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Collective behaviour without collective order in wild swarms of midges.

Attanasi A, Cavagna A, Del Castello L, Giardina I, Melillo S, Parisi L, Pohl O, Rossaro B, Shen E, Silvestri E, Viale M - PLoS Comput. Biol. (2014)

Bottom Line: We find that correlation increases sharply with the swarm's density, indicating that the interaction between midges is based on a metric perception mechanism.By means of numerical simulations we demonstrate that such growing correlation is typical of a system close to an ordering transition.Our findings suggest that correlation, rather than order, is the true hallmark of collective behaviour in biological systems.

View Article: PubMed Central - PubMed

Affiliation: Istituto Sistemi Complessi, Consiglio Nazionale delle Ricerche, UOS Sapienza, Rome, Italy; Dipartimento di Fisica, Università Sapienza, Rome, Italy.

ABSTRACT
Collective behaviour is a widespread phenomenon in biology, cutting through a huge span of scales, from cell colonies up to bird flocks and fish schools. The most prominent trait of collective behaviour is the emergence of global order: individuals synchronize their states, giving the stunning impression that the group behaves as one. In many biological systems, though, it is unclear whether global order is present. A paradigmatic case is that of insect swarms, whose erratic movements seem to suggest that group formation is a mere epiphenomenon of the independent interaction of each individual with an external landmark. In these cases, whether or not the group behaves truly collectively is debated. Here, we experimentally study swarms of midges in the field and measure how much the change of direction of one midge affects that of other individuals. We discover that, despite the lack of collective order, swarms display very strong correlations, totally incompatible with models of non-interacting particles. We find that correlation increases sharply with the swarm's density, indicating that the interaction between midges is based on a metric perception mechanism. By means of numerical simulations we demonstrate that such growing correlation is typical of a system close to an ordering transition. Our findings suggest that correlation, rather than order, is the true hallmark of collective behaviour in biological systems.

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Experiment.a: A natural swarm of midges (Cladotanytarsus atridorsum, Diptera:Chironomidae), in Villa Ada, Rome. The digital image of each midges is, on average, a  pixels light object against a dark background. b: The  trajectories reconstructed for the same swarm as in a. Individual trajectories are visualized for a short time (roughly  frames sec), to avoid visual overcrowding (see also Video S1 and S2). c: A microscope image of an adult male of Cladotanytarsus atridorsum. d: A detailed view of the hypopygium, used for species identification (see Methods); the same midge as in c. e: Scheme of the experimental set-up. Three synchronized cameras recording at  frames per second are used. Two cameras  m apart are used as the stereoscopic pair for the three dimensional reconstruction. The third one is used to reduce tracking ambiguities and resolve optical occlusions. Three dimensional trajectories are reconstructed in the reference frame of the right stereoscopic camera. f: The mutual geometric positions and orientations of the cameras are retrieved by taking several pictures of a known target. The accuracy we achieve in the determination of the mutual camera orientation is of the order of  radians.
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pcbi-1003697-g001: Experiment.a: A natural swarm of midges (Cladotanytarsus atridorsum, Diptera:Chironomidae), in Villa Ada, Rome. The digital image of each midges is, on average, a pixels light object against a dark background. b: The trajectories reconstructed for the same swarm as in a. Individual trajectories are visualized for a short time (roughly frames sec), to avoid visual overcrowding (see also Video S1 and S2). c: A microscope image of an adult male of Cladotanytarsus atridorsum. d: A detailed view of the hypopygium, used for species identification (see Methods); the same midge as in c. e: Scheme of the experimental set-up. Three synchronized cameras recording at frames per second are used. Two cameras m apart are used as the stereoscopic pair for the three dimensional reconstruction. The third one is used to reduce tracking ambiguities and resolve optical occlusions. Three dimensional trajectories are reconstructed in the reference frame of the right stereoscopic camera. f: The mutual geometric positions and orientations of the cameras are retrieved by taking several pictures of a known target. The accuracy we achieve in the determination of the mutual camera orientation is of the order of radians.

Mentions: To reconstruct the 3d trajectories of individual insects we use three synchronized cameras shooting at frames-per-seconds (trifocal technique – Fig. 1e and Methods). Our apparatus does not perturb the swarms in any way. The technique is similar to the one we used for starling flocks [22], with one notable difference. To reach the desired experimental accuracy we need to know the mutual geometric relations between the three cameras very accurately. In the case of flocks, this could be achieved only by an a priori alignment of the cameras. In the case of swarms, though, we proceed differently. After each swarm acquisition, we pin down the geometry of the camera system by taking multiple images of a calibrated target (Fig. 1f). This procedure is so accurate that the error in the 3d reconstruction is dominated by the image segmentation error due to the pixel resolution. If we assume this to be equal to pixel (typically it is smaller than that because midges occupy many pixels), we make an error of in the determination of the distance between two points apart from each other (a reference value for nearest neighbour distance). The absolute error is the same for more distant points, making the relative precision of our apparatus even higher. This accuracy makes the determination of the correlation functions we study here very reliable.


Collective behaviour without collective order in wild swarms of midges.

Attanasi A, Cavagna A, Del Castello L, Giardina I, Melillo S, Parisi L, Pohl O, Rossaro B, Shen E, Silvestri E, Viale M - PLoS Comput. Biol. (2014)

Experiment.a: A natural swarm of midges (Cladotanytarsus atridorsum, Diptera:Chironomidae), in Villa Ada, Rome. The digital image of each midges is, on average, a  pixels light object against a dark background. b: The  trajectories reconstructed for the same swarm as in a. Individual trajectories are visualized for a short time (roughly  frames sec), to avoid visual overcrowding (see also Video S1 and S2). c: A microscope image of an adult male of Cladotanytarsus atridorsum. d: A detailed view of the hypopygium, used for species identification (see Methods); the same midge as in c. e: Scheme of the experimental set-up. Three synchronized cameras recording at  frames per second are used. Two cameras  m apart are used as the stereoscopic pair for the three dimensional reconstruction. The third one is used to reduce tracking ambiguities and resolve optical occlusions. Three dimensional trajectories are reconstructed in the reference frame of the right stereoscopic camera. f: The mutual geometric positions and orientations of the cameras are retrieved by taking several pictures of a known target. The accuracy we achieve in the determination of the mutual camera orientation is of the order of  radians.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4109845&req=5

pcbi-1003697-g001: Experiment.a: A natural swarm of midges (Cladotanytarsus atridorsum, Diptera:Chironomidae), in Villa Ada, Rome. The digital image of each midges is, on average, a pixels light object against a dark background. b: The trajectories reconstructed for the same swarm as in a. Individual trajectories are visualized for a short time (roughly frames sec), to avoid visual overcrowding (see also Video S1 and S2). c: A microscope image of an adult male of Cladotanytarsus atridorsum. d: A detailed view of the hypopygium, used for species identification (see Methods); the same midge as in c. e: Scheme of the experimental set-up. Three synchronized cameras recording at frames per second are used. Two cameras m apart are used as the stereoscopic pair for the three dimensional reconstruction. The third one is used to reduce tracking ambiguities and resolve optical occlusions. Three dimensional trajectories are reconstructed in the reference frame of the right stereoscopic camera. f: The mutual geometric positions and orientations of the cameras are retrieved by taking several pictures of a known target. The accuracy we achieve in the determination of the mutual camera orientation is of the order of radians.
Mentions: To reconstruct the 3d trajectories of individual insects we use three synchronized cameras shooting at frames-per-seconds (trifocal technique – Fig. 1e and Methods). Our apparatus does not perturb the swarms in any way. The technique is similar to the one we used for starling flocks [22], with one notable difference. To reach the desired experimental accuracy we need to know the mutual geometric relations between the three cameras very accurately. In the case of flocks, this could be achieved only by an a priori alignment of the cameras. In the case of swarms, though, we proceed differently. After each swarm acquisition, we pin down the geometry of the camera system by taking multiple images of a calibrated target (Fig. 1f). This procedure is so accurate that the error in the 3d reconstruction is dominated by the image segmentation error due to the pixel resolution. If we assume this to be equal to pixel (typically it is smaller than that because midges occupy many pixels), we make an error of in the determination of the distance between two points apart from each other (a reference value for nearest neighbour distance). The absolute error is the same for more distant points, making the relative precision of our apparatus even higher. This accuracy makes the determination of the correlation functions we study here very reliable.

Bottom Line: We find that correlation increases sharply with the swarm's density, indicating that the interaction between midges is based on a metric perception mechanism.By means of numerical simulations we demonstrate that such growing correlation is typical of a system close to an ordering transition.Our findings suggest that correlation, rather than order, is the true hallmark of collective behaviour in biological systems.

View Article: PubMed Central - PubMed

Affiliation: Istituto Sistemi Complessi, Consiglio Nazionale delle Ricerche, UOS Sapienza, Rome, Italy; Dipartimento di Fisica, Università Sapienza, Rome, Italy.

ABSTRACT
Collective behaviour is a widespread phenomenon in biology, cutting through a huge span of scales, from cell colonies up to bird flocks and fish schools. The most prominent trait of collective behaviour is the emergence of global order: individuals synchronize their states, giving the stunning impression that the group behaves as one. In many biological systems, though, it is unclear whether global order is present. A paradigmatic case is that of insect swarms, whose erratic movements seem to suggest that group formation is a mere epiphenomenon of the independent interaction of each individual with an external landmark. In these cases, whether or not the group behaves truly collectively is debated. Here, we experimentally study swarms of midges in the field and measure how much the change of direction of one midge affects that of other individuals. We discover that, despite the lack of collective order, swarms display very strong correlations, totally incompatible with models of non-interacting particles. We find that correlation increases sharply with the swarm's density, indicating that the interaction between midges is based on a metric perception mechanism. By means of numerical simulations we demonstrate that such growing correlation is typical of a system close to an ordering transition. Our findings suggest that correlation, rather than order, is the true hallmark of collective behaviour in biological systems.

Show MeSH
Related in: MedlinePlus