What makes an effective warning signal?

Lead Research Organisation: University of Abertay Dundee
Department Name: Sch of Social and Health Sciences

Abstract

Many animals exhibit camouflage patterns that help them remain hidden against their background and be less visible to predators. But some animals have vivid, bright colouring that makes them stand out in their environment. Whilst some conspicuous patterns are known to be involved in attracting a mate, others have evolved to warn a predator that the animal is poisonous or unpalatable. These warning patterns are described as being 'aposematic', and are commonly found in insects, for example, monarch butterflies, ladybirds and wasps. Although aposematic patterns look like they might attract predators, in fact they act as a deterrent. Predators are wary towards prey that are warningly coloured, such as being red or yellow, and are quick to learn that warning colours signal danger and avoid aposematically coloured prey. Although warning signals, like camouflage patterns, have fascinated biologists for more than 150 years, there is still no clear understanding of what features make these patterns distinctive and effective against predators, or how they are designed to exploit the ways in which predators see the world. Indeed, definitions of aposematic patterns are loosely descriptive, for example, they are described as 'striking', 'conspicuous' or 'distinctive'. But what is it that sets these patterns apart from others in the natural world: what makes an effective warning signal?

In this project, we propose to tackle this important question through mathematical modeling, and experiments with chicks and humans. For the first time, we will measure the patterns of aposematic and non-aposematic species, and use image processing techniques to quantify the characteristics of aposematic patterns. We will collect photographs of butterflies, moths and beetles from museum collections using techniques that allow us to 'see' the patterns as a foraging bird would. For example, we know what colours and patterns avian visual systems are most sensitive to, and can calculate how warning signals stimulate their visual systems. Once the models have made their predictions we can test them using behavioural experiments that measure how birds react to the aposematic patterns and what features enhance prey survival.

We also plan to test a novel hypothesis for why aposematic patterns act as warning signals. Humans find particular classes of pattern (e.g. stripes or spots of specific sizes and arrangements) aversive or uncomfortable. It has been suggested that these patterns could 'overload' the brain, and make these signals aversive. We will build a computational model of the early stages of visual processing in the brain, and test if aposematic patterns do deliver excessive responses. We will then test the model by choosing patterns that should visually overload humans, and taking classic visual discomfort measures.

The project will allow us to understand the form and function of aposematic patterns, and finally give us a precise and working definition. The work will broad appeal to the general public, and potentially improve the efficacy of visual alerts and avian deterrents.

Technical Summary

Aposematic species use 'distinctive' and 'conspicuous' colour patterns to advertise a defence, such as being toxic or unprofitable. Understanding why such vibrant warning signals have evolved has provided a test bed for evolutionary theory for more than 150 years. It is therefore surprising that we have no analytical understanding of signal design, i.e. what makes natural warning signals 'conspicuous' or 'distinct'. In this project we take a novel approach to characterise real aposematic patterns, model their effects on the perceptual systems of predators, and test what makes them 'special' via behavioural experiments.
We will develop a database of hyperspectral images of aposematic (AP) and non-aposematic (Non-AP) species. This will allow us to compare the patterns of AP and Non-AP species in a principled way to identify key features of AP patterns. By mathematically analysing the database, we will deliver a set of specific visual features (colour and spatial pattern) that will define a pattern as being AP. We will test which of these features contribute to the efficacy of warning signals using avian predators (via unlearned wariness and avoidance learning paradigms). We will also predict and test the distance at which aposematic patterns become effective against predators.
Recent developments in neuroscience suggest there may be more to AP patterns than being distinctive. Warning patterns may be effective because they are highly unusual in natural scenes, stimulating high levels of neural activity. We will test this 'visual overload hypothesis', using modeling and experiments, and establish if AP patterns trigger stronger brain activity than other conspicuous patterns.
We will disseminate the work across relevant academic disciplines, to the public via school visits, science festivals and museum exhibits, and to stakeholders involved in development of high-visibility clothing and deterrents for birds.

Planned Impact

Our proposal is for core evolutionary and computational biology research with no immediate application to UK-plc. However, we have identified three groups of possible indirect stakeholders, and two groups of direct stakeholders.
(1) Technical developers of high-visibility systems
Our work could be of use to those interested in increasing the visibility of workers and sportsmen through high-visibility clothing. We have obtained interest in the idea from two companies specialising in high-performance sports-wear, Tineli and Raceskin. We will discuss our project findings with them to explore how to improve the design of highly visible sports clothing.
(2) Medical professionals and technologists
Our work will be of relevance to medical professionals interested in visual discomfort and in photo-sensitive epilepsy and allow the prediction of uncomfortable images. Harris has collaborative links with the Department of Optometry at Bradford University (Barratt, Bloj). She will arrange a talk to optometry professionals there on the implications of our work for understanding the symptoms of visual stress and discomfort.
(3) Developers of avian deterrents
Birds can cause significant damage to infrastructure and crops. Our data could lead to significant improvements in the design of avian deterrents, for example, on farmland, at airports and on powerlines. We have established contacts in industry and in wildlife control that we will exploit to explore the development and testing of novel deterrents.
(4) The general public
Our research topic is highly engaging for the general public, who have a passion for wildlife, particularly insects and birds. We will engage the public through school visits and the development of a linked classroom activity, events at local zoos and museums, natural history societies, public displays at Science Fairs, and interactive web-based demonstrations our laboratory websites.
(5) Project researchers
The proposal is an interdisciplinary collaboration. Penacchio has a background in pure maths, but is on his way to becoming an interdisciplinary computational biologist. This project will add another string to his biology bow. Halpin is an expert in animal behaviour and cognition, particularly in how predators learn about what to eat. This project will enable her to better understand the sensory and neural processes underlying signal processing, and allow her to develop new skills in image acquisition and analysis. Both researchers will benefit from the development of new skills and knowledge that transcend traditional disciplinary boundaries.

Publications

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Rowe C (2017) Avian Cognition

 
Description Our new study in virtual reality has shown that visual patterns associated with some forms of visual discomfort in a subset of individuals are avoided in a VR navigation task by ALL participants. This is finding that is unreported elsewhere.
Exploitation Route The patterning that cause wariness in our participants could be adopted in the creation of safety wear and warning signals.
They also inform decisions about patterns that might cause discomfort to those suffering visual migraine.
Sectors Aerospace, Defence and Marine,Leisure Activities, including Sports, Recreation and Tourism,Retail

 
Description Applied Vision Association postdoc travel award (Penacchio)
Amount £700 (GBP)
Organisation Applied Vision Association 
Sector Private
Country United Kingdom
Start 06/2016 
End 06/2016
 
Description Newcastle University Research Excellence Fund
Amount £75,000 (GBP)
Organisation Newcastle University 
Sector Academic/University
Country United Kingdom
Start 10/2016 
End 09/2019
 
Title Extended the ScamperVR software to include scans of butterflies taken at the Natural History Museum 
Description Following a setback in 2018 where our VR equipment was stolen* during building works, the equipment was replaced by the University (Abertay). We have now developed a new experimental paradigm exploring the detection and recognition of aposematic and non-aposematic butterflies in a VR environment. This study is currently underway. * This resulted in the shelving of the current studies, exploring movement relative to aposematic and non-aposematic patterns, the calibration/characterisation of the particular VR system was lost with the equipment. The development of the new study, featuring scanned butterflies, captures the key elements of the original studies while taking advantage of the new data arriving from project partners in St Andrews and Newcastle. 
Type Of Material Improvements to research infrastructure 
Year Produced 2019 
Provided To Others? No  
Impact This is too early to determine. 
 
Description Modelling collaboration with Xavier Otazu 
Organisation Autonomous University of Barcelona (UAB)
Department Department of Computer Science
Country Spain 
Sector Academic/University 
PI Contribution Collaboration with Xavier Otazu and his group from Autonomous University, Barcelona, on computational modelling. He is working with us on ideas that emerged from our grants on camouflage and aposematism. We have hosted him and his group for sabbatical trips to work with us in St. Andrews.
Collaborator Contribution We have been exposed to, and training in, neural computational modelling methods and given a 'modellers perspective' understanding of the kinds of biological and psychological information needed to develop a successful computational model.
Impact Multi-disciplinary: biology, psychology, computer science, neuroscience.
Start Year 2016
 
Description Pennacchio collaboration with Sonke Johnsen 
Organisation Duke University
Country United States 
Sector Academic/University 
PI Contribution Olivier Pennacchio is using work from projects on camouflage and animal warning signals and developing a collaboration on under-water camouflage with Sonke Johnsen.
Collaborator Contribution Sonic Johnsen is an expert on under-water camouflage and interested in our theoretical work.
Impact non yet.
Start Year 2016
 
Description ViiHM network: Visual image interpretation in humans and machines 
Organisation University of Birmingham
Department School of Psychology Birmingham
Country United Kingdom 
Sector Academic/University 
PI Contribution EPSRC funded network, I am a member.
Collaborator Contribution A network funded by EPSRC -- Schofield at Birmingham is the PI
Impact None yet
Start Year 2014
 
Title SCAMPERvr (Search ColourAtion Movement PattERn Virtual Reality) 
Description With industrial partners we have developed new software to present virtual scenes containing patterned objects. This software will be used to explore behaviour in search and detection tasks as we manipulate warning colouration. 
Type Of Technology Software 
Year Produced 2017 
Open Source License? Yes  
Impact We are still in the trial stage, experiments will be undertaking shortly. 
 
Description Explorathon 2017: Harris lab exhibit at this European Researchers night event, highlighting research activity on vision. 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Explorathon 2017: Harris lab exhibit 'Vision: more than meets the eye' at this European Researchers night event, highlighting research activity on vision.
Year(s) Of Engagement Activity 2017
URL http://www.explorathon.co.uk/standrews
 
Description Explorathon 2016: Harris lab exhibit at this European Researchers night event, highlighting research activity on vision. 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Part of a European Researchers Night event, showing academic research taking place at the University of St. Andrews
Year(s) Of Engagement Activity 2016
 
Description Harris talk at Cafe Scientifique, Dunkeld and Pitlochry , Scotland 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Harris talk at Cafe Scientifique, Dunkeld and Pitlochry , Scotland. Talk was primarily on basic 3D vision, but included discussion of how camouflage and animal patterning affects predation.
Year(s) Of Engagement Activity 2016
 
Description Harris talk at Perceptual Representation of Illumination, Shape & Material Conference 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact Invited talk to EU postgraduate training network and industrial collaborators. Title: Counter-shading camouflage: shape from shading in nature.
Year(s) Of Engagement Activity 2016
 
Description International Women's Day - Women in Science 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact The invited talk was to undergraduates and postgraduates at Newcastle University, with the aim of supporting women in their scientific career aspirations. I spoke about my career in science (including my BBSRC-funded research), the challenges associated with being a parent, and what I advice I would give my younger self.
Year(s) Of Engagement Activity 2017
 
Description Invited talk at a science education conference. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Invited Talk at the Association for Science Education Conference (Dundee, 2017)>

https://www.ase.org.uk/conferences/scotland2017/
Year(s) Of Engagement Activity 2017
URL https://www.ase.org.uk/conferences/scotland2017/
 
Description Keynote lecture at conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited keynote lecture, Chinese Ornithological Congress, Xian, China, 22-25 September, 2015. "What camouflage tells us about avian perception and cognition"
Year(s) Of Engagement Activity 2017
 
Description Public Engagement talk: Holmes Lecture 2018 on Animal vision and prey defences 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Over 150 school children aged 10-14 (and their guardians) attended the annual Holmes Lectures on animal vision, which is an annual event in the university's public lecture series. The lecture was highly interactive, and we received excellent feedback from the audience about how engaging and informative the lecture was.
Year(s) Of Engagement Activity 2018
 
Description Public engagement activity - Festival of Nature 2017 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact "Nature expert" at event at the 2017 Festival of Nature, a 2-day free public event organised by the the Bristol Natural History Consortium (http://www.bnhc.org.uk/festival-of-nature/). I took part in "Nature Roulette" talking about animal coloration.
Year(s) Of Engagement Activity 2017
URL http://www.bnhc.org.uk/nature-roulette-will-meet/
 
Description Symposium organiser, "Bird behaviour in a changing world", at the Zoological Society of London 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Symposium co-organiser (with Hannah Rowland, Max Planck Institute, Jena, Germany, and Tom Pike, Lincoln University, UK): "Bird behaviour in a changing world: with a special focus on bird senses", 14-15 September 2017. Funded by the Zoological Society of London and the Association for the Study of Animal Behaviour. Participants from the across Europe, the USA and Australia attended.
Year(s) Of Engagement Activity 2017
URL https://www.zsl.org/science/whats-on/bird-behaviour-in-a-changing-world-with-a-special-focus-on-bird...
 
Description Talk at Behaviour 2017 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented (peer reviewed) talk "Distance-dependent colouration in the poison frog Dendrobates tinctorius". The Behaviour 2017 conference was a joint meeting of the 35th International Ethological Conference (IEC) and the 2017 Summer Meeting of the Association for the Study of Animal Behaviour (ASAB), that brought together researchers and students from all fields of behaviour science.
Year(s) Of Engagement Activity 2017
URL http://behaviour2017.org/welcome/
 
Description Talk at local school 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk to GCSE and lower 6th form students on animal camouflage, followed by presentation and discussion on careers in biology.
Year(s) Of Engagement Activity 2017
 
Description Talk at local school 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk to GCSE and lower 6th form students on animal defensive coloration, followed by presentation and discussion on careers in biology.
Year(s) Of Engagement Activity 2018
 
Description Talk at local school 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk to GCSE and lower 6th form students on animal camouflage, followed by presentation and discussion on careers in biology.
Year(s) Of Engagement Activity 2017
 
Description Talk on animal defensive coloration at the University of Groningen, The Netherlands 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited research talk to graduate students, undergraduates and postdocs at the School of Life Sciences, University of Groningen, The Netherlands
Year(s) Of Engagement Activity 2018
 
Description Visual Perception in Humans and Animal Camouflage, Explorathon 18 exhibit 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Visual Perception in Humans and Animal Camouflage, Interactive presentation at science fair, Explorathon 2018, held at Dundee Science Centre (science museum).
Year(s) Of Engagement Activity 2018