The role and ontogeny of maps in long-distance animal navigation

Impressive feats of long-distance animal navigation raise questions relating to the proximate causes of such behaviours: what mechanisms facilitate long-distance animal navigation? What is the ontogeny of such behaviours? I focus on how animals determine their position in relation to their goals to determine goalward directions in the first step (the map step) of a two-step navigational process termed map and compass navigation.
I begin by introducing a framework that deconstructs animal maps into three interlinked components: (1) map cues, (2) map structure, their organisation of spatial information, and (3) map navigation strategy, the way that animals approach goals and combine multiple map cues. I discuss the ontogeny of animal maps, clarifying the roles of inherited rules, imprinting and latent learning, and suggest that mechanisms for determining vectors of self-motion, known as path integration, could facilitate map learning by allowing animals to integrate changes in map cues with self-motion.
I use two general approaches to examine animal maps. First, I employ artificial neural networks as simple computational models of animal learning. This allows me to investigate the possible ontogenies of navigational behaviours and make predictions about how animals might learn to navigate. Using this approach, I investigate how animals might learn to combine intersecting environmental gradients to navigate with a grid map. I find that neural networks adopt a mechanism of combining environmental gradient cues through first determining displacements in each gradient field independently, leading to predictable orientation errors in some environments. This work clarifies how such mechanisms might arise and change through learning, allowing me to make more nuanced predictions of how navigational mechanisms might develop through learning. Using a similar approach, I investigate how collective decision-making processes impact upon individual learning when animals navigate in groups. I find that leaders learn more quickly than followers, and that individuals in democratic groups, in which compromises are taken between individual preferences, learn by compensating for partner error unlike individuals in despotic groups and solo learners.
My second general approach involves experiments on two model species of long-distance navigation. I attempt to investigate whether Manx shearwaters utilise olfactants as navigational map cues, while minimising impact on the birds, by manipulating their access to olfactory cues before release after long-distance displacement. However, I find no clear evidence that they utilise olfactory cues in their navigation, leaving the sensory basis of their navigational map an open question. I investigate navigational ontogeny in homing pigeons, examining whether passive exposure to a novel release site is sufficient for navigational learning. I find no evidence that passive exposure to the release site impacts upon initial navigational performance and hence no evidence that this is sufficient for learning.
Overall, this work clarifies outstanding questions on the proximate causes of animal navigation, generates predictions on navigational learning, and produces incremental steps forward in our understanding of navigational mechanism and ontogeny in two model systems. Ultimately, advancing these theoretical and empirical approaches together will enable us to better identify and understand the proximate causes of long-distance animal navigation.