Session #3005

Abstract

Avian ophthalmology was founded on the interest of comparative anatomists, physiologists, and visual ecologists. With the advancement of medicine and the study of ophthalmic disease, clinical medicine deviated from the critical study of first the animal, their visual system, and how the animals use that system to interact visually with their environment. This lecture discusses how to approach an avian patient based on the individual species at hand, even prior to the examination, by following three simple steps:

1.  Birds

2.  Birds’ eyes

3.  Birds + birds’ eyes

Using this approach is essential to understanding species differences in treatment and prognosis, as well as welfare and potentially release of free-living individuals.

Introduction

It was in the late 1800s to the early 1900s when a spark of fascination for the comparative anatomy and physiology of animal eyes ignited, as did our search to understand how animals see our shared world. As stated in 1942 by an early visual ecologist:

“If the comparative ophthalmologists of the world should ever hold a convention, the first resolution they would pass would say: ‘Everything in the vertebrate eye means something.’ Except for the brain, there is no other organ in the body of which that can be said…Man can make optical instruments only from such materials as brass and glass. Nature has succeeded with only such things as leather and water and jelly; but the resulting instrument is so delicately balanced that it will tolerate no tampering.”¹

This statement laid a foundation under which the minds of the founders of the American College of Veterinary Ophthalmologists began to grow. Over the following 70 years, our knowledge of comparative ophthalmology expanded at a near exponential rate; however, during that expansion, we nearly lost our early ways as comparative visual ecologists along with our wonder for the beauty of the enormous diversity that is the vertebrate eye. Today, a major gap in our field remains the true comparative nature of how our profession began. Despite much scientific progress, most of our knowledge for wild and exotic animal ophthalmology has depended upon extrapolation from domestic animal ophthalmology. By reaching back to our roots and studying an animal in their natural environment, studying the multidimensional components of their visual system, and then understanding how they use their visual system to interact with their environment, only then are we able to approach comparative ophthalmology more accurately. The purpose of the session is to discuss these often-forgotten principles of the ophthalmic examination in the avian patient.

Birds

The first step is familiarizing oneself with the visual ecology of a given species. It includes:

• Habitat
• Activity pattern
• Prey and foraging behaviors
• Predators and anti-predator behaviors

Most birds are recognized as having superior visual performance^2-6; however, most birds are highly visual in very different ways. Despite our increasing knowledge of avian visual systems, we know very little about their comparative differences. The first step toward understanding the visual system of a given bird species, and thus the first step in our approach to an avian ophthalmic patient, is to study why there are such differences between species. That is, to familiarize oneself with the visual ecology of the species at hand.

A bird’s visual system is tuned for a specific set of uses as it interacts with its environment. The more highly visual the species, the more specific the tuning of the visual system. Gordon Wall’s (1942) statement, “Everything in the vertebrate eye means something” is true and exists because everything in the environment also means something, and it is the function of the eye to interact with a specific environment with precision.¹ Such diversity of visual systems is because the diversity of possible environmental interactions is even greater! One species could live in a barren desert with very little visual complexity other than the vastness of depth, the homogenous contrast of sand, and those organisms camouflaging within it. Another species may live within the dense, tropical rainforest with infinite layers of spatial complexity. But of course, spanning from the forest floor to the canopy you encounter numerous other ecosystems that offer different visual interactions and thus visual requirements. The possibilities are nearly endless.

The diversity only increases (as does our understanding of how a species sees) when we consider at what time period they are most active visually. That is, their activity pattern. Some species are active only in bright daylight, others in the dark of night, and finally others spend time in both night and day or in the between periods of time when the sun is rising or setting. Each of these activity patterns provides an important component of the story that is being told about how they use their eyes.

Finally, we must consider how a species visually interacts with its prey and predators. The methods used to capture prey, from pecking motionless seeds in a high-contrast substrate to actively chasing near-microscopic insects in flight, require very different visual capabilities. And the trade-off? Simultaneously needing to maintain watch for predators in the peripheral visual fields. The combination of foraging modes and methods of monitoring for predators often shape key components of a bird’s visual system (namely the visual field and positions of retinal centers of specialization), as discussed in the next section.

Birds’ Eyes

The second step is understanding the function of the visual system of a given species. It includes:

• Orbit convergence and visual field configuration
• Spatial resolution
• Temporal resolution
• Color vision
• Retinal processing and beyond

Despite relative conservation of the avian eye, the species differences discussed above result in thousands of iterations of the avian eye. These differences go way beyond the face-value of iris color, eye size, and various adnexal structures. Such differences as visual field width and the degree of binocular overlap, visual acuity, and color vision can vary dramatically across species.^7,8 Avian visual systems are multidimensional, and the key to understanding the magnitude of their interspecific differences is to assess each difference and how they function together, something that has traditionally been lacking in vision studies. In addition, we tend to view avian vision through the lens of our own visual experience, thus providing misguided ideas of how birds may perceive their environment.

Specific regions across the retina are specialized for high spatial resolution (visual acuity),^7-9 high temporal resolution (speed of sight),¹⁰ and color vision^10,11. Retinal specializations for visual acuity include the area centralis, visual streak, and the fovea. Specializations for high temporal resolution or color vision can be contained with these regions, overlap with them, or be fully separate (i.e., one part of the retina may function for high visual acuity whereas another may contain a proportionally high number of red cones for color vision). Where these retinal specializations are positioned in space depends on the orbit convergence and the configuration of the visual field. Species with high binocularity and corresponding small visual fields (i.e., a greater degree of blind space) tend to be higher predatory species, whereas wider visual fields are a trade-off for smaller binocular space common in prey species, as they have a greater need to keep watch for predators.⁸ Multiple retinal specializations (e.g., the bifoveate retina of some predatory birds) can be present in a single eye, and the position of specializations can vary, meaning that different regions of a visual field can have different degrees of visual importance or are used for completely different visual tasks.¹² These areas (and what a species uses them for) are important to note when clinically assessing the potential not only for vision, but for acute and highly functional vision, as we will discuss below. Finally, processing of retinal signals and the corresponding areas in the visual cortex are very poorly understood. Together, these different components of the visual system work together to help a species obtain the visual information they need to survive based upon their specific ecology.

Birds + Birds’ Eyes

The third step is understanding how birds visually sample and interact with their ecology. It includes:

• Head movements
• Eye movements
• Other visual behaviors

Finally, by taking the ecology of a given species, and applying what we know about their visual system, we can begin to understand how they visually sample and interreact with their ecology. For example, the combination of the type and location of retinal specializations, along with the orientation of the visual field, are key determinants driving head and eye movement behavior.⁸ For example, songbirds tend to have very wide visual fields, forming small binocular (but also small blind) areas. While this orientation maximizes predator detection, they need to position their single, centrotemporal region of high acuity (fovea) onto an object of interest (e.g., a predator) and thus perform rapid head and eye movements to increased high acuity visual sampling. Similarly, while foraging, the fovea in each eye projects laterally and does not overlap in their narrow binocular field, resulting in side-to-side head movements to visualize food objects with high acuity. Other species have relatively immobile eyes but extreme ranges of head movement (e.g., owls) or high degrees of eye movements in a specific plane to enable them to remain motionless while hunting below their bill (e.g., American bittern).

Clinically, we can deploy our knowledge of a bird’s visual ecology combined with their eyes to help make important decisions regarding treatment, prognosis, and even release of an injured or ill free-living individual. It is critical to assess the visual potential of a patient in a specific way to make appropriate decisions, which unfortunately can be a matter of life and death for the patient. The above discussion provides a groundwork for the following guidelines toward assessing the visual potential for a bird in its natural habitat.¹²

Extent and Location of the Lesion

Extensive lesions are understandably concerning (e.g., complete cataract, rhegmatogenous retinal detachment); however, small focal lesions can be detrimental to visual success depending on their location within the eye of a given species. For example, lesions less than 2 mm in diameter at either fovea in the eye (even in just a single eye of a diurnal raptor) should deem the bird a poor prognosis for release, given the dependence on high acuity vision for foraging and flight. Owls, on the other hand, can even experience complete retinal damage in one eye and still be considered for release because of their dependence on other sensory systems (e.g., hearing). The same consideration should exist for iatrogenic visual compromise. For example, cataract surgery without the placement of an intraocular lens renders a bird severely myopic. Some species tend to severely fibrose their lens capsule following phacoemulsification thus limiting their vision to that of the capsulorhexis and if a planned posterior capsulorhexis is not performed, can completely obscure vision. Corneal scars following ulcer debridement, or surgical repair/grafting, can be substantial and lethal to a bird in the wild depending on the lesion size and location.

Chronicity of the Lesion

If a generally well bird is diagnosed with chronic ocular lesions (e.g., chorioretinal scars and pigmentary changes, cataracts), even if advanced, it is reasonable to suggest that the bird has had success for some time despite the visual disturbance. It is difficult to know whether the ocular lesion was the cause of their presentation, but their thriftiness suggests they had been doing well up to that point. Evidence of trauma on the same side as the chronic ocular lesions should raise suspicion for the chronic lesion being the cause for the clinical presentation. Additionally, vision testing can be challenging in these patients because they often have adapted well to reduced vision.

Age of the Patient

Age typically brings wisdom and increased survivability. Young birds many have not learned all the skills necessary to survive in the wild, let alone with visual compromise. Considering that most raptor young do not survive past 1 year of age without visual compromise, an ocular lesion that reduces their visual potential should raise concern. Adults often tolerate a greater degree of visual impairment.

Ecological Impact of the Lesion

Even closely related species can have markedly different visual ecologies, including hunting style, habitats, the importance of binocular vision, the activity pattern during foraging, and even human environmental interferences (e.g., windmills, powerlines, traffic, etc.). Ultimately, the impact of a lesion needs to be projected into their visual space to properly determine how it may impact the visual ecology of that species.

Success in Flight and Feeding Trials

The final step of evaluating vision if a patient is deemed potentially releasable is observing successful flight and feeding behaviors. Although future trauma cannot always be predicted despite successful flight and foraging tests, some certainty of ability for successful flight and visual navigation can be obtained through behavioral experiments.

References

1.  Walls GL. The Vertebrate Eye and Its Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Institute of Science; 1942.

2.  Martin GR. The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds. Philos Trans R Soc Lond B Biol Sci. 2014;369(1636):1–12.

3.  Moore BA, Paul-Murphy JR, Tennyson AJD, Murphy CJ. Blind free-living kiwi offer a unique window into the evolution of vertebrate vision. BMC Biol. 2017;15(1):85.

4.  Moore BA, Tyrrell LP, Kamilar JM, et al. Structure and function of regional specializations in the vertebrate retina. In: Kaas JH, ed. Evolution of Nervous Systems. Oxford, UK: Elsevier; 2017:351–372.

5.  Moore BA, Maggs DJ, Kim S, et al. Clinical findings and normative ocular data for free-living Anna’s (Calypte anna) and black-chinned (Archilochus alexandri) hummingbirds. Vet Ophthalmol. 2019;22(1):13–23.

6.  Moore BA, Hawkins M, Fernandez-Juricic E, et al. Introduction to avian ophthalmology. In: Montiani-Ferreira F, Moore BA, Ben-Shlomo G, eds. Exotic and Wild Animal Ophthalmology. London, UK: Springer Nature; 2022:321–348.

7.  Moore BA, Doppler M, Young JE, Fernández-Juricic E. Interspecific differences in the visual system and scanning behavior of three forest passerines that form heterospecific flocks. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2013;199:263–277.

8.  Moore BA, Tyrrell LP, Pita D, Bininda-Emonds ORP, Fernández-Juricic E. Does retinal configuration make the head and eyes of foveate birds move? Sci Rep. 2017;7:38406.

9.  Fernandez-Juricic E, Moore BA, Doppler M, et al. Testing the terrain hypothesis: Canada geese see their world laterally and obliquely. Brain Behav Evol. 2011;77(3):147–158.

10.  Tyrrell LP, Teixeira LBC, Dubielzig RR, et al. A novel cellular structure in the retina of insectivorous birds. Sci Rep. 2019;9(1):15230.

11.  Moore BA, Baumhardt P, Doppler M, et al. Oblique color vision in an open-habitat bird: spectral sensitivity, photoreceptor distribution, and behavioral implications. J Exp Biol. 2012;215:3442–3452.

12.  Montiani-Ferreira F, Moore BA. Ophthalmology of raptors. Introduction to avian ophthalmology. In: Montiani-Ferreira F, Moore BA, Ben-Shlomo G, eds. Exotic and Wild Animal Ophthalmology. London, UK: Springer Nature; 2022:429–504.