The Evolution of Simplifying Heuristics in Visual Cognition: Categorization, Specialization, and Visual Illusions.

Animals live in visually complex environments. As a result, visual systems have evolved mechanisms that simplify visual processing and allow animals to focus on the information that is most relevant to adaptive decision making. This review explores two key mechanisms that animals use to efficiently process visual information: categorization and specialization. Categorization occurs when an animal's perceptual system sorts continuously varying stimuli into a set of discrete categories. Specialization occurs when particular classes of stimuli are processed using distinct cognitive operations that are not used for other classes of stimuli. We also describe a nonadaptive consequence of simplifying heuristics: visual illusions, where visual perception consistently misleads the viewer about the state of the external world or objects within it. We take an explicitly comparative approach by exploring similarities and differences in visual cognition across human and nonhuman taxa. Considering areas of convergence and divergence across taxa provides insight into the evolution and function of visual systems and associated perceptual strategies.

Backgrounds and the evolution of visual signals.

Color signals which mediate behavioral interactions across taxa and contexts are often thought of as color 'patches' - parts of an animal that appear colorful compared to other parts of that animal. Color patches, however, cannot be considered in isolation because how a color is perceived depends on its visual background. This is of special relevance to the function and evolution of signals because backgrounds give rise to a fundamental tradeoff between color signal detectability and discriminability: as its contrast with the background increases, a color patch becomes more detectable, but discriminating variation in that color becomes more difficult. Thus, the signal function of color patches can only be fully understood by considering patch and background together as an integrated whole.

Ecological and morphological correlates of visual acuity in birds.

Birds use their visual systems for important tasks, such as foraging and predator detection, that require them to resolve an image. However, visual acuity (the ability to perceive spatial detail) varies by two orders of magnitude across birds. Prior studies indicate that eye size and aspects of a species' ecology may drive variation in acuity, but these studies have been restricted to small numbers of species. We used a literature review to gather data on acuity measured either behaviorally or anatomically for 94 species from 38 families. We then examined how acuity varies in relation to (1) eye size, (2) habitat spatial complexity, (3) habitat light level, (4) diet composition, (5) prey mobility and (6) foraging mode. A phylogenetically controlled model including all of the above factors as predictors indicated that eye size and foraging mode are significant predictors of acuity. Examining each ecological variable in turn revealed that acuity is higher in species whose diet comprises vertebrates or scavenged food and whose foraging modes require resolving prey from farther away. Additionally, species that live in spatially complex, vegetative habitats have lower acuity than expected for their eye sizes. Together, our results suggest that the need to detect important objects from far away - such as predators for species that live in open habitats, and food items for species that forage on vertebrate and scavenged prey - has likely been a key driver of higher acuity in some species, helping us to elucidate how visual capabilities may be adapted to an animal's visual needs.

Weber's Law.

Bullough et al. introduce Weber's Law and proportional processing during perception.

Measures and models of visual acuity in epipelagic and mesopelagic teleosts and elasmobranchs.

Eyes in low-light environments typically must balance sensitivity and spatial resolution. Vertebrate eyes with large "pixels" (e.g., retinal ganglion cells with inputs from many photoreceptors) will be sensitive but provide coarse vision. Small pixels can render finer detail, but each pixel will gather less light, and thus have poor signal relative-to-noise, leading to lower contrast sensitivity. This balance is particularly critical in oceanic species at mesopelagic depths (200-1000 m) because they experience low light and live in a medium that significantly attenuates contrast. Depending on the spatial frequency and inherent contrast of a pattern being viewed, the viewer's pupil size and temporal resolution, and the ambient light level and water clarity, a visual acuity exists that maximizes the distance at which the pattern can be discerned. We develop a model that predicts this acuity for common conditions in the open ocean, and compare it to visual acuity in marine teleost fishes and elasmobranchs found at various depths in productive and oligotrophic waters. Visual acuity in epipelagic and upper mesopelagic species aligned well with model predictions, but species at lower mesopelagic depths (> 600 m) had far higher measured acuities than predicted. This is consistent with the prediction that animals found at lower mesopelagic depths operate in a visual world consisting primarily of bioluminescent point sources, where high visual acuity helps localize targets of this kind. Overall, the results suggest that visual acuity in oceanic fish and elasmobranchs is under depth-dependent selection for detecting either extended patterns or point sources.

Proportional processing of a visual mate choice signal in the green swordtail, Xiphophorus hellerii.

During mate choice, receivers often assess the magnitude (duration, size, etc.) of signals that vary along a continuum and reflect variation in signaller quality. It is generally assumed that receivers assess this variation linearly, meaning each difference in signalling trait between signallers results in a commensurate change in receiver response. However, increasing evidence shows receivers can respond to signals non-linearly, for example through Weber's Law of proportional processing, where discrimination between stimuli is based on proportional, rather than absolute, differences in magnitude. We quantified mate preferences of female green swordtail fish, Xiphophorus hellerii, for pairs of males differing in body size. Preferences for larger males were better predicted by the proportional difference between males (proportional processing) than the absolute difference (linear processing). This demonstration of proportional processing of a visual signal implies that receiver perception may be an important mechanism selecting against the evolution of ever-larger signalling traits.

Sex differences in behavioural and anatomical estimates of visual acuity in the green swordtail, Xiphophorus helleri.

Among fishes in the family Poeciliidae, signals such as colour patterns, ornaments and courtship displays play important roles in mate choice and male-male competition. Despite this, visual capabilities in poeciliids are understudied, in particular, visual acuity, the ability to resolve detail. We used three methods to quantify visual acuity in male and female green swordtails (Xiphophorus helleri), a species in which body size and the length of the male's extended caudal fin ('sword') serve as assessment signals during mate choice and agonistic encounters. Topographic distribution of retinal ganglion cells (RGCs) was similar in all individuals and was characterized by areas of high cell densities located centro-temporally and nasally, as well as a weak horizontal streak. Based on the peak density of RGCs in the centro-temporal area, anatomical acuity was estimated to be approximately 3 cycles per degree (cpd) in both sexes. However, a behavioural optomotor assay found significantly lower mean acuity in males (0.8 cpd) than females (3.0 cpd), which was not explained by differences in eye size between males and females. An additional behavioural assay, in which we trained individuals to discriminate striped gratings from grey stimuli of the same mean luminance, also showed lower acuity in males (1-2 cpd) than females (2-3 cpd). Thus, although retinal anatomy predicts identical acuity in males and females, two behavioural assays found higher acuity in females than males, a sexual dimorphism that is rare outside of invertebrates. Overall, our results have implications for understanding how poeciliids perceive visual signals during mate choice and agonistic encounters.

Why and how to apply Weber's Law to coevolution and mimicry.

In mimicry systems, receivers discriminate between the stimuli of models and mimics. Weber's Law of proportional processing states that receiver discrimination is based on proportional, not absolute, differences between stimuli. Weber's Law operates in a variety of taxa and modalities, yet it has largely been ignored in the context of mimicry, despite its potential relevance to whether receivers can discriminate models from mimics. Specifically, Weber's Law implies that for a given difference in stimulus magnitude between a model and mimic, as stimulus magnitudes increase, the mimic will be less discriminable from their model. This implies that mimics should benefit when stimulus magnitudes are high, and that high stimulus magnitudes will reduce selection for mimetic fidelity. Whether models benefit from high stimulus magnitudes depends on whether mimicry is honest or deceptive. We present four testable predictions about evolutionary trajectories of models and mimics based on this logic. We then provide a framework for testing whether receiver discrimination adheres to Weber's Law and illustrate it using coevolutionary examples and case studies from avian brood parasitism. We conclude that, when studying mimicry systems, researchers should consider whether receiver perception conforms to Weber's Law, because it could drive stimulus evolution in counterintuitive directions.

The behavioural ecology of marine cleaning mutualisms.

Cleaning interactions, in which a small 'cleaner' organism removes and often consumes material from a larger 'client', are some of the most enigmatic and intriguing of interspecies interactions. Early research on cleaning interactions canonized the view that they are mutualistic, with clients benefiting from parasite removal and cleaners benefiting from a meal, but subsequent decades of research have revealed that the dynamics of these interactions can be highly complex. Despite decades of research on marine cleaning interactions (the best studied cleaning systems), key questions remain, including how the outcome of an individual cleaning interaction depends on ecological, behavioural, and social context, how such interactions arise, and how they remain stable over time. Recently, studies of marine parasites, long-term data from coral reef communities with and without cleaners, increased behavioural observations recorded using remote video, and a focus on a larger numbers of cleaning species have helped bring about key conceptual advances in our understanding of cleaning interactions. In particular, evidence now suggests that the ecological, behavioural, and social contexts of a given cleaning interaction can result in the outcome ranging from mutualistic to parasitic, and that cleaning interactions are mediated by signals that can also vary with context. Signals are an important means by which animals extract information about one another, and thus represent a mechanism by which interspecific partners can determine when, how, and with whom to interact. Here, I review our understanding of the behavioural ecology of marine cleaning interactions. In particular, I argue that signals provide a useful framework for advancing our understanding of several important outstanding questions. I discuss the costs and benefits of cleaning interactions, review how cleaners and clients recognize and assess one another using signals, and discuss how signal reliability, or 'honesty', may be maintained in cleaning systems. Lastly, I discuss the sensory ecology of both cleaners and clients to highlight what marine cleaning systems can tell us about signalling behaviour, signal form, and signal evolution in a system where signals are aimed at multiple receiver species. Overall, I argue that future research on cleaning interactions has much to gain by continuing to shift the research focus toward examining the variable outcomes of cleaning interactions in relation to the broader behavioural, social, and ecological contexts.

Hosts elevate either within-clutch consistency or between-clutch distinctiveness of egg phenotypes in defence against brood parasites.

In host-parasite arms races, hosts can evolve signatures of identity to enhance the detection of parasite mimics. In theory, signatures are most effective when within-individual variation is low ('consistency'), and between-individual variation is high ('distinctiveness'). However, empirical support for positive covariation in signature consistency and distinctiveness across species is mixed. Here, we attempt to resolve this puzzle by partitioning distinctiveness according to how it is achieved: (i) greater variation within each trait, contributing to elevated 'absolute distinctiveness' or (ii) combining phenotypic traits in unpredictable combinations ('combinatorial distinctiveness'). We tested how consistency covaries with each type of distinctiveness by measuring variation in egg colour and pattern in two African bird families (Cisticolidae and Ploceidae) that experience mimetic brood parasitism. Contrary to predictions, parasitized species, but not unparasitized species, exhibited a negative relationship between consistency and combinatorial distinctiveness. Moreover, regardless of parasitism status, consistency was negatively correlated with absolute distinctiveness across species. Together, these results suggest that (i) selection from parasites acts on how traits combine rather than absolute variation in traits, (ii) consistency and distinctiveness are alternative rather than complementary elements of signatures and (iii) mechanistic constraints may explain the negative relationship between consistency and absolute distinctiveness across species.

The sensory impacts of climate change: bathymetric shifts and visually mediated interactions in aquatic species.

Visual perception is, in part, a function of the ambient illumination spectrum. In aquatic environments, illumination depends upon the water's optical properties and depth, both of which can change due to anthropogenic impacts: turbidity is increasing in many aquatic habitats, and many species have shifted deeper in response to warming surface waters (known as bathymetric shifts). Although increasing turbidity and bathymetric shifts can result in similarly large changes to a species' optical environment, no studies have yet examined the impact of the latter on visually mediated interactions. Here, we examine a potential link between climate change and visual perception, with a focus on colour. We discuss (i) what is known about bathymetric shifts; (ii) how the impacts of bathymetric shifts on visual interactions may be distributed across species; (iii) which interactions might be affected; and (iv) the ways that animals have to respond to these changes. As warming continues and temperature fluctuations grow more extreme, many species may move into even deeper waters. There is thus a need for studies that examine how such shifts can affect an organism's visual world, interfere with behaviour, and impact fitness, population dynamics, and community structure.

Comparison of Categorical Color Perception in Two Estrildid Finches.

AbstractSensory systems are predicted to be adapted to the perception of important stimuli, such as signals used in communication. Prior work has shown that female zebra finches perceive the carotenoid-based orange-red coloration of male beaks-a mate choice signal-categorically. Specifically, females exhibited an increased ability to discriminate between colors from opposite sides of a perceptual category boundary than equally different colors from the same side of the boundary. The Bengalese finch, an estrildid finch related to the zebra finch, is black, brown, and white, lacking carotenoid coloration. To explore the relationship between categorical color perception and signal use, we tested Bengalese finches using the same orange-red continuum as in zebra finches, and we also tested how both species discriminated among colors differing systematically in hue and brightness. Unlike in zebra finches, we found no evidence of categorical perception of an orange-red continuum in Bengalese finches. Instead, we found that the combination of chromatic distance (hue difference) and Michelson contrast (difference in brightness) strongly correlated with color discrimination ability on all tested color pairs in Bengalese finches. The pattern was different in zebra finches: this strong correlation held when discriminating between colors from different categories but not when discriminating between colors from within the same category. These experiments suggest that categorical perception is not a universal feature of avian-or even estrildid finch-vision. Our findings also provide further insights into the mechanism underlying categorical perception and are consistent with the hypothesis that categorical perception is adapted for signal perception.

The cleaner shrimp Lysmata amboinensis adjusts its behaviour towards predatory versus non-predatory clients.

In cleaning mutualisms, small cleaner organisms remove ectoparasites and dead skin from larger clients. Because cheating by predatory clients can result in cleaner death, cleaners should assess the potential risk of interacting with a given client and adjust their behaviour accordingly. Cleaner shrimp are small marine crustaceans that interact with numerous client fish species, many of which are potential predators. We use in situ observations of cleaner-client interactions to show that the cleaner shrimp Lysmata amboinensis adjusts several behaviours when interacting with predatory versus non-predatory clients. Predatory clients were cleaned in a significantly lower proportion of interactions than non-predatory clients, and cleaners also exhibited a leg rocking behaviour-potentially signalling their identity or intent to clean-almost exclusively toward predatory clients. Incidence of leg rocking was positively correlated with client size, and laboratory experiments showed that it can be elicited by dark visual stimuli and decreases in illumination level. Thus, cleaners clean less frequently when predation risk is higher, and may use leg rocking as a signal advertising cleaning services and directed specifically at predators.

Categorical colour perception occurs in both signalling and non-signalling colour ranges in a songbird.

Although perception begins when a stimulus is transduced by a sensory neuron, numerous perceptual mechanisms can modify sensory information as it is processed by an animal's nervous system. One such mechanism is categorical perception, in which (1) continuously varying stimuli are labelled as belonging to a discrete number of categories and (2) there is enhanced discrimination between stimuli from different categories as compared with equally different stimuli from within the same category. We have shown previously that female zebra finches ( Taeniopygia guttata) categorically perceive colours along an orange-red continuum that aligns with the carotenoid-based coloration of male beaks, a trait that serves as an assessment signal in female mate choice. Here, we demonstrate that categorical perception occurs along a blue-green continuum as well, suggesting that categorical colour perception may be a general feature of zebra finch vision. Although we identified two categories in both the blue-green and the orange-red ranges, we also found that individuals could better differentiate colours from within the same category in the blue-green as compared with the orange-red range, indicative of less clear categorization in the blue-green range. We discuss reasons why categorical perception may vary across the visible spectrum, including the possibility that such differences are linked to the behavioural or ecological function of different colour ranges.

Von Uexküll Revisited: Addressing Human Biases in the Study of Animal Perception.

More than 100 years ago, the biologist Jakob von Uexküll suggested that, because sensory systems are diverse, animals likely inhabit different sensory worlds (umwelten) than we do. Since von Uexküll, work across sensory modalities has confirmed that animals sometimes perceive sensory information that humans cannot, and it is now well-established that one must account for this fact when studying an animal's behavior. We are less adept, however, at recognizing cases in which non-human animals may not detect or perceive stimuli the same way we do, which is our focus here. In particular, we discuss three ways in which our own perception can result in misinformed hypotheses about the function of various stimuli. In particular, we may (1) make untested assumptions about how sensory information is perceived, based on how we perceive or measure it, (2) attribute undue significance to stimuli that we perceive as complex or striking, and (3) assume that animals divide the sensory world in the same way that we as scientists do. We discuss each of these biases and provide examples of cases where animals cannot perceive or are not attending to stimuli in the same way that we do, and how this may lead us to mistaken assumptions. Because what an animal perceives affects its behavior, we argue that these biases are especially important for researchers in sensory ecology, cognition, and animal behavior and communication to consider. We suggest that studying animal umwelten requires integrative approaches that combine knowledge of sensory physiology with behavioral assays.

Variation in rod spectral sensitivity of fishes is best predicted by habitat and depth.

Rod spectral sensitivity data (λmax ), measured by microspectrophotometry, were compiled for 403 species of ray-finned fishes in order to examine four hypothesized predictors of rod spectral sensitivity (depth, habitat, diet and temperature). From this database, a subset of species that were known to be adults and available on a published phylogeny (n = 210) were included in analysis, indicating rod λmax values averaging 503 nm and ranging from 477 to 541 nm. Linear models that corrected for phylogenetic relatedness showed that variation in rod sensitivity was best predicted by habitat and depth, with shorter wavelength λmax values occurring in fishes found offshore or in the deep sea. Neither diet, nor the interaction of diet and habitat, had significant explanatory power. Although temperature significantly correlated with rod sensitivity, in that fishes in temperate latitudes had longer wavelength rod λmax values than those in tropical latitudes, sampling inequity and other confounds require the role of the temperature to be studied further. Together, these findings indicate that fish rod λmax is influenced by several ecological factors, suggesting that selection can act on even small differences in fish spectral sensitivity.

Spectral sensitivity in ray-finned fishes: diversity, ecology and shared descent.

A major goal of sensory ecology is to identify factors that underlie sensory-trait variation. One open question centers on why fishes show the greatest diversity among vertebrates in their capacity to detect color (i.e. spectral sensitivity). Over the past several decades, λmax values (photoreceptor class peak sensitivity) and chromacy (photoreceptor class number) have been cataloged for hundreds of fish species, yet the ecological basis of this diversity and the functional significance of high chromacy levels (e.g. tetra- and pentachromacy) remain unclear. In this study, we examined phylogenetic, physiological and ecological patterns of spectral sensitivity of ray-finned fishes (Actinoptergyii) via a meta-analysis of data compiled from 213 species. Across the fishes sampled, our results indicate that trichromacy is most common, ultraviolet λmax values are not found in monochromatic or dichromatic species, and increasing chromacy, including from tetra- to pentachromacy, significantly increases spectral sensitivity range. In an ecological analysis, multivariate phylogenetic latent liability modeling was performed to analyze correlations between chromacy and five hypothesized predictors (depth, habitat, diet, body coloration, body size). In a model not accounting for phylogenetic relatedness, each predictor with the exception of habitat significantly correlated with chromacy: a positive relationship in body color and negative relationships with body size, diet and depth. However, after phylogenetic correction, the only remaining correlated predictor was depth. The findings of this study indicate that phyletic heritage and depth are important factors in fish spectral sensitivity and impart caution about excluding phylogenetic comparative methods in studies of sensory trait variation.

Categorical perception of colour signals in a songbird.

In many contexts, animals assess each other using signals that vary continuously across individuals and, on average, reflect variation in the quality of the signaller1,2. It is often assumed that signal receivers perceive and respond continuously to continuous variation in the signal2. Alternatively, perception and response may be discontinuous3, owing to limitations in discrimination, categorization or both. Discrimination is the ability to tell two stimuli apart (for example, whether one can tell apart colours close to each other in hue). Categorization concerns whether stimuli are grouped based on similarities (for example, identifying colours with qualitative similarities in hue as similar even if they can be distinguished)4. Categorical perception is a mechanism by which perceptual systems categorize continuously varying stimuli, making specific predictions about discrimination relative to category boundaries. Here we show that female zebra finches (Taeniopygia guttata) categorically perceive a continuously variable assessment signal: the orange to red spectrum of male beak colour. Both predictions of categorical perception5 were supported: females (1) categorized colour stimuli that varied along a continuum and (2) showed increased discrimination between colours from opposite sides of a category boundary compared to equally different colours from within a category. To our knowledge, this is the first demonstration of categorical perception of signal-based colouration in a bird, with implications for understanding avian colour perception and signal evolution in general.

Mutual visual signalling between the cleaner shrimp Ancylomenes pedersoni and its client fish.

Cleaner shrimp and their reef fish clients are an interspecific mutualistic interaction that is thought to be mediated by signals, and a useful system for studying the dynamics of interspecific signalling. To demonstrate signalling, one must show that purported signals at minimum (a) result in a consistent state change in the receiver and (b) contain reliable information about the sender's intrinsic state or future behaviour. Additionally, signals must be perceptible by receivers. Here, we document fundamental attributes of the signalling system between the cleaner shrimp Ancylomenes pedersoni and its clients. First, we use sequential analysis of in situ behavioural interactions to show that cleaner antenna whipping reliably predicts subsequent cleaning. If shrimp do not signal via antenna whipping, clients triple their likelihood of being cleaned by adopting darker coloration over a matter of seconds, consistent with dark colour change signalling that clients want cleaning. Using experimental manipulations, we found that visual stimuli are sufficient to elicit antenna whipping, and that shrimp are more likely to 'clean' dark than light visual stimuli. Lastly, we show that antenna whipping and colour change are perceptible when accounting for the intended receiver's visual acuity and spectral sensitivity, which differ markedly between cleaners and clients. Our results show that signalling by both cleaners and clients can initiate and mediate their mutualistic interaction.

Visual Acuity and the Evolution of Signals.

Acuity, the fineness with which sensory systems perceive and parse information, limits the information that organisms can extract from stimuli. Here, we focus on visual acuity (the ability to perceive static spatial detail) to discuss relationships between acuity and signal form and evolution. Research suggests that acuity varies by orders of magnitude across species, and that most animals have much lower acuity than humans. Thus, hypotheses regarding the function of spatial patterns must account for the acuity of relevant viewers. New data quantifying acuity in a range of taxa allow us to examine correlations between acuity and ecology, elucidate the selective forces that receiver acuity places on signal evolution, and examine how signals might appear to viewers with different acuities.