This electronic thesis or dissertation has been downloaded from Explore Bristol Research, http://research-information.bristol.ac.uk Author: Wainwright, Benito Title: Overcoming the predation costs of bilaterally symmetrical colouration General rights Access to the thesis is subject to the Creative Commons Attribution - NonCommercial-No Derivatives 4.0 International Public License. A copy of this may be found at https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode This license sets out your rights and the restrictions that apply to your access to the thesis so it is important you read this before proceeding. Take down policy Some pages of this thesis may have been removed for copyright restrictions prior to having it been deposited in Explore Bristol Research. However, if you have discovered material within the thesis that you consider to be unlawful e.g. breaches of copyright (either yours or that of a third party) or any other law, including but not limited to those relating to patent, trademark, confidentiality, data protection, obscenity, defamation, libel, then please contact [email protected] and include the following information in your message: •Your contact details •Bibliographic details for the item, including a URL •An outline nature of the complaint Your claim will be investigated and, where appropriate, the item in question will be removed from public view as soon as possible. Overcoming the predation costs of bilaterally symmetrical colouration MSc project by Benito Wainwright A dissertation submitted to the University of Bristol in accordance with the requirements for award of the degree of MSc Biology in the Faculty of Biological Sciences. Word Count: 16,916 1 Abstract For camouflaged prey animals which benefit from remaining undetected by predators, increased conspicuousness due to bilaterally symmetrical colouration is costly. The ubiquity of symmetrical body patterns in nature is assumed to be due to tight genetic and developmental constraints. Given these evolutionary restrictions, we investigated how animals might have evolved to optimise their surface colouration in order to reduce the predation cost of bilaterally symmetrical colouration. One way of doing this is by placing discrete, high contrast markings away from the axis of symmetry (or midline). Artificial camouflaged prey with symmetry placed at different distances from the axis were used in both laboratory visual search tasks with humans and field survival experiments with wild avian predators. By measuring response time (Experiment 1) and predation rate (Experiment 2), I showed that for targets that were symmetrical only near their midline, detectability was the same as for targets that were symmetrical all over their surface. Prey were significantly less conspicuous when symmetry was placed outside of this ‘critical zone’. To see whether living animals have evolved as predicted from the trends suggested by these experiments, the saliency of features at different distances from the midline of the cryptically coloured forewings from 36 Lepidopteran species was measured. Measures of both absolute salience and relative to wing area demonstrated that salience is indeed greatest away from the ‘critical zone’ near the axis of symmetry. My results suggest similarities in the mechanisms of bilateral symmetry detection by mammalian and avian predators. They also suggest that evolution has resulted in pattern elements being positioned in such a way that the detectability cost imposed by symmetry is reduced. Keywords: bilateral symmetry; camouflage; Lepidoptera; predation; salience; visual search 2 Acknowledgements I would like to give an enormous thanks to my primary supervisor, Professor Innes Cuthill, for his incredible expertise and support throughout all aspects of this MSc, and to my secondary supervisor, Professor Nick Scott-Samuel, for his help and advice, especially regarding experimental design. Thank you also to Kelly-Louise Ray and Leah Costello for their assistance in the field, Rhian Rowson for enabling access to Bristol Museum and Art Gallery’s Lepidoptera collection, and to my parents and close friends for their moral support. 3 Author’s Declaration I declare that the work in this dissertation was carried out in accordance with the requirements of the University's Regulations and Code of Practice for Research Degree Programmes and that it has not been submitted for any other academic award. Except where indicated by specific reference in the text, the work is the candidate's own work. Work done in collaboration with, or with the assistance of, others, is indicated as such. Any views expressed in the dissertation are those of the author. SIGNED: ............................................................. DATE:.......................... 4 Contents 1 Literature Review Page 1.1 Background……………………………………………………………………….……………………………………………8 1.2 An introduction to symmetry in appearance 1.2.1 Early ideas on symmetry and camouflage…………………………………………………………………………9 1.2.2 Symmetry perception in non-human animals…………………………………..……………………..………10 1.3 The cost of symmetrical colouration………………………………………………….………………………11 1.4 Symmetry perception in human experimental psychology 1.4.1 Random-dot studies…………………………………………………………………………………………………..……12 1.4.2 Studies with biologically relevant stimuli……………………………………………………………..…………13 1.5 Artificial neural networks and emergent properties of sensory systems………….……14 1.6 Asymmetrical exceptions in vertebrates…………………..……………………………….………………14 1.7 Symmetry and camouflage in cephalopods…………………………………….…………………………16 1.8 Opposing ideas…………………………………………….……………………………………………...………………18 1.9 Fluctuating asymmetries and sexual selection………………………………….………………………19 1.10 Aposematism and symmetry………………………………..………………………….…………………………21 1.11 Genetic and developmental constraints in arthropods………………………………….…………22 1.12 A review of methodologies 1.12.1 Molecular approaches……………………………………………………………………….……………………………23 5 1.12.2 Laboratory and field artificial target studies……………………………………………………………………23 1.12.3 Image analysis…………………………………………………………..……………………………………………………24 1.13 Concluding observations…………………………………………………………………………..…………………25 2 The significance of the symmetry midline in animal camouflage 2.1 Introduction…………………………………….…………………………………..………………………………………27 2.2 Methods 2.2.1 Experiment 1: human visual search 2.2.1.1 Creation of the stimuli…………………………………………………………………………………….………29 2.2.1.2 Running the trials……………………………………………………………………………………………………30 2.2.1.3 Analyses…………………………………………………………………………………………………………….……31 2.2.2 Experiment 2: avian predation in the field 2.2.2.1 Procedure…………………………………………………………………………………………………………….…32 2.2.2.2 Analyses………………………………………………………………………………………………….………………32 2.2.3 Natural pattern analysis 2.2.3.1 Photographing, image editing and categorisation of specimens………………..……………33 2.2.3.2 Image analyses……………………………………………………………………………………………….………36 2.2.3.3 Statistical analysis………………………………………………………………………………………………..…38 2.3 Results 2.3.1 Experiment 1……………………………………………………………………………………………..……………………38 2.3.2 Experiment 2……………………………………………………………………………………..……………………………39 2.3.3 Natural pattern analysis…………………………………………………………..…………………………………….41 2.4 Discussion 2.4.1 Presence of a critical zone…………………………………………………………………………….…………………43 2.4.2 The significance of body pattern properties……………………………….……………………………………44 2.4.3 Visual mechanisms………………………………………………………………………………………………………….45 2.4.4 Comparisons between Experiments 1 and 2………………………………………………………………….…46 2.4.5 Body orientation……………………………………………………………………………………………….……………47 6 2.4.6 Constraints due to wing area…………………………………………………………………………….……………48 2.4.7 Alternative explanations for enhanced salience away from the midline………………….………49 2.4.8 The significance of phylogeny…………………………………………………………………………………...……49 2.4.9 Conclusions and future work…………………………………………………………………………………..………50 References……………………………………………………………………………….……………………………….……………52 List of Figures Figure 1.1 Stimuli previously used by Cuthill et al. (2006) and Merilaita & Lind (2006)………11 Figure 1.2 “Six-slice experiment” target design used by Barlow Reeves (1979)….…...…………13 Figure 1.3 Camouflaged cephalopod displaying bilateral symmetry from Langridge (2006).19 Figure 1.4 Partial regression plots from Badyaev et al. (2001)…………………………….….…………20 Figure 1.5 Images of moth species used by Forsman & Merilaita (2003)……………………………24 Figure 2.1 Artificial targets used in Experiments 1 and 2……………………….…………………….……30 Figure 2.2 Targeting accuracy of human participants in Experiment 1……………….………………31 Figure 2.3 Images of the species from the museum used in the Natural Pattern Analysis…..35 Figure 2.4 Images of the species from the field guide used in the Natural Pattern Analysis.36 Figure 2.5 Output from the wing salience computer program……………………………………..……37 Figure 2.6 Representation of how saliency measures correlate across images………………..…38 Figure 2.7 Experiment 1 Results………………………………….……………………….……………….…………39 Figure 2.8 Experiment 2 Results……………………………………………………………………………….………41 Figure 2.9 Saliency boxplots from the Natural Pattern Analysis…………….....................………42 Figure 2.10 Boxplots denoting differences in absolute salience between inner and middle treatments.…………………………………………………………………………………………………………………….42 Figure 2.11 Boxplots denoting differences in relative salience between inner and middle treatments……………………………………………………………………………………………….…………………….42 Figure 2.12 Differences between inner and middle salience treatments across species…….43 7 List of Tables Table