Hermit crabs use vision, olfaction, and eavesdropping to detect potentially available gastropod shells on a natural rocky shore

Abstract

Intertidal marine crustaceans use multimodal cues to find resources, relying most heavily on chemical cues. However, water movement on intertidal shores acts as a sensory stressor, diluting and modifying the direction of waterborne chemicals, which may increase the relative importance of visual cues. We compared the influence of visual cues, chemical cues, and their combination in attracting free-living hermit crabs (Calcinus californiensis) to potentially available shells in shallow natural wave-protected tide pools. We used the tissue of dead gastropods as a chemical cue and clean, varnished shells as a visual cue from the gastropod species whose shell is most preferred by C. californiensis. The visual, chemical, or combined (bimodal) cue was placed in the center of a circular arena. We counted the crabs that entered the arena and classified their behavior into one of three mutually exclusive categories: touching the stimulus, remaining in the arena without reaching the stimulus, or leaving the arena without touching the stimulus. We ranked the quality of each hermit crab's current shell and recorded the time they took to reach the stimulus. Since more than one hermit crab participated in each trial in the field, we explored potential eavesdropping by comparing the time required to reach the stimulus among the first three hermit crabs. Cue type did not affect the number of crabs that entered the arena. However, most hermit crabs that entered the arena reached the chemical and bimodal shell cues; in contrast, with the visual cue alone most crabs remained in the arena without touching the stimulus, and those that touched it took longer to do so. Hermit crabs were more likely to touch the stimuli when a bimodal cue was presented in the arena and when they were in a broken shell (a low-quality refuge). Interestingly, there was only an apparent eavesdropping effect in the unimodal visual cue; subsequent crabs touched the visual stimulus more quickly once a pioneer crab had already touched it. Previous demonstrations that C. californiensis can visually discriminate shells suggest that the reduced number of crabs that touched the visual stimulus and their longer latency to do so was not due to low visual acuity or inability to interpret the image. Rather, it is likely due to the incongruous set of cues (visible shell without odor), which may reduce the perceived value or certainty about the shell, therefore the benefit/risk relationship in the natural environment. Our results highlight the importance of matching chemical sensing with vision as a trigger for decision-making in dynamic and unpredictable environments.