Mindaugas Mitkus

Ultraviolet vision in birds: the importance of transparent eye media

Ultraviolet (UV)-sensitive visual pigments are widespread in the animal kingdom but many animals, for example primates, block UV light from reaching their retina by pigmented lenses. Birds have UV-sensitive (UVS) visual pigments with sensitivity maxima around 360–373 nm (UVS) or 402–426 nm (violet-sensitive, VS). We describe how these pigments are matched by the ocular media transmittance in 38 bird species. Birds with UVS pigments have ocular media that transmit more UV light (wavelength of 50% transmittance, λT0.5, 323 nm) than birds with VS pigments (λT0.5, 358 nm). Yet, visual models predict that colour discrimination in bright light is mostly dependent on the visual pigment (UVS or VS) and little on the ocular media. We hypothesize that the precise spectral tuning of the ocular media is mostly relevant for detecting weak UV signals, e.g. in dim hollow-nests of passerines and parrots. The correlation between eye size and UV transparency of the ocular media suggests little or no lens pigmentation. Therefore, only small birds gain the full advantage from shifting pigment sensitivity from VS to UVS. On the other hand, some birds with VS pigments have unexpectedly low UV transmission of the ocular media, probably because of UV blocking lens pigmentation.

Ultraviolet sensitivity and colour vision in raptor foraging

SUMMARY Raptors have excellent vision, yet it is unclear how they use colour information. It has been suggested that raptors use ultraviolet (UV) reflections from vole urine to find good hunting grounds. In contrast, UV plumage colours in songbirds such as blue tits are assumed to be ‘hidden’ communication signals, inconspicuous to raptors. This ambiguity results from a lack of knowledge about raptor ocular media transmittance, which sets the limit for UV sensitivity. We measured ocular media transmittance in common buzzards (Buteo buteo), sparrowhawks (Accipiter nisus), red kites (Milvus milvus) and kestrels (Falco tinnunculus) so that, for the first time, raptor UV sensitivity can be fully described. With this information, and new measurements of vole urine reflectance, we show that (i) vole urine is unlikely to provide a reliable visual signal to hunting raptors and (ii) blue tit plumage colours are more contrasting to blue tits than to sparrowhawks because of UV reflectance. However, as the difference between blue tit and sparrowhawk vision is subtle, we suggest that behavioural data are needed to fully resolve this issue. UV cues are of little or no importance to raptors in both vole and songbird interactions and the role of colour vision in raptor foraging remains unclear.

Specialized photoreceptor composition in the raptor fovea

The retinae of many bird species contain a depression with high photoreceptor density known as the fovea. Many species of raptors have two foveae, a deep central fovea and a shallower temporal fovea. Birds have six types of photoreceptors: rods, active in dim light, double cones that are thought to mediate achromatic discrimination, and four types of single cones mediating color vision. To maximize visual acuity, the fovea should only contain photoreceptors contributing to high‐resolution vision. Interestingly, it has been suggested that raptors might lack double cones in the fovea. We used transmission electron microscopy and immunohistochemistry to evaluate this claim in five raptor species: the common buzzard (Buteo buteo), the honey buzzard (Pernis apivorus), the Eurasian sparrowhawk (Accipiter nisus), the red kite (Milvus milvus), and the peregrine falcon (Falco peregrinus). We found that all species, except the Eurasian sparrowhawk, lack double cones in the center of the central fovea. The size of the double cone‐free zone differed between species. Only the common buzzard had a double cone‐free zone in the temporal fovea. In three species, we examined opsin expression in the central fovea and found evidence that rod opsin positive cells were absent and violet‐sensitive cone and green‐sensitive cone opsin positive cells were present. We conclude that not only double cones, but also single cones may contribute to high‐resolution vision in birds, and that raptors may in fact possess high‐resolution tetrachromatic vision in the central fovea.

Eye Size, Fovea, and Foraging Ecology in Accipitriform Raptors

Birds with larger eyes are predicted to have higher spatial resolution because of their larger retinal image. Raptors are well known for their acute vision, mediated by their deep central fovea. Because foraging strategies may demand specific visual adaptations, eye size and fovea may differ between species with different foraging ecology. We tested whether predators (actively hunting mobile prey) and carrion eaters (eating dead prey) from the order Accipitriformes differ in eye size, foveal depth, and retinal thickness using spectral domain optical coherence tomography and comparative phylogenetic methods. We found that (1) all studied predators (except one) had a central and a temporal fovea, but all carrion eaters had only the central fovea; (2) eye size scaled with body mass both in predators and carrion eaters; (3) predators had larger eyes relative to body mass and a thicker retina at the edge of the fovea than carrion eaters, but there was no difference in the depth of the central fovea between the groups. Finally, we found that (4) larger eyes generally had a deeper central fovea. These results suggest that the visual system of raptors within the order Accipitriformes may be highly adapted to the foraging strategy, except for the foveal depth, which seems mostly dependent upon the eye size.

Change of ultraviolet light transmittance in growing chicken and quail eyes

The ocular media transmittance (OMT), the amount of light transmitted by the ocular media (the cornea, aqueous humour, lens and vitreous humour) to the retina, determines the sensitivity of vertebrate eyes to short-wavelength light, such as ultraviolet (UV). Earlier, we have measured the OMT of adult birds from a range of species and found that smaller eyes transmitted more UV-light to the retina than larger eyes. In the current study we measured OMT during post-hatch development in Japanese quails and domestic chickens. We show that in both species, OMT decreases as the eye size increases similarly to that what was found across various species, but that quails have lower OMT than expected from eye size. In both species, lens transmittance decreases linearly with lens thickness suggesting that UV-transmittance through the lenses is not actively controlled, but instead determined by UV-absorbance and scattering that occur in all biological tissues. Contrary to earlier assumptions of high cornea transmittance, we found that cornea transmittance is more variable, substantially influencing whole eye transmittance in all age groups of quail and in young chickens. It seems that additional absorbing pigments are used to more actively control cornea transmittance and thereby also overall OMT.

Vision on the high seas: spatial resolution and optical sensitivity in two procellariiform seabirds with different foraging strategies.

ABSTRACT Procellariiform or ‘tubenosed’ seabirds are challenged to find prey and orient over seemingly featureless oceans. Previous studies have found that life-history strategy (burrow versus surface nesting) was correlated to foraging strategy. Burrow nesters tended to track prey using dimethyl sulphide (DMS), a compound associated with phytoplankton, whereas surface-nesting species did not. Burrow nesters also tended to be smaller and more cryptic, whereas surface nesters were larger with contrasting plumage coloration. Together these results suggested that differences in life-history strategy might also be linked to differences in visual adaptations. Here, we used Leachs storm petrel, a DMS-responder, and northern fulmar, a non-responder, as model species to test this hypothesis on their sensory ecology. From the retinal ganglion cell density and photoreceptor dimensions, we determined that Leachs storm petrels have six times lower spatial resolution than the northern fulmars. However, the optical sensitivity of rod photoreceptors is similar between species. These results suggest that under similar atmospheric conditions, northern fulmars have six times the detection range for similarly sized objects. Both species have extended visual streaks with a central area of highest spatial resolution, but only the northern fulmar has a central fovea. The prediction that burrow-nesting DMS-responding procellariiforms should differ from non-responding species nesting in the open holds true for spatial resolution, but not for optical sensitivity. This result may reflect the fact that both species rely on olfaction for their nocturnal foraging activity, but northern fulmars might use vision more during daytime. Summary: Procellariiform seabirds with different nesting and foraging strategies have also evolved predictable differences in their ability to see their prey or other foraging seabirds.

High resolution of colour vision, but low contrast sensitivity in a diurnal raptor

Animals are thought to use achromatic signals to detect small (or distant) objects and chromatic signals for large (or nearby) objects. While the spatial resolution of the achromatic channel has been widely studied, the spatial resolution of the chromatic channel has rarely been estimated. Using an operant conditioning method, we determined (i) the achromatic contrast sensitivity function and (ii) the spatial resolution of the chromatic channel of a diurnal raptor, the Harriss hawk Parabuteo unicinctus. The maximal spatial resolution for achromatic gratings was 62.3 c deg−1, but the contrast sensitivity was relatively low (10.8–12.7). The spatial resolution for isoluminant red-green gratings was 21.6 c deg−1—lower than that of the achromatic channel, but the highest found in the animal kingdom to date. Our study reveals that Harriss hawks have high spatial resolving power for both achromatic and chromatic vision, suggesting the importance of colour vision for foraging. By contrast, similar to other bird species, Harriss hawks have low contrast sensitivity possibly suggesting a trade-off with chromatic sensitivity. The result is interesting in the light of the recent finding that double cones—thought to mediate high-resolution vision in birds—are absent in the central fovea of raptors.

Development of the Visual System in a Burrow-Nesting Seabird: Leach's Storm Petrel

Little is known about the development of vision in wild birds. It is unknown, for example, whether the ability to see can be predicted by the level of prenatal growth or whether the eyes are open at hatching in a particular species. In this study, we investigated the growth of eyes, the formation of retinal ganglion cell topography, and the appearance of simple, visually guided behaviours in chicks of a small procellariiform seabird, Leachs storm petrel (Oceanodroma leucorhoa). This semi-precocial species, which has a well-developed sense of smell, nests in underground burrows where adults provision chicks for 6-8 weeks in the dark before fledging. Retinal ganglion cell topographic maps revealed that fine-tuning of cell distribution does not happen early in development, but rather that the ganglion cell layer continues to mature throughout provisioning and probably even after fledging. While the olfactory bulbs reached adult size around 7 weeks after hatching, the eyes and telencephalon continued to grow. Optokinetic head response and artificial burrow finding experiments indicated that chicks in the 2nd week after hatching lack even the most basic visually guided behaviours and are probably blind. Thus, vision in Leachs storm petrel chicks starts to function sometime around the 3rd week after hatching, well after the eyes have opened and the olfactory system is functional.