Interspecifc variation in eye shape and retinal topography in seven species of galliform bird (Aves: Galliformes: Phasianidae)

Eye morphology and the retinal topography of animals that live in either 'open' (e.g., grassland) or 'enclosed' (e.g., forest) terrestrial habitats show common adaptations to constraints imposed by these different habitat types. Although relationships between habitat and the visual system are well documented in most vertebrates, relatively few studies have examined this relationship in birds. Here, we compare eye shape and retinal topography across seven species from the family Phasianidae (Galliformes) that are diurnally active in either open or enclosed habitats. Species from enclosed habitats have significantly larger corneal diameters, relative to transverse diameters, than species from open habitats, which we predict serves to enhance visual sensitivity. Retinal topography, however, was similar across all seven species and consisted of a centrally positioned area centralis and a weak horizontal visual streak, with no discernible fovea. In the Japanese quail (Coturnix japonica), there was also a dorso-temporal extension of increased neuron density and, in some specimens, a putative area dorsalis. The total number of neurons in the retinal ganglion cell layer was correlated with retinal whole-mount area. Average and peak neuron densities were similar across species, with the exception of the Japanese quail, which had greater average and peak densities. Peak anatomical spatial resolving power was also similar among species, ranging from approximately 10-13?cycles/°. Overall, the pattern of retinal topography we found in phasianids is associated with ground-foraging in birds and presumably facilitates the identification of small food items on the ground as well as other visually guided behaviors, irrespective of habitat type.     

Vision and the foraging technique of skimmers (Rynchopidae)

In birds, the position and extent of the region of binocular vision appears to be determined primarily by feeding ecology. Of prime importance is the degree to which vision is used for the precise control of bill position when foraging. Skimmers (Rynchops, Rynchopidae, Charadriiformes) exhibit a unique foraging behaviour and associated structural adaptations. When foraging they fly low and straight over water with the mouth open and the mandible partially submerged. Items that are hit by the lower mandible are grasped by a rapid reflex bill closure. It is believed that this unique ‘skimming’ foraging technique is guided by tactile rather than visual cues. It is predicted therefore that the visual fields of skimmers will have similar topography to those of other tactile feeding birds. We determined retinal visual fields in Black Skimmers Rynchops niger using an ophthalmoscopic reflex technique. Contrary to expectation the visual fields of Black Skimmers are not like those of other tactile feeders. They show high similarity with those of birds that feed by precision‐pecking. The projection of the bill tip when the mouth is closed and when open (as in skimming) falls within the frontal binocular field and there is an extensive blind area above and behind the head. We argue that this visual field topography functions to achieve accurate bill positioning with respect to the water surface when skimming and, because foraging skimmers cannot determine the identity of what they are seizing as they skim, to permit the visual identification of prey items held between the mandibles after they have been taken from the water surface. When skimming, only a small portion of the binocular field, approximately 5° wide and extending 5° above the horizontal, looks in the direction of travel. The small size of this forward‐facing region of binocularity in skimmers suggests that control of locomotion in birds does not necessarily require extensive binocularity in the direction of travel.     

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention.     

Recolonization of breeding waterfowl communities by the whooper swan: vacant niches available

Breeding population of the whooper swan Cygnus cygnus has increased dramatically in Finland during the last 50 yr, from ca 15 to 1500 pairs. We studied if the recent recolonization by the whooper swan into waterfowl communities in Finland has had negative effects on Anas species belonging to the same foraging guild. Using data of foraging behaviour and ecomorphology of the whooper swan and Anas species, we studied the position of the former in the dabbling guild. We used long-term duck census data from different parts of Finland to study changes in breeding numbers of Anas species in lakes that have been recently colonized by the whooper swan and in control lakes that have not been colonized. Overall, foraging and ecomorphological similarity between the whooper swan and the other species decreased in the following order: pintail A. acuta (most similar), mallard A. platyrhynchos , shoveler A. clypeata , garganey A. querquedula. wigeon A. penelope. teal A. crecca (least similar). We did not find evidence of adverse impact by the whooper swan colonization on population densities of the other species. Neither did we find any indication that species relatively more similar with the whooper swan in terms of foraging ecology would show relatively more negative response to the whooper swan colonization. Our results suggest that whooper swans have occupied vacant niche space when colonizing boreal waterfowl communities.     

Differences in foraging ecology determine variation in visual fields in ibises and spoonbills (Threskiornithidae)

Variations in visual field topography among birds have been interpreted as adaptations to the specific perceptual challenges posed by the species’ foraging ecology. To test this hypothesis we determined visual field topography in four bird species which have different foraging ecologies but are from the same family: Puna Ibis Plegadis ridgwayi (probes for prey in the soft substrates of marsh habitats), Northern Bald Ibis Geronticus eremita (surface pecks for prey in dry terrestrial habitats), African Spoonbill Platalea alba and Eurasian Spoonbill Platalea leucorodia (bill‐sweeps for prey in shallow turbid waters). All four species employ tactile cues provided by bill‐tip organs for prey detection. We predicted that the visual fields of these species would show general features similar to those found in other birds whose foraging is guided by tactile cues from the bill (i.e. bill falling outside the frontal binocular field and comprehensive visual coverage of the celestial hemisphere). However, the visual fields of all four species showed general features characteristic of birds that take food directly in the bill under visual guidance (i.e. a narrow and vertically long binocular field in which the projection of the bill tip is approximately central and with a blind area above and behind the head). Visual fields of the two spoonbills were very similar but differed from those of the ibises, which also differed between themselves. In the spoonbills, there was a blind area below the bill produced by the enlarged spatulate bill tip. We discuss how these differences in visual fields are related to the perceptual challenges of these birds’ different foraging ecologies, including the detection, identification and ingestion of prey. In particular we suggest that all species need to see binocularly around the bill and between the opened mandibles for the identification of caught prey items and its transport to the back of the mouth. Our findings support the hypothesis that sensory challenges associated with differences in foraging ecology, rather than shared ancestry or the control of locomotion, are the main determinants of variation in visual field topography in birds.     

Shape at the cross‐roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory

Patterns of skull shape in Carnivora provide examples of parallel and convergent evolution for similar ecomorphological adaptations. However, although most researchers report on skull homoplasies among hypercarnivorous taxa, evolutionary trends towards herbivory remain largely unexplored. In this study, we analyse the skull of the living herbivorous carnivorans to evaluate the importance of natural selection and phylogenetic legacy in shaping the skulls of these peculiar species. We quantitatively estimated shape variability using geometric morphometrics. A principal components analysis of skull shape incorporating all families of arctoid carnivorans recognized several common adaptations towards herbivory. Ancestral state reconstructions of skull shape and the reconstructed phylogenetic history of morphospace occupation more explicitly reveal the true patterns of homoplasy among the herbivorous carnivorans. Our results indicate that both historical constraints and adaptation have interplayed in the evolution towards herbivory of the carnivoran skull, which has resulted in repeated patterns of biomechanical homoplasy.     

Vision and the foraging technique of Great Cormorants Phalacrocorax carbo: pursuit or close‐quarter foraging?

Predatory diving birds, such as cormorants (Phalacrocoracidae), have been generally regarded as visually guided pursuit foragers. However, due to their poor visual resolution underwater, it has recently been hypothesized that Great Cormorants do not in fact employ a pursuit-dive foraging technique. They appear capable of detecting typical prey only at short distances, and primarily use a foraging technique in which prey may be detected only at close quarters or flushed from a substratum or hiding place. In birds, visual field parameters, such as the position and extent of the region of binocular vision, and how these are altered by eye movements, appear to be determined primarily by feeding ecology. Therefore, to understand further the feeding technique of Great Cormorants we have determined retinal visual fields and eye movement amplitudes using an ophthalmoscopic reflex technique. We show that visual fields and eye movements in cormorants exhibit close similarity with those of other birds, such as herons (Ardeidae) and hornbills (Bucerotidae), which forage terrestrially typically using a close-quarter prey detection or flushing technique and/or which need to examine items held in the bill before ingestion. We argue that this visual field topography and associated eye movements is a general characteristic of birds whose foraging requires the detection of nearby mobile prey items from within a wide arc around the head, accurate capture of that prey using the bill, and visual examination of the caught prey held in the bill. This supports the idea that cormorants, although visually guided predators, are not primarily pursuit predators, and that their visual fields exhibit convergence towards a set of characteristics that meet the perceptual challenges of close-quarter prey detection or flush foraging in both aquatic and terrestrial environments.     

Retinal topography of ganglion cells and putative UV-sensitive cones in two Antarctic fishes: Pagothenia borchgrevinki and Trematomus bernacchii (Nototheniidae)

Accessory corner cones (ACC) have recently been suggested to be UV-sensitive photoreceptor cells. With a view toward explaining prey detection, we examined the topography of retinal ganglion cells and ACCs in two Antarctic nototheniids occupying different ecological niches: the cryopelagic Pagothenia borchgrevinki and the benthic Trematomus bernacchii. Isodensity maps of retinal ganglion cells showed that the main visual axis, coincident with the feeding vector, was in a forward direction in both species. Visual acuity was determined as 3.64 and 4.77 cycles/degree for the respective species. In P. borchgrevinki the highest density of ACCs was associated with the eye's main visual axis. This suggested that this species uses UV-vision during forward-swims and probably in encounters with prey. On the other hand, T. bernacchii possessed two horizontal band-shaped high-density areas of ACCs, which stretched from temporal to nasal and ventral to peripheral retinal regions. Therefore, this species appears to use UV-vision to watch prey across the entire circumference of the lateral area and in the water column above its head.     

Does morphology predict behavior? Correspondence between behavioral and morphometric data in a Tyrant‐flycatcher (Tyrannidae) assemblage in the Santa Marta Mountains,Colombia

ABSTRACT Morphology is commonly used as a predictor of ecological relationships among species when studying local assemblages of Neotropical birds. Nevertheless, most evidence supporting ecomorphological correspondence in birds comes from studies of communities and not from local assemblages and, moreover, from temperate latitudes. To increase our understanding of ecomorphological correspondence in Neotropical assemblages, we used three multivariate approaches to evaluate correspondence between morphological and foraging behavior data in a tyrant‐flycatcher assemblage (N= 12 species) in the Santa Marta Mountains in Colombia. Principal components analyses revealed similar species ordinations when using morphological measurements (beak size and shape, tarsus length, wing length, and tail length) or behavioral data (behavioral types of searching for prey and prey capture) separately. Discriminant function analyses tested the ability of morphological traits to predict foraging behavior, showing that more than 90% of all measured individuals (N= 267) were correctly classified in previously defined categories of search and attack behavior. Finally, Canonical correlation analyses revealed a significant correlation between morphological data and two independent datasets of search and attack behavior. Our results demonstrate that morphology can accurately predict ecology in an assemblage of Neotropical tyrannids, and similar results have been reported in previous studies of temperate Tyrant‐flycatchers. Our results also show that bill size and shape, wing length, and tarsus length are the best predictors of foraging behavior in this assemblage. Testing for ecomorphological correspondence in other Neotropical taxa would help identify subsets of phenotypic traits that could be used for a practical, but reliable, determination of ecological relationships within different assemblages.     

Visual fields in woodcocks Scolopax rusticola (Scolopacidae; Charadriiformes)

Woodcocks, Scolopax rusticola, are long-billed terrestrial wading birds (Scolopacidae; Charadriiformes) which forage primarily by probing in soft substrates for invertebrates. Visual field topography in restrained alert birds was investigated using an ophthalmoscopic reflex technique.

1. Eye movements of significant amplitude are absent.
2. The retinal binocular field is long and narrow. It extends through 190° in the median sagittal plane. When the head adopts a normal posture (bill at an angle of 40° below the horizontal) the binocular field stretches from 25° above the bill to 5° above the horizontal behind the head. Thus, woodcocks have comprehensive visual coverage of the hemisphere above them but the bill falls outside the visual field. Maximum binocular field width equals 12° and occurs perpendicular to the line of the bill. To the rear of the head binocular field width is less than 5° except in an area 40° above the horizontal where it increases to 7°.
3. Monocular retinal fields in the horizontal plane are 182° wide. There is no blind sector at the margin of the optical fields.
4. The general structure of woodcock skulls facilitates panoramic vision in a horizontal plane.
5. Interspecific comparisons are consistent with the hypothesis that visual field topography among birds is closely associated with the role of vision in foraging. Comprehensive visual coverage of the celestial hemisphere probably occurs only in species, such as woodcocks, which rely primarily upon senses other than vision to guide foraging.

     

Ecomorphological patterns of aerial feeding in oscines (Passeriformes: Passeri)

The hindlimb (myology and osteology) of swallows (Hirundinidae) is studied and compared with that of seven other passerine families to identify ecomorphological patterns. Muscular and osteological differences are found among swallow species and associations between morphology and foraging technique are examined. We explain morphological differences found in hirundinids as adaptations favouring flexion and adduction of the legs in these aerial foragers, which devote very little time to cursorial locomotion. This adaptive hypothesis is tested using a phylogenetic approach on the basis of an available molecular phylogenetic hypothesis. A clear ecomorphological pattern emerges relating foraging behaviour and pelvic morphology in hirundinids: aerial feeding technique is correlated with short distal leg segments, a large pelvis, a medial insertion of M. iliotibialis cranialis, an absence of pars accessoria of M. flexor cruris lateralis and a fused M. pubo-ischiofemoralis.     

Insights into the adaptive significance of vertical pupil shape in snakes

Pupil shape in vertebrates ranges from circular to vertical, with multiple phylogenetic shifts in this trait. Our analyses challenge the widely held view that the vertical pupil evolved as an adaptation to enhance night vision. On functional grounds, a variable‐aperture vertical pupil (i) allows a nocturnal species to have a sensitive retina for night vision but avoid dazzle by day by adjusting pupil closure, and (ii) increases visual acuity by day, because a narrow vertical pupil can project a sharper image onto the retina in the horizontal plane. Detection of horizontal movement may be critical for predators that wait in ambush for moving prey, suggesting that foraging mode (ambush predation) as well as polyphasic activity may favour the evolution of vertical pupil shape. Camouflage (disruption of the circular outline of the eye) also may be beneficial for ambush predators. A comparative analysis in snakes reveals significant functional links between pupil shape and foraging mode, as well as between pupil shape and diel timing of activity. Similar associations between ambush predation and vertically slit pupils occur in lizards and mammals also, suggesting that foraging mode has exerted major selective forces on visual systems in vertebrates.     

Eye structure and amphibious foraging in albatrosses

Anterior eye structure and retinal visual fields were determined in grey-headed and black-browed albatrosses, Diomedea melanophris and D. chrysostoma (Procellariiformes, Diomedeidae), using keratometry and an ophthalmoscopic reflex technique. Results for the two species were very similar and indicate that the eyes are of an amphibious optical design suggesting that albatross vision is well suited to the visual pursuit of active prey both on and below the ocean surface. The corneas are relatively flat (radius ca. 14.5 mm) and hence of low absolute refractive power (ca. 23 dioptres). In air the binocular fields are relatively long (vertical extent ca. 70 degrees) and narrow (maximum width in the plane of the optic axes 26–32 degrees), a topography found in a range of bird species that employ visual guidance of bill position when foraging. The cyclopean fields measure approximately 270 degrees in the horizontal plane, but there is a 60 degrees blind sector above the head owing to the positioning of the eyes below the protruding supraorbital ridges. Upon immersion the monocular fields decrease in width such that the binocular fields are abolished. Anterior eye structure, and visual field topography in both air and water, show marked similarity with those of the Humboldt penguin.     

Absorbance of retinal oil droplets of the budgerigar: sex,spatial and plumage morph-related variation

Intraspecific variation in photoreceptor physiology is known in several vertebrate taxa, but is currently unknown in birds, despite many avian traits varying intraspecifically, and avian visual ecology encompassing a wide range of environments and visual stimuli, which might influence spectral sensitivity. Avian retinal photoreceptors contain light absorbing carotenoid-rich oil droplets that affect vision. Carotenoids are also important plumage components. However, our understanding of the regulation of carotenoids in oil droplets remains rudimentary. Among birds, Melopsittacus undulatus has probably the best-studied colour vision, shows profound intraspecific variation in plumage colour, and increased plasma carotenoids during moult. We used microspectrophotometry to determine whether a relationship exists between oil droplet carotenoid concentration and plumage pigmentation, and tested for sex and spatial variation in droplet absorbance across the retina. Absorbance of one variety of P-type droplets was higher in males. No relationship was found between droplet absorbance and plumage colour. We found a spatial pattern of droplets absorbance across the retina that matched a pattern found in another parrot, and other avian species. Our work provides insights into the development and maintenance of retinal oil droplets and suggests a common mechanism and function for carotenoid deposition in the retina across bird species.     

Ecogeographical variation in skull morphometry of howler monkeys (Primates: Atelidae)

Our aim is to identify ecomorphological adaptations in the skull shape of the South American howler monkeys (species of the genus Alouatta, Lacépède, 1799, Primates, Atelidae). Since Alouatta is relatively homogenous in feeding ecology, we expect skull shape variation to be relatively conservative across species. We used geometric morphometrics to quantify craniodental morphology in six species of Alouatta. Multivariate regression, two-block Partial Least Squares, and variation partitioning were used to test for the impact of taxonomy, sexual dimorphism, allometry, geography and climate on skull shape. We found morphological overlap among species and sexes, although some discrimination occurs between species living in seasonal environments as opposed to rain forest species. There was a negative latitudinal gradient in skull size across species, with size explaining 34% of total shape variance. Latitude and climate, though important, were secondary in explaining shape variance. Amazonian Alouatta are larger, have thinner molars, wide incisors, and proportionally larger neurocranium. Overall, the shape of southern species seem well adapted to cope with proportionally tougher food items, whereas Amazonian species seem better equipped to deal with a diet richer in fruits, as confirmed by independent field observations. The small size of Alouatta in the South is possibly linked to the effect of competition with the larger folivorous atelid Brachyteles.     

From optics to attention: visual perception in barn owls

Barn owls are nocturnal predators which have evolved specific sensory and morphological adaptations to a life in dim light. Here, some of the most fundamental properties of spatial vision in barn owls are reviewed. The eye with its tubular shape is rigidly integrated in the skull so that eye movements are very much restricted. The eyes are oriented frontally, allowing for a large binocular overlap. Accommodation, but not pupil dilation, is coupled between the two eyes. The retina is rod dominated and lacks a visible fovea. Retinal ganglion cells form a marked region of highest density that extends to a horizontally oriented visual streak. Behavioural visual acuity and contrast sensitivity are poor, although the optical quality of the ocular media is excellent. A low f-number allows high image quality at low light levels. Vernier acuity was found to be a hyperacute percept. Owls have global stereopsis with hyperacute stereo acuity thresholds. Neurons of the visual Wulst are sensitive to binocular disparities. Orientation based saliency was demonstrated in a visual-search experiment, and higher cognitive abilities were shown when the owl’s were able to use illusory contours for object discrimination.     

Retinal ganglion cell topography and visual acuity of the sleepy lizard (<Emphasis Type="Italic">Tiliqua rugosa</Emphasis>)

The spatial distribution of retinal ganglion cells provides valuable insight into the importance species place on observing objects in specific regions of their visual field with higher spatial resolving power. We estimate the total number, distribution and peak density of ganglion cells in retinal wholemounts of the sleepy lizard, Tiliqua rugosa, a scincid lizard endemic to southern Australia. Ganglion cells were readily discernable from amacrine cells by their size and shape, prominent nuclei and the accumulation of Nissl-positive substances in their cytoplasm. A total of 1,654,200 (±59,400) presumed ganglion cells were estimated throughout the retina, distributed irregularly and forming a loose horizontal streak of high cell density peaking at 15,500 cells per mm². With a post nodal distance of 6.25 mm, we calculate an upper limit of visual acuity of 6.8 c/deg.     

The costs of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic Salmon

1. Most animals are active by day or by night, but not both; juvenile salmonids are unusual in that they switch from being predominantly diurnal for most of the year to being nocturnal in winter. They are visual foragers, and adaptations for high visual acuity at daytime light intensities are generally incompatible with sensitive night vision. Here we test whether juvenile Atlantic Salmon Salmo salar are able to maintain their efficiency of prey capture when switching between diurnal and nocturnal foraging.
2. By testing the ability of the fish to acquire drifting food items under a range of manipulated light intensities, we show that the foraging efficiency of juvenile salmon is high at light intensities down to those equivalent to dawn or dusk, but drops markedly at lower levels of illumination: even under the best night condition (full moon and clear sky), the feeding efficiency is only 35% of their diurnal efficiency, and fish will usually be feeding at less than 10% (whenever the moon is not full, skies are overcast or when in the shade of bankside trees). Fish were unable to feed on drifting prey when in complete darkness.
3. The ability of juvenile salmon to detect prey under different light intensities is similar to that of other planktivorous or drift-feeding species of fish; they thus appear to have no special adaptations for nocturnal foraging.
4. While winter drift abundance is slightly higher by night than by day, the difference is not enough to compensate for the loss in foraging efficiency. We suggest that juvenile salmon can nonetheless switch to nocturnal foraging in winter because their food requirements are low, many individuals adopting a strategy in which intake is suppressed to the minimum that ensures survival.     

Sex-specific ecomorphological variation and the evolution of sexual dimorphism in dwarf chameleons (Bradypodion spp.)

Natural selection can influence the evolution of sexual dimorphism through selection for sex-specific ecomorphological adaptations. The role of natural selection in the evolution of sexual dimorphism, however, has received much less attention than that of sexual selection. We examined the relationship between habitat structure and both male and female morphology, and sexual dimorphism in size and shape, across 21 populations of dwarf chameleon (genus Bradypodion). Morphological variation in dwarf chameleons was strongly associated with quantitative, multivariate aspects of habitat structure and, in most cases, relationships were congruent between the sexes. However, we also found consistent relationships between habitat and sexual dimorphism. These resulted from both differences in magnitude of ecomorphological relationships that were otherwise congruent between the sexes, as well as in sex-specific ecomorphological adaptations. Our study provides evidence that natural selection plays an important role in the evolution of sexual dimorphism.