Coping with life in aquatic habitats: can fish use hydrostatic pressure to orient through volumetric environments?

Lead Research Organisation: University of Oxford
Department Name: Zoology

Abstract

Unlike most terrestrial environments, aquatic systems are volumes through which animals can move in all directions; up and down as well as side to side. Aquatic animals need to orient efficiently through their volumetric habitats to exploit resources and avoid adverse conditions or predators. Indeed, being able to learn, remember and re-use information about local environments is key to their success. Despite this, we do not know how aquatic animals such as fish, or in fact how any animal learns and remembers information about volumetric environments. In comparison to a surface, the amount of information contained in a volume is massively increased. Artificial intelligence systems and humans find orienting through volumes extremely difficult, how then do animals such as fish cope? In relation to terrestrial habitats, aquatic environments have an extra available cue that could aid three-dimensional orientation - hydrostatic pressure. This cue could provide information about the vertical axis of space, either by allowing a fish to work out exactly where it is in the water column, or by giving compass-like information - telling a fish which way is up and down. We aim to discover whether fish can use hydrostatic pressure to orient, and what type of information it gives. Fish are known to be able to perceive small incremental changes in hydrostatic pressure, and a number of potential receptive mechanisms have been found. It therefore seems highly likely that fish have adapted to use this cue that is unique to aquatic systems as a way of coping with the unique problems associated with finding their way around a volumetric environment. In this project, we aim to find out whether fish use hydrostatic pressure to orient vertically, and if so how this cue is used. We will test whether fish use other potential vertical cues such as light, and distance to the surface, to determine whether one cue type is preferred (maybe pressure, as it is ever-present and usable at night or in conditions where visibility is poor), and whether there is redundancy in the cue-use system. We will build on this to consider orientation through three-dimensions, and whether fish orient using different mechanisms when in landmark-rich versus landmark-poor environments. Is pressure always the preferred cue as it is always available, or can the use of landmarks improve precision in orientation? Finally, we will consider orientation through a full volume, and whether fish can encode distance and direction within such a complex 3D space, or whether errors occur in either the horizontal or vertical dimensions. In other words, we aim to work out how fish learn and remember the features and cues of their volumetric habitat, so as to make the correct directional choices when they have to get somewhere in a hurry.

Technical Summary

We aim to test what information fish learn and remember in the vertical axis of space, and how this interrelates with cues in the horizontal axis to allow efficient orientation through local environments. Aquatic animals, such as fish, must orient through volumes through which they can swim with three degrees of freedom of movement. This leads to a potential information-processing problem in comparison to animals that orient over surfaces. These environments have a unique vertical cue that could potentially aid fish in this task - hydrostatic pressure. Using three new behavioural paradigms we aim to test whether fish make use of this ever-present cue to aid orientation. We will test the nature of the hydrostatic pressure cue - whether it allows fish to pinpoint their vertical position, or whether it gives directional information. We will then explore other potential vertical cues to test whether there is a hierarchy in vertical cue use and redundancy in the system. Building from this we will explore the mechanisms and processes that underlie the ability of fish to orient through volumes by manipulating the intensity and type of cues in both the vertical and horizontal axes of space and by putting these in conflict. In particular we will test whether fish in landmark poor or landmark rich environments use different mechanisms to orient - are global pressure cues more salient, and more heavily weighted in an internal representation of space than other cues? Finally, we will introduce a newly developed 3D tracking system to test how fish swim through a volume when they are first restricted to a 3D Y-maze and then unconstrained and allowed to swim free. Can fish accurately encode distance and directional information in 3D, and if so how? In summary, we aim to discover whether fish are able to use hydrostatic pressure, a cue that is unique to aquatic systems, to cope with the unique complexities embedded in the problem of orienting through volumetric environments.

Planned Impact

While the communication of the main results of this project will be via conference presentations and scientific journals, we believe that further benefits can be achieved through a programme developed to target communities that would not usually keep up with this field of research. We have already produced a webpage on our group's work, but aim to enhance this with a section that will be specifically set up for school and college users. We are already involved in a number of outreach initiatives to impart information to these groups. For example, I recently participated in two workshops at the Royal Institute of Navigation (composed of all levels of the public with a general interest in navigation) where I reported on our work to date. I also participated at the 2009 Cheltenham Science Festival, giving a presentation on our group's work to children between the ages of 7 and 11. I will give a similar talk at the Royal Society Summer Exhibition in 2009, again aimed at school-age children, and also at the Brighton Science Festival 2010. I regularly give presentations on our work to local schools, aimed at specific parts of the curriculum. Our work has been widely disseminated to the general public through radio and television (including BBC World Service and the ABC Science Programme), and has also been featured in national and international newspapers and popular science magazines. We will continue to develop these outreach activities to children of all ages. I am also involved in the support of Women in Science at a broad level, and have given interviews to the media, and helped organise workshops to stimulate discussion and also to encourage young women who are starting their careers in all fields of science. This is an area that I feel very strongly about, and will continue to support via workshops, interviews, talks, and mentoring groups. We will pursue collaborations with scientists in other fields to cross over data and research findings. For example, we have recently contacted Huosheng Hu from the University of Essex, with a view to collaborating on his robotic fish, that he has designed to detect pollution in aquatic systems. We will also indentify policy-makers involved in fish welfare and aquaculture, and will disseminate our results with a view to increasing the spread of knowledge on fish cognition to those involved in the care and keeping of fish at all levels. We believe that it is important for scientists to engage with the public, and with policy makes to ensure that data and research results have the widest impact possible. Our impact plan reflects this belief, and indicates the wide-ranging work we have been involved with in our outreach activities, and how we plan to expand and develop upon this broad base.

Publications

10 25 50
 
Title Filming for National Geographic television programe 
Description A film crew recorded an edited version of a section of an experiments in which we explored the active electrosensory system of fish. This formed a section of a programme on animal intelligence due to be aired around the world in 2015. 
Type Of Art Film/Video/Animation 
Year Produced 2014 
Impact Unknown as yet. 
 
Description Unlike most terrestrial environments, aquatic systems are volumes through which animals can move in all directions; up and down as well as side to side. Aquatic animals need to orient efficiently through their volumetric habitats to exploit resources and avoid adverse conditions or predators. Indeed, being able to learn, remember and re-use information about local environments is key to their success. Despite this, we did not know how aquatic animals such as fish, or in fact how any animal learns and remembers information about volumetric environments. In comparison to a surface, the amount of information contained in a volume is massively increased. There are also qualitative reasons as to why the way the information is learned and remembered might be difficult. Artificial intelligence systems and humans find orienting through volumes extremely difficult, how then do animals such as fish cope?

In relation to terrestrial habitats, aquatic environments have an extra available cue that could aid three-dimensional orientation - hydrostatic pressure. This cue could provide information about the vertical axis of space, either by allowing a fish to work out exactly where it is in the water column, or by giving compass-like information - telling a fish which way is up and down. In a theoretical paper we overturned the received wisdom of more than 100 years to show that, in principle, fish can estimate their depth using hydrostatic pressure. Our model shows they could do this if they combine a measurement of their vertical speed with a measurement of the fractional change of their swim-bladder volume. Data collected (and submitted for publication) give empirical support to this theoretical study. In short, we have shown compellingly, that fish can use hydrostatic pressure to ascertain their depth. Fish have adapted to use this pressure cue that is unique to aquatic systems as a way of coping with the unique problems associated with finding their way around a volumetric environment. These results have clear implications for the design of underwater submersibles.

Building from this finding, we then considered the problems of orientation through full three-dimensional space. We found that the vertical axis (and presumably therefore pressure cues) are always extremely important to fish, even overriding other cues, such as visual landmarks. Surprisingly, this is the case for fish that feeling swim through the water column (pelagic) and for those that tend to remain on the substrate (benthic). In a final set of experiments, we developed new high resolution 3D tracking systems that allowed us to track fish that had been trained to swim through a 3D maze. By interrogating these tracks in detail we found that fish can encode distance and direction within a complex 3D space, and that the surprising very small errors accrued in the horizontal or vertical dimensions are equal. In other words, we have worked out how fish learn and remember the features and cues of their volumetric habitat, so as to make the correct directional choices when they have to get somewhere in a hurry.

We have written (accepted for publication in Frontiers in Behavioural Neuroscience) a review that puts together all of our findings, and suggests that fish (like mammals) have place cells, which encode space.
Exploitation Route The main aims of the grant were to test: 1. Which cues are used to orient in the vertical axis of space, and how they interact. 2. The nature of the hydrostatic cue and whether it can be used to determine absolute location in the vertical column, or whether it gives directional compass-like information. 3. The effect of the presence of landmarks on the relative weighting given to the vertical and horizontal components of space in fishes' internal representation of space. 4. Whether fish can encode distance and direction in a volume. We not only fulfilled these aims, but also used the funded research as a scaffold for four new projects, which are all funded. These projects have already yielded publications, and support PDRAs and DPhil students. These projects are: 1) Multisensing in the weakly electric fish (in collaboration with Gerhard von der Emde, Germany), 2) 3D collective behaviour (with Dora Biro, Oxford and Mate Nagy Hungary), 3) Exploring how 3D space is encoded in vertebrates (with Kate Jeffery, UCL), 4) Adaptations to extreme flow in millstream loaches (with Adrian Thomas, Oxford).
Sectors Aerospace, Defence and Marine,Education,Environment

 
Description Exploiting the potential of biological principles, particularly in animal navigation, could be an important step for the engineering design of autonomous systems. I have had meetings with representatives from the Office of Naval Research with a view to exploring this further. A further, follow up project (funded by Leverhulme) aims to explore novel drag reducing properties in millstream loach. My collaborator has set up a spin-out company, via which we intend to produce engineered models based on the drag reducing features that we expect to identify in the loaches. The company will act as a conduit in between our research findings and the public/commercial domain. My research has been used by National Geographic on a program about animal intelligence (2015). A 10 minute segment discusses our research on electrosensing in weakly electric fish. I have also discussed our work at various outreach events to school, and at science festivals, in order to engage the public with our work and with science in general.
First Year Of Impact 2014
Sector Aerospace, Defence and Marine,Education,Environment,Other
Impact Types Societal,Economic

 
Description ASAB Research Grant
Amount £5,000 (GBP)
Organisation University of Nottingham 
Sector Academic/University
Country United Kingdom
Start 04/2014 
End 09/2014
 
Description BBSRC DTP studentship
Amount £150,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 05/2013 
End 04/2016
 
Description German Research Foundation
Amount € 250,000 (EUR)
Organisation German Research Foundation 
Sector Charity/Non Profit
Country Germany
Start 01/2014 
End 12/2017
 
Description Leverhulme Trust
Amount £221,752 (GBP)
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 10/2015 
End 09/2018
 
Title Three dimensional tracking system and associated photogrammetry 
Description We developed a high-resolution 3D tracking tool to produce detailed trajectories of freely swimming fish, but which could also be adapted for other animals that move within 3D (eg insects). Our tracking system is based on two orthogonally placed cameras, connected to a computer via a FireWire connection, and a function generator which was used to generate a pulsed signal set at 25 Hz maintaining a regular frame rate and synchronization. Recording was carried out using the free program VirtualDub. The two dimensional trajectories of the fish in each camera view were determined by manually identifying the fish in each frame using custom written software in Matlab (Mathworks). The two-dimensional trajectories from each camera view were then reconstructed into a three-dimensional trajectory using freely available photogrammetric software. The same technique was used to reconstruct the three-dimensional coordinates of the corners of the tank that contained the maze for an external frame of reference. We have made this tracking tool freely available to other researchers. 
Type Of Material Physiological assessment or outcome measure 
Year Produced 2013 
Provided To Others? Yes  
Impact With this tool, it is possible to produce accurate trajectories of moving animals in 3D. These trajectories can be interrogated and used to answer questions on animal behaviour, ecology and collective systems in 3D. 
 
Title Databases in 3D animal movement, both individually and collectively 
Description We have approx 1TB of data relating to movements of fish shoals in 3D under different behaviours (goal and non goal directed). In addition we have very large data sets that relate to 3D trajectories of fish under different experimental manipulations. These data are currently held on an internal server within the University of Oxford. Once our work has been published, we intend to make all of this data available to other researchers. Information of how to do this will be uploaded onto our website. 
Type Of Material Database/Collection of data 
Year Produced 2013 
Provided To Others? Yes  
Impact These data have allowed us, and other groups, to explore principles of 3D movements of collective behaviour, and also to identify the mechanisms and processes relating to 3D animal navigation (from sensory and cognitive perspectives) 
 
Description BBSRC funded studentship shared with Kate Jeffery (UCL, UK) 
Organisation University College London
Department Division of Psychology & Language Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution In a direct extension from the BBSRC funded project, we are exploring how 3D space is encoded in the brain of vertebrates. My expertise lies in behavioural paradigms and methodologies.
Collaborator Contribution My Collaborator is a neuroethologist and provides the equipment and training for single cel recordings in the hippocampus and the entorhinal cortex of rats.
Impact N/A (too early a stage)
Start Year 2016
 
Description DFG funded collaboration on sensory ecology with Prof Gerhard von der Emde in the University of Bonn, Germany and Prof. Mario Wullimann, University of Munich, Germany 
Organisation University of Bonn
Country Germany 
Sector Academic/University 
PI Contribution We are studying the interaction of multiple senses using the weakly electric fish as a model. The current project takes a holistic approach by fusing together my two streams of research (cognition and sensory ecology) and considering how multiple sensory systems interact and shape behavioural output. I provide expertise in spatial cognition and navigation and the equipment therein. So far, we have investigated the types of information that sensory systems of the weakly electric fish can obtain, and whether these systems can operate redundantly, synergistically, and whether they are tuned to different functions. Our work has also identified how the information from these sensory systems integrate in the fishes' brain. Four publications will result from this study: two have been submitted (PNAS and Animal Behaviour), we have completed drafts on the other two (for Animal Cognition and Current Biology).
Collaborator Contribution Gerhard von er Emde provides expertise in neurophysiology and the mechanics of the electrosensory system and the the equipment associated with this side of the study. We share two PhD students and have been awarded a DFG grant from Germany (250,000 Euros) to support this work. We are now writing a follow-up grant to the DFG, and have also built a collaboration with a neuroanatomist (Mario Wullimann, University of Munich, Germany).
Impact This collaboration crosses over the disciplines of animal behaviour and neurophysiology. Manuscripts in progress include: Schumacher, S. Burt de Perera, T. and von der Emde, G. 2016. Sensory system shapes the mechanism of orientation in Gnathonemus petersii. Submitted. Schumacher, S. Burt de Perera, T. and von der Emde, G. 2016.The lateral line of Gnathonemus petersii: a neuoranatomical and behavioural study. Manuscript in progress.
Start Year 2016
 
Description Leverhulme funded Collaboration with Prof. Adrian Thomas on adaptations for low drag, downforce and eddy use in hill stream loaches 
Organisation University of Oxford
Department Department of Zoology
Country United Kingdom 
Sector Academic/University 
PI Contribution This project aims to study adaptations for low drag downforce and eddy use in hill stream loaches. Hillstream loaches effortlessly exploit environments where flow rates are so high that they wash potential competitors away. To cope with these extreme flow rates hillstream loaches have evolved adaptations to stick to the bottom, equivalent to the downforce generating wings and skirts of F1 racing cars, and skin architecture reminiscent of the drag-reducing riblets of Mako sharks. However, the flows hillstream loaches live in are more severe than either Mako sharks or F1 cars experience. Hillstream loaches exhibit far more diverse flow-modifying morphological features than fast pelagic predators, suggesting as yet unknown drag reducing systems remain to be discovered. My team contributes behavioural expertise to this project. I contribute behavioural expertise to this project, and Adrian Thomas provides knowledge on biomechanics and engineering.
Collaborator Contribution Adrian Thomas is an expert in biomechanics, and brings an engineering perspective to the project. He also has a spin-out company, via which we intend to produce engineered models based on the drag reducing features that we expect to identify in the loaches. The company will act as a conduit in between our research findings and the public/commercial domain.
Impact We have obtained a Leverhulme grant with a postdoctoral RA to work on this project.
Start Year 2015
 
Description Mechanisms underlying navigational leadership hierachies with Dr Dora Biro, Richard Mann, Mathematics Institute, Uppsala University, Sweden and Mate Nagy, Budapest University, Hungary. 
Organisation University of Oxford
Department Department of Zoology
Country United Kingdom 
Sector Academic/University 
PI Contribution We seek to study the dynamics of animal group movements, and, specifically, how information propagates between individuals during navigation in three dimensions. We are using homing pigeons and fish as model species, and apply state-of-the-art tracking technologies to gather high-resolution data on both systems. Data from two model species will allow us both to identify general principles of collective motion, and to highlight differences that may be shaped by the species' ecology or biology. This is collaboration with Dora Biro (Oxford), Richard Mann (Mathematics Institute, Uppsala University, Sweden), and Mate Nagy (University of Budapest, Hungary). We contribute expertise in fish behaviour and 3D tracking systems.
Collaborator Contribution Dora Biro's expertise is on avian models, Richard Mann's training is in engineering (contributing to models of collective motion in fish), and Mate Nagy's is in statistics (inputting into models that underpin hierarchies in groups). Dora Biro and I jointly supervise a BBSRC funded DPhil student.
Impact A number of manuscripts from this work, one has been accepted for publication, one is submitted, we have one draft complete and ready to submit, there others are in progress: Watts, I., Petit, B., Nagy, M., Burt de Perera, T. and Biro, D. 2016. Lack of experience-based stratification in homing pigeon leadership hierarchies. Royal Society Open Science Journal. In Press. Watts, I., Burt de Perera, T. and Biro, D. 2016. Misinformed leaders lose influence over pigeon flocks. Submitted to Biology Letters. Watts, I., Burt de Perera, T. Holbrook, R. and Biro, D. 2016. Mechanisms of 3D information transfer in fish shoals. Draft complete.
Start Year 2014
 
Title Three dimensional tracking systems 
Description We developed a high-resolution 3D tracking tool to produce detailed trajectories of freely swimming fish, but which could also be adapted for other animals that move within 3D (eg insects). Our tracking system is based on two orthogonally placed cameras, connected to a computer via a FireWire connection, and a function generator which was used to generate a pulsed signal set at 25 Hz maintaining a regular frame rate and synchronization. Recording was carried out using the free program VirtualDub. The two dimensional trajectories of the fish in each camera view were determined by manually identifying the fish in each frame using custom written software in Matlab (Mathworks). The two-dimensional trajectories from each camera view were then reconstructed into a three-dimensional trajectory using freely available photogrammetric software. The same technique was used to reconstruct the three-dimensional coordinates of the corners of the tank that contained the maze for an external frame of reference. We intend to make this tracking tool freely available to other researchers. 
Type Of Technology Software 
Year Produced 2013 
Impact Other researchers have approached us for information on our tracking system. They have told us that they it has enabled them to obtain data that will be vital to their research. 
 
Description Cheltenham Science Festival 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact I gave a talk on my research and on evolution in general - aimed at children ages 8-12, at the Cheltenham Science Festival
Year(s) Of Engagement Activity 2009
 
Description International Conference of Comparative Psychology 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research and patient groups
Results and Impact Talk sparked discussion and questions. I am working to create links between the disciplines of animal behaviour. psychology and neuroethology,

Post conference contacts from attendees
Year(s) Of Engagement Activity 2014
 
Description International Conference of neuroethology, Japan 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Participants in your research and patient groups
Results and Impact Talk stimulated discussion and developed interdisciplinary collaboration

Much discussion from presentation - stimulated two grant proposals for submission this year
Year(s) Of Engagement Activity 2014
 
Description National Geographic filming 
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 I contributed (interview and filming my fish) a 10 minute segment to a programme on animal intelligence.
Year(s) Of Engagement Activity 2015
 
Description Open days within Oxford 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Each year I contribute to several open days that are held in the Zoology Department, Oxford, and also St John;s College. I advocate for Science and Biology, encouraging students from different backgrounds to apply to Oxford. I also visit schools across the UK, with the same intention, and I host school visits to Oxford.
Year(s) Of Engagement Activity 2007,2008,2009,2010,2011,2012,2013,2014,2015,2016
 
Description Royal Society Summer Exhibition 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact I was asked to lead a workshop on evolution (using my research as to make particular points) - aimed at children ages 8-12.
Year(s) Of Engagement Activity 2009
 
Description Various talks to schools and festivals, 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact I have given a number of talks to schools (primary and secondary) on my research. I am also involved in access events and open days both through the Department of Zoology, Oxford and through St John's College. These events give me the opportunity to publicise my research and also to educate students about the field of animal behavior in general. These talks have always been well received by pupils and staff alike.

Difficult to directly assess impact, but we have noticed a jump ion applications to Science from State Schools
Year(s) Of Engagement Activity 2009,2010,2011,2012,2013,2014,2015,2016
 
Description many interviews given for local and national media outlets 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Each year I give a number of interviews on my research to various media outlets. My work has been reported in the New Scientist, and various broadsheets (the Telegraph), also the Daily Mail and the Sun newspaper!

I have also been interviewed for local and national radio programmes.
Year(s) Of Engagement Activity 2009,2010,2011,2012,2013,2014,2015,2016