Comparative biology of spatial navigation in three arachnid orders (Amblypygi, Araneae, and Scorpiones).

From both comparative biology and translational research perspectives, there is escalating interest in understanding how animals navigate their environments. Considerable work is being directed towards understanding the sensory transduction and neural processing of environmental stimuli that guide animals to, for example, food and shelter. While much has been learned about the spatial orientation behavior, sensory cues, and neurophysiology of champion navigators such as bees and ants, many other, often overlooked animal species possess extraordinary sensory and spatial capabilities that can broaden our understanding of the behavioral and neural mechanisms of animal navigation. For example, arachnids are predators that often return to retreats after hunting excursions. Many of these arachnid central-place foragers are large and highly conducive to scientific investigation. In this review we highlight research on three orders within the Class Arachnida: Amblypygi (whip spiders), Araneae (spiders), and Scorpiones (scorpions). For each, we describe (I) their natural history and spatial navigation, (II) how they sense the world, (III) what information they use to navigate, and (IV) how they process information for navigation. We discuss similarities and differences among the groups and highlight potential avenues for future research.

Homing in the arachnid taxa Araneae and Amblypygi.

Adequate homing is essential for the survival of any animal when it leaves its home to find prey or a mate. There are several strategies by which homing can be carried out: (a) retrace the outbound path; (b) use a 'cognitive map'; or (c) use path integration (PI). Here, I review the state of the art of research on spiders (Araneae) and whip spiders (Amblypygi) homing behaviour. The main strategy described in the literature as being used by these arachnids is PI. Behavioural and neural substrates of PI are described in a small group of spider families (Agelenidae, Lycosidae, Gnaphosidae, Ctenidae and Theraphosidae) and a whip spider family (Phrynidae). In spiders, the cues used to detect the position of the animal relative to its home are the position of the sun, polarized light patterns, web elasticity and landmarks. In whip spiders, the cues used are olfactory, tactile and, with a more minor role, visual. The use of a magnetic field in whip spiders has been rejected both with field and laboratory studies. Concerning the distance walked in PI, the possibility of using optic flow and idiothetic information in spiders is considered. The studies about outbound and inbound paths in whip spiders seem to suggest they do not follow the PI rules. As a conclusion, these arachnids' navigation relies on multimodal cues. We have detailed knowledge about the sensory origin (visual, olfactory, mechanosensory receptors) of neural information, but we are far from knowing the central neural structures where sensory information is integrated.

Role of the different eyes in the visual odometry in the wolf spider Lycosa tarantula (Araneae, Lycosidae).

The wolf spider Lycosa tarantula returns home by means of path integration. Previous studies demonstrated: (i) that the angular component of the outbound run is measured using a polarized-light compass associated with the anterior median eyes; (ii) changes in direction of the substratum are detected by the anterior lateral eyes (ALEs); and (iii) in relation to the linear component of the outbound run, an increase of optic flow, in either the lateral or ventral fields of view, caused spiders to search for the burrow at a point nearer to the goal. However, the role of the secondary eyes [ALEs, posterior lateral eyes (PLEs) and posterior median eyes (PMEs)] in the perception of this optic flow and the importance of them for gauging the distance walked is still unknown. In this study, lateral or ventral gratings of wavelength λ=1 cm were used, with two groups of spiders in each setup: (1) PLEs+PMEs covered and (2) ALEs covered. The largest reduction in the distance walked to return to the burrow was observed with the ventral grating/ALEs covered. These results show the importance of the previously neglected ALEs for the visual behavior of these spiders. The possibility of gathering information for locomotion from the three pairs of secondary eyes in the mushroom bodies is discussed.

Anterior lateral eyes of Lycosa tarantula (Araneae: Lycosidae) are used during orientation to detect changes in the visual structure of the substratum.

Previous studies in the wolf spider Lycosa tarantula (Linnaeus 1758) have shown that homing is carried out by path integration and that, in the absence of information relative to the sun's position or any pattern of polarized light, L. tarantula obtains information as to the angle it must turn to home through the anterior lateral eyes (ALEs). In the present study, spiders were trained to walk over a black-and-white grating and afterwards tested either over a white substratum, the same substratum used for training or the same substratum rotated 90 deg (two groups: ALEs covered and only ALEs uncovered; they were tested first without their eyes covered and then with their eyes covered). The directional bearing was measured both in training and test conditions. Under the white or the same substratum in test conditions, the directional bearing had the same mean direction and a distribution similar to that of the training sessions. When the substratum was rotated 90 deg, the directional bearing had the same mean direction but the distribution was significantly different from that of the training sessions. Moreover, if ALEs were covered, spiders behaved as if the substratum had not been rotated and the directional bearing distribution was similar to that of the training sessions. But, if ALEs were the only eyes uncovered, spiders behaved as if no eyes were covered and directional bearing distribution was similar to that of the test condition. It is suggested that, when homing, L. tarantula uses both idiothetic information and visual information gathered through ALEs. These findings present the first evidence that spiders can use the visual structure of the substratum to return home.

Homing in the wolf spider Lycosa tarantula (Araneae, Lycosidae): the role of active locomotion and visual landmarks.

Previous studies on the homing of the wolf spider Lycosa tarantula have shown that it is carried out by path integration. Animals using this mechanism must measure the distance walked and the angles turned. This study aims to understand if wolf spider L. tarantula is able to estimate the walked distance in an outward path. As this information is more likely obtained by proprioceptive mechanisms, active or passive displacements have been performed. An active locomotion was found essential to estimate distances. During passive locomotion, spiders searched for their burrows near the release point while when displaced actively the inbound journey was longer than the outbound one. The possible use of visual landmarks near the burrow was also tested as a cue to complete the inbound journey. Our results did not show that L. tarantula used these visual landmarks to find the burrow. L. tarantula seems to use only proprioceptive information obtained during the outbound path to estimate the distance traveled.