Specific reactions of Starling flocks to predator attacks
What underlies waves of agitation in Starling flocks. Hemelrijk, C. K., Zuidam, L. v. & Hildenbrandt, H. 2015. Behavioral Ecology and Sociobiology 69 (5), 755-764. DOI 10.1007/s00265-015-1891-3
What behavioural signal and transmission process underlies waves of agitation in Starling flocks?
The beautiful displays by huge flocks of Common Starlings Sturnus vulgaris are admired by everyone. When flocks are under attack by a raptor, often from a Peregrine Falcon Falco peregrinus or Eurasian Sparrowhawk Accipiter nisus, they can take on extraordinary shapes and display remarkable changes in density. Most remarkably, a flock under attack may show a dark band moving over itself away from the predator, while its shape remains constant (Procaccini et al. 2011). This reduces the catching-success of the raptor and is called a ‘terror wave’ or a ‘wave of agitation’ (Fig. 1). It is moving faster than the flock moves itself. Such waves have also been observed during predator attacks on Dunlin flocks (Potts 1984) and on fish schools (Gerlotto et al. 2006).
There are a number of burning questions when studying such waves:
- Specific for Starlings: what behavioural escape reaction underlies their agitation wave? We cannot see it, because when displaying a wave the huge flock of Starlings is too far away.
- What makes these waves move so fast? It is thought that during the wave birds need to anticipate the behaviour of flock members over a larger distance than when they normally coordinate in flocks (Potts 1984).
To try and answer these questions we have used a computational model, StarDisplay (Hildenbrandt et al. 2010, Hemelrijk & Hildenbrandt 2011, Hemelrijk et al. 2015).
In the StarDisplay model, individuals fly a bit like an airplane (following fixed-wing aerodynamics) and they coordinate with flock members by adjusting their movement such that they
- stay in a flock,
- do not collide and
- move approximately in the same direction as others do.
For such coordination, they only watch the behaviour of their seven closest neighbours. They adjust their motion merely to them, they do not watch what the whole flock does (Ballerini et al. 2008). The flocks look very much like real flocks, and are quantitatively similar in many respects (Fig. 2) (Hemelrijk & Hildenbrandt 2015a; Hemelrijk & Hildenbrandt 2015b).
To discover what the underlying escape reaction during an agitation wave may be, we needed to investigate escape manoeuvres that do not change the shape of a flock. We tried out two escape manoeuvres in the model, namely speeding up forwards into the flock away from the predator and rolling side-wards and back like in a kind of zigzag. We represented the attack by making a few neighbouring birds escape simultaneously.
When, after individuals were attacked, the neighbouring birds merely adjusted their motion following the rules of coordination, we did not observe an agitation wave.
Subsequently, we made neighbours repeat the escape manoeuvre they observed close by. Indeed, when the escape manoeuvre was a zigzag (rolling side-wards and back), we observed an agitation wave (Figs. 3 and 4 (movie clip)). When the escape manoeuvre was a fast speeding up into the swarm, no wave was observed at all.
We measured the speed of the agitation wave in the computational model. It appeared similar to the speed of the wave of real Starlings (3 – 25 m/s). To reach the same wave-speed as in empirical data, modelled-birds needed to repeat the escape manoeuvre from only the single closest neighbour up to seven of them.
Figure 3. Left side: wave of agitation due to the zigzag-like manoeuvre in Stardisplay (black band moving to the right). Right side: shape of bird when observing wing area from above and from the side.
Figure 4. Movie of wave in StarDisplay
To detect whether during an orientation wave based on a zigzag-like manoeuvre, flock-density increased temporarily, we changed the body-shape of the bird into a ball. After this we observed no wave anymore (Fig. 5).
Interpretation and discussion
This means that in the model the observation of a wave of agitation is merely due to the changing orientation of the bird during the zigzag manoeuvre. When rolling sideward in the zigzag, we temporarily observe a larger surface of the wing. This causes us to perceive a dark band moving over the flock. This is similar to what we observe during a wave of agitation in dunlins under attack (Potts 1984). During a wave in dunlins, the flock colour changes also, because the back of a dunlin is dark in colour and its belly is light. So the wave of agitation in dunlins is due to a zigzag of rolling sideward on one side and then on the other side.
Since the speed of the agitation waves was reproduced when birds in the model repeated escape manoeuvres of only their single closest neighbour up to their seven closest neighbours, birds do no need to anticipate the wave over a longer range. This contrasts with previous ideas that anticipation over a longer range is needed (Potts 1984).
The main predictions of our model, StarDisplay, are that also in real flocks of Starlings
- the agitation wave is due to changes of orientation of the individual Starlings (zigzag-like manoeuvre) rather than due to changes in flock density.
- the speed of the wave results from the repetition by individual Starlings of the escape-manoeuvre from one up to seven of their closest neighbours (without anticipation over a longer range).Other predictions can be found in the paper. Whether these predictions hold for real Starlings, needs to be studied empirically.
References and/or further reading
Ballerini, M., Cabibbo, N., Candelier, R., Cavagna, A., Cisbani, E., Giardina, I., Lecomte, V., Orlandi, A., Parisi, G., Procaccini, A., Viale, M. & Zdrakoviv, V. 2008 Interaction ruling animal collective behaviour depends on topological rather than metric distance: evidence from a field study. P. Natl. Acad. Sci. USA. 105, 1232-1237. View
Gerlotto, F., Bertrand, S., Bez, N. & Gutierrez, M. 2006 Waves of agitation inside anchovy schools observed with multibeam sonar: a way to transmit information in response to predation. ICES J. Mar. Sci. 63, 1405-1417. View
Hemelrijk, C. K. & Hildenbrandt, H. 2011 Some causes of the variable shape of flocks of birds. PLoS ONE. 6, e22479. View
Hemelrijk, C. K. & Hildenbrandt, H. 2012 Schools of fish and flocks of birds: their shape and internal structure by self-organization. Interface Focus 2, 726-737. View
Hemelrijk, C. K. & Hildenbrandt, H. 2015a Diffusion and topological neighbours in flocks of Starlings: relating a model to empirical data. PLoS ONE, 10(5), e0126913. doi:10.1371/journal.pone.0126913 View
Hemelrijk, C. K. & Hildenbrandt, H. 2015b Scale-Free Correlations, Influential Neighbours and Speed Control in Flocks of Birds. Journal of Statistical Physics 158, 563-578. View
Hildenbrandt, H., Carere, C. & Hemelrijk, C. K. 2010 Self-organized aerial displays of thousands of starlings: a model. Behav Ecol. 21, 1349-1359 doi:10.1093/beheco/arq149. View
Hemelrijk, C. K., van Zuidam, L. & Hildenbrandt, H. 2015 What underlies waves of agitation in starling flocks. Behavioural Ecology and Sociobiology. 69, 755-764. View
Potts, W. K. 1984 The chorus-line hypothesis of manoeuvre coordination in avian flocks. Nature. 309, 344-345. View
Procaccini, A., Orlandi, A., Cavagna, A., Giardina, I., Zoratto, F., Santucci, D., Chiarotti, F., Hemelrijk, C. K., Alleva, E., Parisi, G. & Carere, C. 2011 Propagating waves in starling, Sturnus vulgaris, flocks under predation. Anim. Behav. 82, 759-765. View
Top image: Peregrine Falcon attacking Starling flock by © Nick Dunlop
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