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Behavioral Evidence Illuminating the Visual Abilities of the Terrestrial Caribbean Hermit Crab Coenobita Clypeatus

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Behavioral Evidence Illuminating the Visual Abilities of the Terrestrial Caribbean Hermit Crab Coenobita Clypeatus UCLA UCLA Previously Published Works Title Behavioral evidence illuminating the visual abilities of the terrestrial Caribbean hermit crab Coenobita clypeatus. Permalink https://escholarship.org/uc/item/97x9h2vj Authors Ping, Xiaoge Lee, Ji Sun Garlick, Dennis et al. Publication Date 2015-09-01 DOI 10.1016/j.beproc.2015.06.003 License https://creativecommons.org/licenses/by-nc/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Behavioural Processes 118 (2015) 47–58 Contents lists available at ScienceDirect Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc Behavioral evidence illuminating the visual abilities of the terrestrial Caribbean hermit crab Coenobita clypeatus a,b b b a b,∗ Xiaoge Ping , Ji Sun Lee , Dennis Garlick , Zhigang Jiang , Aaron P. Blaisdell a Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China b Department of Psychology, University of California, Los Angeles, USA a r t i c l e i n f o a b s t r a c t Article history: Hermit crabs hide into shells when confronted with potential dangers, including images presented on a Received 14 November 2014 monitor. We do not know, however, what hermit crabs can see and how they perceive different objects. Received in revised form 26 May 2015 We examined the hiding response of the Caribbean hermit crab (Coenobita clypeatus) to various stim- Accepted 1 June 2015 uli presented on a monitor in seven experiments to explore whether crabs could discriminate different Available online 4 June 2015 properties of a threatening digital image, including color, brightness, contrast, shape and orientation. We found crabs responded differently to expanding circles presented in wavelengths of light corresponding Keywords: to what humans see as red, blue, and green. “Blue” stimuli elicited the strongest hiding response (Experi- Color Discrimination ments 1, 2, & 7). “Blue” was also more effective than a gray stimulus of similar brightness (Experiment 3). Habituation Hermit crabs were sensitive to the amount of contrast between a stimulus and its background rather than Hiding response absolute brightness of the stimulus (Experiment 4). Moreover, we did not find evidence that crabs could Shape discriminate orientation (Experiment 6), and mixed evidence that they could discriminate stimulus shape Threat detection (Experiments 5 & 7). These results suggest that the Caribbean hermit crab is sensitive to color features, but not spatial features, of a threatening object presented on a computer screen. This is the first study to use the hiding response of the hermit crab to examine its visual ability, and demonstrates that the hiding response provides a useful behavioral approach with which to study learning and discrimination in the hermit crab. © 2015 Elsevier B.V. All rights reserved. 1. Introduction mainly focuses on hexapods and crustaceans (Avarguès-Weber et al., 2011; Gärtner, 2000). The honeybee (Apis spp.), bumble- Visual perception provides an important source of information bees (Bombus terrestris), stingless bee (Scaptotrigona mexicana), for many animals to find food and mates, detect potential predators parasitoid wasp (Ichneumonidae) and butterflies (Superfamily and threats, and notice changes in their surroundings (Baldwin and Papilionoidea) are found to have the ability to perceive color and Johnsen, 2009; Kinoshita and Arikawa, 2014). Color and shape are shape (Ings et al., 2012; Martínez-Harms et al., 2014; Pérez et al., two reliable and useful dimensions in visual signals. The use of color 2012; Sánchez and Vandame, 2012; Stavenga and Arikawa, 2006 and shape information to make decisions can reduce the uncer- Zhang et al., 2004). tainty in the environment and lead to better behavioral adaptation Most crustaceans possess only one or two photoreceptor types, (Behrens et al., 2007). which are maximally sensitive to blue/green light between 480 nm Color and shape vision have been studied thoroughly in verte- and 540 nm (blue/green sensitive R1-7 cells), while in some species brates, especially in humans (Homo sapiens), many primates, and a secondary set of UV/blue photoreceptors sensitive near to 400 nm pigeons (Colomba livia) (Bovet and Vauclair, 2000; Jacobs, 2013; (UV/violet sensitive R8 cells) could also be found (Marshall et al., Lombardi, 2008). While color and shape vision in invertebrates 1999). However, the stomatopods (mantis shrimps) are found to possess up to 16 different photoreceptor types, which is far exceed- ing any other animal known (Chiao et al., 2009; Thoen et al., 2014). ∗ Crabs use compound eyes to perceive visual signals, which were Corresponding author at: 1285 Franz Hall, Box 951563, Los Angeles, CA 90095- thought to have simple apposition eyes like many species of Crus- 1563, USA. E-mail address: [email protected] (A.P. Blaisdell). tacea, but Nilsson (1988) found that the eyes of many true crabs http://dx.doi.org/10.1016/j.beproc.2015.06.003 0376-6357/© 2015 Elsevier B.V. All rights reserved. 48 X. Ping et al. / Behavioural Processes 118 (2015) 47–58 and hermit crabs work as parabolic superposition eyes by employ- 2. General methods ing imaging optics of a conceptually new kind. Color discrimination is found to be not only possible but widespread among many crab 2.1. Subjects taxa at the retinal level, and the discrimination of colors in these taxa is best between blue and yellow, or yellow and ultraviolet Subjects were medium-sized, experimentally-naïve Caribbean (Leggett, 1979). Among crabs, the visual abilities of fiddler crabs hermit crabs (Coenobita clypeatus) purchased from a local aquar- (Uca spp.) have been most studied, from eye structure, electron ium store. Upon arrival, they were given a minimum of two weeks micrographs, microvillar banding patterns to functional anatomy. to adjust to their new environment. Each crab was marked with a These species are very visual animals which employ a variety of number on the major claw. Crabs were housed in groups of one, visual signals, from claw-waving displays to brilliant body colors two, or four in clear plastic bins (50 cm × 25 cm × 25 cm) lined with (Alkaladi and Zeil, 2014; Detto, 2007; Zeil and Hemmi, 2006), for coconut fiber substrate (Zoo Med Eco Earth). Each tub contained social communication. two ceramic water dishes (one for 1.00% NaCl solution, the other A number of studies suggest that the hermit crab (Paguroidea) for distilled water), a paper plate, and a moist sponge to maintain may also have sophisticated visual abilities. One hermit crab 70% humidity in the bins. Plastic lids covered the bins to maintain species, Pagurus bernhardus, has been found to avoid shells that humidity. Each bin was supplied with Tetrafauna Hermit Crab pel- have the greatest contrast with the background, and choose shells lets and new dishes of fresh and salt water three times per week. that best match the color of their surroundings (Briffa et al., The coconut substrate was checked regularly and replaced if wet to 2008). Another hermit crab, Clibanarius vittatus, can discriminate prevent fungus growth. A heat lamp provided warmth in the room, ◦ between different geometric shapes with equal surface area, and and room temperature was maintained at 25 C. The room was illu- are also found to be more attracted to horizontal rectangles and minated on a 14h/10h day-night schedule and room humidity was less attracted to vertical diamonds (Diaz et al., 1994). maintained at 50–75%. Experimental procedures were conducted Previous studies in our lab have also found that the terres- during the light portion of the cycle. The same subjects partici- trial Caribbean hermit crab (Coenobita clypeatus) shows hiding pated in several experiments, with a minimum interval of 20 days responses to looming visual images (Chan et al., 2010a,b; Stahlman between experiments to allow rest and recovery. et al., 2011). The methods we have employed consist of present- ing visual displays on a monitor designed for human vision to 2.2. Apparatus explore simple learning and attention in the hermit crab. Given that the monitor is designed for human vision, it is unclear The experiment was conducted in a 52 cm × 72 cm × 42 cm open what aspects of the visual display the hermit crabs are sensitive field on a desk surrounded by white wooden planks in a large room to. The aim of the experiments reported below was to explore (3.7 m × 6.1 m × 2.4 m) lit by two incandescent ceiling lights. Room the aspects of the stimuli we typically use, especially color and lights were turned off during experimental procedures. We used shape, that the hermit crabs in our experiments can detect and a 43 cm Dell LCD monitor (1704FPVt) set at 1024 × 768 resolution discriminate. to present the visual stimulus. The monitor was set at the default To study hermit crab visual characteristics with the computer factory settings in all parameters unless otherwise specified. All monitor, we presented expanding (threatening) images in seven experimental manipulations of the display and recording of sub- experiments utilizing the procedures previously developed in our ject response were conducted using Visual Basic 6.0 (Microsoft, laboratory. An expanding image on the monitor is perceived as Redmond, CA, USA). The crab was secured with ArtMinds Crafty threatening and causes the crab to hide in its shell. Unpublished Tack Putty onto a 5.5 cm tall pedestal that was positioned 28.5 cm experiments from our lab reveal that neither the movement of a in front of the LCD monitor. Two Logitech webcams (C250) were visual image across the screen (e.g., from left to right), nor the con- used to record all trials. One camera was located 5 cm on the right traction of an image created by reversing the “looming” image so side of the pedestal to serve as a detector camera to monitor and that it appears to be receding, reliably evoke a hiding response from record the subject’s response.
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