Abstract
A great diversity of adaptations is found among animals with compound eyes and even closely related taxa can show variation in their light-adaptation strategies. A prime example of a visual system evolved to function in specific light environments is the fiddler crab, used widely as a model to research aspects of crustacean vision and neural pathways. However, questions remain regarding how their eyes respond to the changes in brightness spanning many orders of magnitude, associated with their habitat and ecology. The fiddler crab Afruca tangeri forages at low tide on tropical and semi-tropical mudflats, under bright sunlight and on moonless nights, suggesting that their eyes undergo effective light adaptation. Using synchrotron X-ray tomography, light and transmission electron microscopy and in vivo ophthalmoscopy, we describe the ultrastructural changes in the eye between day and night. Dark adaptation at dusk triggered extensive widening of the rhabdoms and crystalline cone tips. This doubled the ommatidial acceptance angles and increased microvillar surface area for light capture in the rhabdom, theoretically boosting optical sensitivity 7.4 times. During daytime, only partial dark-adaptation was achieved and rhabdoms remained narrow, indicating strong circadian control on the process. Bright light did not evoke changes in screening pigment distributions, suggesting a structural inability to adapt rapidly to the light level fluctuations frequently experienced when entering their burrow to escape predators. This should enable fiddler crabs to shelter for several minutes without undergoing significant dark-adaptation, their vision remaining effectively adapted for predator detection when surfacing again in bright light.
Highlights
Many terrestrial animals must cope with light levels that vary from bright sunny skies to moonless nights a billion times dimmer (Warrant, 1999)
Several different light- and dark-adaptation strategies have been described among members of the arthropods, the most successful animal phylum, which occupy an enormous diversity of visual niches on land (Stansbury & Moczek, 2013)
Fiddler crabs provide an excellent model for studying adaptations to light level fluctuations as they have evolved to forage during both the day and night, can be found in dense colonies on their mudflat habitats, and make a robust laboratory animal
Summary
Many terrestrial animals must cope with light levels that vary from bright sunny skies to moonless nights a billion times dimmer (Warrant, 1999). From our own observations (Figure 1) during breeding periods, males continue to wave their major chelipeds for at least 2 hr after sunset, a behavior used to visually signal to potential mates (Oliveira & Custódio, 1998) This suggests that effective vision is possible in very dim light and led us to the hypothesis that this species undergo considerable adaptation between day and night to cope with the large changes in available light levels, spanning 10 orders of magnitude. Focussing a camera deeper within the eye on the distal tip of the fused rhabdom of an apposition eye produces a superimposed image of the combined apertures of several neighboring ommatidia (Ro & Nilsson, 1993) This is known as the “deep pseudopupil,” the centre of which is dark due to the light-absorbing central rhabdoms, surrounded by a ring of more reflective screening pigment cells. The samples were infiltrated and embedded in EPON resin blocks and polymerized in an oven (60C for 48 hr)
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