and Reduction of in vivo experimentation.