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Visual Signals
Abstract
Esteban Fernández-Juricic completed his undergraduate studies at the Universidad Nacional de Cordoba (Argentina). He did his Ph.D. on animal ecology at the Universidad Complutense de Madrid (Spain). He then did two postdocs in behavioral ecology at the University of Oxford (United Kingdom) and the University of Minnesota (USA). He was an assistant professor for almost 6 years at California State University Long Beach. He is now an associate professor at Purdue University. He is interested in behavioral ecology, visual ecology, and human–wildlife interactions. Website: http://estebanfj.bio.purdue.edu/.
Between-individual variation has been documented in a wide variety of taxa, especially for behavioral characteristics; however, intra-population variation in sensory systems has not received similar attention in wild animals. We measured a key trait of the visual system, the density of retinal cone photoreceptors, in a wild population of house sparrows (Passer domesticus). We tested whether individuals differed from each other in cone densities given within-individual variation across the retina and across eyes. We further tested whether the existing variation could lead to individual differences in two aspects of perception: visual resolution and chromatic contrast. We found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision. Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions. However, there was no evidence for a relationship between individual visual resolution and chromatic contrast. The implication is that some birds may have the sensory potential to perform "better" in certain visual tasks, but not necessarily in both resolution and contrast simultaneously. Overall, our findings (a) highlight the need to consider multiple individuals when characterizing sensory traits of a species, and (b) provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities) and for testing the predictions of several widely accepted hypotheses (e.g., honest signaling).
Predator–prey interactions are regulated by the ability of individuals to detect, and then approach or avoid, each other. In visually guided organisms, the prevalent view is that predators have large binocular visual fields and high acuity, whereas prey have wide lateral areas and low acuity, which could affect vigilance behaviour. We characterized the configuration of the visual system (visual fields, retinal topography, visual acuity) and vigilance behaviour (head movement rate) of two ground-foraging avian prey (white-crowned sparrow, Zonotrichia leucophrys, California towhee, Pipilo crissalis) with laterally placed eyes. We found that the binocular field of both species (45°) was actually wider than those of some of their avian predators. Both species also had a single retinal specialization (high ganglion cell density area) located in the centro-temporal sector of the retina, which projected into the lateral and frontal part of the head. Wide binocular fields may increase binocular contrast to detect and visually guide the bill towards prey items. Both species had wider lateral visual fields and faster head movement rates than some of their predators, probably to enhance detection and visual tracking of predators. California towhees made faster sideways movements of the head than did white-crowned sparrows, probably to cover visual space more quickly with their retinal specialization because of the comparatively lower spatial resolution of their retinal periphery. Alternatively, California towhees might move their heads more rapidly to monitor for potential risks (e.g. competitors, predators), as they rely mostly on personal information because of their degree of territoriality. Our findings suggest that the visual system and vigilance behaviour of these two avian prey species combine traits to enhance predator detection through large visual coverage and fast head movements, but also to enhance food detection at close range through enhanced binocular vision.
Theoretical work suggests that both negative frequency-dependent payoffs and state-dependent payoffs can lead to individual variation in behavioural plasticity. We investigated the roles of both frequency- and state-dependence on the occurrence of individual variation in behavioural plasticity in a series of experiments where we manipulated perceived predation danger for red knots (Calidris canutus islandica). We found individual variation in plasticity in a trait with negative frequency-dependent payoffs (vigilance), but not in a trait with positive frequency-dependent payoffs (escape flights). Furthermore, there was no correlation between the average level of vigilance under low predation danger and the magnitude of response to increased predation danger, as would be expected under state-dependence. Thus, our results provide support for the hypothesis that negative-frequency dependence favours individual variation in plasticity. However, negative-frequency dependence alone cannot explain why plasticity would be consistent within individuals, and future studies should address the factors that might favour individual consistency.
This chapter presents a detailed account of how the pigeon brain detects moving objects, derives depth information from motion parallax, and perceives self-motion. All of these functions are critically important to survival and are accomplished in birds by brain regions along each of the three visual pathways: the collothalamic and lemnothalamic pathways from the retina to the telencephalon, and the pathway consisting of nuclei in the accessory optic system and pretectum. Each pathway processes slightly different aspects of visual motion. © 2012 by Olga F. Lazareva, Toru Shimizu, and Edward A. Wasserman. All rights reserved.
Animal signals are characterized by two design components: efficacy (detectability) and content (message being conveyed). Selection for efficient signal perception should favor the evolution of traits that exhibit an optimal balance between these two design components. We examined the evolution of signal design in the colorful plumage ornaments of manakins (Aves: Pipridae). We used a model of avian color space to quantify how differences in plumage coloration would be perceived by a typical passerine bird and examined patterns of coloration across 50 species of manakin. Using phylogenetically independent contrasts, we show that plumage contrast against the background increases with sexual dichromatism in males but not females, suggesting that sexual selection has favored the evolution of male plumage ornaments that enhance signal efficacy. Plumage contrast within individuals also increased with dichromatism in males but not females. Finally, plumage colors produced by different mechanisms, which may reveal different aspects of quality, resulted in different degrees of contrast against the background. Our findings suggest that selection for signal efficacy and content may sometimes be opposing, creating a trade-off between these two components of signal design. Manakins may mediate this trade-off by combining multiple plumage ornaments that differ in efficacy and content.
Understanding how animals achieve simultaneous con- spicuousness to intended receivers and crypsis to unintended re- ceivers requires investigating the distribution, size, and spectral char- acteristics of color patches. Here we characterize plumage patterns of 40 rainforest bird species living in understory or canopy. Visual signals maximizing (or minimizing) detection are expected to differ between these contrasted light habitats, making rainforests appro- priate to test hypotheses of color signal evolution. Using spectrometry and comparative analyses, we show that canopy and understory act as distinct selective regimes that strongly influence bird coloration. Birds reduce detectability by displaying countershaded patterns, by matching background color and contrast, and by reducing in size the most conspicuous patches. More intense on males than on fe- males, selection for conspicuousness acts on large patches by in- creasing contrast on ventral parts likely to be seen by conspecifics. It also operates on small patches by focusing visual contrast on chest, head, and tail in understory and on wing and tail in canopy, by increasing local brightness contrast compared to general contrast in canopy, and by exploiting different wavelengths for contrast (short in canopy and long in understory). These results are of general in- terest to understanding the evolution of color patterns for all or- ganisms living in contrasted light environments.
Animal ritualized displays have been classically viewed as behavioral characters that decrease signal ambiguity or that facilitate the evaluation of costly exhibitions. It has been shown that their prevalence and level of complexity across species can reflect phylogenetic relationships between them, but the adaptive function of these behavioral traits is poorly known. Here, I hypothesize that, given that the efficacy of visual displays basically depends on conspicuousness and level of performance, species with low levels of conspicuousness may be forced to perform more complex varieties of a given display to get the same signal efficiency than other more conspicuous species. Thus, the evolution of display complexity, considered as the level of exaggeration of ritualized movements, may be explained as an adaptive trait and not only by phylogenetic inertia. I illustrate and test this hypothesis with the case of black-and-white plumage patches of pelecaniform birds. As predicted, there was a negative correlation between level of complexity and species conspicuousness (proportion of unmelanized plumage) for two different social displays. This indicates that classical ideas on the adaptiveness of ritualized displays should be considered to understand the present variation in signal form across species, which sheds light on the evolution of multiple signals.
Effective visual communication requires signals that are easy to detect, transmit, receive, and discriminate. Animals can increase the probability that their visual signals would be detected by evolving signals that contrast with their visual background. Animals can further enhance this contrast by behaviorally modifying the existing visual background. Male golden-collared manakins (Manacus vitellinus) clear leaf litter from the ground to form courts, which are used as display arenas. Using reflectance measures of the signal (male plumage) and the visual background (cleared court and adjacent litter), the irradiance measures of ambient light during display, and published measures of photoreceptor sensitivity of a Passerine, we test the hypothesis that court-clearing augments the contrast between male plumage and the visual background. We find that the chromatic and brightness contrasts of golden patches used during courtship are greater against the cleared court than against adjacent litter. In addition, we find that cleared courts provide a less variable background for these color patches, resulting in displays that consistently contrast the visual background. These results suggest that behavioral modification of the visual background may act to increase the conspicuousness of colorful male plumage during display, providing an explanation for why golden-collared manakins, and possibly other species, build or clear display courts. Copyright 2004.
Evolutionary shifts in species-typical group size ('sociality') probably reflect natural selection on motivational processes such as social arousal, approach-avoidance, reward, stress/anxiety and dominance. Using four songbird species that differ selectively in sociality (one territorial, one modestly gregarious, and two highly gregarious species), we here examined immediate early gene (IEG) responses of relevant brain regions following exposure to a same-sex conspecific. The paradigm limited behavioural performance, thus species differences should reflect divergence in motivational and/or perceptual processes. Within the extended medial amygdala (which is involved in appetitive approach, social arousal and avoidance), we observed species differences in IEG response that are negatively graded in relation to sociality. In addition, brain areas that are involved in social stress and dominance-related behaviour (ventrolateral septum, anterior hypothalamus and lateral subdivision of the ventromedial hypothalamus) exhibited IEG responses that dichotomously distinguish the territorial species from the three gregarious species. The IEG responses of areas involved in reward (nucleus accumbens and ventral pallidum) and general stress processes (e.g. paraventricular hypothalamus, lateral bed nucleus of the stria terminalis and most areas of the lateral septum) do not correlate with sociality, indicating that social evolution has been accompanied by selection on a relatively discrete suite of motivational systems.
Extensive research over the last few decades has revealed that many acoustically communicating animals compensate for the masking effect of background noise by changing the structure of their signals. Familiar examples include birds using acoustic properties that enhance the transmission of vocalizations in noisy habitats. Here, we show that the effects of background noise on communication signals are not limited to the acoustic modality, and that visual noise from windblown vegetation has an equally important influence on the production of dynamic visual displays. We found that two species of Puerto Rican lizard, Anolis cristatellus and A. gundlachi, increase the speed of body movements used in territorial signalling to apparently improve communication in visually 'noisy' environments of rapidly moving vegetation. This is the first evidence that animals change how they produce dynamic visual signals when communicating in noisy motion habitats. Taken together with previous work on acoustic communication, our results show that animals with very different sensory ecologies can face similar environmental constraints and adopt remarkably similar strategies to overcome these constraints.
Publisher Summary Birds can see ultraviolet (UV) light because, unlike humans, their lenses and other ocular media transmit UV, and they possess a class of photoreceptor, which is maximally sensitive to violet or UV light, depending on the species. Birds have a tetrachromatic color space, as compared to the trichromacy of humans. Birds, along with some reptiles and fish, also possess double cones in large numbers and a cone class. This chapter discusses a range of behavioral experiments, from several species, which show that UV information is utilized in behavioral decisions, notably in foraging and signaling. Removal of UV wavelengths affects mate choice even in species that are colorful to humans. These studies emphasize that avian and human color perceptions are different and that the use of human color standards, and even artificial lighting, may produce misleading results. However, genuinely objective measures of color are available, as are, importantly, models for mapping the measured spectra into an avian color space.
Summary 1. Studies of visual ecology generally focus on the tuning of the eye to the spectral environment. However, the environment may also shape vision if the availability of nutrients or other extrinsic stressors impact eye structure or function. 2. Carotenoids are diet-derived pigments that accumulate in the retinas of birds, where they provide photoprotection and tune colour vision. In domesticated species, carotenoid accumulation in retina is dependent on dietary intake, but little is known about the variability in or control of these pigments in the eyes of wild animals. 3. Carotenoids are also deposited in the integument of many animals, where they generate colourful sexually selected displays that communicate information about individual health and nutrition. We hypothesize that retinal carotenoid accumulation is subject to the same health and nutritional constraints as the use of carotenoids in colour signals. 4. As a first test of this hypothesis, we examined retinal carotenoid accumulation in relation to season, sex, body condition, circulating plasma carotenoid concentrations, and plumage colouration in a free ranging population of house finches ( Carpodacus mexicanus ) - a model species for studies of carotenoid ecology. 5. Retinal carotenoid accumulation varied considerably among individuals and differed significantly among seasons, with the highest levels observed in late fall and winter. Body condition and plasma zeaxanthin levels were significantly positively correlated with retinal carotenoid accumulation, but retinal carotenoid concentrations did not differ between the sexes. Plumage redness covaried positively with retinal carotenoid concentration as well, though this relationship was no longer significant when accounting for seasonal variation. 6. Our results, although correlational, do suggest that retinal carotenoid accumulation is a variable trait that may be influenced by environmental and physiological conditions, raising the intriguing possibility that plumage colouration and colour vision could be linked through a common biochemical mechanism.
In studies of animal colouration it is no longer necessary to rely on subjective assessments of colour and conspicuousness, nor on methods which rely upon human vision. This is important because animals vary greatly in colour vision and colour is context-dependent. New methods make it practical to measure the colour spectrum of pattern elements (patches) of animals and their visual backgrounds for the conditions under which patch spectra reach the conspecific's, predator's or prey's eyes. These methods can be used in both terrestrial and aquatic habitats. A patch's colour is dependent not only upon its reflectance spectrum, but also upon the ambient light spectrum, the transmission properties of air or water, and the veiling light spectrum. These factors change with time of day, weather, season and microhabitat, so colours must be measured under the conditions prevalent when colour patterns are normally used. Methods of measuring, classifying and comparing colours are presented, as well as techniques for assessing the conspicuousness of colour patterns as a whole. Some implications of the effect of environmental light and vision are also discussed.
Hitherto, most of the investigation on the perceptual efficacy of begging signals has dwelled on how patterns of nestling colouration adjust to predominant nest luminosity. However, visual sensitivity of birds varies across species, which raises the question of whether colouration of traits involved in begging displays is adjusted to parent visual capacities. Here, by comparing nestling colouration and visual sensitivity across 22 altricial bird species, we provide a first test of this hypothesis. Firstly, we assessed differences in performance of typical UV-tuned and violet-tuned bird eyes when looking at the nestling traits under the light regimes prevailing at their nests. Secondly, while controlling for common ancestry in a comparative approach, we explored variation in colouration of nestlings in relation to parent visual system. The colour discrimination model indicated a general higher performance of the ultraviolet over the violet eye at detecting gape and body skin traits in either open- or hole-nest light conditions. Gape colouration was associated with parental visual system as the nestlings of UVS species displayed more yellow and less pure ultraviolet mouths than the nestlings of VS species. Thus, our results agree with an adaptive parent-offspring communication scenario where the nestlings' colours tuned the perception capacities of their parents.
The Ecology of Vision
- Jn Lythgoe
Lythgoe JN (1979) The Ecology of Vision. New York, NY: Oxford
University Press.
Alarm Calls in Birds and Mammals; Evolution and Phylogeny of Communication; Food Signals; Information Content and Signals; Mating Signals; Multimodal Signaling; Parent–Offspring Signaling; Vision: Vertebrates. Further Reading
- See Also
See also: Alarm Calls in Birds and Mammals; Evolution
and Phylogeny of Communication; Food Signals; Information Content and Signals; Mating Signals; Multimodal
Signaling; Parent–Offspring Signaling; Vision: Vertebrates.
Further Reading
Optimization, constraint, and history in the evolution of eyes
- Th Goldsmith
Goldsmith TH (1990) Optimization, constraint, and history in the
evolution of eyes. Quarterly Review of Biology 65: 281–322.