Dietary cognition in educated predators: implications for the evolution of prey defence strategies

Lead Research Organisation: Newcastle University
Department Name: Institute of Neuroscience

Abstract

Many insects defend themselves against predation with toxic chemicals. They often advertise their chemical defences to potential attackers (generally birds attempting to eat them) using conspicuous warning colouration, as seen in ladybirds, wasps and brightly-coloured butterflies. Typically, scientists have assumed that birds learn to associate the warning colouration with the effects of the toxins, and as a result totally avoid individuals with similar colour patterns in the future. However, this assumption has recently been shown to be wrong. Birds actually continue to eat toxic insects at low levels, even when they know that they are defended. They carefully control the number of toxic insects that they eat in order to gain the nutrients contained in the toxic prey, but ensuring they do not eat enough insects to cause them any serious health problems. The proposed experiments aim to investigate what factors influence birds' choices to eat toxic prey. We would expect that birds will eat fewer toxic insects when they can gain the nutrients they need from other sources i.e. when there are more alternative non-toxic prey in the environment, or when non-toxic prey have higher levels of nutrients. We would also expect the presence of other toxic species to influence birds' foraging decisions. However, we do not currently know what predators learn about their prey, or how they decide how 'valuable' toxic prey are as a food source. We will investigate this by giving wild-caught starlings, which are housed in a laboratory, sequences of toxic and non-toxic insects, and measuring which insects they choose to eat. The toxicity of the insects will be manipulated by injecting them with quinine solution (a mild toxin), and their nutrient content can be manipulated by injecting them with a protein solution. The results will allow us to understand what birds learn about the food they eat, how they use this information when deciding what to eat, and how the nutrition of a prey species influences the benefit of it being toxic. We will also produce mathematical simulations that investigate what foraging strategies predators' should use to maximize their nutrient intake whilst keeping their toxin intake as low as possible. These simulations will then be extended to investigate how predators' foraging strategies determine under what circumstances prey will benefit from being toxic, and when such prey will benefit from advertising their toxicity with bright warning colouration. These simulations will also be used to help us to understand how spraying crops with toxic chemicals (to stop birds eating them) influences birds decisions to eat toxic insects like ladybirds and bees. This might also allow us to decide how best to stop these insect species declining in numbers.

Technical Summary

Dating back to Wallace and Darwin, anti-predator strategies have been a fundamental test-case for refining our understanding of evolutionary processes. None more so than for aposematism, where species have conspicuous warning coloration to advertise their toxins to predators. Predator cognition has been crucial to understanding the evolution of aposematism and mimicry (where species share the same warning pattern), and the process of avoidance learning by naïve predators has underpinned theories in this field. Our research takes a necessary and alternative view by considering the role of 'educated' predators in the evolution of defensive strategies. Predators do not just learn to avoid toxic prey, but learn to balance toxin intake with nutritional value - even toxic prey can be nutritionally profitable. Predators are not naive for long, but soon become knowledgeable educated predators. By studying the dietary cognition of educated predators, we will understand how they integrate information about nutrients and toxins in their dietary choices, and the effects that this has on prey defence strategies. We predict that our empirical data will significantly challenge current evolutionary theories, and lead to a re-evaluation of the study of aposematism and mimicry. We will also use computer simulations to predict optimal predator strategies in complex prey environments, and provide the first models to explore the co-evolution between cognitive strategies of predators and the nutrients and defensive strategies in prey. Whilst our main aim is to develop a new theoretical framework for the study of aposematism and mimicry, our empirical work can be extended and applied across a broad spectrum of different research fields, such as neuroscience, experimental psychology, evolutionary ecology and animal nutrition and welfare. Our work may also contribute to developing more effective avian crop repellents, and conservation strategies for declining aposematic species.

Publications

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Skelhorn J (2016) What do predators do? A response to comments on Skelhorn et al. in Behavioral Ecology

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Skelhorn J (2016) Learning about aposematic prey in Behavioral Ecology

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Smith KE (2016) The benefits of being toxic to deter predators depends on prey body size. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

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Rowe C (2013) Why are warning displays multimodal? in Behavioral Ecology and Sociobiology

 
Description Many prey are 'aposematic', meaning that they have conspicuous signals to warn predators that they contain toxins. Our project investigated how birds make decisions to eat aposematic prey when they also need to balance their nutrient and toxin intake. We found:

1) The first empirical evidence for 'toxin mutualism' whereby toxic prey living in the same environment benefit by sharing the same toxin making it hard for predators to ingest large numbers.

2) That the nutrient content as well as the toxin content of aposematic prey affects birds decisions to eat them, which has a significant impact on our understanding of this prey defence strategy.

3) The size and nutrient content of other palatable (non-toxic) prey in the environment affect predation on aposematic prey.

4) Birds living at lower temperatures are more likely to eat prey known to contain toxins.

5) The size of aposematic prey affects how predators reduce their intake of them as they learn to associate their toxicity with their warning signal.

6) Mathematical models based on our birds' decisions indicate surprising physiological mechanisms (e.g. toxin processing may not be energetically costly), and show strong effects on the evolution of aposematism and mimicry (where prey share the same warning signal, but are not necessarily equally toxic).
Exploitation Route See above. Understanding how birds make decisions to eat toxic and distasteful foods can be important for designing more effective avian repellents, particularly for starlings (our study species) that cause significant agricultural damage.
Sectors Environment

 
Description Evolutionary arms races in 3-D'
Amount £100,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2012 
End 09/2016
 
Description Research Grant
Amount £212,000 (GBP)
Funding ID BB/N00602X/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 04/2016 
End 03/2019
 
Description Collaborative BBSRC grant 
Organisation Abertay University
Country United Kingdom 
Sector Academic/University 
PI Contribution Developed collaborative grant with researchers across 3 other universities. Contributing skills in evolutionary biology and behavioural experiments.
Collaborator Contribution Bringing expertise in visual neuroscience and visual perception in humans and other animals.
Impact The grant starts 01/04/2016. The grant is interdisciplinary: visual neuroscience, visual psychophysics and evolutionary biology.
Start Year 2016
 
Description Collaborative BBSRC grant 
Organisation University of Bristol
Department School of Biological Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution Developed collaborative grant with researchers across 3 other universities. Contributing skills in evolutionary biology and behavioural experiments.
Collaborator Contribution Bringing expertise in visual neuroscience and visual perception in humans and other animals.
Impact The grant starts 01/04/2016. The grant is interdisciplinary: visual neuroscience, visual psychophysics and evolutionary biology.
Start Year 2016
 
Description Collaborative BBSRC grant 
Organisation University of St Andrews
Department School of Psychology
Country United Kingdom 
Sector Academic/University 
PI Contribution Developed collaborative grant with researchers across 3 other universities. Contributing skills in evolutionary biology and behavioural experiments.
Collaborator Contribution Bringing expertise in visual neuroscience and visual perception in humans and other animals.
Impact The grant starts 01/04/2016. The grant is interdisciplinary: visual neuroscience, visual psychophysics and evolutionary biology.
Start Year 2016
 
Description Modelling collaborations 
Organisation University of Bristol
Department School of Biological Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution We have provided empirical data and ideas for developing theoretical models.
Collaborator Contribution Bringing novel perspectives and modelling skills.
Impact Two manuscripts have been submitted, and are in revision for resubmission. One more manuscript in prep.
Start Year 2012
 
Description Modelling collaborations 
Organisation University of St Andrews
Department School of Biology
Country United Kingdom 
Sector Academic/University 
PI Contribution We have provided empirical data and ideas for developing theoretical models.
Collaborator Contribution Bringing novel perspectives and modelling skills.
Impact Two manuscripts have been submitted, and are in revision for resubmission. One more manuscript in prep.
Start Year 2012
 
Description 'Educated predators and the evolution of prey defences' 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research or patient groups
Results and Impact Invited talk in NIOO-KNAW, Centre for Terrestrial Ecology, The Netherlands based on BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2009
 
Description Camouflage and mimicry 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach local
Primary Audience Schools
Results and Impact Schools workshop and the British Science Festival, Newcastle

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
Description Decisions, decisions How important are nutrients in predators' decisions to eat aposematic prey? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Invited talk at Jyvaskyla University based on BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
Description Decisions, decisions How important are nutrients in predators' decisions to eat aposematic prey? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited talk at the University of Oslo, based on BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
Description Decisions, decisions How important are nutrients in predators' decisions to eat aposematic prey? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Invited talk based on my BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
Description Decisions, decisions How important are nutrients in predators' decisions to eat aposematic prey? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited talk based on BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
Description Dietary cognition and aposematism: survival of the fattest? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Invited talk on BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description Dietary cognition of educated predators and the evolution of prey defences' 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research or patient groups
Results and Impact Invited talk at Queen Mary University London based on BBSRC-funded work.

no actual impacts realised to date
Year(s) Of Engagement Activity 2009
 
Description Educated predators and the evolution of prey defences 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach local
Primary Audience Postgraduate students
Results and Impact Invited talk at the University of Liverpool

no actual impacts realised to date
Year(s) Of Engagement Activity 2009
URL http://mudshark.brookes.ac.uk/Projects/Rice
 
Description Educated predators and the evolution of prey defences' 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach local
Primary Audience Participants in your research or patient groups
Results and Impact Invited talk at the University of Exeter based on BBSRC-funded work.

no actual impacts realised to date
Year(s) Of Engagement Activity 2009
URL http://frenchtribune.com/teneur/1317029-neonicotinoid-pesticides-damage-brain-honeybees-study
 
Description How important are nutrients in predators' decisions to eat aposematic prey?' 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited talk.

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description How important are nutrients in predators' decisions to eat aposematic prey?' 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited talk based on the BBSRC-funded project.

no actual impacts realised to date
Year(s) Of Engagement Activity 2013
 
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 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 Tasting the differences: how do birds use taste to regulate toxin intake? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited talk at Waltham Pet Centre based on BBSRC-funded work.

no actual impacts realised to date
Year(s) Of Engagement Activity 2009