A novel cellular structure in the retina of insectivorous birds.

The keen visual systems of birds have been relatively well-studied. The foundations of avian vision rest on their cone and rod photoreceptors. Most birds use four cone photoreceptor types for color vision, a fifth cone for achromatic tasks, and a rod for dim-light vision. The cones, along with their oil droplets, and rods are conserved across birds - with the exception of a few shifts in spectral sensitivity - despite taxonomic, behavioral and ecological differences. Here, however, we describe a novel photoreceptor organelle in a group of New World flycatchers (Empidonax spp.) in which the traditional oil droplet is replaced with a complex of electron-dense megamitochondria surrounded by hundreds of small, orange oil droplets. The photoreceptors with this organelle were unevenly distributed across the retina, being present in the central region (including in the fovea), but absent from the retinal periphery and the area temporalis of these insectivorous birds. Of the many bird species with their photoreceptors characterized, only the two flycatchers described here (E. virescens and E. minimus) possess this unusual retinal structure. We discuss the potential functional significance of this unique sub-cellular structure, which might provide an additional visual channel for these small predatory songbirds.

Does retinal configuration make the head and eyes of foveate birds move?

Animals move their heads and eyes to compensate for movements of the body and background, search, fixate, and track objects visually. Avian saccadic head/eye movements have been shown to vary considerably between species. We tested the hypothesis that the configuration of the retina (i.e., changes in retinal ganglion cell density from the retinal periphery to the center of acute vision-fovea) would account for the inter-specific variation in avian head/eye movement behavior. We characterized retinal configuration, head movement rate, and degree of eye movement of 29 bird species with a single fovea, controlling for the effects of phylogenetic relatedness. First, we found the avian fovea is off the retinal center towards the dorso-temporal region of the retina. Second, species with a more pronounced rate of change in ganglion cell density across the retina generally showed a higher degree of eye movement and higher head movement rate likely because a smaller retinal area with relatively high visual acuity leads to greater need to move the head/eye to align this area that contains the fovea with objects of interest. Our findings have implications for anti-predator behavior, as many predator-prey interaction models assume that the sensory system of prey (and hence their behavior) varies little between species.

Collective behaviour in vertebrates: a sensory perspective.

Collective behaviour models can predict behaviours of schools, flocks, and herds. However, in many cases, these models make biologically unrealistic assumptions in terms of the sensory capabilities of the organism, which are applied across different species. We explored how sensitive collective behaviour models are to these sensory assumptions. Specifically, we used parameters reflecting the visual coverage and visual acuity that determine the spatial range over which an individual can detect and interact with conspecifics. Using metric and topological collective behaviour models, we compared the classic sensory parameters, typically used to model birds and fish, with a set of realistic sensory parameters obtained through physiological measurements. Compared with the classic sensory assumptions, the realistic assumptions increased perceptual ranges, which led to fewer groups and larger group sizes in all species, and higher polarity values and slightly shorter neighbour distances in the fish species. Overall, classic visual sensory assumptions are not representative of many species showing collective behaviour and constrain unrealistically their perceptual ranges. More importantly, caution must be exercised when empirically testing the predictions of these models in terms of choosing the model species, making realistic predictions, and interpreting the results.

Vision in two cyprinid fish: implications for collective behavior.

Many species of fish rely on their visual systems to interact with conspecifics and these interactions can lead to collective behavior. Individual-based models have been used to predict collective interactions; however, these models generally make simplistic assumptions about the sensory systems that are applied without proper empirical testing to different species. This could limit our ability to predict (and test empirically) collective behavior in species with very different sensory requirements. In this study, we characterized components of the visual system in two species of cyprinid fish known to engage in visually dependent collective interactions (zebrafish Danio rerio and golden shiner Notemigonus crysoleucas) and derived quantitative predictions about the positioning of individuals within schools. We found that both species had relatively narrow binocular and blind fields and wide visual coverage. However, golden shiners had more visual coverage in the vertical plane (binocular field extending behind the head) and higher visual acuity than zebrafish. The centers of acute vision (areae) of both species projected in the fronto-dorsal region of the visual field, but those of the zebrafish projected more dorsally than those of the golden shiner. Based on this visual sensory information, we predicted that: (a) predator detection time could be increased by >1,000% in zebrafish and >100% in golden shiners with an increase in nearest neighbor distance, (b) zebrafish schools would have a higher roughness value (surface area/volume ratio) than those of golden shiners, (c) and that nearest neighbor distance would vary from 8 to 20 cm to visually resolve conspecific striping patterns in both species. Overall, considering between-species differences in the sensory system of species exhibiting collective behavior could change the predictions about the positioning of individuals in the group as well as the shape of the school, which can have implications for group cohesion. We suggest that more effort should be invested in assessing the role of the sensory system in shaping local interactions driving collective behavior.

Vision in avian emberizid foragers: maximizing both binocular vision and fronto-lateral visual acuity.

Avian species vary in their visual system configuration, but previous studies have often compared single visual traits between two to three distantly related species. However, birds use different visual dimensions that cannot be maximized simultaneously to meet different perceptual demands, potentially leading to trade-offs between visual traits. We studied the degree of inter-specific variation in multiple visual traits related to foraging and anti-predator behaviors in nine species of closely related emberizid sparrows, controlling for phylogenetic effects. Emberizid sparrows maximize binocular vision, even seeing their bill tips in some eye positions, which may enhance the detection of prey and facilitate food handling. Sparrows have a single retinal center of acute vision (i.e. fovea) projecting fronto-laterally (but not into the binocular field). The foveal projection close to the edge of the binocular field may shorten the time to gather and process both monocular and binocular visual information from the foraging substrate. Contrary to previous work, we found that species with larger visual fields had higher visual acuity, which may compensate for larger blind spots (i.e. pectens) above the center of acute vision, enhancing predator detection. Finally, species with a steeper change in ganglion cell density across the retina had higher eye movement amplitude, probably due to a more pronounced reduction in visual resolution away from the fovea, which would need to be moved around more frequently. The visual configuration of emberizid passive prey foragers is substantially different from that of previously studied avian groups (e.g. sit-and-wait and tactile foragers).