Standing out from the crowd

29 April 2018 - By: Alex Evans

Standing out from the crowd

By Alex Evans 

Nature is teeming with weird and wonderful relationships between individuals and their social groups, leading to a whole host of interesting and observable differences in physiological and behavioural traits. An upcoming session at the 2018 SEB Annual Main Meeting this summer entitled the “Role of individual variation in the behaviour of animal groups” aims to bring these issues into the spotlight, and Alex Evans gets to know a few of the speakers in advance of the session...

Shaun Killen
Fishtanks Photo: Shaun Killen



Session organisers, Shaun Killen from the University of Glasgow, UK, and Stefano Marras from the National Research Council (CNR), Italy, believe that now is an ideal time to make the most of the SEB’s diverse and interdisciplinary roster of delegates for a discussion of this topic. “Understanding how individuals within social groups contribute to leadership, decision-making, hierarchy formation and group cohesion are all critical for gaining a basic understanding of ecology,” Shaun explains. This fascinating topic has attracted researchers from a wide breadth of research angles, which, while useful, has also led to gaps in communication between scientists working in separate fields - an issue that Shaun and Stefano hope to tackle. “There are so many fantastic researchers in different parts of the world that are studying this subject that it made sense to try to get a bunch of them in the same place at the same time to exchange ideas”, explains Shaun. “We hope that this session can facilitate more discussion from people working on different sides of the same problem.”

Nature’s social network

Shaun, the recipient of the Animal Section’s President’s Medal at 2017’s SEB Annual Meeting, has plenty of experience working on the social interactions of animals and presented some of the research from his lab during his medallist’s session talk last year in Gothenburg. “It was a great honour,” says Shaun of receiving the award, “but science is by nature an extremely collaborative process and none of what I have done would have been possible without working with such amazing mentors, colleagues and students along the way”. Recently, the focus of Sean’s research has been on the interactions between the physiology of individuals and group behaviours in social animals. “We use fish in our work and tend to focus on how energy demand and swimming ability interact with leadership and other types of social behaviour,” he says. The costs of swimming solo and in groups are also intrinsically linked with variability in sensitivities to environmental conditions such as temperature and food availability, which is another topic of interest to Shaun and his lab. “Learning more about social behaviours is critical for predicting how animals might respond to environmental change,” he explains, adding that “we are also finding that physiological factors and social behaviours in fish are important for determining which individuals are likely to be captured by various fishing practices, so there are a range of potential conservation applications”1.

With the potential for a diverse offering of talks and posters, Shaun proposes that this session is a great choice for first-time attendees to SEB, and is looking forward to seeing research featuring animals from all walks, swims and flights of life. “It is always amazing how, despite the obvious differences among these types of animals, there are often incredible similarities in how they behave socially.” he says, adding: “We can’t wait to see you all in Florence!”

The right ant for the job

Social behaviours aren’t just a vertebrate fad, and there are many insect species that can also be found living in communities with interesting inter-individual dynamics. In particular, eusocial insects, such as ants, bees, wasps and termites, have developed complex societies where individual variation is pushed to the extreme in order to partition up tasks between its members. The division of labour observed in ants is one of the most impressive examples of how animal societies can dictate not only the general behaviour of a society’s individuals to suit specific roles, but also their size and shape.

It is currently believed that individuals within these social ant societies develop different sensitivities to certain tasks, and that workers are more likely to engage in tasks to which they are more sensitive. But what are the sources of these variations in sensitivity? This is a question that Dr Raphael Jeason of Université Paul Sabatier, France, was very keen to answer. “By manipulating the social environment experienced by ants, we aim to examine how this impacts the range of behavioural variations between workers,” explains Raphael. Utilising both theoretical and experimental approaches, Raphael and his team are working to understand how such a diverse community structure as those seen in ants and other social insects can be acquired and regulated. “Social insects provide some of the most familiar and spectacular examples of social groups with large inter-individual differences,” he says, “and behavioural variability among the workers of a colony is increasingly regarded as fundamental for a key feature of social insects.”

At the upcoming session in Florence, Raphael will be presenting a talk on the different mechanisms underlying the expression of behavioural variability that can give rise to this impressive division of labour in insect societies2. He believes that now is an important time to examine the issues of heterogeneity and variation in insect communities, saying that “there is currently a need to identify the proximate causes and ultimate consequences of variations among entities in biological systems, at all scales of analysis.”

Raphael hopes that future research into this field will certainly benefit from the input of a wide range of researchers interested in the division of labour amongst social insects: “Most studies have focused on behavioural variability based on genetic variability, while other mechanisms that may be responsible for the behavioural differentiation have been largely neglected,” he says. Finally, Raphael predicts that this session will be a good opportunity to develop and grow new ideas, concluding that “the interdisciplinary attendance of the SEB Annual Meeting offers the ideal condition for stimulating and exciting discussions around the concept of variation.”

Muddying the waters

Predators and prey alike rely on their keen senses to keep aware of each other, be it through any number of their physical senses. Previous research on collective behaviour has shown that group tactics can often be the key to successfully utilising these senses in both hunting prey and avoiding predation for many animal species. Dr Lesley Morrell, of the University of Hull, UK, is eager to understand more about the effects that environmental changes can have on how animals detect their prey or evade predation, and some of her latest research has expanded to investigate the additional interactions when group sizes are considered. Working with a former PhD student, Ása Johannesen, Lesley’s starting point was investigating the effects of olfactory clues on foraging sticklebacks by reducing the visibility of their environment and seeing how the size of prey groups affected the ease at which they were detected and devoured3. However, inspired by the interesting overlap in their findings with those from work carried out by another former PhD student, Ben Chapman, now at the University of Leeds, UK, on how environmental effects can affect olfactory cues in guppy foraging4, a new grouping behaviour project was born.

“I recruited Helen Kimbell to a PhD to try rearing fish in turbid environments and looking at their behaviour,” explains Lesley, adding that it is important to investigate these environmental changes, as “water bodies are increasingly impacted by human activities such as agriculture, industry and mining. ” The primary goal of Helen and Lesley’s work was to assess how social behaviours in sticklebacks can be disrupted by the visual clarity of the water in their habitat. By placing stickleback shoals in tanks containing clear or turbid water, the team were able to film the fish and track the positions of individuals to see how the shoaling patterns changed. “One of the key findings from that study was that turbidity seemed to make the fish in groups behave as they would when they were alone and not in groups,” says Lesley5. These disruptions to grouping strategies could have consequences for the health of wild fish populations, as Lesley explains: “Social behaviour carries with it a wide range of anti-predator benefits for shoaling fish and, if turbidity disrupts these behaviours, they could be left vulnerable to predation.” Group-living has benefits beyond avoiding predators however, and Lesley stresses the importance of their role in the wider ecological community. “Changes in behaviour can also have implications for mating success and finding food, and so can have important knock-on implications throughout the ecological network,” says Lesley.

The brave and the bold

Just as the attendees of conference presentation sessions may behave as an organised social group of animals, so too can the dominant behaviour of a few individuals (you know who you are) dictate the flow of the group’s focus. This is also the case for wildlife, where the behaviour of a few atypical individuals can play a large role in the group dynamics of a population. These traits can often be a valuable asset for an animal society, but how do they arise in the first place? And under which circumstances does it pay to be bold?

These were questions that Dr Jonathan Pruitt, at the University of California in Santa Barbara, was keen to answer. His initial interest in the topic was inspired by the tales of wildlife biologists lamenting the actions of one or two individuals of their study populations acting differently, which affected the behaviour of the group, and often, the poor biologist’s data collection. Later, he noticed that, even in his own study organisms (spiders), a small number of risk-taking individuals could have an unexpectedly large influence on the behaviour and success of their colonies. “This sparked my ongoing interest in how rare or extreme-phenotyped individuals evolutionarily come to be, how they wield such social influence, and how they influence group performance in contrasting situations,” Jonathan explains.

Spiders
Painted Spiders .Photo:Jonathan Pruitt



In order to evaluate how the rare bold-phenotype spiders affected the collective behaviour of their colonies, Jonathan created experimental colonies along two precipitation gradients in the Kalahari and Namib deserts, producing so-called “arid sites” and “wet sites”, and ensured that both sites had some colonies containing bold individuals and some without6. “We then monitored the behaviour of each group and observed which colonies lived and died over the next 6 months,” says Jonathan. Interestingly, Jonathan found that, while the braver individuals increased the collective aggresiveness and survivability of the colonies, this was only observed in the arid sites, leading him to question how differences in the environment can affect the importance of headstrong individuals in a social setting. “It seemed odd that bold individuals only appeared to be influential at arid sites and not wet sites,” says Jonathan, “and this got us thinking...are bold individuals at arid sites particularly socially influential, relative to their counterparts at wet sites?”

In order to learn more about this, Jonathan replicated the original experiments, but this time created chimeric societies that contained a mixture of bold individuals from arid sites with shy individuals from wet sites, and vice versa, to produce surprising results. “What we found was pretty astonishing!” says Jonathan. “When we paired bold, influential individuals from arid sites with shy individuals from elsewhere, these bold individuals had no effect on colony behaviour,” he explains, “but when we paired the less-influential bold individuals from wet sites with shy individuals from wet sites, we found that bold individuals were just as effective at changing the behaviour of their foster societies.” These results demonstrate that it is not purely down to variations in the key behavioural traits that makes bold individuals hold sway over a group, but also factors that affect the willingness of the group to follow. “Their social susceptibility is the key for emergence of social influence,” adds Jonathan, ”and in the truly socially susceptible, anything approximating a leader will do.” Jonathan hopes that more research like this will open the door to a deeper understanding of individual and group behaviours, and that the meeting of minds during the session this summer will be an ideal place for people to discuss their ideas and collaborate on new and innovative projects.

Stay in School!

“I have always wondered how fish schools work, who makes the decisions and how are they transmitted within the group,” says Dr Jens Krause, a collective behaviour researcher at Leibniz Institute of Freshwater Ecology and Inland Fishery, Germany. While Jens’ work includes many aspects of research into group behaviour, he is especially interested in how self-organisation within animal groups develops into social decision making. “Collective cognition is a particular interest of mine and we run experimental work both on fish schools and human groups on this topic,” says Jens.

Many of Jens’ experiments are designed to compare the abilities of single fish against increasingly large schools of fish in order to examine how group size affects the way the fish function7. And to make things more interesting, Jens’ research isn’t just limited to the natural world, as he is also interested in how live fish react to the presence of robotic fish8. “Our new generation of fish robots are fully interactive and can both lead and follow in a social context,” explains Jens. “This allows us to do many experiments that were not possible before as we can now decouple the appearance of a fish from its natural behaviour.” The robot fish also allow Jens and his team to experimentally test the collective behaviour algorithms they have developed from theoretical studies, and evaluate the performance of group behaviours against simulated models.

Robofish
Robofish. Photo: Jens Krause



Jens and his research group are very keen on the biomimetic applications of their research, especially in generating new ways of thinking about group problem solving. “We have regular meetings with public institutions and private companies to inform them about potential applications of collective behaviour and collective intelligence,” says Jens. By further studying group-living animals, Jens and his team hope to develop models and algorithms that can apply to decision making processes in human society, such as improving crowd management and improving communication between medical professionals for improved diagnoses. This session will be Jens’ first visit to the SEB Annual Main Meeting, but he is looking forward to seeing the research available: “I am excited about making new connections with scientists who have matching research interests and to be inspired by those who do something completely different!

1. Killen, S., Nati, J., Suski, C., (2015) Vulnerability of individual fish to capture by trawling is influenced by capacity for anaerobic metabolism. Proc. R. Soc B., 282(1813) 
2. Pasquaretta, C., Jeanson, R., (2017) Division of labor as a bipartite network. Behavioural Ecology 
3. Johannesen, A., Dunn, A., Morrell, L., (2012) Olfactory cue use by three-spined sticklebacks foraging in turbid water: Prey detection or prey location? Animal Behaviour, 84(1) 
4. Chapman, B., Morrell, L., Tosh, C., & Krause, J., (2010) Behavioural consequences of sensory plasticity in guppies. Proceedings of the Royal Society of London Series B, 277 
5. Kimbell, H., & Morrell, L., (2015) Turbidity influences individual and group level responses to predation in guppies (Poecilia reticulata). Animal Behaviour, 103 
6. Pruitt, J., Goodnight, C., Riechert, S., (2018) Intense group selection selects for ideal group compositions, but selection within groups maintains them. Animal Behaviour, 124 
7. Ioannou, C., Krause, J., (2008) Searching for prey: the effects of group size and number. Animal Behaviour, 75(4) 
8. Bierbach D., Lukas J., Bergmann A., Elsner K., Höhne L., Weber C., Weimar N., Arias-Rodriguez L., Mönck H.J., Nguyen H., Romanczuk P., Landgraf T., Krause J. (2018) Insights into the Social Behavior of Surface and Cave- Dwelling Fish (Poecilia mexicana) in Light and Darkness through the Use of a Biomimetic Robot. Frontiers in Robotics and AI, 5
 

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Alex Evans

Alex Evans is a PhD student at the University of Leeds investigating the energetics of bird flight. In his spare time, Alex enjoys writing about the natural world, contributing to the Bird Brained Science blog and exploring other avenues of science communication.