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Visual Odometry in the Wolf Spider Lycosa Tarantula

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Visual Odometry in the Wolf Spider Lycosa Tarantula © 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 395-401 doi:10.1242/jeb.091868 RESEARCH ARTICLE Visual odometry in the wolf spider Lycosa tarantula (Araneae: Lycosidae) J. Ortega-Escobar1,* and M. A. Ruiz1 ABSTRACT insects were trained in one channel and tested in a different one in The wolf spider Lycosa tarantula homes using path integration. The which the relevant stimuli had been changed, or some insect body angular component of the displacement is measured using a parts modified. Several hymenopteran species have been studied polarized-light compass associated with the functioning of the anterior using this method not only in relation to odometry but also with median eyes. However, how L. tarantula estimates the linear regard to the visual control of flight speed. Among the species component of the displacement was not known prior to this studied are honeybees (Apis mellifera) either walking (Schöne, investigation. The ability of L. tarantula to gauge the distance walked 1996) or flying (Baird et al., 2005; Dacke and Srinivasan, 2007; after being displaced from its burrow was investigated using Esch et al., 2001; Si et al., 2003; Srinivasan et al., 1997; Srinivasan experimental channels placed in an indoor setup. Firstly, we and Zhang, 2004), bumblebees (Bombus terrestris) (Baird et al., manipulated the perception of visual stimuli by covering all the 2010), stingless bees (Melipona seminigra) (Hrncir et al., 2003; spider’s eyes. Secondly, we changed the optic flow supplied by a Eckles et al., 2012) and desert ants [Cataglyphis fortis (Ronacher black-and-white grating (λ=2 cm) perceived either in the lateral or in and Wehner, 1995; Ronacher et al., 2000; Sommer and Wehner, the ventral field of view. Finally, the period of the lateral or ventral 2004; Steck et al., 2009; Wittlinger et al., 2007; Wohlgemuth et al., grating was changed from λ=2 cm to λ=1 cm. Our results indicate that 2002) and Melophorus bagoti (Narendra, 2007; Narendra et al., visual information contributes to distance estimation because when 2007; Narendra et al., 2008; Schwarz and Cheng, 2011; Schwarz et the spider’s eyes were covered, the spiders tended to search for the al., 2012)]. burrow at very variable distances. This visual information is created There have only been a few studies carried out on spiders using by the motion of the image as the spider walks, the motion in the channels to investigate aspects of their orientation. Seyfarth and lateral field of view being the most important. The preference of a colleagues (Seyfarth et al., 1982) investigated how the wandering lateral optic flow over the ventral flow can be explained by the spider Cupiennius salei estimated the distance to a goal, in this case difference in the resolution capacity of the posterior lateral eyes and some prey, when the spiders were moved away either rectilinearly the anterior lateral eyes. or through a semicircular corridor. All the spiders were blinded and divided into two groups: one group in which the lyriform organs KEY WORDS: Orientation, Spiders, Optic flow (cuticular proprioceptors) on all leg femora had been surgically removed and one group of intact spiders. The intact spiders did not INTRODUCTION retrace their steps but walked back following a multiple-step The wolf spider Lycosa tarantula (Linnaeus 1758) (Araneae, trajectory that took them near to the point where they had abandoned Lycosidae) homes by means of path integration. This mechanism the prey, and when they were near to their goal they made a Turner’s implies the measurement of angular and linear displacement. Under loop as has been described in desert ants (Turner, 1907; Wehner and natural conditions, the angular component of this displacement is Srinivasan, 1981). The operated spiders had similar multiple-step measured using a polarized-light compass, which is associated with trajectories but most of them did not return to their starting point. the functioning of the anterior median eyes (Ortega-Escobar and Regarding odometry, the distance estimated by the experimental Muñoz-Cuevas, 1999). Under indoor conditions, we (Ortega- animals (all of which were blinded) remained quite accurate, Escobar, 2002b; Ortega-Escobar, 2006) have shown that this spider suggesting that no visual input was necessary to gauge the distance needs some visual input for the integration of the angular component walked. Reyes-Alcubilla and colleagues (Reyes-Alcubilla et al., and that this input is only obtained through its anterior lateral eyes 2009) in their study of the wolf spider L. tarantula, used (ALEs). When the visual structure of the substratum (black-and- longitudinal channels to investigate the influence of active versus white grating) was rotated by 90deg, there was a significant passive displacement, and the presence or absence of a visual dispersion of the directional bearings (Ortega-Escobar, 2011) that landmark near the burrow, on the distance walked. After active was prevented when the ALEs were masked, although masking the displacement, and without a visual landmark, the spiders walked a other eyes had no effect. Therefore, it would appear that the angular mean distance of 27.6±9.3 cm (the burrow was 30 cm from the point component of the displacement seems to be processed through only of release). The authors deduced that L. tarantula could gauge the one of the four pairs of eyes, i.e. the ALEs. distance from the burrow by idiothetic information and that The use of linear displacement in homing (odometry) has been changing a visual landmark placed near the burrow had no effect on analyzed in several flying or walking insects, using channels of the search density distributions. However, they did not study the different lengths and visual textures. In these investigations, the effect of blinding the spiders on their estimate of distance, or what would happen if the self-induced optic flow perceived by the spiders 1Faculty of Psychology, University Autónoma of Madrid, 28049-Madrid, Spain. was changed. In this study, we analyzed the effect of temporarily blinding all *Author for correspondence ([email protected]) the eyes of the spider L. tarantula on the distance walked. This was Received 31 May 2013; Accepted 25 September 2013 carried out in order to ascertain whether the information was gauged The Journal of Experimental Biology 395 RESEARCH ARTICLE The Journal of Experimental Biology (2014) doi:10.1242/jeb.091868 Exp. 1 Exp. 2 Exp. 3 Exp. 4 Exp. 5 Fig.1. Turning points of inbound searches by 50 spiders. Data are shown for Lycosa tarantula in the ***** control (‘all eyes’) and ‘no eyes’ conditions, and in the different channels with gratings in the walls or 40 substratum. Boxes show medians and interquartiles, whiskers correspond to the extreme values and circles represent outliers. *Significant difference 30 (P<0.05). The dashed line at 30cm indicates the position of the virtual burrow; vertical dashed lines 20 separate different experiments. Each experiment is summarized by two boxes, the one on the left corresponding to the control condition and the one 10 on the right corresponding to the experimental Turning point (cm) Turning condition. 0 –10 No grating All eyes No eyes Frequency: λ=2 λ=2 λ=2 λ=2 λ=2 λ=1 λ=2 λ=1 Grating: Longitudinal Cross Longitudinal Cross Cross Cross Cross Cross Position: Walls Substratum Walls Substratum solely by idiothetic means. We also modified the self-induced optic which the spiders walked through the central part of the channel flow perceived either laterally or ventrally, to investigate the effect were not observed. Spiders made their inbound path in a multiple- of this modification on the odometry of the spider and to ascertain step trajectory, i.e. they walked, stopping several times until whether this modification was important in both fields of view as performing either the return loop or the search patterns. The perceived by different eyes. locomotive behavior of the spiders with covered eyes was similar to that of the same animals when their eyes were uncovered; the RESULTS homeward path was a multiple-step trajectory in contact with a wall Figs 1 and 2 represent, for all experiments and experimental that included crossings from one wall to the other (Fig. 3, ‘no eyes’ conditions, the central tendency (median) and dispersion condition). The spiders did not make exploratory leg movements (interquartile range) of the distance walked and latency period, during displacement. respectively. The spiders with all their eyes uncovered walked a mean distance before turning or searching of 26.5±11 cm (t79=–2.87, P<0.05) but Experiment 1: does the spider need visual information to when their eyes were covered the mean distance was 18.4±18.8 cm gauge the distance walked? (t79=–5.55, P<0.001). As can be seen in Fig. 1, there was more This experiment was used as a control because there was no variation in the distance to the searching movements or turning point information available as to the kind of behavior L. tarantula would when the spiders had all their eyes covered (‘no eyes’ condition). exhibit in the absence of visual information to estimate the distance Sometimes they did not turn and therefore walked away from the walked. Initially, odometry was studied using spiders whose eyes virtual burrow, which suggests that the proprioceptive information were uncovered and consequently had complete visual information. was insufficient for them to be able to return to the virtual burrow. Subsequently, this experiment was repeated using the same spiders Spiders with uncovered eyes were also observed to continue but with their eyes masked. The animals were submitted to 10 trials walking in the same direction they were walking in when taken from with all their eyes uncovered; they were moved a distance of 30 cm the spider channel, although this was a very small proportion when away from their burrow, placed in a clear glass cup and transferred compared with the ‘no eyes’ condition (0.06% and 25%, to the test channel.
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