Multisensory Control of Homing Behavior of Whip Spiders (Arachnida: Amblypygi)
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MULTISENSORY CONTROL OF HOMING BEHAVIOR IN WHIP SPIDERS (ARACHNIDA: AMBLYPYGI) Patrick E. Casto A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE August 2018 Committee: Daniel D. Wiegmann, Advisor Verner P. Bingman Paul A. Moore © 2018 Patrick E. Casto All Rights Reserved iii ABSTRACT Daniel D. Wiegmann, Advisor Navigation in arthropods has been well studied in terrestrial model organisms such as ants, fiddler crabs, and spiders and there is an emerging understanding that arthropods are much more complex in their spatial abilities than once thought, based on their relatively small nervous systems. Whip spiders (Order Amblypygi) are of interest because, unlike most well-studied terrestrial arthropods, they are nocturnal and live in spatially complex habitats. In addition to the dense terrestrial substrate that creates navigational challenges, navigation at night adds seemingly more adverse conditions for goal-oriented spatial behavior. The integration of multimodal sensory information is hypothesized to facilitate navigation under these conditions, where odor cues are apparently crucial. The goal of this project was to establish a rich dataset of spatial movements of amblypygids under controlled laboratory conditions and determine the relative salience of sensory cues in a multimodal, navigational context. This study used an automated video tracker to record the return paths of amblypygids displaced from a shelter in an arena with a spatially heterogeneous array of sensory cues, where light and odor sources were experimentally manipulated. We found that removal of the light or odor cue did not affect their ability to home to a shelter, but in the absence of the light cue return paths were more circuitous and contained more pauses. Surprisingly, removal of the odor source from the arena had no effect on trajectory kinematics. In addition, our analyses revealed general species differences in return paths. iv ACKNOWLEDGMENTS I would like to thank my committee; Dan Wiegmann, Vern Bingman and Paul Moore for their constructive criticism and clear investment in my academic growth. I thank both Jake Graving, and Martin Heck for their help in learning to code in Python and R. Lacy Arnold, Timothy Huth and Inés Sotelo have been momentous help for their tireless editing of multiple manuscript drafts experimental assistance and unending encouragement. David Gesicki has been an extraordinary help teaching me statistical analyses. I appreciate Vince Coppola for his friendship and help with multiple aspects of the project. Erica Forstater has also been a terrific friend and help. Connie Santangelo was a critical help to the beginning and preliminary stages of the project. Kaylyn Flanigan, Meghan Moore and Brittany Cordova have also been sources of great encouragement and academic conversation. Finally, I am grateful for my family who always have unending faith in me and push me to be better. v TABLE OF CONTENTS Page INTRODUCTION ................................................................................................................. 1 METHODS ............................................................................................................................ 6 Subjects ...................................................................................................................... 6 Experimental Arena ................................................................................................... 6 Procedures…... ........................................................................................................... 7 Return Paths…. .......................................................................................................... 9 Variables……. ........................................................................................................... 10 RESULTS…………… .......................................................................................................... 12 Displacement Trials ................................................................................................... 12 Path Kinematics ......................................................................................................... 13 Homing Path Departure Points .................................................................................. 13 Principal Component Analysis .................................................................................. 14 DISCUSSION………. ........................................................................................................... 16 Homing Ability .......................................................................................................... 16 Sensory Stimuli .......................................................................................................... 16 An Unexpected Result of Visual Control .................................................................. 17 Species Comparisons ................................................................................................. 19 REFERENCES……… .......................................................................................................... 22 APPENDIX A: FIGURES ..................................................................................................... 29 APPENDIX B: TABLES ....................................................................................................... 35 1 INTRODUCTION The ability for animals to navigate their environment is crucial in supporting behavior such as foraging and relocating a safe refuge. Navigation has been studied intensively in a select group of terrestrial arthropods like fiddler crabs, dung beetles, spiders and desert ants (Cheng, 2012; Perry et al., 2013; Ortega-Escobar & Ruiz, 2014, 2017). These animals mostly inhabit open, two-dimensional environments and the strategies they employ for navigation share a number of properties. Fiddler crabs, wolf spiders and desert ants, for instance, often utilize path integration to relocate their refuge where a time-compensated sun compass is used for heading orientation and idiothetic, proprioceptive cues provide directional and distance information as an animal moves through the environment (Mittelstaedt & Mittelstaedt, 1982; Layne et al., 2003a, b; Wehner, 2003; Reyes-Alcubilla et al., 2009; Cheng, 2012). With distance and direction updated during an often-tortuous outward journey, an estimation of an outbound-path’s tangent can lead to a good approximation of the direction and distance back to the nest (Mittelstaedt, 1983, 1985; Collett et al., 1999, Wehner, 2003). Desert ant species of Melophorus live in the semi-arid shrub deserts of Australia where there are more local cues to help guide them when near their nest (Kohler and Wehner, 2005). In these cluttered habitats, alternative navigational strategies appear to have evolved. They follow learned routes, often using local visual landmarks as guides (Bregy et al., 2008; Bühlmann et al., 2011; Collett, 2010; Fleischmann et al., 2016; Merkle & Wehner, 2008; Schwarz & Cheng, 2010; Steck et al., 2011; Ziegler & Wehner, 1997; Wehner, 2003), and fail to successfully navigate when such visual cues are disrupted along the route (Cheng et al., 2009). Nocturnal arthropods are challenged by low light levels which may constrain visually guided navigation. Animals that use polarized light, the skyline panorama, or visual landmarks 2 for navigation are disadvantaged as light decreases (Kelber et al., 2006; Somanathan et al., 2008; Narendra et al., 2013). However, many of these nocturnal arthropods have optical adaptations to compensate for a dark environment (Warrant & Dacke, 2010, 2016; el Jundi et al., 2015; Narendra & Ramirez-Esquivel, 2017). The cursorial wolf spider Lycosa tarantula, for example, has enlarged median eyes that help collect light at night (Reyes-Alcubilla et al., 2009). In the Namib desert, the huntsman spider Leucorchestris arenicola likely recovers enough light from the brightest stars and moonlight by temporal summation, characterized by phases of movement and stillness (Nørgaard et al., 2008). While vision in dark conditions is still possible, many nocturnal animals use other sensory modes like odors emitted from the environment to serve as landmarks in place of a visual landscape (Jacobs, 2012). Indeed, many animals have evolved the ability to track odors at very precise scales (Svensson et al., 2014). Even the desert ant Cataglyphis fortis, which uses path integration as its primary navigation strategy, has been found to use odors emitted from its nest to pinpoint the entrance on a return journey (Steck et al., 2009, 2011). Additionally, recent evidence suggests that C. fortis might use the distribution of odor gradients within near vicinity of its nest in a map-like manner (Steck et al., 2010). For amblypygids—commonly known as whip spiders—olfactory cues appear to guide their spatial behavior at remarkably far distances from a spatial goal. Amblypygi are nocturnal arachnids that are typically found in tropical and subtropical rainforests. They can be observed at the base of the same tree for weeks or months, but intermittently wander distances of 30 m or more from their usual residence before they return several nights later (Beck and Görke, 1974 as cited in Weygoldt, 2000; Weygoldt, 1977a; Hebets, 2002; Hebets et al., 2014a, b). The anterior legs of amblypygids, which are not used for locomotion, are thin and elongated,