Abstract
Studies on whip spider navigation have focused on their ability to locate goal locations in the horizontal plane (e.g., when moving along the ground). However, many species of tropical whip spiders reside and move along surfaces in the vertical plane (e.g., trees). Under controlled laboratory conditions, the current study investigated the ability of the tropical whip spider, Paraphrynus laevifrons, to return to a home shelter on a vertical surface in the presence of numerous, similar and competing refuge sites, as well as the distribution of navigational errors in the vertical, horizontal and diagonal plane. We also assessed the relative importance of sensory cues originating from a previously occupied home shelter compared to the position of a previously occupied shelter in guiding shelter choice. It was found that P. laevifrons displays robust fidelity in re-locating a home shelter on a vertical surface. When navigational errors did occur, they were not significantly different in all three directions. Additionally, cue-conflict test trials revealed that cues associated with an original home shelter, likely self-deposited chemical signals, were more important than sources of positional information in guiding the shelter choice of P. laevifrons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Barth FG (2002) Proprioreception. In: Barth FG (ed) A Spider’s World. Springer, Berlin, pp 113–127
Barth FG, Stagl J (1976) The slit sense organs of arachnids: a comparative study of their topography on the walking legs (Chelicerata, Arachnida). Zoomorphology 86:1–23
Beck L, Görke K (1974) Tagesperiodik, Revierverhalten und Beutefang der Geisselspinne Admetus pumilio CL Koch. Im: Freiland. Zeitschrift für Tierpsychologie 35(2):173–186. https://doi.org/10.1111/j.1439-0310.1974.tb00442.x
Bingman VP, Graving JM, Hebets EA, Wiegmann DD (2017) Importance of the antenniform legs, but not vision, for homing by the neotropical whip spider Paraphrynus laevifrons. J Exp Biol 220(5):885–890. https://doi.org/10.1242/jeb.149823
Brandt T, Dieterich M (2013) "Right Door," wrong floor: a canine deficiency in navigation. Hippocampus 23(4):245
Buehlmann C, Graham P, Hansson BS, Knaden M (2015) Desert ants use olfactory scenes for navigation. Anim Behav 106:99–105. https://doi.org/10.1016/j.anbehav.2015.04.029
Casali G, Bush D, Jeffery K (2019) Altered neural odometry in the vertical dimension. Proc Natl Acad Sci USA 116(10):4631–4636. https://doi.org/10.1073/pnas.1811867116
Casto P, Gosser J, Wiegmann DD, Hebets EA, Bingman VP (2019) Self-derived chemical cues support home refuge recognition in the whip spider Phrynus marginemaculatus (Amblypygi: Phrynidae). J Arachnol 47(2):290. https://doi.org/10.1636/JoA-S-18-067
Chapin KJ (2014) Microhabitat and spatial complexity predict group size of the whip spider Heterophrynus batesii in Amazonian Ecuador. J Trop Ecol 30(02):173–177. https://doi.org/10.1017/S0266467413000850
Chapin KJ (2015) Cave-epigean behavioral variation of the whip spider Phrynus longipes (Arachnida: Amblypygi) evidenced by activity, vigilance, aggression. J Arachnol 43(2):214–219. https://doi.org/10.1636/J15-04
Chapin KJ, Hebets EA (2016) The behavioral ecology of amblypygids. J of Arachnol 44(1):1–14. https://doi.org/10.1636/V15-621
Cheng K (2012) Arthropod navigation: ants, bees, crabs, spiders finding their way. In: Zentall TR, Wasserman EA (eds) The Oxford handbook of comparative cognition. Oxford Univ Press, Oxford, pp 347–365
Cheng K, Middleton EJT, Wehner R (2012) Vector-based and landmark-guided navigation in desert ants of the same species inhabiting landmark-free and landmark-rich environments. J Exp Biol 215(18):3169–3174. https://doi.org/10.1242/jeb.070417
Collett M (2010) How desert ants use a visual landmark for guidance along a habitual route. Proc Natl Acad Sci USA 107(25):11638–11643. https://doi.org/10.1073/pnas.1001401107
Corey TB, Hebets EA (2017) Microhabitat use in the amblypygid Paraphrynus laevifrons. J Arachnol 45(2):223–230. https://doi.org/10.1636/JoA-S-16-0551
Davis VA, Holbrook RI, Burt de Perera T (2018) The influence of locomotory style on three-dimensional spatial learning. Anim Behav 142:39–47. https://doi.org/10.1016/j.anbehav.2018.06.002
Davis VA, Holbrook RI, Schumacher S, Guilford T, Burt de Perera T (2014) Three-dimensional spatial cognition in a benthic fish Corydoras aeneus. Behav Proc 109(Pt B):151–156. https://doi.org/10.1016/j.beproc.2014.08.011
de Armas LF, Víquez C (2001) Nueva especie de Phrynus (Amblypygi: Phrynidae) de Costa Rica Rica. Rev Ibér Aracnol 4:11–15
Foelix RF, Hebets E (2001) Sensory Biology of Whip Spiders (Arachnida, Amblypygi). Andrias 15:129–140
Freas C, Wystrach A, Narendra A, Cheng K (2018) The view from the trees: Nocturnal bull ants, myrmecia midas, use the surrounding panorama while descending from trees. Front Psychol 9:16. https://doi.org/10.3389/fpsyg.2018.00016
Graham P, Cheng K (2009) Which portion of the natural panorama is used for view-based navigation in the Australian desert ant? J Comp Physiol A 195:681–689. https://doi.org/10.1007/s00359-009-0443-6
Grieves RM, Jedidi-Ayoub S, Mishchanchuk K, Liu A, Renaudineau S, Jeffery KJ (2020) The place-cell representation of volumetric space in rats. Nature Commun 11(1):1–13
Grobéty MC, Schenk F (1992) Spatial learning in a three-dimensional maze. Anim Behav 43(6):1011–1020
Hayman R, Verriotis MA, Jovalekic A, Fenton AA, Jeffery KJ (2011) Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat Neurosci 14:1182–1188. https://doi.org/10.1038/nn.2892
Hebets EA (2002) Relating the unique sensory system of amblypygids to the ecology and behavior of Phrynus parvulus from Costa Rica (Arachnida, Amblypygi). Can J Zool 80(2):286–295. https://doi.org/10.1139/z02-006
Hebets EA, Aceves-Aparicio A, Aguilar-Argüello S, Bingman VP, Escalante I, Gering EJ, Nelson DR, Rivera J, Sánchez-Ruiz JÁ, Segura-Hernández L, Settepani V, Wiegmann DD, Stafstrom JA (2014a) Multimodal sensory reliance in the nocturnal homing of the amblypygid Phrynus pseudoparvulus (Class Arachnida, Order Amblypygi). Behav Proc 108(2014):123–130. https://doi.org/10.1016/j.beproc.2014.09.014
Hebets EA, Chapman RF (2000) Electrophysiological studies of olfaction in the whip spider Phrynus parvulus (Arachnida, Amblypygi). J Insect Physiol 46(11):1441–1448. https://doi.org/10.1016/S0022-1910(00)00068-8
Hebets EA, Gering EJ, Bingman VP, Wiegmann DD (2014b) Nocturnal homing in the tropical amblypygid Phrynus pseudoparvulus (Class Arachnida, Order Amblypygi). Anim Cogn 17(4):1013–1018. https://doi.org/10.1007/s10071-013-0718-8
Holbrook RI, de Perera TB (2009) Separate encoding of vertical and horizontal components of space during orientation in fish. Anim Behav 78(2):241–245
Holbrook RI, de Perera TB (2013) Three-dimensional spatial cognition: freely swimming fish accurately learn and remember metric information in a volume. Anim behav 86(5):1077–1083
Hölldobler B, Wilson EO (1990) The ants. Belknap, Cambridge
Hurly TA, Franz S, Healy SD (2010) Do rufous hummingbirds (Selasphorus rufus) use visual beacons? Anim Cogn 13(2):377–383
Jeffery KJ, Jovalekic A, Verriotis M, Hayman R (2013) Navigating in a three-dimensional world. Behav Brain Sci 36(5):523–543
Jeffery KJ, Wilson JJ, Casali G, Hayman RM (2015) Neural encoding of large-scale three-dimensional space—properties and constraints. Front Psychol 6(July):1–12. https://doi.org/10.3389/fpsyg201500927
Jovalekic A, Hayman R, Becares N, Reid H, Thomas G, Wilson J, Jeffery K (2011) Horizontal biases in rats’ use of three-dimensional space. Behav Brain Res 222(2):279–288. https://doi.org/10.1016/jbbr201102035
Nardi D, Newcombe NS, Shipley TF (2011) The world is not flat: can people reorient using slope? J Exp Psychol 37(2):354–367. https://doi.org/10.1037/a0021614
Nieh JC, Contrera FA, Ramı́rez Imperatriz-Fonseca SVL (2003) Variation in the ability to communicate three-dimensional resource location by stingless bees from different habitats. Anim Behav 66(6):1129–1139
Rheinlaender J, Hartbauer M, Römer H (2007) Spatial orientation in the bushcricket leptophyes punctatissima (phaneropterinae; orthoptera): I. phonotaxis to elevated and depressed sound sources. J Comp Physiol A 193(3):313–320. https://doi.org/10.1007/s00359-006-0186-6
Ronacher B (2020) Path integration in a three-dimensional world: the case of desert ants. J Comp Physiol A 206:379–387. https://doi.org/10.1007/s00359-020-01401-1
Santer RD, Hebets EA (2009) Tactile learning by a whip spider, Phrynus marginemaculatus CL Koch (Arachnida, Amblypygi). J Comp Physiol A 195(4):393–399. https://doi.org/10.1007/s00359-009-0417-8
Segovia JMG, Neco LC, Willemart RH (2018) On the habitat use of the neotropical whip spider Charinus asturius (Arachnida: Amblypygi). Zool 35:1–6. https://doi.org/10.3897/zoologia35e12874
Steck K, Hansson BS, Knaden M (2009) Smells like home: Desert ants, Cataglyphis fortis, use olfactory landmarks to pinpoint the nest. Front Zool 6(1):5. https://doi.org/10.1186/1742-9994-6-5
Sumiya M, Fujioka E, Motoi K, Kondo M, Hiryu S (2017) Coordinated control of acoustical field of view and flight in three-dimensional space for consecutive capture by echolocating bats during natural foraging. PLoS ONE 12(1):e0169995
Ulanovsky N (2011) Neuroscience: How is three-dimensional space encoded in the brain. Curr Biol 21(21):R886–R888. https://doi.org/10.1016/j.cub.2011.09.031
Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189(8):579–588. https://doi.org/10.1007/s00359-003-0431-1
Weygoldt P (2000) Whip Spiders (Chelicerata: Amblypygi): their biology, morphology and systematics. Apollo Books, Stenstrup
Wiegmann DD, Moore CH, Flesher NR, Harper ED, Keto KR, Hebets EA, Bingman VP (2019) Nocturnal navigation by whip spiders: antenniform legs mediate near-distance olfactory localization of a shelter. Anim Behav 149:45–54. https://doi.org/10.1016/j.anbehav.2019.01.005
Yartsev MM, Ulanovsky N (2013) Representation of three-dimensional space in the hippocampus of flying bats. Science 340(6130):367–372
Zwergal A, Schöberl F, Xiong G, Pradhan C, Covic A, Werner P, Dieterich M (2016) Anisotropy of human horizontal and vertical navigation in real space: behavioral and PET correlates. Cereb Cortex 26(11):4392–4404
Acknowledgements
We are grateful for financial support from the National Geographic Society and the National Science Foundation (IOS 1457304). The data presented were collected by Meghan E. Moore and submitted in partial fulfillment for the requirements of a Master of Arts degree at Bowling Green State University.
Funding
Funding was provided by a grant from the National Geographic Society and the National Science Foundation (IOS 1457304).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study. Conceptualization—VPB, DDW. Formal Analysis—VPB, DDW, VJC. Writing: PC, DDW, VJC, DN, EAH, VPB. All authors approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Casto, P., Wiegmann, D.D., Coppola, V.J. et al. Vertical-surface navigation in the Neotropical whip spider Paraphrynus laevifrons (Arachnida: Amblypygi). Anim Cogn 23, 1205–1213 (2020). https://doi.org/10.1007/s10071-020-01420-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-020-01420-0