The Influence of Individual Physiology on Group Behaviour in Fish Schools

Lead Research Organisation: University of Glasgow
Department Name: College of Medical, Veterinary, Life Sci

Abstract

The behaviour of schooling fishes is one of the most fascinating phenomena in the animal kingdom, and images of shimmering fish schools have become emblematic of the aquatic world. In addition to being aesthetically captivating, schooling behaviour is also of great biological importance, playing a role in the foraging and predator-avoidance behaviour of multiple species in both freshwater and marine ecosystems. The fluid, synchronous movement of fish schools has long been studied, but it is still unknown how the behaviour of individual fish within the school influences the performance of the group as a whole. Understanding the links between individual and group performance is important since future disturbances to aquatic environments - in response to factors such as pollution or climate change, for instance - may cause changes in the physiology and behaviour of individual fish, and by extension, entire fish schools. The effect of environmental change on animals living in groups has been mostly overlooked, and fish schools are perfectly suited for studying this important aspect of biodiversity. This project will examine these issues by investigating how physiological differences between individual fish may affect their behaviour within a school, and in turn, how these individuals affect the behaviour of the entire school in response to environmental stressors such as increased temperature or decreased oxygen availability. To achieve these goals, this Fellowship will include several laboratory-based studies, and, by using Northern Europe's largest public aquarium (located in Denmark), will also incorporate the first ever scientific observations of individual behaviours in a school containing thousands of fish. Fish schools are ideal for studying the interaction between physiology and behaviour in animals, a link which has rarely been demonstrated directly. As such, any advances in this subject are likely to result in a range of questions for future research in both ecophysiology and behavioural ecology.

Planned Impact

The main beneficiaries of this project will be the general public and scientists working in diverse disciplines. The study of animal group behaviour is a rapidly growing field, yielding insights into numerous subject areas with applications in human society including social networks, information transmission and communication, group decision making, disease transmission, and human crowd control. It should also be noted that the study of the role of individual physiology in fish schools could have applications for the commercial fishing industry. Some types of fishing gear, such as nets used for trawling, capture portions of much larger fish schools, and so it would be useful to understand the potential selective impacts of such processes. In addition, some gear types are specifically designed to allow some individuals to escape (e.g. fish of a certain size). If the ability to escape such gear is also related to swimming ability, then individuals could be selected based on intrinsic physiological traits such as aerobic capacity. The behaviour of economically important species could also change in response to changing environmental temperatures or levels of oxygen availability, affecting the size, shape, or geographical distribution of schools and thus affecting their ability to be harvested by commercial fisheries. The proposed Fellowship will allow a greater understanding of the physiological variation present in fish schools, and the effects of this variability on environmental tolerances. The general public is inherently fascinated with fish schools due to their spectacular appearance and perceived capacity for "group intelligence" due to the synchronous movements of school-members. The public will be exposed to the research of this Fellowship via work done at the Nordsoen Oceanarium Public Aquarium in Hirtshals, Denmark, where there will be a public display describing the purpose and methods behind the project. This display will later be adapted to include results of the work and will be incorporated into the Hunterian Zoology Museum at the University of Glasgow.

Publications

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Norin T (2018) Anemone bleaching increases the metabolic demands of symbiont anemonefish. in Proceedings. Biological sciences

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Palacios MM (2016) Top predators negate the effect of mesopredators on prey physiology. in The Journal of animal ecology

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Pilakouta N (2023) Testing the predictability of morphological evolution in contrasting thermal environments. in Evolution; international journal of organic evolution

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Pilakouta N (2023) A warmer environment can reduce sociability in an ectotherm. in Global change biology

 
Title Naturally Speaking Podacst 
Description A podcast discussing various topics in biology. 
Type Of Art Performance (Music, Dance, Drama, etc) 
Year Produced 2014 
Impact The podcast and website reach thousands of people monthly from countries all over the globe. 
URL https://naturallyspeakingpodcast.wordpress.com/about/
 
Description This research grant has allowed me to study interactions between individual physiology and group behaviours, including socially-facilitated foraging and predator-avoidance, dominance hierarchies, group locomotion, and animal social networks. My findings in this field have already begun to transform perspectives on how fish and other animals arrange themselves when moving in groups, showing for the first time that physiological traits underpin numerous behavioural trade-offs associated with group membership. Further, this work allowed me to wonder whether social and physiological traits may be related to capture vulnerability in commercial fisheries, which has lead directly to having a major project funded by the European Research Council.
Exploitation Route The findings of this project of contributed to understanding how social influences may play an important role in plastic and evolutionary responses to environmental change. This framework can be used by other researchers. Applications to commercial fishing scenarios are being explored in partial collaboration with Marine Scotland.
Sectors Education,Energy,Environment

URL http://www.shaunkillen.com
 
Description The findings from this work of been used to fuel a large amount of public engagement activities. Furthermore, my work examining fish biomechanics in swimming groups has lead to a collaboration with researchers in engineering to investigate whether wave energy harvesters can be modeled after fish swimming movements to maximise energy extraction efficiency.
First Year Of Impact 2014
Sector Education,Energy
Impact Types Cultural,Economic

 
Description Aides à la Formation- Recherche
Amount £48,000 (GBP)
Organisation Luxembourg National Research Fund (FNR) 
Sector Public
Country Luxembourg
Start 09/2012 
End 03/2016
 
Description European Research Council Starting Grant
Amount € 1,500,000 (EUR)
Funding ID 640004 
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 05/2015 
End 05/2020
 
Description Leadership Fellowship
Amount £70,000 (GBP)
Funding ID AH/L503551/1 
Organisation University of Glasgow 
Sector Academic/University
Country United Kingdom
Start 09/2012 
End 09/2014
 
Description Marie Curie Intra-European Fellowship
Amount £183,455 (GBP)
Organisation European Commission 
Department Horizon 2020
Sector Public
Country European Union (EU)
Start 03/2017 
End 03/2019
 
Description NERC Studentship
Amount £46,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2012 
End 09/2015
 
Description Royal Society International Exchange
Amount £3,000 (GBP)
Organisation The Royal Society 
Sector Charity/Non Profit
Country United Kingdom
Start 03/2016 
End 04/2016
 
Description Short-Term Scientific Mission
Amount € 1,500 (EUR)
Organisation European Cooperation in Science and Technology (COST) 
Sector Public
Country Belgium
Start 04/2012 
End 05/2012
 
Title Adaptive effects of parental and developmental environments on offspring survival, growth, and phenotype 
Description Phenotypic adjustments to environmental variation are particularly relevant to cope with putative environmental mismatches often imposed by natal dispersal. We used an inter-generational cross-transplant field-based experiment to evaluate the morphological and physiological effects of parental and post-settlement water flow environments on the orange-fin anemonefish Amphiprion chrysopterus through ontogeny (at pre- and post-settlement stages). Offspring born from parents under high water flow had an 18% higher caudal fin aspect ratio (a compound measure of shape) at the pre-settlement stage, 10% slower growth after settlement, and 55% lower survival after settlement compared to offspring from low-water-flow parents. At the pre-settlement stage, caudal fin length was determined by parental caudal fin length. At the post-settlement stage, fish survived equally well with similar phenotypes in both high- and low-developmental-flow environments. However, results suggest potential developmental phenotypic plasticity in caudal fin length, which increases more under low water flow during development. After settlement growth was the only morphological or physiological trait that was associated with parental water flow, which was lower from parents under high flow, as was survival. These results give important insights into the parental contribution, both genetic and non-genetic, in determining early offspring phenotype and subsequent growth and survival. Our results also suggest that offspring may possess the flexibility to cope with a wide range of local environments including those different from their parents. Overall, the findings of this study show the fitness consequences of living in different environments and the likely trade-offs between parental and offspring fitness in a wild population. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.j6q573nhp
 
Title Density influences the heritability and genetic correlations of fish behaviour under trawling-associated selection 
Description The dataset encompasses zebrafish behavioral data obtained after testing the fish through different behavioral assays. The dataset was created to address the underlying question of fisheries-induced evolution being if fishing can indeed induce a selection on heritable behavioral traits. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://researchdata.gla.ac.uk/id/eprint/1167
 
Title Genomic basis of fishing-associated selection varies with population density 
Description  
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://researchdata.gla.ac.uk/id/eprint/1011
 
Title Simulated trapping and trawling exert similar selection on fish morphology 
Description Commercial fishery harvest can influence the evolution of wild fish populations. Our knowledge of selection on morphology is however limited, with most previous studies focusing on body size, age and maturation. Within species, variation in morphology can influence locomotor ability, possibly making some individuals more vulnerable to capture by fishing gears. Additionally, selection on morphology has the potential to influence other foraging, behavioural, and life-history related traits. Here we carried out simulated fishing using two types of gears: a trawl (active gear) and trap (a passive gear), to assess morphological trait-based selection in relation to capture vulnerability. Using geometric morphometrics, we assessed differences in shape between high and low vulnerability fish, showing that high vulnerability individuals display shallower body shapes regardless of gear type. For trawling, low vulnerability fish displayed morphological characteristics that may be associated with higher burst-swimming, including a larger caudal region and narrower head, similar to evolutionary responses seen in fish populations responding to natural predation. Taken together, these results suggest that divergent selection can lead to phenotypic differences in harvested fish populations. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.pk0p2ngq2
 
Description Ecophysiology and Social Behaviours of Coral Reef Fishes 
Organisation Australian Research Council
Department ARC Centre of Excellence for Coral Reef Studies
Country Australia 
Sector Public 
PI Contribution Expertise in animal physiology and physiological measures; the use of respirometry equipment; equipment for conducting behavioural experiments (e.g. cameras).
Collaborator Contribution Expertise in field work; boat costs; sustenance and accommodation while doing field work; contribution of technician time
Impact Killen, S.S., Mitchell, M.D., Rummer, J.L., Chivers, D.P., Ferrari, M.C.O., Meekan, M., McCormick, M.I. In Press. Aerobic scope predicts dominance during early life in a tropical damselfish. Functional Ecology. 28: 1367-1376. DOI: 10.1111/1365-2435.12296. IF = 4.86
Start Year 2012
 
Description Effects of Environmental Stress on Group Behaviours in Chinese Carp Species 
Organisation Chongqing Normal University
Country China 
Sector Academic/University 
PI Contribution Expertise in respirometry, behavioural experimentation
Collaborator Contribution Expertise in local fish biology and habitats; contribution of staff and student time
Impact Two manuscripts are currently under preparation. One Chinese student will likely come to the UK for several months research experience sometime in the next two years.
Start Year 2012
 
Description Effects of Metabolic Traits on Individual Vulnerability to Trawling for Fish within Schools 
Organisation University of Illinois at Urbana-Champaign
Country United States 
Sector Academic/University 
PI Contribution Expertise in animal physiology; equipment for measurement of fish metabolic rates and swimming ability; supply of fish.
Collaborator Contribution Expertise in commercial fisheries, fish physiology.
Impact Killen, S.S., Nati, J., Suski, C.D. Submitted. Catchability of individual fish by trawling is driven by capacity for anaerobic metabolism. Proceedings of the Royal Society B.
Start Year 2014
 
Description Effects of metabolic and behavioural traits on the spread of invasive species 
Organisation Roehampton University
Country United Kingdom 
Sector Academic/University 
PI Contribution Expertise in physiology and behaviour.
Collaborator Contribution Expertise in phylogenetic analysis.
Impact Killen, S.S., Glazier, D.G., Rezende, E.L., Clark, T.D., Atkinson, D., Willener, A., Halsey, L.G. In Press. Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. American Naturalist.
Start Year 2015
 
Description Effects of physiological traits and behaviour on vulnerability to commercial fisheries in the wild 
Organisation Marine Scotland Science (MSS)
Country United Kingdom 
Sector Public 
PI Contribution Expertise in physiology and ecology.
Collaborator Contribution Expertise in fisheries, access to field gear.
Impact N/A
Start Year 2016
 
Description Schooling Behaviour of Atlantic Mackerel 
Organisation North Sea Oceanarium
Country Denmark 
Sector Private 
PI Contribution Expertise in fish physiology and behaviour; equipment for 3D stereo camera recordings of swimming fish schools.
Collaborator Contribution University of Copenhagen - use of respirometry equipment for physiological studies North Sea Oceanarium - access to pelagic fish tank with thousands of live mackerel
Impact One manuscript in preparation; public engagement while working on site at the public aquarium; re-design of some aquarium exhibits
Start Year 2012
 
Description Schooling Behaviour of Atlantic Mackerel 
Organisation University of Copenhagen
Country Denmark 
Sector Academic/University 
PI Contribution Expertise in fish physiology and behaviour; equipment for 3D stereo camera recordings of swimming fish schools.
Collaborator Contribution University of Copenhagen - use of respirometry equipment for physiological studies North Sea Oceanarium - access to pelagic fish tank with thousands of live mackerel
Impact One manuscript in preparation; public engagement while working on site at the public aquarium; re-design of some aquarium exhibits
Start Year 2012
 
Description The Role of Physiology in Animal Social Networks 
Organisation University of Exeter
Country United Kingdom 
Sector Academic/University 
PI Contribution Expertise in physiology; equipment for the measurement of metabolic rates and swim performance.
Collaborator Contribution Expertise in the analysis of social networks; access to mesocosm tanks and wild caught Trinidadian guppies.
Impact Two posters at international conferences; one manuscript in preparation.
Start Year 2013
 
Description The effects of oil exposure on social networks in marine fishes 
Organisation University of Texas at Austin
Country United States 
Sector Academic/University 
PI Contribution Expertise in social behaviours and social networks, ecophysiology.
Collaborator Contribution Expertise in oil toxicity.
Impact N/A
Start Year 2016
 
Description The effects of social behaviour on synchronous air-breathing in an Amazonian catfish 
Organisation Federal University of Sao Carlos
Country Brazil 
Sector Academic/University 
PI Contribution Expertise in social behaviours and metabolic traits.
Collaborator Contribution Expertise in the physiology of air-breathing fishes.
Impact N/A
Start Year 2016
 
Description The effects of social behaviours on vulnerability of fish to capture by commercial fisheries 
Organisation University of Bergen
Country Norway 
Sector Academic/University 
PI Contribution Expertise in social behaviours and physiology.
Collaborator Contribution Expertise in fisheries and theoretical modelling.
Impact N/A
Start Year 2016
 
Description Using Accelerometry to Study Energy Expenditure of Fish While Swimming in Schools 
Organisation Centre For Environment, Fisheries And Aquaculture Science
Country United Kingdom 
Sector Public 
PI Contribution Expertise in fish schooling behaviour, swimming, physiology; cameras and computing equipment; accelerometers.
Collaborator Contribution Expertise in biotelemetry; access to large swim flume; access to sea bass; staff time.
Impact None so far. Data has been collected and is currently being analysed.
Start Year 2013
 
Description Using Accelerometry to Study Energy Expenditure of Fish While Swimming in Schools 
Organisation Roehampton University
Country United Kingdom 
Sector Academic/University 
PI Contribution Expertise in fish schooling behaviour, swimming, physiology; cameras and computing equipment; accelerometers.
Collaborator Contribution Expertise in biotelemetry; access to large swim flume; access to sea bass; staff time.
Impact None so far. Data has been collected and is currently being analysed.
Start Year 2013
 
Description Appearance on popular science podcast "Level Up Human" 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Appeared for discussion panel on popular podcast "Level Up Human". Recording was done in front of live audience; recorded broadcast reaches tens of thousands of listeners.
Year(s) Of Engagement Activity 2016
URL https://soundcloud.com/leveluphuman/human18
 
Description Bright Club Performances 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact The event centred on discussing academic research in a humorous way, and it was obvious that the audience had fun at the event. There was also a lot of discussion with audience members one-on-one after the main performance.

After the performances I talked with several audience members directly about my work. The event also lead to Glasgow Science Festival organisers seeking my further involvement with other events and activities related to the Science Festival.
Year(s) Of Engagement Activity 2011,2012
URL http://www.brightclub.org/
 
Description British Science Festival (Bradford) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Approximately 110 people from the general public attended my invited talk at the British Science Festival. This included a wide age range from children to older adults. There was a large amount of discussion throughout the presentation and afterwords. There were also several blog posts by media members concerning my talk topic (similarities between social behaviours in animals and humans).
Year(s) Of Engagement Activity 2015
 
Description European Researchers Night 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Approximately 30 people attended my talk at the European Researchers night. This talk was followed by nearly an hour of fantastic discussion with several of the audience members.
Year(s) Of Engagement Activity 2015
 
Description Movie Screenings with Q&A 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Along with two other marine biologists in my institute, we have screened several films for the public that have a "marine biology" theme, which we then follow with a Q&A session with the public.

We always engage in extremely interesting and productive exchanges with the audience during these events. An example is a recording from our screening of "Jaws", in the URL below.
Year(s) Of Engagement Activity 2013,2014
URL https://naturallyspeakingpodcast.wordpress.com/2014/06/17/episode-15-the-science-of-jaws-from-shark-...
 
Description Naturally Speaking Podcast 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact With the help of some institute students and post-docs I successfully launched out institute podcast, which is downloaded by thousands of unique listeners per episode.

The podcast has lead to numerous communications and email interactions with member of the general public.
Year(s) Of Engagement Activity 2012,2013,2014
URL https://naturallyspeakingpodcast.wordpress.com/
 
Description Posting of Research Videos to YouTube 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I've posted several videos related to my research on YouTube, several of which have been linked to by Bloggers and have been viewed thousands of times.

I have had many message exchanges with members of the public stemming from these videos, and one request to use one of my videos (in the URL below) in an Australian Children's educational television program ("Wild But True", by Beyond Productions).
Year(s) Of Engagement Activity 2011,2012,2013,2014
URL https://www.youtube.com/watch?v=XdfO72ODyWo
 
Description Production of Exhibits for the North Sea Oceanarium, Denmark 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact As part of my collaboration with the North Sea Oceanarium in Hirtshals, Denmark, I have actively interacted with them on the production of material for exhibits and have also helped to create a specific exhibit describing the research I performed at the aquarium (and describing why some of the fish in the aquariums have visible tags).

These exhibits are seen by hundreds of tourists on a daily basis, and during my research at the aquarium I engage in discussions with visitors each day as we perform our research.
Year(s) Of Engagement Activity 2012,2013,2014
URL http://en.nordsoenoceanarium.dk/
 
Description Public Lecture at Glasgow Science Festival 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Around 120 people in attendance for interactive lecture on animal social behaviours.
Year(s) Of Engagement Activity 2016
 
Description Public lecture at British Science Festival (Swansea) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Approximately 100 members of the general public attended and discussed issues surrounding fisheries induced evolution.
Year(s) Of Engagement Activity 2016
URL https://issuu.com/britishscienceassociation/docs/g1267_bsa_bsf16_prog_final
 
Description Several media interviews including BBC Scotland, BBC Wales, and BBC World 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Much of my work has been covered in the popular press including the BBC and BBC World Service. I have also had my work covered by print outlets such as the Guardian and Daily Mail.
Year(s) Of Engagement Activity 2015