Investigating the Social Lives of Juvenile Cod

Much of our work understanding the links between physiology and social behavior have taken place in the lab. While this allows us a high degree of control of environmental variables to clearly answer specific questions, the links between a fish’s actions in a tank and what it really does in the wild are not always clear. We were lucky enough to have the opportunity to travel to the Institute of Marine Research (IMR) in Flødevigen, Norway to work with Dr. Esben Oslen to study how the behavior of fish in the lab relates to their movement and social behavior in the wild.

At IMR, there is a unique outdoor pool with a rocky bottom that is feed with water directly from the ocean. Esben has raised Atlantic cod (Gadus morhua) in these large saltwater ponds, where they can swim about freely but are still relatively easy to capture. He has information about the genetic of each individual, their growth rates and the activity patterns of their parents. We will combine this information with the work we are doing to get a better snapshot of these fish’s lives.

 When we arrived, we began catching the fish using fishing traps. We are able to identify individuals using “passive integrated transponder” (PIT) tags. It is the same technology that vets use to “microchip” our pets.

 We brought the fish into the lab where we first measured their activity and social behavior. Activity is easy—we just put the fish in a tank and take a video of it swimming around. We always use video cameras that we set up above the tank because the fish are very sensitive to our presence. We will then take these videos back to Glasgow with us and using tracking software to figure out their exact movement pattern. Social behavior is also fairly straight forward. Just like the activity trials we record their behavior of a fish from above, but now there are four see through tubes, one in each corner of the tank. Two of them are empty, but two of them have fish in them. One with one fish and one with a group of 4 fish. We will just track the movements of the fish that is free to swim around the tank. Fish that spend more time next to the tube with fish in it are considered more social then fish that spend time in the center of the tank or next to the empty tubes.

 In addition to their behavior we use an intermittent-flow respirometer to measure their metabolism. To do this we put each fish in their own individual tube and measure how fast they deplete the oxygen in the water. All night long there are alternating periods of measurement of oxygen and flushing of the system with clean oxygenated water, so the fish never experience any oxygen stress and we are able to get multiple measurements of oxygen depletion throughout the night. Because oxygen is the fuel for many metabolic processes, this is a good proxy of their metabolic rate. We are most interested in their baseline—the minimum amount of oxygen they need when they are relaxed, which is why we measure it at night. In order to further ensure that fish are relaxed, we don’t want them to be able to see each other so we tie little black sheets of plastic around the tubes to “tuck them in” every night.

 We repeated all of these measures twice for each individual so we will be able to get an idea of how consistent they are. For example, we want to know if individuals that are more active during the first measure are also more active during the second measure.

 After taking these measures we surgically implanted acoustic tags in the fish and rereleased them in the pond. A network of receivers in the pond will then triangulate the locations of our fish and allow us to track their movement relative to each other. We are excited to see whether fish that are the most active in the lab are also the most active in the wild. We are hoping to also answer questions relating to their social preference. For example, do fish swim with fish that are behaviorally and physiologically similar to them?

 Our fish are currently in swimming away in the pond and the receivers are gathering information while we watch the videos we recorded in the lab. We are hoping to return in the summer to remeasure their behavior… and hopefully take some more dips in the sea ourselves!

- Daphne and Amelia

Marie and Shaun in Moorea

This year we continued our annual study of coral reef fishes around the stunningly beautiful island of Moorea in French Polynesia. Based at the French research station CRIOBE, our ongoing work in this area, in partnership with the amazing Suzie Mills, Ricardo Beldade, and the rest of their team, has been looking at how various stressors affect the physiological ecology of reef fishes. In previous years, this has involved studying the effects of things like artificial light at night, coral and anemone bleaching, and variation in water current speed and water temperature.

This year we decided to examine how coral bleaching interacts with fish social behaviour to influence the water temperatures that fish choose to occupy. To study this, we used a shuttlebox apparatus, in which fish can move between areas and select the temperatures that they are exposed to. The cool part of this equipment is that you add additional factors to each side — in this case we added either bleached or healthy corals, or the presence of other members of the same species — to see how these factors offset or alter the temperatures chosen by individual fish. For example, a fish might be more willing to tolerate being exposed to a warmer temperature if it means they can be close to their friends.

Overhead view of a shuttlebox setup. Here, the left chamber is relatively cool while the right side is relatively warm. The green line shows the tracked movement of an individual fish. In the center of each chamber, you can see the silhouette of bleached or healthy corals. The fish can decide which coral to associate with, but to do so it must also experience the thermal environment present in each chamber.

A shuttlebox is an effective but notoriously complicated and fiddly piece of equipment. For this reason, we needed to have a shuttlebox expert on our team. Luckily reknowned Shuttleboxer Marie Levet was able to come to Moorea with us! Marie is an extremely talented PhD student working with Sandra Binning and myself, and as part of her PhD she is studying how parasites and other activators of the immune response interact with temperature selection in fish. Marie routinely uses shuttleboxes in her work, and along with her combined expertise in other aspects of fish ecophysiology, she was an ideal addition to our team.

Focusing on the humbug damselfish, we exposed individual animals to various treatment combinations of occupying healthy versus bleached corals, being alone versus with conspecifics, and experiencing warm versus cool water. Like may other reef fishes, Humbug damselfish have complex social dynamics, and our aim is understand how their social behaviour interacts with the costs and benefits exposure to variable habitat types and water temperatures.

The relatively short timeline + finicky equipment meant a lot of long days in the lab, but luckily there was also a lot of time to experience the beauty of Moorea while collecting fish, biking/kayaking around the island, and trying the amazing local cuisine. Amazingly, Marie has been working hard on wading her way through the data and interesting results are already becoming evident. Check out her poster at the upcoming SEB conference to see what we found!

- Shaun

Amelia and Daphne in Trondheim

By Daphne Cortese and Amelia Munson

Our postdoctoral research in Glasgow focuses on the physiological and behavioral responses of fish living in a dynamic and changing environment. We are particularly fascinated by fish social behavior and more specifically by how environmental effects on individual performance modify the behavior of group-living fish. While it is well known that there is variation in how individuals respond to environmental variation, i.e. each individual may have a different sensitivity to the environment and different optimal conditions, things may be slightly more complicated when considering the effects on groups of animals. Is each individual willing to adjust its performance and physiological needs in order to stay in a group or are individual’s actions mainly driven by individual motivation to run (or swim) after their own optimal condition?

Because of the large variation in individual performance traits across environmental conditions it can be tricky to fully answer this question. Luckily, at the International Conference of Fish Biology in Montpellier last summer (2022), we had the opportunity to discuss our research with Fredrik Jutfelt, professor at the Norwegian University of Science and Technology. Fredrik and his team have been selecting zebrafish based on their upper and lower thermal tolerance. The possibility to work on fish that have been genetically selected for environmental sensitivity seemed an excellent opportunity to test how much individual differences in performance affect social behavior. We started to brainstorm project specifics and plan a collaboration.

 In January 2023 we flew to Trondheim in order to run an ambitious experiment to better understand how individual thermal tolerance affects fish social behavior. We were particularly excited to see whether acute exposure to higher temperature changed the effect of inter-individual differences in thermal maximum on social behavior. We hit the ground running, by building multiple group and individual behavioral arenas so we could run multiple trials at the same time (see the video for a better understanding of our set up!).

We were slightly worried about how we would do in the cold Norwegian winter weather but ended up having the opposite issue—studying thermal stress in fish sometimes requires running experiments in rooms heated to 40˚C! A quick trip to the mall to stock up on more shorts and t-shirts later and we were ready. We ended up collecting more than 200 hours of videos and are very excited to analyze them to better understand fish social behavior. Stay tuned to find out our results!

Our time in Trondheim has been full of rich experiences involving science and fun, including cross-country skiing and eating brown cheese and cinnamon buns. We can’t thank Shaun and Fredrik enough for this amazing opportunity and all of the Fish Ecophysiology Lab at NTNU for their warm welcome.

Shaun in Sicily

This week Shaun was lucky enough to visit Francesca Falco and other colleagues at the CNR in Mazara, Sicily. Francesca and Shaun previously collaborated on this paper, outlining strategies for using physiological data to understand the ecological impacts of Mediterranean fisheries. This trip served as an opportunity for Shaun to give a seminar as well as discuss plans for furthering this line of research. Thank you so much to Francesca and colleagues for being such outstanding hosts!

An Amazonian Adventure: We travel to Brazil, canoe through the Amazon, and go on a quest to find the cardinal tetra

By Mar Pineda

As part of my PhD research, I was fortunate enough to go to the Amazon and find out more about the aquarium trade, including how animals are harvested, and how this impacts not only fish populations, but the human communities that depend on them. The aim was to collect data to explore whether fishing for the aquarium trade could have a potential for fishing-induced selection, as has been studied in recreational and commercial food fisheries. To do this, Shaun and I set off to the Brazilian Amazon, which hosts an incredible diversity of fish, including one of the most well-known aquarium species, the cardinal tetra (Paracheirodon axelrodi).

After a two-day trip we arrived in Manaus where we met up with our collaborator Daiani Kochhann at the National Institute for Amazonian Research (INPA). From there, we then headed to our first field site in a protected area of the Amazon, where we were hosted by the Bare community, who were extremely welcoming. Here, we met our expert guide and fisherman, Lindoso, who navigated our boat through the igarapes (forest streams) and led us on our venture to find the cardinal tetra. In this particular region, fish populations are not fished for the aquarium trade. While we were hoping to use the fish from this area as a sort of “non-fished” control population, we weren’t completely sure of what we might find here.

The environments we saw were incredibly dynamic and with water levels rapidly declining due to the dry season, our field sites were under a constant state of flux. 

Despite our best efforts, we didn’t find any cardinal tetra in this first area, but we did see an abundance of other ornamental species, from various tetra species, to angelfish and other cichlids, and even stingrays. Seeing aquarium fishes in their natural habitat was incredible and also allowed us to gain more insight into the conditions that they live in, with many fishes living in extremely hypoxic (5% oxygen saturation) and low pH (4.0) water with seemingly no ill effects. We were also able to take many underwater videos showing fascinating displays of fish behaviour, as well as footage of our fishing trials. We hope to use this footage to provide some of the first recorded behaviours of ornamental fish interacting with artisanal fishing gears. We also managed to do an exciting project using the spotted tetra (Copella nattereri), where we filmed fish being trapped by a cacuri, a traditional fishing trap, and brought them back to a makeshift lab to undergo behavioural and physiological trials to compare fish that were captured using different methods. Stay tuned to find out more about this.

After a 30 hour boat trip (and a bout of food poisoning) Shaun and I then arrived at our next destination along the Rio Negro, Barcelos, which has been the hub of the ornamental fishing industry in Brazil for decades. The historic importance and legacy of the aquarium trade was evident here, with many murals dedicated to the industry, as well as a yearly carnival that celebrates its most iconic species, the cardinal tetra, and the blue and green discus. Throughout our trip, the importance of fishing, and the way fishing was ingrained into Amazonian culture became apparent, but we had never seen a dedication to the ornamental trade like we had here. This is perhaps not surprising, given that at its peak, the export of cardinal tetra alone provided up to 60% of yearly income for local communities in and around Barcelos.

It was in Barcelos that we partnered up with Deco, a local fisher with over 30 years of experience fishing for the ornamental trade, a clear love of the environment that he grew up in, and one of the fastest boat drivers we have ever met. He navigated our boat through remote jungle for hours, and knew the labyrinth-like streams inside and out. After a couple of days of searching we struck gold and finally found cardinal tetra. We found them clustered together in the drying igarapes in both small and large group sizes. We collected them using cacuris as well as rapiches (a specialised artisanal net), recording the process underwater. 

While in Barcelos we were also able to get further insight into the capture of wild-caught fishes for the aquarium trade. Through conversations, we gained insight into which fish were most valuable, changes in abundance, attitudes towards local conservation programs, and changes in fishing practices overtime. A few things became apparent. Fishing for the aquarium trade has happened in Barcelos for decades, with local knowledge and techniques being passed down through multiple generations. Maintaining the environments that tetra and other aquarium species live in, is key to ensuring the trade can continue and is therefore an incentive for environments being protected. We saw this in person during our search for tetra, where sites that were no longer used for the aquarium trade had been transformed for agriculture. There was a stark contrast between these two environments.

An area with active ornamental fishing

An area where fishing has stopped and has since been converted to agriculture

Following our successful hunt for the tetra, we then transported hundreds of fish back to the labs in Manaus. Here, Daiani and I did several tests to explore whether mode of capture may target different traits. This involved many tests including the use of swim tunnels for swimming performance, mazes for exploratory behaviour, and arenas for social behaviour. We’re excited to see where this takes us next over the course of my PhD.

This was a huge undertaking, and would not have been possible without Daiani (our logistical powerhouse), our local guides and partner fishers (who we would literally be lost without), and the Bare community, who welcomed us into their homes, made us incredible food, and allowed us to use their restaurant as a makeshift Lab. I am also thankful to the Fisheries Society of the British Isles for funding this project. The work would have been impossible without all of these partners and I am extremely grateful. 

PhD Position Open: Links between mitochondrial efficiency and social behaviour in fish

Myself, Neil Metcalfe and Mike Webster (St Andrews) are searching for a suitable candidate to put forward for a PhD studentship in the IAPTEUS2 training program. You can apply here! (deadline January 6, 2023)

How does an animal’s physiology affect its sociability, and how will this be altered in a warming world? Group living is key to foraging, predator-avoidance, migration, and reproduction in many animal species, but the costs and benefits of living in groups differ between individuals, partly in relation to their energetic needs (Ward & Webster 2016; Webster, Whalen & Laland 2017). This leads to variation in the sociability of animals within a species: it is not only in humans that we find a spectrum of social behaviour from those that are gregarious to those that are loners.

This diversity is partially explained by physiological differences. It is a widespread finding that there are consistent differences among members of a species in both their minimum and maximum rates of metabolism, and that this variation in metabolic rates influences a range of behaviours (Metcalfe, Van Leeuwen & Killen 2016). For instance, individuals with a higher metabolic rate are often observed to be less social, possibly because they prioritise food acquisition over the safety of group membership (Killen et al. 2021). It also influences the spatial structure of such groups. For example, the position of an individual within a school of fish is not random, but is influenced by both its capacity for aerobic swimming (Killen et al. 2012) and the energetic costs it incurs when digesting a meal (McLean et al. 2018).

In the case of ectotherms, this means that global warming – which causes increases in metabolic costs – will potentially alter the dynamics of social groups. However, the mechanisms underlying these effects are currently unclear. Metabolic rate is usually measured in terms of oxygen consumption by the whole animal, but using this proxy of metabolic rate may generate variability in links between behaviour and metabolic traits. Furthermore, it provides limited insight into the root causes of variation in metabolic demand and potential links with sociability.

A more informative approach is to examine the production rate of ATP, the molecule that powers all cellular processes. ATP is generated in the mitochondria of cells, which consume oxygen in the process. Interestingly, the efficiency of this process is highly variable: some animals require 2-3 times as much oxygen to produce a molecule of ATP as do others (Salin et al. 2015). This is a striking finding, and has led to work revealing that mitochondrial efficiency predicts whole animal performance, such as variation in growth rate (Salin et al. 2019). Moreover, in the case of ectotherms such as fish, mitochondrial efficiency is a stronger predictor of growth when they are living at high temperatures, when metabolic costs are more severe (Dawson et al. 2022). However, no one has yet examined whether mitochondrial efficiency influence social interactions.

This project will use an experimental approach to test for the first time how the social interactions of shoaling fish are influenced by the efficiency with which an individual’s cells can generate energy; it will also test how these interactions are likely to change in the face of global warming. Preliminary data with a social fish species shows that while some individuals display changes in gregariousness as temperature increases, the sociability of others remains constant. This project will test whether this plasticity in sociability with temperature is underpinned by variation in mitochondrial function. Specifically, individuals least able to thermally compensate at the mitochondrial level may be those that show the greatest changes in social behaviour as environmental conditions shift. This interdisciplinary project will thus combine behavioural ecology with ecophysiology, and will be the first to examine how thermal shifts brought on by climate change will alter the biochemical basis of energy metabolism and the potential links with the costs and benefits of group living.

PhD Position Open: The calming effect of group living in social fishes

Along with Lauren Nadler and Clive Trueman of the University of Southhampton, we’re searching for a PhD student to examine how group living may offset the effects of stress in fish. Apply here! (deadline January 3, 2023).

Group living is common across the animal kingdom, ranging from the tiniest insects to the largest mammals. The ubiquity of sociality suggests that it imparts several benefits to individual group members. However, the evolutionary drivers of social behaviour within and among animal species remain obscure. One advantage of group living may come in the form of energy savings. Group-living individuals may reduce energy needs by sharing the costs associated with daily activities, such as movement and finding food. Social individuals may also benefit from the “calming effect”, in which energy use drops as the group can take advantage of having “many eyes” to scan for predators and reduce everyone’s investment in predator avoidance. Recent work in a social fish species found that socializing can reduce metabolic rate by 25% on average when compared to social isolation, with this calming effect persisting even under projected future ocean acidification. This project will take a comparative approach to social fishes to identify what characteristics predispose a fish species to be “calmer” in a social context and determine whether environmental traits alter the magnitude of this energetic benefit. 

Methodology

Using social fishes as models, this project will combine techniques in animal behaviour, ecophysiology, and otolith geochemistry to explore the energetic consequences of sociality, with results applicable to social species from a range of taxa and habitat types. This PhD project will take advantage of recent technological advances for measuring the metabolic rate of social fishes in the laboratory and field to test: 1) the prevalence of the calming effect among social fishes, 2) the role of environment and social context in modifying the strength of this effect, and 3) the mechanistic drivers underpinning calming effects. These research questions will be addressed using techniques such as animal personality tests, intermittent-flow respirometry, and assays of otolith geochemistry. Comparisons will be drawn among temperate and tropical fishes, with potential for fieldwork in a range of settings depending on the interests of the candidate.

Searching for Two Postdocs!

Our team is looking to hire two postdocs to start in the autumn of 2020. The project is funded by a NERC Standard Grant, with the overall aim of examining how temperature and hypoxia affect fish social behaviour in the context of climate change, using a mix of laboratory work, field work, and modelling. The postdocs will work with Shaun Killen (PI, University of Glasgow), Colin Torney (University of Glasgow), Kiran Ramesh (University of Glasgow), and Christos Ioannou (University of Bristol). Both positions will be funded for at least 2 years with the possibility of extension. DEADLINE FOR APPLCATION IS AUGUST 16th.

Group living is key to foraging, predator-avoidance, migration, and reproduction in many animal species but has been mostly overlooked in the context of managing the consequences of environmental change. Recent studies by PI Killen have demonstrated that among-individual variation in energy metabolism and locomotor capacity are important to costs and benefits of group-living in fishes, and link behaviour of individual animals to group behaviour. Relationships between metabolism and social behaviour also suggest that temperature change and hypoxia – two consequences of climate change in aquatic environments – may have profound effects on group living. To date, work examining behavioural and physiological responses to climate change has focussed on isolated animals, without inquiry into how effects at the individual level may affect social behaviour. Conversely, how social dynamics feedback to influence phenotypes and responses to environmental change is also unknown. To address these issues, the proposed project will: (1) examine how temperature and hypoxia affect interplay between behaviour of individual animals and their social group; (2) investigate how temperature and hypoxia influence group formation and functioning; and (3) produce a robust movement model of group behaviour that can be applied to a range of environmental conditions and ecological contexts. By adopting innovative empirical and theoretical approaches and combining behaviour and physiology in the lab and field, this project will be the first to examine how thermal shifts and hypoxia brought on by climate change will affect social behaviour.

One postdoc will focus on the design and implementation of field work with fish and analysing the resulting data. The post holder will play an especially large role in managing an acoustic array for tracking the habitat preference and movements of wild fish and their behavioural responses to variation in temperature and hypoxia. For more info and to apply, click here.

The other postdoc will be more involved with lab-based behavioural and physiological experiments experiments with fish and analysing the resulting data. This person will play an especially large role in using experimental results to inform a theoretical model of how collective behaviour changes in response to temperature and hypoxia. For more info and to apply, click here.

Both post-docs will have the opportunity to collaborate on all projects.

Please get in touch for more information!

Shaun Receives Medal from Fisheries Society of the British Isles

Shaun was recently very fortunate to receive the FSBI medal, awarded this year at the symposium at the University of Hull. The medal is given each year to “an early career scientist who is deemed to have made exceptional advances in the study of fish biology and/or fisheries science in recognition of their achievements”. The occasion was even more special because Shaun received the award along side long time mentor Neil Metcalfe (who received the Beverton Medal) and Isabelle Cote (who received the Le Cren Medal). More information here!

Shaun in Abu Dhabi

This month Shaun was in Abu Dhabi to give a departmental seminar at NYU Abu Dhabi and to start a few experiments with old pal Mat Mitchell. Thanks so much to John Burt’s team for hosting, it was an amazing time and looking forward to a return trip!

Amelie and Shaun Aboard the Marion Dufresne

Last month Amelie and Shaun and the amazing fortune to work aboard the French research vessel Marion Dufresne for several weeks. The aim was to study thermal adaptation in anemone fishes from different Islands at different latitudes around Madagascar. The project was coordinated by Suzie Mills and Ricardo Beldade, and our team also included Isabelle Côté, Giacomo Bernardi, Manfredi DiLorenzo, and Nao Nakamura.

It was an experience of a lifetime. An amazing research endeavor with more than a dozen research teams working from one huge vessel. Thank you so much to Suzie and team for having us along for the ride!

Visit from Steve Portugal

This week our group hosted Steve Portugal from Royal Holloway University of London. Steve gave an amazing talk on his work with collective behaviour in pigeons and stuck around to brainstorm potential projects with air-breathing fishes (and have a few drinks!).

Barbara and Shaun in Norway

Recently Barbara and Shaun were off to Tvedestrand, Norway, to visit colleagues Esben Olsen and Katja Enberg and kick off their NERC-funded project to look at how physiological and behavioural traits influence vulnerability to capture by fishing in wild, free-ranging Atlantic cod. The meeting was a great success and it was amazing to see the field site and start visualizing the project!

Departmental Seminar by Natalie

This week Natalie Pilakouta gave a seminar about her amazing work on thermal adaptation in Icelandic sticklebacks in our IBAHCM PIs and Postdocs seminar series. Great talk Natalie!

Visit from Jenni Prokkola

This week we hosted Jenni Prokkola, who was visiting from the University of Liverpool to do some work with fish swimming and to tell us about her work on fish ecophysiology. Thank you Jenni for a great visit!

Visit from Warren Burggren

This week we were fortunate to have Warren Burggren visit our group and give a departmental seminar about his work looking at transgenerational effects of stress. We were very lucky to spend time with such an amazing scientist and all around great guy!

Welcome to Alexis!

For the next several weeks Alexis Khursigara will be visiting our lab to perform experiments looking at the role of variation in cardiac performance on learning capacity on zebrafish. Alexis is a PhD student at the University of Texas at Austin Marine Science Institute in Port Aransas, supervised by Andrew Esbaugh.

Alexis trying to adjust to the Glasgow autumn weather.

Goodbye Anita!

It’s the end of an era for our lab, as we recently said farewell to our resident zebrafish guru and all-around amazing person Anita Racz. Anita has been an invaluable member of our team and we will miss her tremendously now that she has headed back to her native Hungary. We wish her all the best and look forward to working together in the future whenever possible!

It was an anime-themed goodbye party for Anita, so the spikey anime hair was in full effect!

Just a few of Anita’s farwell gifts!

Davide and Shaun Travel to Calgary

This week Davide and Shaun headed to the International Congress on the Biology of Fishes. It was a week full of fantastic talks and meetups with great friends.

Extremely blurry photo of Shaun talking about digestive costs and positioning of fish within schools.

David McKenzie talking about our work on air-breathing fish in Brazil.

Shaun Travels to Ireland

This week Shaun travelled to Ireland to meet with friends and colleagues Christos Ioannou, Phil McGinnity, and Valentin Lecheval, to perform work on some ongoing projects. The weather wasn’t very cooperative but it was a productive and fun trip nonetheless!