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Self-derived chemical cues support home refuge recognition in the whip spider Phrynus marginemaculatus (Amblypygi: Phrynidae).

Arthropods, as a group, are surprisingly skilled navigators (Cheng 2012; Perry et al. 2013; Ortega-Escobar & Ruiz 2014). For instance, tropical whip spiders (Class Arachnida: Order Amblypygi) navigate considerable distances at night in structurally dense rain forests, where, after a nighttime of activity, they consistently return to their daytime refuges located in tree crevices, cliff fissures or under rocks (reviews by Weygoldt 2000; Santer & Hebets 2011; Chapin & Hebets 2016). Displacement experiments in the field revealed that, unlike most studied invertebrates, whip spider navigation does not depend on path integration (Beck & Gorke 1974; Hebets et al. 2014b; Bingman et al. 2017). Instead, whip spiders are hypothesized to rely on multimodal sensory cues to navigate successfully and olfaction is hypothesized to be involved (Wiegmann et al. 2016).

Field experiments suggest that whip spider navigation is supported by olfactory inputs to their specialized antenniform legs, which are covered with olfactory receptors and contact chemoreceptors (Foelix 1975; Beck et al. 1977; Weygoldt 2000; Foelix & Hebets 2001; Santer & Hebets 2011). Indeed, navigation after displacement is severely hindered when inputs to these receptors are prevented (Hebets et al. 2014a; Bingman et al. 2017). Exactly how chemical cues support navigation by whip spiders has not yet been elucidated and likely varies with the distance of an individual to its shelter. In the current study, we conducted two experiments to determine whether self-deposited chemical cues might be used at the end of a return journey home to facilitate identification of a shelter.

Test subjects were Phrynus marginemaculatus C.L. Koch, 1840 collected in Florida (Key Deer National Wildlife Refuge, Big Pine Key, Monroe County, FL) and lab-borne progeny of subjects collected in Florida. The sex of subjects was not recorded. In the laboratory, P. marginemaculatus establish rapid fidelity to artificial shelters and can be trained to associate plant-derived odors or tactile cues with access to a shelter (Santer & Hebets 2009; Graving et al. 2017; Wiegmann et al. 2019). Prior to our experiments, individuals were housed semi-communally in a 19 or 38 liter terrarium (30 cm x 19 cm X 20 cm or 50 cm X 25 cm X 30 cm, L X W X H) that contained a coconut fiber substrate and pieces of foam insulation for refuge (FOAMULAR, 1.5 cm thickness). Lab-reared sibs were housed in the same terrarium and were not paired together in either of the experiments. Field collected subjects were assumed to be non-sibs because they were collected remotely from each other. Individuals were fed crickets two times per week and had continual access to water. The room in which individuals were housed--the same room used for experiments--was lit by overhead broad-spectrum fluorescent lights (400-750 nm) set on a 12:12 h light:dark cycle (19:45-07:45 dark phase). Room humidity ranged between 25-65% and temperature ranged between 23-28 [degrees]C.

The first experiment involved n = 17 subjects. Each subject was given a choice between a shelter that contained a piece of filter paper with which it had extensive prior contact, referred to as self-cued filter paper, and a shelter that contained a piece of filter paper that was never in contact with a subject, referred to as blank filter paper. To prepare the self-cued filter paper a subject was housed for five consecutive nights--approximately 120 hours--in a small plastic deli cup (diameter 17.1 cm, height 10.8 cm) that contained a piece of 90 mm diameter filter paper (Whatman 1001-090 Qualitative Circles). A small plastic dish that held a water-laden cellulose sponge for water and humidity was also placed in the container. An identical deli cup, with similarly treated sponge, that contained no subject was simultaneously prepared to create the blank filter paper.

The day after its fifth night in a deli cup, one hour before lights off, a subject was transferred to a circular (diameter 12 cm, height 3 cm) opaque plastic shelter, which was placed in a rectangular acrylic arena with two identical shelters that a subject would later choose between (Fig. 1). Each shelter had a 3 cm X 1 cm (L X H) entrance and a removable lid. The shelters were positioned in an equilateral triangle configuration, with the unoccupied shelters in the middle of the arena such that the entrance of the shelter that held the subject (start shelter) was equidistant from the entrances of the two other shelters (choice shelters). The entrances of the two unoccupied choice shelters were separated by 15 cm, a distance that exceeds the span of the antenniform legs of P. marginemaculatus and, hence, prevented simultaneous contact with the two shelters (Graving et al. 2017). The self-cued filter paper was placed into the bottom of one of the unoccupied shelters and the blank filter paper into the other. The assignment of filter paper to the two unoccupied shelters was determined randomly.

A subject was given 45 minutes after lights-off to freely exit the occupied shelter and, after it exited, that shelter was removed from the arena. If a subject failed to exit the shelter in 45 minutes, we removed the shelter lid and gently coerced it to exit with a small paint brush and removed the shelter. The subject was then allowed to meander around the arena and its location at lights-on was recorded by visual inspection of the shelters. In addition, we video recorded the movements of a sample of n = 12 subjects throughout the night with Swann Alpha Series infrared cameras (model SWDVK-432502).

In this experiment we hypothesized that subjects would preferentially utilize the shelter that contained the self-cued filter paper. We used a one-tailed binomial test to determine whether subjects were more likely to be found at lights-on in the shelter that contained the self-cued filter paper. In laboratory situations where multiple shelters are available, as in this experiment, P. marginemaculatus regularly explore alternative shelters (Santer & Hebets 2009; Graving et al. 2017). Therefore, the digital records of movements of the video recorded subjects were inspected to determine the number of times a subject entered and switched between shelters before lights-on, as well as occupancy times in each of the shelters. We hypothesized that during the night subjects would spend more time in the shelter that contained the self-cued filter paper. We used a one-tailed binomial test to determine whether the majority of subjects spent more time in the self-cued shelter and a one-tailed, paired t test to compare individual differences in shelter occupancy times.

Results of the experiment revealed an affinity of subjects for the shelter that held the self-cued filter paper. Thirteen of the 17 subjects were found in this shelter at lights-on and four were observed in the alternative shelter that contained the blank filter paper (one-tailed binomial test, n = 17, [pi] [less than or equal to] 0.5, P = 0.0245). The 12 video recorded subjects switched between shelters on average 6 [+ or -] 1.6 times in the course of the night and 10 of these subjects spent more time in the self-cued shelter (one-tailed binomial test, n = 12, [pi] [less than or equal to] 0.5, P = 0.0193). The time that these subjects spent in the two shelters was also concordant with our hypothesis. Individuals spent on average X [+ or -] SE = 358 [+ or -] 59 minutes in the shelter that held the self-cued filter paper before lights-on and just 137 6 99 minutes in the alternative shelter that held the blank filter paper. The average difference of occupancy times between the two shelters was 222 6 105 minutes, significantly higher than zero (Fig. 2, S-B). These results suggest that shelter recognition may be facilitated by self-deposited chemical cues.

In our second experiment subjects were given a choice between a shelter that contained a piece of self-cued filter paper and a shelter that contained a piece of filter paper with which a conspecific had contacted, referred to as conspecific-cued filter paper. Ten individuals from the first experiment were arbitrarily selected as test subjects and, as before, subjects were placed into deli cups to generate self-cued filter paper. To generate conspecific-cued filter paper we haphazardly sampled a conspecific from the terrarium in which a test subject was not housed and simultaneously placed it in a deli cup with a piece of filter paper for five nights. The procedures were otherwise identical to those already described. The nocturnal movements of all subjects in the arena were video recorded and we again hypothesized that subjects would preferentially utilize the shelter that contained the self-cued filter paper.

Results of our second experiment revealed no clear affinity of subjects for the shelter that held the self-cued filter paper. Six of the 10 subjects were found in the shelter that contained the self-cued filter paper at lights-on and four subjects were found in the shelter that contained the conspecific-cued filter paper (one-tailed binomial test, n = 10, [pi] [less than or equal to] 0.5, P = 0.3770). Video records revealed that subjects switched between the shelters 12 6 1.7 times on average before lights-on and that the time subjects spent in the two shelters was similar. Individuals spent on average X [+ or -] SE = 71 6 97 minutes longer in the shelter that held the self-cued filter paper before lights-on (270 [+ or -] 52) compared to the shelter that contained the conspecific-cued filter paper (200 [+ or -] 49; Fig. 2, S-C). Though not statistically significant, it is notable that eight of the 10 subjects spent more time in the self-cued shelter (one-tailed binomial test, n = 10, [pi] [less than or equal to] 0.5, P = 0.0547).

Displacement experiments with amblypygids in the field suggest that olfactory cues guide return routes from locations that are remote from the refuge site (Beck & Gorke 1974; Hebets et al. 2014a,b; Wiegmann et al. 2016; Bingman et al. 2017). The results of our first experiment suggest that self-deposited chemical cues could support shelter recognition at the end of a nocturnal homing journey, when an individual is in close proximity to its shelter, just as the desert ant Cataglyphis fortis, which uses path integration as its primary navigation strategy, exploits odors emitted from its nest to pinpoint the nest entrance (Steck et al. 2009, 2011). Whether the chemical cue that guided choices in our first experiment was olfactory or chemotactile, however, remains to be determined.

In our second experiment subjects switched repeatedly between shelters and were ultimately as likely to take refuge in the shelter that contained the conspecific-cued filter paper as in the shelter that contained the self-cued filter paper, which suggests prima facie that the chemical cue detected by subjects in the first experiment did not serve as a self-recognition signal. Indeed, a self-recognition cue may be unnecessary for refuge recognition if longer-distance navigation mechanisms are sufficiently accurate and precise because P. margin-emaculatus, like other whip spiders, are largely solitary (Chapin & Hebets 2016). Results of earlier experiments with P. marginemaculatus revealed, however, that males are able to recognize rivals over an extended time period (Fowler-Finn & Hebets 2006). Likewise, immature Damon diadema (Simon, 1876) can discriminate kin from non-kin and, based solely on olfactory cues, recognize their mother (Walsh & Rayor 2008). These observations suggest that uncontrolled factors in our second experiment, like the sex of focal animals or the sexual receptivity of individuals used to create conspecific-cued filter paper, may have influenced shelter choices and movements between shelters. Further experiments will be necessary to establish whether self-derived chemical cues can be discriminated from conspecific-derived cues and the specific role of self-recognition signals in the identification of a shelter.

ACKNOWLEDGMENTS

This study was supported by a grant from the National Science Foundation to V.P.B. and D.D.W. (IOS-1457304). Animals were collected under U.S. Fish and Wildlife permit FFO4RFKD-2015-06. We are grateful to two anonymous reviewers for helpful comments.

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Patrick Casto (1,2), Jillian Gosser (1,2), Daniel D. Wiegmann (1,2), Eileen A. Hebets (3) and Verner P. Bingman (2,4): (1) Department of Biological Sciences, Bowling Green State University, 1001 East Wooster Street, Bowling Green, OH 43403, USA. E-mail: pcasto@bgsu.edu; (2) J.P. Scott Center for Neuroscience, Mind and Behavior, Bowling Green State University, Bowling Green, OH; (3) School of Biological Sciences, University of Nebraska - Lincoln, Lincoln, NE; (4) Department of Psychology, Bowling Green State University, Bowling Green, OH.

Manuscript received 30 July 2018, revised 26 March 2019.
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Title Annotation:SHORT COMMUNICATION
Author:Casto, Patrick; Gosser, Jillian; Wiegmann, Daniel D.; Hebets, Eileen A.; Bingman, Verner P.
Publication:The Journal of Arachnology
Date:May 1, 2019
Words:2609
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