2461
INTRODUCTION
The movements of animals and humans are, in many cases, fast,
complex and continuous. Often such behaviour is segregated into
ordered components (Flash and Hochner, 2005; Jenkins and Mataric,
2003; Mussa-Ivaldi and Bizzi, 2000). For example, in the face-
grooming behaviour of mice, distinct movements were identified
and their ordering analysed (Fentress and Stilwell, 1973). In
computer science movement templates are used to recognise human
sign language (Liang and Ouhyoung, 1998) and to analyse the
movements of players in complex simulation games (Thurau and
Hlavac, 2007). Also in robotics or in developing computer games,
simple movements are sequenced to facilitate the generation of
naturalistic locomotion patterns. The common ground for these
examples, which are taken from behavioural analysis, computer-
based recognition and machine motion planning, is the segregation
of complex and continuous behaviour into simple consecutive
building blocks of movement.
In many species a segregation of flight sequences into reoccurring
rotational and translational flight segments has been described
(Bender and Dickinson, 2006; Boeddeker and Hemmi, 2010;
Boeddeker et al., 2010; Collett and Land, 1975a; Eckmeier et al.,
2008; van Hateren and Schilstra, 1999; Mronz and Lehmann, 2008;
Schilstra and van Hateren, 1999; Wagner, 1986). This finding
motivated us to investigate whether the flight manoeuvres of free-
flying hoverflies (Eristalis tenax, Linnaeus) can be segregated into
more detailed consecutive movement components.
We chose hoverflies for our analysis because of their rich
repertoire of extremely fast and virtuosic flight manoeuvres, even
under spatially constrained conditions. They can move in nearly
every direction and their translational velocities range from 10 m s
–1
to an almost total lack of movement in mid-air (hovering) (Collett
and Land 1975a). Moreover, its rather small brain with less than a
million neurons makes Eristalis an interesting model organism for
subsequent neurophysiological experiments in motion vision
(Barnett et al., 2007; Nordström et al., 2008; O’Carroll et al., 1996;
O’Carroll et al., 1997).
We used clustering algorithms to identify movement
components within flight trajectories of Eristalis, which we call
prototypical movements (PMs) in this article. Clustering allows
us to segregate behaviour without having to predefine behavioural
components. Instead, this approach relies on the assumption (1)
that the behavioural data can be represented quantitatively in a
suitable way, and (2) that an appropriate distance measure can be
found that attributes small distances to similar behaviours. Merely
identifying PMs is not sufficient for understanding behavioural
control. In the context of visually guided flight behaviour of
Eristalis, one might also wish to know the rules for the arrangement
of PMs into complex flight trajectories. By calculating transition
probabilities between PMs, such rules may be derived, and can
be regarded as the grammar of a formal language (Chomsky and
Schützenberger, 1963) in which the PMs are treated like an
alphabet. In combination, this grammar and alphabet give us a
syntax of movement.
How variable is this syntax in the real world? In monkeys,
prototypical limb movements elicited by prolonged
microstimulation of the motor cortex are not constant, but vary
depending on the starting positions of the joints (Graziano et al.,
2002; Graziano et al., 2005; Stepniewska et al., 2005). This finding
motivated our investigation of whether PMs of Eristalis also vary
with the situational context. We analysed whether this is the case
for PMs that represent fast rotational movements called saccades.
Saccades are sometimes described or modelled as a fixed motion
pattern, as for example in the fruit fly Drosophila (Mronz and
Lehmann, 2008; Tammero and Dickinson, 2002) or as a flexible
The Journal of Experimental Biology 213, 2461-2475
© 2010. Published by The Company of Biologists Ltd
doi:10.1242/jeb.036079
A syntax of hoverfly flight prototypes
Bart R. H. Geurten
1,
*, Roland Kern
1,2
, Elke Braun
1,2
and Martin Egelhaaf
1,2
1
Neurobiology, Bielefeld University, PO Box 10 01 31, D-33501 Bielefeld, Germany and
2
Center of Excellence ‘Cognitive Interaction
Technology’, Bielefeld University, PO Box 10 01 31, D-33501 Bielefeld, Germany
*Author for correspondence (bart.geurten@uni-bielefeld.de)
Accepted 23 March 2010
SUMMARY
Hoverflies such as Eristalis tenax Linnaeus are known for their distinctive flight style. They can hover on the same spot for several
seconds and then burst into movement in apparently any possible direction. In order to determine a quantitative and structured
description of complex flight manoeuvres, we searched for a set of repeatedly occurring prototypical movements (PMs) and a set
of rules for their ordering. PMs were identified by applying clustering algorithms to the translational and rotational velocities of
the body of Eristalis during free-flight sequences. This approach led to nine stable and reliable PMs, and thus provided a
tremendous reduction in the complexity of behavioural description. This set of PMs together with the probabilities of transition
between them constitute a syntactical description of flight behaviour. The PMs themselves can be roughly segregated into fast
rotational turns (saccades) and a variety of distinct translational movements (intersaccadic intervals). We interpret this
segregation as reflecting an active sensing strategy which facilitates the extraction of spatial information from retinal image
displacements. Detailed analysis of saccades shows that they are performed around all rotational axes individually and in all
possible combinations. We found the probability of occurrence of a given saccade type to depend on parameters such as the
angle between the long body axis and the direction of flight.
Key words: hoverfly, flight behaviour, clustering, syntax, movement segregation, saccades.
THE JOURNAL OF EXPERIMENTAL BIOLOGY