Sensory Systems/Arthropods/Fiddler Crabs

= The Visual System of Fiddler Crabs =

Introduction
Fiddler crabs are a species very well suited for investigations into their visual system, and how this system has been tuned to the conditions in which they live and the behaviours they exhibit. They do not range far from their burrows, typically living within an area of 1 m2. Their eye stalks give them a panoramic field of view, so they don't need to orient themselves to view salient objects. Additionally, their habitat predominantly consists of open mud flats with a simple visual structure. These factors make it possible to monitor in natural conditions both the behaviour of the crabs, and the visual information to which they are exposed, allowing detailed analysis of the visual processing taking place within their nervous systems. Finally, the limited resolution of fiddler crabs' vision allows the manipulation of their behaviour by simple visual dummies, mistaken for predatory birds or other crabs. Investigating such aspects of the visual systems of fiddler crabs clearly shows that their vision has not evolved to faithfully relay all image information, but to detect only events relevant to their survival, including the presence of predators or potential mates.

Biology of the Fiddler Crab Visual System
There is a strong link between the visual system of the fiddler crab, its behavioural repertoire, and the environment in which it lives. While the fiddler crab's visual acuity may be limited, this reflects the burrow dwelling nature of most species who do not need to perform long range navigation and therefore are not known to be guided by visual landmarks. Some species of fiddler crab make long excursions in search of food or mates, and these are known to orient themselves using the panoramic image of distant landmarks and patterns of polarised sunlight. For most of a fiddler crab's behaviours, the visual environment serves as a changing background to be filtered out so salient events can be detected. Some key features of the visual system of the fiddler crab are that its eyes are located on the end of vertical eye stalks, granting them panoramic vision; and that these eyes have a compound structure which allow a non-uniform distribution of photoreceptors.

Vertical eye stalks
The eyes of fiddler crabs are located atop vertical eye stalks, giving them a larger field of view as less of the scene is obstructed by their bodies. Having elevated eyes also allows fiddler crabs to use the horizon to serve as a discriminating line between predators - birds flying above the horizon - and other crabs below the horizon. Different species of crabs have different eye stalk arrangements, as dictated by the structure of the environment in which they live. Crabs living in flat environments have more closely spaced, taller eye stalks. This close spacing limits stereoscopic depth estimation, but in a flat environment the position of an object on the ground in the visual field can be used as a more reliable indicator of distance, as closer objects will appear lower. Alternatively, crab species living in less flat environments such as rocky shores or dense mangrove forests have more widely spaced, shorter eye stalks. There is a trade off for the crabs between eye stalk length and spacing, because they have horizontal grooves on the front of their bodies into which their eyes can be lowered for protection. Examples of crabs with varying eye stalk lengths are shown in the images below.

Compound Eyes and the Distribution of Photoreceptors
In addition to the placement of their eyes, the structure and arrangement of the photoreceptors within the eyes of fiddler crabs have also been evolved to suit their environment. They have compound eyes consisting of hundred or thousands of independent photosensitive structures called ommatidia, each having its own cornea, lens and photoreceptors. Compared to simple eyes, compound eyes are limited in their resolution but enable receptor density to be varied over the visual field, so the visual information acquired by a fiddler crab can be optimised for its behaviours. In particular, fiddler crabs have a much higher resolution in the vertical direction than the horizontal, thanks to very ellipsoidal, almost cylindrical shaped eyes with greater vertical radius. This allows greater detail to be resolved along the ground plane, which is somewhat compressed in the crab's visual field due to its view being so close to the ground. Additionally, the distribution of ommatidia is heavily skewed towards the horizon: despite the crab's visual field covering approximately 72% of the vertical axis, 30% of ommatidia look within ±9° of the horizon, and 50% within ±18°. Recent imaging techniques have shown there are actually two distinct streaks of high resolution vision in fiddler crab's eyes, one just above and another just below the horizon line. Predatory birds are larger than fiddler crabs and fly above them, so almost exclusively appear above the horizon from the crabs' perspective. And because fiddler crabs' eyes are located on top of vertical stalks, they always see the bodies of other crabs below the horizon line. It is therefore hypothesised that the high resolution streak above the horizon is to detect predators, and the streak below the horizon to identify conspecifics. The sparse distribution of ommatidia away from the horizon suggest that the crabs do not aim to reconstruct detailed images of these parts of the visual world, but rather to rapidly detect potential threats and react appropriately. Indeed, at the distance that fiddler crabs react to avoid predatory birds these birds only occupy the field of view of a few individual ommatidia.

Capability for Colour Vision
Whether fiddler crabs are capable of colour vision has been a matter of contention for some time. It has been hard to analyse experimentally due to the measurements being distorted by the presence of screening pigment 'sun-shades' between individual ommatidia, which prevent stray light bouncing between them. Each ommatidium has eight photosensitive receptors, R1-R8, the first seven being significantly larger than the eighth. Measurements from the first seven receptors showed a consistent spectral sensitivity between them, peaking between 508 nm and 530 nm. However, behavioural studies suggested that some fiddler crab species could discriminate between differently coloured stimuli. More recent molecular analysis of fiddler crab vision determined that three genes are responsible for encoding their colour-receptive opsin pigments. R1-R7 contained either or both of 2 middle-wavelength sensitive pigments, while a third short-wavelength sensitive pigment was found exclusively in R8, providing evidence of the possibility for colour vision in fiddler crabs.



Burrow Defence Behaviour
A fiddler crab's burrow serves many functions. It protects a crab from predators, provides access to food and water, and positions the crab in a neighbourhood with other crabs - both potential mates and competitors. But due to the short stature of the fiddler crab and the flat environment it inhabits, the burrow entrance becomes invisible from only a short distance away. Fiddler crabs therefore monitor their own movements as they roam the world around their burrows, tracking them in a process called path integration, so as to approximately know the direction and distance back to their burrows at any point in time. Additionally, the fiddler crab continually aligns one side of its body to face its burrow, allowing it to rush back home in the case of a predator approaching, or a rival crab seeking to take over its burrow.

This burrow defence behaviour is of particular interest because it does not habituate to being triggered by dummies, and because the crabs respond based on a rival's distance from the burrow, not the rival's distance from the crab itself. That is, these crabs seem to combine information from their path integration systems with visual information to compute the location of a rival crab in an allocentric reference frame. A possible implementation of such computation could exploit the fact that, in a flat world, each receptor in the crab's eye corresponds to a particular position in space. Additionally, the crab maintains a sideways alignment with the burrow so the same area of its eye is always monitoring the area for rival crabs. The distance between the burrow and an intruding crab could therefore be computed by considering only the ommatidia being stimulated by the rival crab, modulated by the crab's current distance from its burrow given by path integration. Fiddler crabs do seem to respond as if they exploit this method of computing based on a simple visual filter, rushing back to their burrows when an intruder gets too close. But definite neurophysiological evidence has not yet been gathered. See Figure 10 in Zeil, 2006 for a clear visualisation.

Predator avoidance and fleeing
Another fiddler crab behaviour closely tied to their visual system is that of fleeing to avoid predators. Unlike for burrow defence, fiddler crabs react to approaching predators in an egocentric manner, fleeing to their burrows when the predator comes to close. This behaviour is also somewhat modulated by the crabs' path integration system, with crabs fleeing earlier when further from their burrows. However, their reactions do not consistently reflect the impending danger of a predator because, as previously mentioned, they typically begin to flee a predator when its image falls upon only a few individual ommatidia. At this range, the crab cannot accurately distinguish the size, direction, or speed of an approaching predator. But the high predation pressure forces the crab to be cautious and flee anyway. This can cause some counter-intuitive responses, such as crabs fleeing more quickly from birds passing at a distance than approaching directly, because the former have a greater retinal velocity.

As previously mentioned, the open environment in which fiddler crabs live and the limited distance over which they range makes it possible to record both their behaviour and the visual stimuli which caused this behaviour. Detailed analysis of camera footage of approaching birds, both predatory and non-predatory, along with the fiddler crabs' responses to these birds have provided more specific knowledge about the visual information that triggers fleeing. In particular, the visual characteristic that best explained the crab's response to a predator was visual flicker - the rate of change over time of local visual contrast at a specific position in the crab's visual field. The distribution of ommatidia significantly above the horizon is very sparse, so distant objects like approaching approaching birds will rarely be seen by multiple ommatidia, making size or motion cues comparatively unreliable.

Behavioural Habituation
Unlike for the fiddler crab's burrow defence behaviour, which does not habituate even after many dummy presentations, fiddler crabs habituate their predator avoidance behaviour when presented with false alarms: most notably, after some exposure they become oblivious to the presence of human experimenters. The neural mechanisms underlying this habituation have been the subject of detailed analysis. Calcium imaging techniques were applied to a different species of crab (Neohelice granulata) and showed that the response of lobula giant (LG) neurons in the crab's eye, located between the retina and midbrain, was suppressed after high-frequency dummy stimulus presentation. This result was consistent with the change in the crabs' behaviour, that they stopped reacting to visual motion but only for a short duration. Additionally, this habituation only affected the region of the retina to which the stimulus was applied.

Furthermore, it was shown that two different populations of the same species of crab exposed to different levels of predation pressure reacted differently to dummy predator stimuli, and that particular neural activity was indicative of this behavioural difference. Crabs in the high risk population reacted more strongly to visual danger stimuli and had higher levels of neural activity in LG neurons. Crabs in the low risk population showed lower levels of both LG neural activity and behavioural response to the same stimuli. In contrast, the behavioural and responses to panoramic visual motion and painful shock stimuli were similar across populations, suggesting the LG neurons are strongly implicated in the predator avoidance behaviour and its habituation.