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Development of Site Fidelity in the Nocturnal Amblypygid, <I>Phrynus

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Development of Site Fidelity in the Nocturnal Amblypygid, <I>Phrynus View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by UNL | Libraries University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Eileen Hebets Publications Papers in the Biological Sciences 4-11-2017 Development of site fidelity in the nocturnal amblypygid, Phrynus marginemaculatus Jacob M. Graving Max Planck Institute, Konstanz, [email protected] Verner P. Bingman Bowling Green State University, [email protected] Eileen Hebets University of Nebraska - Lincoln, [email protected] Daniel D. Wiegmann Bowling Green State University, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/bioscihebets Part of the Animal Sciences Commons, Behavior and Ethology Commons, Biology Commons, Entomology Commons, and the Genetics and Genomics Commons Graving, Jacob M.; Bingman, Verner P.; Hebets, Eileen; and Wiegmann, Daniel D., "Development of site fidelity in the nocturnal amblypygid, Phrynus marginemaculatus" (2017). Eileen Hebets Publications. 79. http://digitalcommons.unl.edu/bioscihebets/79 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Eileen Hebets Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Journal of Comparative Physiology A 203 (2017), pp 313–328. DOI 10.1007/s00359-017-1169-5 Copyright © 2017 Springer-Verlag Berlin Heidelberg. Used by permission. Submitted 9 August 2016; revised 2 February 2017; accepted 30 March 2017; published online 11 April 2017. digitalcommons.unl.edu Development of site fidelity in the nocturnal amblypygid, Phrynus marginemaculatus Jacob M. Graving,1,2 Verner P. Bingman,3,4 Eileen A. Hebets,5 and Daniel D. Wiegmann 1,4 1 Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, USA 2 Present Address: Department of Collective Behaviour, Max Planck Institute for Ornithology, Konstanz 78457, Germany 3 Department of Psychology, Bowling Green State University, Bowling Green, OH 43403, USA 4 J.P. Scott Center for Neuroscience, Mind and Behavior, Bowling Green State University, Bowling Green, OH 43403, USA 5 School of Biological Sciences, University of Nebraska- Lincoln, Lincoln, NE 68588, USA Corresponding author — Jacob M. Graving [email protected] ORCID http://orcid.org/0000-0002-5826-467X Abstract Amblypygids are capable of navigation in the complex terrain of rainforests in near complete darkness. Path inte- gration is unnecessary for successful homing, and the alternative mechanisms by which they navigate have yet to be elucidated. Here, our aims were to determine whether the amblypygid Phrynus marginemaculatus could be trained to reliably return to a target shelter in a laboratory arena—indicating goal recognition—and to document changes in behavior associated with the development of fidelity. We recorded nocturnal movements and space use by indi- viduals over five nights in an arena in which subjects were provided with two shelters that differed in quality. The target shelter, unlike the alternative shelter, shielded subjects from light in daylight hours. Individuals consistently exited and returned to a shelter each night and from the third night onward chose the target shelter more often than the alternative shelter. Indeed, on the fifth night, every subject chose the target shelter. This transition was associated with changes in movement and space use in the arena. Notably, the movement features of outbound and inbound paths differed but did not change across nights. Individuals were also characterized by distinct behavioral strategies reflecting candidate homing mechanisms. Keywords: Amblypygid, Arachnid, Navigation, Nocturnal, Homing Introduction that impose difficult spatial, structural, and informa- tional challenges are comparatively unexplored (War- Navigation in arthropods is supported by a variety of rant and Dacke 2010, 2011, 2016; Jeffery et al. 2013; behavioral mechanisms (Papi 1992; Gould 1998; Dyer Baird and Dacke 2016). 1998; Collett and Graham 2004; Collett and Collett In a recent paper, we proposed that amblypygids, 2006; Collett et al. 2013; Cheng 2012; Cheng and Freas also known as whip spiders or tailless whip scorpi- 2015; Knaden and Graham 2016), and the navigational ons, could serve as potential model organisms for the behavior of diurnal, visually-oriented species is par- study of arthropod navigation in complex environments. ticularly well documented (Perry et al. 2013). The ma- These unusual arachnids are distributed worldwide in jority of these study species inhabit generally unclut- the tropics and subtropics (reviewed by Weygoldt 2000; tered environments in which information from one or Harvey 2007; Chapin and Hebets 2016). The majority of more sensory modalities combined with path integra- amblypygid species inhabit rainforests, where, in day- tion is sufficient to locate a goal. In contrast, relation- light hours, they hide in hollow trees, under tree bark ships among the behavioral–sensory mechanisms that or in the crevices of tree buttresses. They emerge af- underlie navigation and orientation in environments ter dusk to forage and return to their shelter before 313 314 Graving et al. in Journal of Comparative Physiology A 203 (2017) dawn. Unlike spiders, amblypygids walk on six legs. those experienced by previously studied, tropical spe- Their anterior pair of legs—no longer used for locomo- cies of amblypygid, although some populations of P. mar- tion—are called antenniform legs. These legs are highly ginemaculatus do inhabit structurally simpler environ- articulated and covered with thousands of mechano- ments. In this paper, our goals were to establish that P. sensory and chemosensory sensilla (Foelix et al. 1975; marginemaculatus can be trained to show shelter-rec- Beck et al. 1977; Santer and Hebets 2011). Field studies ognition behavior in the laboratory that mirrors—on a of Heterophrynus and Phrynus species revealed that in- smaller scale—the navigation behavior of amblypygids dividuals often wander but typically reside in the same in the field, and more importantly, to describe the de- location for weeks or months (Beck and Görke 1974; velopment of shelter fidelity and characterize changes in Weygoldt 1977; Hebets 2002). movement and space use as fidelity to a shelter develops. Beck and Görke (1974) were the first to document the navigational abilities of amblypygids. These researchers Materials and methods captured nine Heterophrynus batesii (a large Amazonian species) when they emerged at night from tree crevices Experimental animals and displaced them distances of 2.5–7.5 m, where they were placed on the ground. Every individual returned In this study, we used a total of 12 adult P. marginemacu- to the tree on which it was captured on the same night latus. We purchased seven wild-caught individuals from that it was displaced. Beck and Görke (1974) also dis- a commercial supplier (Ken The Bug Guy, LLC). The other placed one subject 10 m and observed that it too re- five individuals were collected at the National Key Deer turned sometime between 2 and 5 nights later. Refuge (Big Pine Key, Florida, USA; USFWS Permit Num- More recent nocturnal displacement experiments ber FFO4RFKD-2015-06). In our laboratory, individuals conducted with two Central American species of am- were housed separately in circular plastic deli cups (di- blypygid revealed similar navigational abilities (Hebets ameter × H: 17.1 cm × 10.8 cm) that had a soil substrate et al. 2014a; Bingman et al. 2017). Paraphrynus laevi- and a piece of cardboard egg carton for shelter. frons (misidentified as Phrynus pseudoparvulus in He- Animals were fed live crickets and misted with re- bets et al. 2014a) were displaced distances of 6–9 m verse osmosis water three times per week. The room and tracked with radio transmitters. Subjects typically in which animals were housed was lit with overhead returned in a single night to the tree from which they broad-spectrum fluorescent lights (400–750 nm) set were captured. Additionally, experiments in which P. to a 12:12 h light:dark cycle (15:00–03:00 laboratory pseudoparvulus were displaced to trees from which res- dusk–dawn). We kept animals on this light cycle for idents were removed showed that particular trees do several weeks before the study was conducted. The not act as attractor beacons (Hebets et al. 2014a). Mem- room temperature ranged from 21 to 26 °C and humid- bers of these species are also capable of navigating from ity ranged from 20 to 60%. more challenging displacement distances, at least as far as 25 m, but these journeys usually involve a temporary Experimental design and apparatus residency at another tree or in a burrow (Hebets 2002). These field experiments revealed that path integration, Each subject was placed individually into one of two a navigation strategy used by all studied terrestrial ar- arenas. Each arena contained two shelters that differed thropods, is not necessary for successful navigation by in their level of protection from light in daytime hours amblypygids. How these animals navigate in the dark- and an odor source that was positioned near the better- ness of a nocturnal rainforest and come to recognize shielded shelter. It is important to note that the odor their particular tree remains a biological mystery. source was not used to test a hypothesis of olfactory In this study, we used the species
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