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 matrix1-3. It is assumed to enhance the efficiency with which animals can exploit resources3-5, 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-ayes6 and tool-use displayed by taxa such as great apes3 and New Caledonian crows7. 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. Complex patterns of extractive foraging behaviour are thought to be cognitively demanding and require extended development to facilitate learning1,10,11, 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 seasonality10,12. We will test the “Extractive foraging hypothesis”1, which suggests that extractive foraging in the absence of specialised morphology is associated with sensory-motor skills and brain size & structure. 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.


Data collection: We will develop a new comparative database on extractive foraging and associated morphological, behavioural and ecological variables. This will be compiled primary literature and existing secondary compilations. We will conduct electronic searches of the primary behavioural ecology literature using the keywords “extractive foraging”, “tool use”. Definitions of different types and complexity levels of extractive foraging will be developed and applied to the literature cases. Phylogenies: Consensus phylogenetic trees for birds and mammals will be obtained from the literature. We will also incorporate phylogenetic uncertainty into analyses (see Analysis). Analysis: Phylogenetic comparative methods now provide a powerful framework for examining evolutionary patterns and processes. We will employ Bayesian implementations of phylogenetic generalised linear models, including control for phylogenetic uncertainty. We will apply the variable rates model for studying individual phenotypic traits and its modification for examining the evolution of traits relative to others, the variable-rates regression model13. These methods permit analysis of correlated evolution among traits along branches of a phylogenetic tree. It is also possible to examine variation in rates of evolutionary change: the background rate of change and individual branch-specific scalars are simultaneously estimated within a Bayesian Markov chain Monte Carlo (MCMC) reversible-jump framework13-15. These methods permit identification of bursts of evolutionary change in a trait of interest, and in one trait relative to others. We will examine temporal sequences of changes in one categorical trait relative to another using Pagel’s discrete method16. Barton’s collaborator at Reading University, Chris Venditti, is a leading exponent in phylogenetic comparative methods and will provide additional input and advice.

Project Timeline

Year 1

Months 1-9: Initial PhD training, literature review, training in data searching/collection & phylogenetic comparative methods (including attendance at advanced phylogenetic methods workshop) and first visit to Venditti, Reading University), hypothesis development, scoping of data collection and sources,
Months 10-12: Data searching/database building (i) Mammals

Year 2

Months 13-17: Data searching/database building (ii) Birds
Months 18-23: Data analysis and outline/draft chapters (mammals), second visit to Venditti at Reading University

Year 3

Months 24-29: Data analysis and outline/draft chapters (birds), 3rd visit to Venditti at Reading University
Months 30-35: Finalise data analyses, Presentations at national and international

Year 3.5

Months 36-42: Finalise writing and completion of thesis.

& Skills

This project offers a dedicated student the opportunity to develop their interests in animal behavior, ecology, evolution and phylogenetic comparative methods. The project will provide training and experience in the collection of comparative data from primary and secondary sources, data management and database use, statistical analysis using phylogenetic comparative methods and producing scientific outputs. The training will include both frequentist and Bayesian methods, with the emphasis on the latter. In addition to expert input from the supervisors, this training will be supported by attendance at a workshop on phylogenetic comparative methods during the first year of the PhD. The student will also develop generic skills in project management, information management, time management and written and oral communication. The supervisors have complementary expertise. Barton and Street are experienced in use of phylogenetic comparative methods which they have applied to broad questions concerning the evolution of brain, behavior, life histories and ecological traits. Barton has published on the relationship between extractive foraging and brain evolution10. Rutz is a leading expert on tool use and avian cognition and behavioural evolution, and also has experience with phylogenetic methods. Tan is a new appointment at Durham, with a research focus on extractive foraging and tool use in primates. Barton (H index=47) & Rutz (H index =26), the two senior supervisors, have an excellent track record of publishing in high-impact journals, including Nature, PNAS, Proc Roy Soc B, while Street and Tan have highly promising trajectories in terms of high-quality papers (e.g. Street – PNAS, Biology Letters, Ecology Letters, Tan – Nature Ecol Evol, Anim Cog The student will be primarily located at Durham, where opportunities to develop communication and presentation skills are provided within the Evolutionary Anthropology Research Group, of which the student will become a member. There are also opportunities to engage in wide-ranging discussions and learn from peers and more senior researchers within Durham’s Centre for Behaviour, Evolution and Ecology Research, which spans several cognate departments, and includes Dr Jonathan Drury, who sues phylogenetic comparative methods and simulation modelling to study animal diversity. Supervision visits to St Andrews will offer the opportunity to interact with researchers in the Centre for Biological Diversity. Additionally, two visits will be made to Reading University to discuss methodology and receive further training under the guidance of Dr Chris Venditti.

References & further reading

1. Parker ST (2015) New Ideas Psychol 37 1e12. 2. Pal et al (2018). Primates. 59(2):173-183. 3. Seed A & Byrne RW (2010) Curr. Biol. 20 (23), R1032-R1039. 4. Biro, D. (ed.), Haslam, M. (ed.) & Rutz, C. (ed.) 2013 Phil Trans Roy Soc B, 368, 1630. 5. St Clair et al (2018) Nature Ecol Evol 10.1038/s41559-017-0429-7. 6. Erickson CJ (1991) Anim Behav 41 793-80. 7. Rutz, C. & St Clair, J. J. H. (2012) Behav Proc. 89, 2, p. 153-165 13. 8. Barton RA (2004) PNAS 101(27): 10113-10115. 9. Troscianko J et al (2012) Nature Comm. 3, 1110. 10. Barton RA (2012) Phil Trans Roy Soc B 367, 2097-2107 11. Tan (2017) J Comp Psychol. 2017 May;131(2):89-114 12. Melin et al (2014) J Hum Evol71 (2014) 77e86. 13. Venditti et al. (2011) Nature 479, 393. 14. Baker et al. (2015) Biol J Linn Soc 118, 96. 15. Pagel, M. and Meade, A. 2008. Phil. Trans Roy Soc. B, 363,3955-3964. 16. Pagel M. (1994) Proc Roy Soc B 255, 37-45

Further Information

Given the highly competitive nature of these studentships it is recommended that candidates get in touch informally, sending a copy of their CV, to discuss a potential application. Please contact Prof Rob Barton for further information: r.a.barton@durham.ac.uk.

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