Hunger and knowledge: foraging decisions in an uncertain and social world

Lead Research Organisation: University of Bristol
Department Name: Biological Sciences

Abstract

Even within seemingly homogeneous habitats there is a great deal of small-scale heterogeneity over time and space. Thus, as animals explore their environment, there is variation between individuals in encountering food, resulting in population-level individual differences in hunger and knowledge. This variation is often further magnified by intrinsic consistent differences in behaviour between individuals (frequently referred to as animal 'personality'), which can be driven by differences in genetics and development that are stable in adulthood. How individuals manage the balance between feeding and avoiding predation risk when they have limited information is a long-running question in understanding animal behaviour. The story becomes much more complicated when we consider that many animals, especially those that are prey to others, live in groups. Living together has benefits in avoiding predators and locating resources, in part because animals can share information and socially learn from one another; on the other hand, coordinating when and where to do particular behaviours becomes a new problem. When and how information is gained and socially transmitted, and how hunger affects decisions and social behaviour, have been studied extensively but separately from one another. In this project, for the first time we will bring these elements together to understand how hunger and information interact when animals make foraging decisions both individually and collectively.

Our study will utilise the recent explosion of interest in decision making by animal groups across taxa and advances in state-of-the-art animal tracking computer vision software. We will address a range of unanswered questions regarding hunger and information in decision making: What are the relative contributions of, and interactions between, hunger and risk taking tendency in the acquisition of information? How do interactions between individuals within groups influence these processes and what is the consequence for how knowledge and food are distributed between individuals? What is the effect of mixing informed and naïve, and hungry and sated, individuals in a group, e.g. do naïve individuals follow and learn better from satiated rather than hungry informed individuals that are likely to leave them behind? Can leadership emerge from differences in hunger that are driven by social interactions? Can more effective foraging in groups be best explained by sharing of information or simply by the extra motivation of having a partner? The project has the potential to greatly increase our understanding of decision making and the factors important in individual variation in social animals.

The experimental work will use small freshwater fish as a model system. Compared to studying more complex animals such as birds or primates, there are a number of advantages to studying fish. Information and hunger can be easily controlled, and the species to be used (three-spined sticklebacks and guppies) have 'fission-fusion' social systems where individuals change group membership often, allowing us to easily manipulate group composition. As decisions and information exchange are evident in changes in speed and direction in most fish species, state-of-the-art computer vision software that tracks each individual's position over time will be used to quantify individual decisions objectively. Moreover, fish show many of the cognitive abilities found in 'smarter' vertebrates, suggesting that our results may be applicable to other animals, even humans. In parallel with the behavioural experiments, we will create new models of animal groups that consider how decision-making occurs when individuals are able to learn about their environment. Developing the models alongside the experimental work will maximise our ability to fully understand the complex interactions expected in the real animals.

Planned Impact

Our proposed project will be the first to integrate inter-individual variation due to hunger, information and consistent individual differences into decision making in a social context. To minimise risk and costs, we will use two widely studied fish species as model systems. Thus, our project is fundamental, pure research that is designed to be widely applicable rather than focused on an applied problem in a particular animal. The immediate non-academic beneficiaries will be the public, who can easily relate to the topics tackled in the project. Additionally, in the longer term, we believe the experimental findings will be of interest to those working in applied research, namely aquaculture and fish stock management.

The general public will benefit through a greater understanding of complex systems. Our proposed topic is instantly recognisable to most people since they can relate directly to it: animals live in societies which benefit them in various ways, but individuals have competing interests, different personalities, different information, and thus desire different things at different times. Understanding that this results in a complex set of interactions which are more difficult to study than simple linear chains of causation is a challenge for the public understanding of science. This is fundamentally important in an increasingly interconnected global world that is, itself, a complex system. Using a simpler system (fish under laboratory conditions) helps to educate the public in how science works as understanding complexity can be facilitated by establishing general principles in systems where important variables can be controlled, manipulated and easily observed, which would be ethically and practically impossible in humans. Fish also have appeal to the public, for example through recreational fishing and keeping fish at home, demonstrated by frequent media coverage of their 'surprising' advanced cognitive abilities.

The majority of fish species live in groups for at least part of their life cycle, so fish biologists working in applied research are likely to benefit from the proposed work. As informational and hunger states will affect exploitation of resources and long-term fish health, our findings will have implications for fish population dynamics and ecology. Current models of fish population dynamics in fish stock management assume a lack of inter-individual variability in information, hunger and risk taking tendency, all of which are known (separately) to be important for survival and reproduction of fish. Our work will highlight the interactions between these sources of individual variation and group dynamics, facilitating the future development of more accurate models of fish movement and population change. We plan to use the findings of our laboratory experiments to bridge the gap to direct application by investigating these trends further in field experiments in collaboration with fish ecologists (Dr. Martin Genner at the University of Bristol).

Our results have potential application in aquaculture (and farming of other animals) where inter-individual variation in growth rates produces additional costs, and considerable effort is invested to minimise this variation. All major sources of farmed animal protein come from social species as this allows high stocking densities, making our social focus particularly suitable. For example, our results may suggest that individual fish that consistently have a greater motivation to feed are more likely to first respond to new feeding methods and learn associated cues. With greater access to food, the resulting correlation between knowledge and motivation may create different growth rates for risk prone, knowledgeable individuals versus other fish that rely on following others. Thus, our study may suggest that new feeding methods should be easy to learn, not just to ensure fast learning rates, but also to minimise inter-individual variation in growth.

Publications

10 25 50
 
Description We have demonstrated that deciding where to forage depends on how healthy an individual is - if they are healthy they go where the best food is, if they are unhealthy, their movement is determined more by how parasite risk varies in their environment (they avoid areas with more ticks).
We have also shown that decisions in animals adapted to high predation risk environments are more egalitarian in their decision making. We have also shown how decisions are affected by water turbidity, which is increasing globally from anthropogenic activity.
Our key findings also related to consistent behavioural differences between individuals, and between groups. In groups, we have shown that collective movement is consistently different between groups, and moreover that the rate that this behaviour changes over time differs between groups too. For individuals, we have also explored the effect of foraging, and demonstrated that the effect of foraging adds additional variation that can hide personality differences.
Exploitation Route They could be developed in livestock farming, including aquaculture.
Sectors Agriculture, Food and Drink,Environment

 
Title Data and code for: Collective motion diminishes, but variation between groups emerges, through time in fish shoals 
Description Despite extensive interest in the dynamic interactions between individuals that drive collective motion in animal groups, the dynamics of collective motion over longer time frames are understudied. Using three-spined sticklebacks, Gasterosteus aculeatus, randomly assigned to twelve shoals of eight fish, we tested how six key traits of collective motion changed over shorter (within trials) and longer (between days) timescales under controlled laboratory conditions. Over both timescales, groups became less social with reduced cohesion, polarisation, group speed and information transfer. There was consistent inter-group variation (i.e. collective personality variation) for all collective motion parameters, but groups also differed in how their collective motion changed over days in their cohesion, polarisation, group speed and information transfer. This magnified differences between groups, suggesting that over time the 'typical' collective motion cannot be easily characterised. Future studies are needed to understand whether such between-group differences in changes over time are adaptive and represent improvements in group performance or are suboptimal but represent a compromise between individuals in their preferences for the characteristics of collective behaviour. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.547d7wm8p
 
Title Netlogo code supporting 'Personality variation is eroded by simple social behaviours in collective foragers' 
Description This Netlogo code supports a preprint 'Personality variation is eroded by simple social behaviours in collective foragers', which will be made available in March 2022 
Type Of Material Computer model/algorithm 
Year Produced 2022 
Provided To Others? Yes  
Impact This model supports an upcoming preprint concerning the erosion of personality in social groups. 
URL https://doi.org/10.6084/m9.figshare.19391651.v1
 
Title Time series of trajectory data for individual three-spined sticklebacks (Gasterosteus aculeatus) swimming in groups of eight individuals 
Description The resource consists of cartesian coordinates, expressed in units of pixels for groups of eight individual fish, swimming in a shoal. The fish were filmed from above with a high resolution video camera. The data were generated from the images and video using automated two-dimensional tracking software. A food stimulus delivering a single food reward was presented six times per trial. The data were collected between July and August 2017 in a controlled fish laboratory at the University of Bristol by the data authors. The data were collected to test the effects of group behaviour in fish shoals on foraging performance. There are instances where one or more fish in a frame could not be tracked. Where such instances occur are indicated in the data files. The research was funded through NERC grant NE/P012639/1 Hunger and knowledge: foraging decisions in an uncertain and social world All procedures regarding the use of animals in research followed United Kingdom guidelines and were approved by the University of Bristol Ethical Review Group (UIN UB/17/060). 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://catalogue.ceh.ac.uk/id/08305a43-79b5-432f-ad20-2ddffe0d1077
 
Title Time series of trajectory data for individual three-spined sticklebacks (Gasterosteus aculeatus) swimming individually and in groups of six individuals 
Description The resource consists of cartesian coordinates, expressed in units of pixels, for fish swimming individually, in groups of six individuals, and in groups of six individuals while presented repeatedly with a food stimulus delivering two food items until satiation. The fish were filmed from above with a high resolution video camera. The data were generated from the images and video using automated two-dimensional tracking software. The data were collected between September 2019 and March 2020 in a controlled fish laboratory at the University of Bristol by the data authors. The data were collected to test how individual temperament and the acquisition of knowledge and satiation interact when animals make foraging decisions in groups. There are instances where one or more fish in a frame could not be tracked. Where such instances occur are indicated in the data files. The research was funded through NERC grant NE/P012639/1 Hunger and knowledge: foraging decisions in an uncertain and social world. All procedures regarding the use of animals in research followed United Kingdom guidelines and were approved by the University of Bristol Ethical Review Group (UIN UB/17/060). 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://catalogue.ceh.ac.uk/id/26f045c3-946b-4115-baf1-defb19bdba42
 
Description Collaboration with Kate Laskowski, UC Davis, USA 
Organisation University of California, Davis
Country United States 
Sector Academic/University 
PI Contribution Ideas and leading on first drafts for review/opinion articles, and a Royal Society meeting and special issue of Phil Trans on "Collective animal behaviour through time".
Collaborator Contribution Knowledge on the development of behaviour and statistical analysis on quantifying inter-individual variation.
Impact Gartland L.A., Firth J.A., Laskowski K.L., Jeanson R., Ioannou C.C. (2021). Sociability as a personality trait in animals: methods, causes and consequences. Biological Reviews, 10.1111/brv.12823
Start Year 2018
 
Title Netlogo code supporting 'Personality variation is eroded by simple social behaviours in collective foragers' 
Description This Netlogo code runs in Netlogo 6.2 (available at https://ccl.northwestern.edu/netlogo/download.shtml), and is provided in support of a manuscript entitled 'Personality variation is eroded by simple social behaviours in collective foragers'. Software is made available for use entirely at the risk of the user, and the authors do not accept any responsibility for any damages or data loss caused by using the software. Note that this is the CORRECTED version of the code should be used - this should run identically to an original version of the submission (see figshare versioning), but has some additional code removed for some risk functions that was not explored in the accompanying manuscript by Rands & Ioannou (preprint at https://doi.org/10.1101/2022.03.21.485155) 
Type Of Technology Software 
Year Produced 2022 
Open Source License? Yes  
URL https://figshare.com/articles/software/Netlogo_code_supporting_Personality_variation_is_eroded_by_si...
 
Description This Netlogo code runs in Netlogo 6.2 (available at https://ccl.northwestern.edu/netlogo/download.shtml), and is provided in support of a manuscript entitled 'Personality variation is eroded by simple social behaviours in collective foragers'. Software is made available for use entirely at the risk of the user, and the authors do not accept any responsibility for any damages or data loss caused by using the software. 
Type Of Technology Software 
Year Produced 2022 
Open Source License? Yes  
URL https://figshare.com/articles/software/Netlogo_code_supporting_Personality_variation_is_eroded_by_si...
 
Description This Netlogo code runs in Netlogo 6.2 (available at https://ccl.northwestern.edu/netlogo/download.shtml), and is provided in support of a manuscript entitled 'Personality variation is eroded by simple social behaviours in collective foragers'. Software is made available for use entirely at the risk of the user, and the authors do not accept any responsibility for any damages or data loss caused by using the software. 
Type Of Technology Software 
Year Produced 2022 
Open Source License? Yes  
URL https://figshare.com/articles/software/Netlogo_code_supporting_Personality_variation_is_eroded_by_si...