Systematic variations in microvilli banding patterns along fiddler crab rhabdoms

Abstract

Polarisation sensitivity is based on the regular alignment of dichroic photopigment molecules within photoreceptor cells. In crustaceans, this is achieved by regularly stacking photopigment-rich microvilli in alternating orthogonal bands within fused rhabdoms. Despite being critical for the efficient detection of polarised light, very little research has focused on the detailed arrangement of these microvilli bands. We report here a number of hitherto undescribed, but functionally relevant changes in the organisation of microvilli banding patterns, both within receptors, and across the compound eye of fiddler crabs. In all ommatidia, microvilli bands increase in length from the distal to the proximal ends of the rhabdom. In equatorial rhabdoms, horizontal bands increase gradually from 3 rows of microvilli distally to 20 rows proximally. In contrast, vertical equatorial microvilli bands contain 15-20 rows of microvilli in the distal 30 µm of the rhabdom, shortening to 10 rows over the next 30 µm and then increase in length to 20 rows in parallel with horizontal bands. In the dorsal eye, horizontal microvilli occupy only half the cross-sectional area as vertical microvilli bands. Modelling absorption along the length of fiddler crab rhabdoms suggests that (1) increasing band length assures that photon absorption probability per band remains constant along the length of photoreceptors, indicating that individual bands may act as units of transduction or adaptation; (2) the different organisation of microvilli bands in equatorial and dorsal rhabdoms tune receptors to the degree and the information content of polarised light in the environment.

Null point of discrimination in crustacean polarisation vision

“…The horizontal/vertical receptor organisation of the fiddler crab could therefore be adapted for detecting small changes in the degree of polarisation in this region. This could be used for enhancing the contrast of conspecific crabs against the mudflat surface, and could therefore be thought of as a 'matched filter' for this environment (Wehner, 1987;Zeil and Hofmann, 2001;Alkaladi et al, 2013;How and Marshall, 2014). However, there are several sources of non-horizontally polarised cues.…”

“…The Journal of Experimental Biology (2014) doi:10.1242/jeb.103457 the eye, each ommatidial unit is more sensitive to vertically polarised light than to horizontally polarised light (Alkaladi et al, 2013). This would have the consequence of screening out some of the horizontally polarised glare reflected from the mudflat, analogous to the effect of wearing polarised sunglasses.…”

“…This is a process somewhat analogous to colour vision and adds to the well-known uses of the polarisation of light for navigation, orientation and habitat localisation (Wehner, 1976;Schwind, 1983;Labhart and Meyer, 1999). Animals may use this channel to improve the detection of objects through veiling light or glare (Schechner and Karpel, 2005;Alkaladi et al, 2013), to enhance the contrast of transparent prey (Shashar et al, 1998;Tuthill and Johnsen, 2006; but see Johnsen et al, 2011), to break camouflage (Shashar et al, 2000;Jordan et al, 2012;Temple et al, 2012) or to allow the detection of polarised body patterns for communication Marshall et al, 1999).…”

Polarization sensitivity as a visual contrast enhancer in the Emperor dragonfly larva,Anax imperator(Leach, 1815)

“…For example, using an opponent two-channel polarization detector could de-haze an image (Bernard and Wehner, 1977;Tyo et al, 1996). Even more simply, a single-channel detector with a vertically oriented axis would decrease the absorption of horizontally polarized light with an example of this mechanism previously being found in certain regions of the fiddler crab eye, where it is thought to remove the glare from mud flats (Alkaladi et al, 2013). It has also been suggested that a similar mechanism exists in the ventral part of the eyes of pond skaters, Gerris lacustris (Schneider and Langer, 1969), serving to filter glare from the surface of the water.…”

Circular polarization vision in stomatopod crustaceans

“…The rhabdomeric photoreceptors of invertebrates, particularly insects and crustaceans, are polarization sensitive due to their orientational order and unidirectional microvilli (Snyder, 1973b, Snyder, 1973a, Roberts et al, 2011. Many crustaceans arrange their microvilli in two interdigitating perpendicular directions and position their photoreceptors relative to the outside world, allowing for maximal sensitivity to H and V polarized light (Waterman and Horch, 1966, Alkaladi et al, 2013. Stomatopods, benthic marine crustaceans, have a more complex retinal structure and organization of photoreceptors ( Fig.…”