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.     

Linking piscivory to spatial–temporal distributions of pelagic prey fishes with a visual foraging model

A visual foraging model (VFM) used light-dependent reaction distance and capture success functions to link observed prey fish abundance and distribution to predation rates and the foraging performance of piscivorous cutthroat trout Oncorhynchus clarki in Lake Washington (WA, U.S.A.). Total prey density did not correlate with predation potential estimated by the foraging model for cutthroat trout because prey were rarely distributed in optically favourable conditions for detection. Predictions of the depth-specific distribution and timing of cutthroat trout foraging were qualitatively similar to diel stomach fullness patterns observed in field samples. Nocturnal foraging accounted for 34–64% of all prey fish consumption in simulations for 2002 and 2003. Urban light contamination increased the access of nocturnally foraging cutthroat trout to vertically migrating prey fishes. These results suggest that VFMs are useful tools for converting observed prey fish density into predictions of predator consumptions and behavioural responses of predators to environmental change.     

Understanding bird collisions with man‐made objects: a sensory ecology approach

Sensory ecology investigates the information that underlies an animal’s interactions with its environment. A sensory ecology framework is used here to seek to assess why flying birds collide with prominent structures, such as power lines, fences, communication masts, wind turbines and buildings, which intrude into the open airspace. Such collisions occur under conditions of both high and low visibility. It is argued that a human perspective of the problems posed by these obstacles is unhelpful. Birds live in different visual worlds and key aspects of these differences are summarized. When in flight, birds may turn their heads in both pitch and yaw to look down, either with the binocular field or with the lateral part of an eye’s visual field. Such behaviour may be usual and results in certain species being at least temporarily blind in the direction of travel. Furthermore, even if birds are looking ahead, frontal vision may not be in high resolution. In general, high resolution occurs in the lateral fields of view and frontal vision in birds may be tuned for the detection of movement concerned with the extraction of information from the optical flow field, rather than the detection of high spatial detail. Birds probably employ lateral vision for the detection of conspecifics, foraging opportunities and predators. The detection of these may be more important than simply looking ahead during flight in the open airspace. Birds in flight may predict that the environment ahead is not cluttered. Even if they are facing forward, they may fail to see an obstacle as they may not predict obstructions; perceptually they have no ‘prior’ for human artefacts such as buildings, power wires or wind turbines. Birds have only a restricted range of flight speeds that can be used to adjust their rate of gain of visual information as the sensory challenges of the environment change. It is argued that to reduce collisions with known hazards, something placed upon the ground may be more important than something placed on the obstacle itself. Foraging patches, conspecific models or alerting sounds placed a suitable distance from the hazard may be an effective way of reducing collisions in certain locations. However, there is unlikely to be a single effective way to reduce collisions for multiple species at any one site. Warning or diversion and distraction solutions may need to be tailored for particular target species.     

Visual fields,foraging and collision vulnerability in Gyps vultures

The visual fields of vultures contain a small binocular region and large blind areas above, below and behind the head. Head positions typically adopted by foraging vultures suggest that these visual fields provide comprehensive visual coverage of the ground below, prohibit the eyes from imaging the sun and provide extensive visual coverage laterally. However, vultures will often be blind in the direction of travel. We conclude that by erecting structures such as wind turbines, which extend into open airspace, humans have provided a perceptual challenge that the vision of foraging vultures cannot overcome.     

Visual fields and foraging ecology of Blacksmith Lapwings Vanellus armatus

The visual fields of Blacksmith Lapwings Vanellus armatus show the characteristics of visual guided foragers that use precision pecking for prey capture – a binocular field of narrow width and limited vertical extent, with the projection of the bill close to its centre and a large blind area above and behind the head. The topography of the total field, particularly the binocular field, is similar to that of European Golden Plovers Pluvialis apricaria. We suggest that the ‘foot‐trembling’ behaviour associated with foraging in Plovers is not under visual guidance but forces the escape of hidden prey, which is detected when the prey item moves into the binocular field to enable its capture in the bill. Foot‐trembling thus functions to extend the effective foraging area of a bird beyond the limits of its visual field.     

Evolution and spectral tuning of visual pigments in birds and mammals

Variation in the types and spectral characteristics of visual pigments is a common mechanism for the adaptation of the vertebrate visual system to prevailing light conditions. The extent of this diversity in mammals and birds is discussed in detail in this review, alongside an in-depth consideration of the molecular changes involved. In mammals, a nocturnal stage in early evolution is thought to underlie the reduction in the number of classes of cone visual pigment genes from four to only two, with the secondary loss of one of these genes in many monochromatic nocturnal and marine species. The trichromacy seen in many primates arises from either a polymorphism or duplication of one of these genes. In contrast, birds have retained the four ancestral cone visual pigment genes, with a generally conserved expression in either single or double cone classes. The loss of sensitivity to ultraviolet (UV) irradiation is a feature of both mammalian and avian visual evolution, with UV sensitivity retained among mammals by only a subset of rodents and marsupials. Where it is found in birds, it is not ancestral but newly acquired.     

Quantitative estimates of visual performance features in fossil birds

Eyeball structures such as the lens diameter (LD) and axial length are generally assumed to be highly correlated with optically meaningful parameters. However, these optical constraints on eyeball macroanatomy have never been tested explicitly. Tradeoffs between benefits of improved visual performance and cost of adaptation from an increase of tissue production predict that when eyeball size increases, optical parameters such as posterior nodal distance and maximum entrance pupil diameter should increase isometrically with eyeball axial length and LD, respectively. Here I show quantitatively that the interspecific allometry of the avian eye largely follows this predicted isometry. Additionally, I elaborate a method to estimate optically significant eyeball soft‐tissue dimensions from scleral ring and orbit morphology based on analyses of interspecific allometry in Aves. The stringent correlations between avian eyeball morphology and optical function render this system ideal for the analysis of form–function relationships and allow for an accurate estimate of optically significant eyeball soft‐tissue dimensions such as diameter, axial length, and LD in fossil species. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Defining the V5/MT neuronal pool for perceptual decisions in a visual stereo-motion task

In the primate visual cortex, neurons signal differences in the appearance of objects with high precision. However, not all activated neurons contribute directly to perception. We defined the perceptual pool in extrastriate visual area V5/MT for a stereo-motion task, based on trial-by-trial co-variation between perceptual decisions and neuronal firing (choice probability (CP)). Macaque monkeys were trained to discriminate the direction of rotation of a cylinder, using the binocular depth between the moving dots that form its front and rear surfaces. We manipulated the activity of single neurons trial-to-trial by introducing task-irrelevant stimulus changes: dot motion in cylinders was aligned with neuronal preference on only half the trials, so that neurons were strongly activated with high firing rates on some trials and considerably less activated on others. We show that single neurons maintain high neurometric sensitivity for binocular depth in the face of substantial changes in firing rate. CP was correlated with neurometric sensitivity, not level of activation. In contrast, for individual neurons, the correlation between perceptual choice and neuronal activity may be fundamentally different when responding to different stimulus versions. Therefore, neuronal pools supporting sensory discrimination must be structured flexibly and independently for each stimulus configuration to be discriminated.This article is part of the themed issue ‘Vision in our three-dimensional world''.     

Flexible responses to visual and olfactory stimuli by foraging Manduca sexta: larval nutrition affects adult behaviour

Here, we show that the consequences of deficient micronutrient (β-carotene) intake during larval stages of Manduca sexta are carried across metamorphosis, affecting adult behaviour. Our manipulation of larval diet allowed us to examine how developmental plasticity impacts the interplay between visual and olfactory inputs on adult foraging behaviour. Larvae of M. sexta were reared on natural (Nicotiana tabacum) and artificial laboratory diets containing different concentrations of β-carotene (standard diet, low β-carotene, high β-carotene and cornmeal). This vitamin-A precursor has been shown to be crucial for photoreception sensitivity in the retina of M. sexta. After completing development, post-metamorphosis, starved adults were presented with artificial feeders that could be either scented or unscented. Regardless of their larval diet, adult moths fed with relatively high probabilities on scented feeders. When feeders were unscented, moths reared on tobacco were more responsive than moths reared on β-carotene-deficient artificial diets. Strikingly, moths reared on artificial diets supplemented with increasing amounts of β-carotene (low β and high β) showed increasing probabilities of response to scentless feeders. We discuss these results in relationship to the use of complex, multi-modal sensory information by foraging animals.     

The Polarization of Light in a Tropical Rain Forest1

The light environment within forests presents complex patterns of brightness and spectral distribution of light. The polarized light field is no less complex. Using an imaging polarized light analyzer, we examined the natural fields of linearly polarized light in the tropical rain forest of Guatopo National Park, Venezuela. We found that the celestial polarization pattern remains visible underneath the forest canopy, although cloud and fog coverage may diffuse the light and reduce the polarization signal. We characterized several distinct light environments, each having a characteristic polarized light field. Furthermore, objects throughout the forest reflect light that is polarized in a predictable fashion depending upon the material, structure, and orientation of the reflecting surface. As a consequence of these patterns in the distribution of polarized light, some functions of polarization vision, such as navigation, must be limited to the spaces exposed to several extended portions of the sky, while others, such as remote sensing of surface orientation, object detection, and breaking of camouflage would be useful throughout the forest. The polarization of light adds another dimension to the complexity of the rain forest photic environment.     

The visual fields of two ground‐foraging birds,House Finches and House Sparrows,allow for simultaneous foraging and anti‐predator vigilance

In birds, differences in the extent and position of the binocular visual field reflect adaptations to varying foraging strategies, and the extent of the lateral portion of the field may reflect anti‐predator strategies. The goal of this study was to describe and compare the visual fields of two ground‐foraging passerines, House Finch Carpodacus mexicanus and House Sparrow Passer domesticus. We found that both species have a binocular field type that is associated with the accurate control of bill position when pecking. Both species have eye movements of relatively large amplitude, which can produce substantial variations in the configuration of the binocular fields. We propose that in these ground foragers, their relatively wide binocular fields could function to increase foraging efficiency by locating multiple rather than single food items prior to pecking events. The lateral fields of both species are wide enough to facilitate the detection of predators or conspecifics while head‐down foraging. This suggests that foraging and scanning are not mutually exclusive activities in these species, as previously assumed. Furthermore, we found some slight, but significant, differences between species: House Sparrow binocular fields are both wider and vertically taller, and the blind area is wider than in House Finches. These differences may be related to variations in the degree of eye movements and position of the orbits in the skull.     

The visual ecology of a deep-sea fish,the escolar Lepidocybium flavobrunneum (Smith, 1843)

Escolar (Lepidocybium flavobrunneum, family Gempylidae) are large and darkly coloured deep-sea predatory fish found in the cold depths (more than 200 m) during the day and in warm surface waters at night. They have large eyes and an overall low density of retinal ganglion cells that endow them with a very high optical sensitivity. Escolar have banked retinae comprising six to eight layers of rods to increase the optical path length for maximal absorption of the incoming light. Their retinae possess two main areae of higher ganglion cell density, one in the ventral retina viewing the dorsal world above (with a moderate acuity of 4.6 cycles deg⁻¹), and the second in the temporal retina viewing the frontal world ahead. Electrophysiological recordings of the flicker fusion frequency (FFF) in isolated retinas indicate that escolar have slow vision, with maximal FFF at the highest light levels and temperatures (around 9 Hz at 23°C) which fall to 1–2 Hz in dim light or cooler temperatures. Our results suggest that escolar are slowly moving sit-and-wait predators. In dim, warm surface waters at night, their slow vision, moderate dorsal resolution and highly sensitive eyes may allow them to surprise prey from below that are silhouetted in the downwelling light.     

蜜蜂复眼的视觉通路研究进展

视觉通路的研究在神经科学、 仿生应用和医学治疗上都具有十分重要的意义。西方蜜蜂Apis mellifera作为神经生物学研究的重要模式生物已被广泛地应用于视觉通路的研究。蜜蜂的视觉器官包括1对复眼和3只单眼, 复眼是形成视觉的主要感觉器官。视叶是蜜蜂传递和处理视觉信息的主要神经构造, 它包括视神经节层、 视髓质层、 视小叶和前视结节4个等级的神经纤维网。复杂的视觉信息在经过大脑的各级神经时被分离, 以许多空间隔离的并行连续的视觉通路传递和加工, 然后汇集到高级脑中枢, 部分甚至与其他感觉模态的信息相整合, 最终输出有效信息来调控蜜蜂的各种行为。本文按照信息在视叶中逐级传递的顺序对蜜蜂复眼的视觉通路研究进展进行综述。     

The visual fields of Common Guillemots Uria aalge and Atlantic Puffins Fratercula arctica: foraging,vigilance and collision vulnerability

Significant differences in avian visual fields are found between closely related species that differ in their foraging technique. We report marked differences in the visual fields of two auk species. In air, Common Guillemots Uria aalge have relatively narrow binocular fields typical of those found in non‐passerine predatory birds. Atlantic Puffins Fratercula arctica have much broader binocular fields similar to those that have hitherto been recorded in passerines and in a penguin. In water, visual fields narrow considerably and binocularity in the direction of the bill is probably abolished in both auk species. Although perceptual challenges associated with foraging are similar in both species during the breeding season, when they are piscivorous, Puffins (but not Guillemots) face more exacting perceptual challenges when foraging at other times, when they take a high proportion of small invertebrate prey. Capturing this prey probably requires more accurate, visually guided bill placement and we argue that this is met by the Puffin's broader binocular field, which is retained upon immersion; its upward orientation may enable prey to be seen in silhouette. These visual field configurations have potentially important consequences that render these birds vulnerable to collision with human artefacts underwater, but not in air. They also have consequences for vigilance behaviour.     

Nest covering in plovers: How modifying the visual environment influences egg camouflage

Camouflage is one of the most widespread antipredator defences, and its mechanistic basis has attracted considerable interest in recent years. The effectiveness of camouflage depends on the interaction between an animal's appearance and its background. Concealment can therefore be improved by changes to an animal's own appearance, by behaviorally selecting an optimal background, or by modifying the background to better match the animal's own appearance. Research to date has largely focussed on the first of these mechanisms, whereas there has been little work on the second and almost none on the third. Even though a number of animal species may potentially modify their environment to improve individual‐specific camouflage, this has rarely if ever been quantitatively investigated, or its adaptive value tested. Kittlitz's plovers (Charadrius pecuarius) use material (stones and vegetation) to cover their nests when predators approach, providing concealment that is independent of the inflexible appearance of the adult or eggs, and that can be adjusted to suit the local surrounding background. We used digital imaging and predator vision modeling to investigate the camouflage properties of covered nests, and whether their camouflage affected their survival. The plovers' nest‐covering materials were consistent with a trade‐off between selecting materials that matched the color of the eggs, while resulting in poorer nest pattern and contrast matching to the nest surroundings. Alternatively, the systematic use of materials with high‐contrast and small‐pattern grain sizes could reflect a deliberate disruptive coloration strategy, whereby high‐contrast material breaks up the telltale outline of the clutch. No camouflage variables predicted nest survival. Our study highlights the potential for camouflage to be enhanced by background modification. This provides a flexible system for modifying an animal's conspicuousness, to which the main limitation may be the available materials rather than the animal's appearance.     

The normalized segment classification model: A new tool to compare spectral reflectance curves

1. Color patterns are complex traits under selective pressures from conspecifics, mutualists, and antagonists. To evaluate the salience of a pattern or the similarity between colors, several visual models are available. Color discrimination models estimate the perceptual difference between any two colors. Their application to a diversity of taxonomic groups has become common in the literature to answer behavioral, ecological, and evolutionary questions. To use these models, we need information about the visual system of our beholder species. However, many color patterns are simultaneously subject to selective pressures from different species, often from different taxonomic groups, with different visual systems. Furthermore, we lack information about the visual system of many species, leading ecologists to use surrogate values or theoretical estimates for model parameters.
2. Here, we present a modification of the segment classification method proposed by Endler (Biological Journal of the Linnean Society, 1990 41, 315–352): the normalized segment classification model (NSC). We explain its logic and use, exploring how NSC differs from other visual models. We also compare its predictions with available experimental data.
3. Even though the NSC model includes no information about the visual system of the receiver species, it performed better than traditional color discrimination models when predicting the output of some behavioral tasks. Although vision scientists define color as independent of stimulus brightness, a likely explanation for the goodness of fit of the NSC model is that its distance measure depends on brightness differences, and achromatic information can influence the decision‐making process of animals when chromatic information is missing.
4. Species‐specific models may be insufficient for the study of color patterns in a community context. The NSC model offers a species‐independent solution for color analyses, allowing us to calculate color differences when we ignore the intended viewer of a signal or when different species impose selective pressures on the signal.

     

Conspicuousness of Dickerson's collared lizard (Crotaphytus dickersonae) through the eyes of conspecifics and predators

Selection should favour coloration in organisms that is more conspicuous to their own visual system than to those of their predators or prey. We tested this prediction in Dickerson's collared lizard ( Crotaphytus dickersonae ), a sexually dichromatic desert reptile that preys on insects and smaller lizard species, and which in turn is prey for birds and snakes. We modelled the spectral sensitivities of the lizards and their avian and snake predators, and compared the conspicuousness of the lizards' entire colour patterns with each class of viewers. Almost all comparisons involving females strongly supported our prediction for greater chromatic and brightness conspicuousness against local terrestrial visual backgrounds to their own modelled visual system than to those of avian and snake predators. Males, in contrast, exhibited far fewer cases of greater conspicuousness to their own visual system than to those of their predators. Our own perception of spectral similarity between blue C. dickersonae males and a local nonterrestrial visual background (i.e. the Sea of Cortéz) prompted a further investigation. We compared sea (and sky) radiance with dorsum radiance of C. dickersonae males and with males from two distantly-related Crotaphytus collaris populations in which males possess blue bodies. In all three visual models, C. dickersonae males exhibited significantly lower chromatic contrast with the sea (and sky) than did their noncoastal, blue-bodied congeners. Among potential explanations, the blue body coloration that is unique to male C. dickersonae may offset, if only slightly, the cost of visibility to predators (and to prey) through reduced contrast against the extensive, local, nonterrestrial blue backgrounds of the sea and sky.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 749–765.     

The stepwise development of the lamprey visual system and its evolutionary implications

Lampreys, which represent the oldest group of living vertebrates (cyclostomes), show unique eye development. The lamprey larva has only eyespot‐like immature eyes beneath a non‐transparent skin, whereas after metamorphosis, the adult has well‐developed image‐forming camera eyes. To establish a functional visual system, well‐organised visual centres as well as motor components (e.g. trunk muscles for locomotion) and interactions between them are needed. Here we review the available knowledge concerning the structure, function and development of the different parts of the lamprey visual system. The lamprey exhibits stepwise development of the visual system during its life cycle. In prolarvae and early larvae, the ‘primary’ retina does not have horizontal and amacrine cells, but does have photoreceptors, bipolar cells and ganglion cells. At this stage, the optic nerve projects mostly to the pretectum, where the dendrites of neurons in the nucleus of the medial longitudinal fasciculus (nMLF) appear to receive direct visual information and send motor outputs to the neck and trunk muscles. This simple neural circuit may generate negative phototaxis. Through the larval period, the lateral region of the retina grows again to form the ‘secondary’ retina and the topographic retinotectal projection of the optic nerve is formed, and at the same time, the extra‐ocular muscles progressively develop. During metamorphosis, horizontal and amacrine cells differentiate for the first time, and the optic tectum expands and becomes laminated. The adult lamprey then has a sophisticated visual system for image‐forming and visual decision‐making. In the adult lamprey, the thalamic pathway (retina–thalamus–cortex/pallium) also transmits visual stimuli. Because the primary, simple light‐detecting circuit in larval lamprey shares functional and developmental similarities with that of protochordates (amphioxus and tunicates), the visual development of the lamprey provides information regarding the evolutionary transition of the vertebrate visual system from the protochordate‐type to the vertebrate‐type.