Pupil morphology in the animal world is both elegant and complex. While we may be most familiar with the round pupils of primates, pupils manifest a variety of shapes. Pupils are configured as vertically oriented slits, horizontally slit, crescent shaped, and even “W” shaped. In addition the aperture is typically open but may be variably occluded with an operculum. Each configuration endows the owner with certain optical characteristics advantageous to its ecological niche.

Humans and other animals with round pupils balance the benefits of visual acuity with the need for light collection. Given the retina’s photoreceptor architecture, in ample lighting conditions, a pupil size of approximately 2–3 mm maximizes the optical system’s resolution potential [14]. Smaller pupil size induces diffraction, and a larger size leads to chromatic and spherical aberration, both deteriorating visual resolution. However, as ambient light decreases, visual acuity declines due to photon noise and the disadvantages of a larger pupil are outweighed by increased light capture.

In the animal kingdom, it is noted that certain predators possess vertically slit pupils [2]. Animals as diverse as cats, certain geckos and snakes have vertical pupils, and while dissimilar in many respects, they all share an ambush hunting style and forage in limited light [3]. These vertical pupils are much more efficient at reducing light passage. Whereas humans can change pupil area 16-fold between light and dark conditions, the domestic cat (Felis catus) is capable of a 135-fold change, or ten times that of humans [14] (see Fig. 6.3). The Tokay gecko (Gekko gecko), a nocturnal hunter, possesses a pupil that in scotopic conditions is round. In daylight however its vertical pupil margins abut, completely closing the pupil aperture saved for two small notches (See Fig. 6.4). The resulting pupil measures 0.1 mm, a 300-fold decrease in pupil area [4]. While in a human, a pupil of that size would result in significant diffraction and degraded resolution, the shorter length of the gecko eye coupled with its retinal photoreceptor spacing permits such a small pupil to be optically functional.

Authors have theorized why such a dramatic ability to limit retinal illumination exists in these animals. To be sure pupil constriction does protect the retina from sudden illumination changes. And as described above, optimizing pupil size strikes a balance between diffraction and aberration at various light levels. An additional reason is retinal sensitivity. This characteristic is dependent on several factors including photoreceptor (PR) spacing, PR alignment relative to incident light, tapetal reflection (see Section – Tapetum Lucidum below), and post PR stimulation signal summation. Various animals use some or all of these to maximize retinal sensitivity to light stimulation, and on an order far greater than man. For example, the helmet gecko’s retina is 350 times more sensitive compared to a human retina at light levels where the eye can discriminate color [23]. This level of sensitivity is an obvious advantage when hunting in dim illumination, but without a means to limit retinal illumination would render an animal blind at higher light levels. Slit pupils therefore, with their more efficient ability to limit pupil area and light passage, permit useful visual function over a broad range of light intensities.

Another consideration of slit pupils besides pupil area is lens exposure. With round pupils, as pupillary dilation increases, not only is more light permitted into the optical system but more of the peripheral lens is exposed, refracting incident light. In dim light levels, the resulting chromatic aberration may be a necessary trade-off for increased retinal illumination. In animals with a slit pupil, relatively more peripheral lens is inevitably exposed for a given light level. This seemingly induced limitation would be explained if lenses of slit pupil animals corrected for chromatic aberration. In fact Malmström and Kröger investigated the optical systems of terrestrial vertebrates both with and without slit pupils and determined that in every case they studied, the lenses of animals with slit pupils did just that [17]. Described as multifocal lenses, these lenses have gradients of refractive indices allowing various wavelengths to be simultaneously well focused, overcoming chromatic aberration. Multifocal lenses were found not only in species with vertical slit pupils like small felines (cats) and small canines (red fox), but also in those with horizontal slit pupils like sheep, reindeer, elk, and horse. In species examined by the authors having round pupils, nearly all exhibited monofocal lenses, or lenses that did not correct for chromatic aberration. This included large felines like the Siberian tiger (Panthera tigris altaica). Interestingly the intermediate felid species Eurasian lynx (Lynx lynx) has oval pupils and an intermediate form of lens.

While a slit pupil is advantageous when one has a multifocal lens system , minimizing chromatic aberration cannot be the sole reason for a non-round pupil. The octopus has a horizontally slit pupil yet is color blind [14]. Chromatic defocus would not be noted in this species. Like external color, spot patterns, and contour, a slit pupil may provide camouflage or perhaps not be as noticeable as a round pupil while still maintaining visual function [7]. This may be at least one of the reasons the cuttlefish has a W-shaped pupil in bright illumination. The dolphin pupil possesses a dorsal (superior) operculum which shades the inferior retina from the disproportionate amount of light originating from above in marine environments [7]. Similarly the cuttlefish’s W-shaped pupil is effective in balancing a vertically uneven light field [18]. Elongated or complex-shaped pupils also appear to convey visual advantage in terms of contrast, pinhole effect, depth of field, and enhancing vertical or horizontal contour depending on pupil orientation [2, 18, 23].

The human eye functions effectively over a wide range of illumination. Spanning luminance levels from bright sunlight to less than nighttime star light, human sensitivity extends between 10²⁰ and 10¹⁰ photons per second per square meter [14]. In terms of absolute sensitivity, however, we like other diurnal species are poorly suited for nocturnal visual endeavors. Many animals that typically spend much of their active periods in dim light exhibit sensitivities greater than man. Various optical and anatomic methods account for this increased sensitivity including photoreceptor size and spacing, maximum pupil diameter, and overall eye size. An interesting additional ocular structure, common even in our household pets, is the tapetum lucidum.

One of the better known examples of the tapetum lucidum [Latin: “bright/shining tapestry or carpet”] is found in the domestic cat (Felis catus) and is responsible for the phenomenon often called “eye shine ” (see Fig. 6.3) [15, 21]. It functions as a biological mirror, reflecting incident light not initially captured back through the photoreceptors, providing a second opportunity for photon-photoreceptor stimulation and thereby increasing light sensitivity [19]. Nearly all primates, birds, and rodents, as well as the squirrel and pig, do not possess a tapetum [19, 26]. Yet it appears a tapetum confers some ecological advantage since it is found in a number of species including numerous vertebrates, as well as invertebrate mollusk and arthropods [26, 29]. While the method of its employment varies both in location and how reflectance is accomplished in these animals, the commonality is that the tapetum can result in high reflectance due to a structural arrangement that produces exceedingly efficient constructive interference, theoretically approaching 100% [14]. Blood vessels, cell nuclei, and variation in cell spacing interfere, but this is overcome by making use of multiple layers of the tapetal tissue, improving reflectance by summation [14]. The actual reflective material differs among species but include lipid, guanine crystals, riboflavin, and zinc cysteine [19, 26]. Even melanin and collagen under the correct conditions are transformed to become efficient reflectors.

The three general types of tapeta are a retinal tapetum and two choroidal tapeta, the tapetum cellulosum and tapetum fibrosum. The retinal tapetum is found in various fishes, reptiles like crocodiles and alligators, opossums, and fruit bats [26]. It is subdivided as non-occlusible or occlusible. The reflecting medium is composed of lipid, guanine, or melanin. The retinal tapetum, occlusible type is found in some fish and is responsible for variation in tapetal reflectance. Unlike the static or non-occlusible tapetum, in the occlusible form, the reflecting media migrate within the retinal pigment epithelium (RPE) toward or away from the vitreous depending on illumination level. This exposes or masks the reflecting tapetum in dim or bright light, respectively [19]. In other fish species instead of pigment migration, tapetal reflectance is blocked by visual cell movement and migration of RPE processes. The occlusible tapetum is less efficient and thought to primarily benefit the animal by reducing “eye shine”-mediated detection.

Both types of choroidal tapeta are interspaced just external to the choriocapillaris and internal to the remaining choroidal stroma. The RPE overlying the tapetal region has no melanin granules permitting light to both pass through and be reflected back toward the retinal photoreceptors [30]. The area over which the tapetum is present varies between species but is not typically complete, frequently occupying a swath most prominent in the dorsal retina and tapering with a covering RPE layer more peripherally [19, 29, 30]. The cellular variant, the choroidal tapetum cellulosum, is found in many mammalian carnivores, like cats and dogs, and cartilaginous (sharks, dogfishes) and lobe-fined (lungfishes) fish [19, 26]. The cat possesses one of the most refined cellular tapeta, consisting of rodlets containing riboflavin and zinc cysteine and arranged in a precise hexagonal lattice pattern [19]. The remarkable structural organization, and uniform thickness and spacing tolerance per layer, provides a highly efficient quarter wavelength interference reflector [14].

Unlike the cellular tapetum, which requires a secondary spectral substance, the choroidal tapetum fibrosum accomplishes reflection by the arrangement and orientation of its collagen fibers. Just external to the choriocapillaris, the collagen fibrils are aligned parallel to the retina and at a right angle to incident light [29, 30]. Like the cellular tapetum, the collagen is arranged in a hexagonal array with regular spacing [19]. Fibrous tapeta are noted in ungulates (cow, goats, sheep, and horses) and cetacea (whales, dolphins).