Couzin, Iain D.
Sensory collectives in natural systems
2023-11-29, Williams, Hannah J., Sridhar, Vivek H., Hurme, Edward, Gall, Gabriella E., Borrego, Natalia, Finerty, Genevieve E., Couzin, Iain D., Galizia, C. Giovanni, Dominy, Nathaniel J., Strandburg-Peshkin, Ariana
Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a ‘sensory collective’; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify ‘sensescapes’. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.
3D-POP : An Automated Annotation Approach to Facilitate Markerless 2D-3D Tracking of Freely Moving Birds with Marker-Based Motion Capture
2023-06, Naik, Hemal, Chan, Hoi Hang, Yang, Junran, Delacoux, Mathilde, Couzin, Iain D., Kano, Fumihiro, Nagy, Mate
Recent advances in machine learning and computer vision are revolutionizing the field of animal behavior by enabling researchers to track the poses and locations of freely moving animals without any marker attachment. However, large datasets of annotated images of animals for markerless pose tracking, especially high-resolution images taken from multiple angles with accurate 3D annotations, are still scant. Here, we propose a method that uses a motion capture (mo-cap) system to obtain a large amount of annotated data on animal movement and posture (2D and 3D) in a semi-automatic manner. Our method is novel in that it extracts the 3D positions of morphological keypoints (e.g eyes, beak, tail) in reference to the positions of markers attached to the animals. Using this method, we obtained, and offer here, a new dataset - 3D-POP with approximately 300k annotated frames (4 million instances) in the form of videos having groups of one to ten freely moving birds from 4 different camera views in a 3.6m x 4.2m area. 3D-POP is the first dataset of flocking birds with accurate keypoint annotations in 2D and 3D along with bounding box and individual identities and will facilitate the development of solutions for problems of 2D to 3D markerless pose, trajectory tracking, and identification in birds.
Inferring social influence in animal groups across multiple timescales
2023-02-20, Sridhar, Vivek H., Davidson, Jacob D., Twomey, Colin R., Sosna, Matthew M. G., Nagy, Mate, Couzin, Iain D.
Many animal behaviours exhibit complex temporal dynamics, suggesting there are multiple timescales at which they should be studied. However, researchers often focus on behaviours that occur over relatively restricted temporal scales, typically ones that are more accessible to human observation. The situation becomes even more complex when considering multiple animals interacting, where behavioural coupling can introduce new timescales of importance. Here, we present a technique to study the time-varying nature of social influence in mobile animal groups across multiple temporal scales. As case studies, we analyse golden shiner fish and homing pigeons, which move in different media. By analysing pairwise interactions among individuals, we show that predictive power of the factors affecting social influence depends on the timescale of analysis. Over short timescales the relative position of a neighbour best predicts its influence and the distribution of influence across group members is relatively linear, with a small slope. At longer timescales, however, both relative position and kinematics are found to predict influence, and nonlinearity in the influence distribution increases, with a small number of individuals being disproportionately influential. Our results demonstrate that different interpretations of social influence arise from analysing behaviour at different timescales, highlighting the importance of considering its multiscale nature. This article is part of a discussion meeting issue ‘Collective behaviour through time’.
How honeybees respond to heat stress from the individual to colony level
2023-10, Jhawar, Jitesh, Davidson, Jacob D., Weidenmüller, Anja, Wild, Benjamin, Dormagen, David M., Landgraf, Tim, Couzin, Iain D., Smith, Michael L.
A honey bee colony functions as an integrated collective, with individuals coordinating their behaviour to adapt and respond to unexpected disturbances. Nest homeostasis is critical for colony function; when ambient temperatures increase, individuals switch to thermoregulatory roles to cool the nest, such as fanning and water collection. While prior work has focused on bees engaged in specific behaviours, less is known about how responses are coordinated at the colony level, and how previous tasks predict behavioural changes during a heat stress. Using BeesBook automated tracking, we follow thousands of individuals during an experimentally induced heat stress, and analyse their behavioural changes from the individual to colony level. We show that heat stress causes an overall increase in activity levels and a spatial reorganization of bees away from the brood area. Using a generalized framework to analyse individual behaviour, we find that individuals differ in their response to heat stress, which depends on their prior behaviour and correlates with age. Examining the correlation of behavioural metrics over time suggests that heat stress perturbation does not have a long-lasting effect on an individual’s future behaviour. These results demonstrate how thousands of individuals within a colony change their behaviour to achieve a coordinated response to an environmental disturbance.
Quantifying the movement, behaviour and environmental context of group‐living animals using drones and computer vision
2023-03-21, Koger, Benjamin, Deshpande, Adwait, Kerby, Jeffrey T., Graving, Jacob M., Costelloe, Blair R., Couzin, Iain D.
1. Methods for collecting animal behaviour data in natural environments, such as direct observation and biologging, are typically limited in spatiotemporal resolution, the number of animals that can be observed and information about animals'social and physical environments. 2. Video imagery can capture rich information about animals and their environments, but image-based approaches are often impractical due to the challenges of processing large and complex multi-image datasets and transforming resulting data, such as animals' locations, into geographical coordinates. 3. We demonstrate a new system for studying behaviour in the wild that uses drone-recorded videos and computer vision approaches to automatically track the location and body posture of free-roaming animals in georeferenced coordinates with high spatiotemporal resolution embedded in contemporaneous 3D landscape models of the surrounding area. 4. We provide two worked examples in which we apply this approach to videos of gelada monkeys and multiple species of group-living African ungulates. We demonstrate how to track multiple animals simultaneously, classify individuals by species and age–sex class, estimate individuals' body postures (poses) and extract environmental features, including topography of the landscape and animal trails. 5. By quantifying animal movement and posture while reconstructing a detailed 3D model of the landscape, our approach opens the door to studying the sensory ecology and decision-making of animals within their natural physical and social environments.
SMART-BARN : Scalable multimodal arena for real-time tracking behavior of animals in large numbers
2023-09, Nagy, Mate, Naik, Hemal, Kano, Fumihiro, Carlson, Nora V., Koblitz, Jens C., Wikelski, Martin, Couzin, Iain D.
The SMART-BARN (scalable multimodal arena for real-time tracking behavior of animals in large numbers) achieves fast, robust acquisition of movement, behavior, communication, and interactions of animals in groups, within a large (14.7 meters by 6.6 meters by 3.8 meters), three-dimensional environment using multiple information channels. Behavior is measured from a wide range of taxa (insects, birds, mammals, etc.) and body size (from moths to humans) simultaneously. This system integrates multiple, concurrent measurement techniques including submillimeter precision and high-speed (300 hertz) motion capture, acoustic recording and localization, automated behavioral recognition (computer vision), and remote computer-controlled interactive units (e.g., automated feeders and animal-borne devices). The data streams are available in real time allowing highly controlled and behavior-dependent closed-loop experiments, while producing comprehensive datasets for offline analysis. The diverse capabilities of SMART-BARN are demonstrated through three challenging avian case studies, while highlighting its broad applicability to the fine-scale analysis of collective animal behavior across species.
A simple cognitive model explains movement decisions in zebrafish while following leaders
2023-05-04, Oscar, Lital, Li, Liang, Gorbonos, Dan, Couzin, Iain D., Gov, Nir S.
While moving, animals must frequently make decisions about their future travel direction, whether they are alone or in a group. Here we investigate this process for zebrafish (Danio rerio), which naturally move in cohesive groups. Employing state-of-the-art virtual reality, we study how real fish follow one or several moving, virtual conspecifics (leaders). These data are used to inform, and test, a model of social response that includes a process of explicit decision-making, whereby the fish can decide which of the virtual conspecifics to follow, or to follow in some average direction. This approach is in contrast with previous models where the direction of motion was based on a continuous computation, such as directional averaging. Building upon a simplified version of this model [Sridhar et al., 2021], which was limited to a one-dimensional projection of the fish motion, we present here a model that describes the motion of the real fish as it swims freely in two-dimensions. Motivated by experimental observations, the swim speed of the fish in this model uses a burst and-coast swimming pattern, with the burst frequency being dependent on the distance of the fish from the followed conspecific(s). We demonstrate that this model is able to explain the observed spatial distribution of the real fish behind the virtual conspecifics in the experiments, as a function of their average speed and number. In particular, the model naturally explains the observed critical bifurcations for a freely swimming fish, which appear in the spatial distributions whenever the fish makes a decision to follow only one of the virtual conspecifics, instead of following them as an averaged group. This model can provide the foundation for modeling a cohesive shoal of swimming fish, while explicitly describing their directional decision-making process at the individual level.
Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
2023-03-10, Davidescu, Mircea R., Romanczuk, Pawel, Gregor, Thomas, Couzin, Iain D.
How collectives remain coordinated as they grow in size is a fundamental challenge affecting systems ranging from biofilms to governments. This challenge is particularly apparent in multicellular organisms, where coordination among a vast number of cells is vital for coherent animal behavior. However, the earliest multicellular organisms were decentralized, with indeterminate sizes and morphologies, as exemplified by Trichoplax adhaerens , arguably the earliest-diverged and simplest motile animal. We investigated coordination among cells in T. adhaerens by observing the degree of collective order in locomotion across animals of differing sizes and found that larger individuals exhibit increasingly disordered locomotion. We reproduced this effect of size on order through a simulation model of active elastic cellular sheets and demonstrate that this relationship is best recapitulated across all body sizes when the simulation parameters are tuned to a critical point in the parameter space. We quantify the trade-off between increasing size and coordination in a multicellular animal with a decentralized anatomy that shows evidence of criticality and hypothesize as to the implications of this on the evolution hierarchical structures such as nervous systems in larger organisms.