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Mechanisms of Homing in the Fiddler Crab Uca Rapax

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Mechanisms of Homing in the Fiddler Crab Uca Rapax The Journal of Experimental Biology 206, 4425-4442 4425 © 2003 The Company of Biologists Ltd doi:10.1242/jeb.00661 Mechanisms of homing in the fiddler crab Uca rapax 2. Information sources and frame of reference for a path integration system John E. Layne*, W. Jon P. Barnes and Lindsey M. J. Duncan Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, Scotland, UK *Author for correspondence at present address: Department of Entomology, Cornell University, Ithaca, NY 14853, USA (e-mail: [email protected]) Accepted 11 August 2003 Summary Fiddler crabs Uca rapax are central-place foragers, the digitized paths of the real crabs. The home vector making feeding excursions of up to several meters from computed by the model crab was then compared to the their burrows. This study investigates the sources of homing direction observed in the real crab. The model directional and distance information used by these crabs home vector that most closely matched that of the real when returning to their burrows. We tested the spatial crab was taken to comprise the path integration frame of reference (egocentric or exocentric), and the mechanism employed by fiddler crabs. The model that source of spatial information (idiothetic or allothetic) used best matched the real crab gained direction and distance during homing. We also tested which components of their idiothetically (from internal sources such as locomotion they integrated (only voluntary, or voluntary proprioceptors), and integrated only voluntary plus reflexive). locomotory information. Fiddler crabs in their natural mudflat habitat were Crabs were also made to run home across a patch of wet passively rotated during normal foraging behavior using acetate, on which they slipped and were thus forced to experimenter-controlled disks, before they returned home. take more steps on the homeward path than theoretically Crabs resisted passive rotations on the disk by counter- required by the home vector. Crabs whose running rotating when the disk turned, which was a compensatory velocity across the patch was unusually low also stopped response to unintended movement. Crabs were usually short of their burrow before finding it. Crabs whose situated eccentrically on the disk, and therefore were also running velocity was not impeded by the patch did not subjected to a translation when the disk rotated. No crab stop short, but ran straight to the burrow entrance, as did actively compensated for this translation. Crabs that fully control crabs that ran home with no slippery patch. We compensated for disk rotation made no directional homing interpret this to mean that the velocity of some crabs was error. Crabs that did not fully compensate homed in a impeded because of slipping, and these therefore stopped direction that reflected their new body orientation. In short of their burrow after having run out their homing other words, if we succeeded in reorienting a crab (i.e. it vector. This is positive evidence in support of the undercompensated for disk rotation), its homing error hypothesis that path integration is mediated either by leg was equal to the angle by which it had been reoriented, proprioceptors or by efferent commands, but our data do regardless of the magnitude of the optomotor not allow us to distinguish between these two possibilities. compensation. Computer-modelled crabs, each equipped with a path integrator utilizing different combinations of external Key words: fiddler crab, Uca rapax, path integration, homing, spatial (allothetic) and path-related (idiothetic) input, traversed orientation, optomotor response, central-place forager. Introduction In order to return to a place they have previously visited, current location with the goal (for example reviews, see many animals use a form of coding of their movements, called Schöne, 1984; Gallistel, 1990; Papi, 1990, 1992; Wehner, path integration by Mittelstaedt and Mittelstaedt (1980), 1992; Maurer and Seguinot, 1995; Etienne et al., 1996; wherein information arising from the animal’s own movement Benhamou and Poucet, 1996; Wehner, 1996; Benhamou, 1997; is used to update the animal’s memory of its position Healy, 1998; Capaldi et al., 1999; Giurfa and Capaldi, 1999; continuously in the form of a vector joining the animal’s Redish, 1999; Collett and Collett, 2000). Thus a desert ant, 4426 J. E. Layne, W. J. P. Barnes and L. M. J. Duncan having reached a feeding site over 100·m from home after egocentric home vector (see Benhamou et al., 1990). In any following a sinuous path several hundred meters long, is able, case, this categorization of the source of sensory information using path integration, to return home in a straight line marks the starting point for the study of the sense organs (Wehner and Wehner, 1990). involved, from which point work on the neurophysiology of To understand how an animal homes – that is, returns to a path integration can proceed. place previously visited – there are two pre-eminent questions Homing in fiddler crabs is of particular interest for a number to be answered. First, what is the frame of reference – of reasons. They are central-place foragers with a uniquely egocentric or exocentric – in which the goal location is strong attachment to their point of reference (von Hagen, 1967; encoded? There is ambiguity in the literature about what Land and Layne, 1995; Zeil, 1998; Layne et al., 2003). Indeed, constitutes egocentric and exocentric reference systems they maintain a fairly rigid orientation relative to it by pointing (Etienne et al., 1999). Path integration was originally the transverse axis of their body more or less towards home formulated in exocentric coordinates (Mittelstaedt and throughout their foraging excursions. Thus, for the study of Mittelstaedt, 1973); it might conceivably be encoded that way, homing, fiddler crabs are exceptional in that they may not have and this can be explicitly tested (Benhamou, 1997). A defining to return home in order to give an observer a read-out of their feature of an egocentric reference system is that the home notion of the direction of home. They also have an unusual vector is head-referred, that is, the goal direction is at all times mode of locomotion in that, like most other crabs, they can specified by an angle relative to the animal’s head or walk in virtually any direction relative to their body axis. anterior/posterior body axis. This does not preclude the use of Therefore, a change in direction of travel can be effected by a an external compass for estimating changes in direction during change in walking direction, with no body turn necessary an excursion, which may then be integrated to update the head- (Barnes, 1990). This gives them an additional degree of referred direction of home without reference to the absolute freedom compared to forward-walking animals, but also compass direction. In contrast to this, in an exocentric frame additional sensory information that must be integrated. of reference (also called geocentric, allocentric or earth-bound) Path integration appears to be the principal mode of homing the goal location is specified in terms of its relation to, for in all fiddler crabs during their short-range foraging excursions. instance, the spatial layout of landmarks in the region of the However, evidence for the cues relevant to this task is largely goal, or by a home vector whose direction is specified by an inconclusive or incomplete (Vannini and Cannicci, 1995), and angle relative to the sun’s azimuth or to arbitrary earth-bound we are still largely ignorant of the sensory systems involved. axes, regardless of the current orientation of the animal’s head. The fact that all fiddler crab species tested ignore landmarks An effective way to distinguish between ego- and exocentric near their burrows when displaced a short distance (von Hagen, systems, then, is to passively rotate animals in the presence of 1967; Zeil, 1998; Cannicci et al., 1999; Layne et al., 2003) stationary external cues, or in the dark if the animals are also suggests that the relevant spatial information does not include known to utilize exocentric landmarks. The home vector local landmarks. However, it may still include global cues, (generated under the particular experimental conditions) is such as the sun, and it has been suggested that fiddler crabs use truly egocentric if the animals make a directional homing error an exocentric compass to maintain body orientation (Zeil, equal to the amount by which they were rotated. This approach 1998). This indicates not only that they might utilize allothetic can be confounded if the animals sense and integrate passive direction information, but it also raises the question of whether rotations, for instance via the vestibular system (Etienne, 1980; the home vector direction might be coded with respect to the Etienne et al., 1986). The apparent ‘internal compass’ resulting same exocentric cue. from this integration does not indicate a true absolute reference The present paper is devoted to identifying fiddler crabs’ or compass, however, but rather a sensitive integration spatial frame of reference (exo- or egocentric), and their apparatus, which can be overcome if the animals are rotated at sources of spatial information (allo- or idiothetic) using two low angular velocities (Mittelstaedt and Mittelstaedt, 1980, types of experiment: passive rotation, and running on a 1982). slippery patch where distance covered per step was often The second question to be answered, irrespective of whether reduced. In the former, we passively reoriented the crabs the frame of reference is egocentric or exocentric, is what is relative to their natural surroundings, and observed their the source of spatial information used to compute the home attempts to return home. Specific hypotheses about the vector? This may be idiothetic or allothetic, depending on information used in path integration were tested by digitally, whether the spatial information to be integrated is internal or recursively reconstructing the paths while altering or removing external, respectively, to the animal.
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