Evolution and ecology of extractive foraging in birds and mammals

Extractive foraging is the act of locating and processing embedded or encased foods such as underground plant storage organs, wood-boring arthropods, shellfish or plant parts protected by a thorny, tough or hard matrix. It is assumed to enhance the efficiency with which animals can exploit resources, enabling them to inhabit otherwise inhospitable environments, but its large-scale evolution and ecological consequences have been surprisingly little studied. A variety of specializations have evolved in birds and mammals to enable extractive foraging, including both specialised morphologies such as the elongated snouts and tongues and curved foreclaws of anteaters, and specialised behaviours, such as the auditorily-guided excavation seen in aye-ayes and tool-use displayed by taxa such as great apes and New Caledonian crows. Similar adaptations for extractive foraging, such as binocular vision in birds and primates8-9 appear to have evolved multiple times independently in different taxa, but these potential cases of convergent evolution have not been formally studied. We also know little about the evolutionary relationship between extractive foraging and tool use: does the former predispose to the latter, and if so under what conditions? Despite its potential advantages, extractive foraging is phylogenetically patchily distributed across birds and mammals, suggesting that it evolves under only certain conditions, and that such conditions have recurred repeatedly in independent cases, across the tree of life. These recurrences provide an opportunity to use phylogenetic comparative methods to examine not only the ecological conditions favouring extractive foraging, such as diet type and seasonality, but also morphological predisposing factors, constraints on its emergence, and its evolutionary feedback effects on behaviour, niche occupancy, evolutionary rates and speciation. For example, the conditions favouring specialised behaviours such as tool-use versus specialised morphologies are currently unknown, as are the effects on population dynamics, clade diversification and evolutionary rates after it appears. Complex patterns of extractive foraging behaviour are thought to be cognitively demanding and require extended development to facilitate learning, predicting associations between complex extractive foraging, brain size or structure, age at maturity, juvenile period and amount of time spent in non-social play. Extractive foraging may buffer individuals against environmental perturbations, predicting associations between extractive foraging and environmental unpredictability or seasonality. We will test the "Extractive foraging hypothesis" for brain size evolution, which suggests that extractive foraging in the absence of specialised morphology is associated with sensory-motor skills and brain size. We will examine these questions in two clades within which extractive foraging has evolved multiple times, birds and mammals, and examine the parallels and differences in the patterns observed within each. This project will use recently developed phylogenetic methods that permit inference of the patterns and processes of evolutionary change, allowing us to address four major questions: (i) Correlated evolution between traits, including behaviour, neuroanatomy and cognition; (ii) Evolutionary sequences, using directional methods, to test causal hypotheses and examine questions such as whether extractive foraging and/or tool using behaviour is equally likely to be lost as gained on phylogenetic branches and whether these behaviours tends to increase in complexity after their initial emergence; (iii) Rates of evolutionary change and their variability in relation to extractive foraging and tool use (e.g. does the emergence of such behaviours increase or decrease rates of change in morphology and/or behaviour); (iv) Relationships between emergence of extractive foraging, population density, invasion of new niches, and speciation