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.

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.

Multiple origins of green coloration in frogs mediated by a novel biliverdin-binding serpin.

Many vertebrates have distinctive blue-green bones and other tissues due to unusually high biliverdin concentrations-a phenomenon called chlorosis. Despite its prevalence, the biochemical basis, biology, and evolution of chlorosis are poorly understood. In this study, we show that the occurrence of high biliverdin in anurans (frogs and toads) has evolved multiple times during their evolutionary history, and relies on the same mechanism-the presence of a class of serpin family proteins that bind biliverdin. Using a diverse combination of techniques, we purified these serpins from several species of nonmodel treefrogs and developed a pipeline that allowed us to assemble their complete amino acid and nucleotide sequences. The described proteins, hereafter named biliverdin-binding serpins (BBS), have absorption spectra that mimic those of phytochromes and bacteriophytochromes. Our models showed that physiological concentration of BBSs fine-tune the color of the animals, providing the physiological basis for crypsis in green foliage even under near-infrared light. Additionally, we found that these BBSs are most similar to human glycoprotein alpha-1-antitrypsin, but with a remarkable functional diversification. Our results present molecular and functional evidence of recurrent evolution of chlorosis, describe a biliverdin-binding protein in vertebrates, and introduce a function for a member of the serpin superfamily, the largest and most ubiquitous group of protease inhibitors.

Collective movement as a solution to noisy navigation and its vulnerability to population loss.

Many animals use the geomagnetic field to migrate long distances with high accuracy; however, research has shown that individual responses to magnetic cues can be highly variable. Thus, it has been hypothesized that magnetoreception alone is insufficient for accurate migrations and animals must either switch to a more accurate sensory cue or integrate their magnetic sense over time. Here we suggest that magnetoreceptive migrators could also use collective navigation strategies. Using agent-based models, we compare agents utilizing collective navigation to both the use of a secondary sensory system and time-integration. Our models demonstrate that collective navigation allows for 70% success rates for noisy navigators. To reach the same success rates, a secondary sensory system must provide perfect navigation for over 73% of the migratory route, and time integration must integrate over 50 time-steps, indicating that magnetoreceptive animals could benefit from using collective navigation. Finally, we explore the impact of population loss on animals relying on collective navigation. We show that as population density decreases, a greater proportion of individuals fail to reach their destination and that a 50% population reduction can result in up to a 37% decrease in the proportion of individuals completing their migration.

Influence of visual background on discrimination of signal-relevant colours in zebra finches (Taeniopygia guttata).

Colour signals of many animals are surrounded by a high-contrast achromatic background, but little is known about the possible function of this arrangement. For both humans and non-human animals, the background colour surrounding a colour stimulus affects the perception of that stimulus, an effect that can influence detection and discrimination of colour signals. Specifically, high colour contrast between the background and two given colour stimuli makes discrimination more difficult. However, it remains unclear how achromatic background contrast affects signal discrimination in non-human animals. Here, we test whether achromatic contrast between signal-relevant colours and an achromatic background affects the ability of zebra finches to discriminate between those colours. Using an odd-one-out paradigm and generalized linear mixed models, we found that higher achromatic contrast with the background, whether positive or negative, decreases the ability of zebra finches to discriminate between target and non-target stimuli. This effect is particularly strong when colour distances are small (less than 4 ΔS) and Michelson achromatic contrast with the background is high (greater than 0.5). We suggest that researchers should consider focal colour patches and their backgrounds as collectively comprising a signal, rather than focusing on solely the focal colour patch itself.

Environmental sources of radio frequency noise: potential impacts on magnetoreception.

Radio frequency electromagnetic noise (RF) of anthropogenic origin has been shown to disrupt magnetic orientation behavior in some animals. Two sources of natural RF might also have the potential to disturb magnetic orientation behavior under some conditions: solar RF and atmospheric RF. In this review, we outline the frequency ranges and electric/magnetic field magnitudes of RF that have been shown to disturb magnetoreceptive behavior in laboratory studies and compare these to the ranges of solar and atmospheric RF. Frequencies shown to be disruptive in laboratory studies range from 0.1 to 10 MHz, with magnetic magnitudes as low as 1 nT reported to have effects. Based on these values, it appears unlikely that solar RF alone routinely disrupts magnetic orientation. In contrast, atmospheric RF does sometimes exceed the levels known to disrupt magnetic orientation in laboratory studies. We provide a reference for when and where atmospheric RF can be expected to reach these levels, as well as a guide for quantifying RF measurements.

The movement ecology of fishes.

Movement of fishes in the aquatic realm is fundamental to their ecology and survival. Movement can be driven by a variety of biological, physiological and environmental factors occurring across all spatial and temporal scales. The intrinsic capacity of movement to impact fish individually (e.g., foraging) with potential knock-on effects throughout the ecosystem (e.g., food web dynamics) has garnered considerable interest in the field of movement ecology. The advancement of technology in recent decades, in combination with ever-growing threats to freshwater and marine systems, has further spurred empirical research and theoretical considerations. Given the rapid expansion within the field of movement ecology and its significant role in informing management and conservation efforts, a contemporary and multidisciplinary review about the various components influencing movement is outstanding. Using an established conceptual framework for movement ecology as a guide (i.e., Nathan et al., 2008: 19052), we synthesized the environmental and individual factors that affect the movement of fishes. Specifically, internal (e.g., energy acquisition, endocrinology, and homeostasis) and external (biotic and abiotic) environmental elements are discussed, as well as the different processes that influence individual-level (or population) decisions, such as navigation cues, motion capacity, propagation characteristics and group behaviours. In addition to environmental drivers and individual movement factors, we also explored how associated strategies help survival by optimizing physiological and other biological states. Next, we identified how movement ecology is increasingly being incorporated into management and conservation by highlighting the inherent benefits that spatio-temporal fish behaviour imbues into policy, regulatory, and remediation planning. Finally, we considered the future of movement ecology by evaluating ongoing technological innovations and both the challenges and opportunities that these advancements create for scientists and managers. As aquatic ecosystems continue to face alarming climate (and other human-driven) issues that impact animal movements, the comprehensive and multidisciplinary assessment of movement ecology will be instrumental in developing plans to guide research and promote sustainability measures for aquatic resources.

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 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.

Evidence that eye-facing photophores serve as a reference for counterillumination in an order of deep-sea fishes.

Counterillumination, the masking of an animal's silhouette with ventral photophores, is found in a number of mesopelagic taxa but is difficult to employ because it requires that the animal match the intensity of downwelling light without seeing its own ventral photophores. It has been proposed that the myctophid, Tarletonbeania crenularis, uses a photophore directed towards the eye, termed an eye-facing photophore, as a reference standard that it adjusts to match downwelling light. The potential use of this mechanism, however, has not been evaluated in other fishes. Here, we use micro-computed tomography, photography and dissection to evaluate the presence/absence of eye-facing photophores in three families of stomiiform fishes. We found that all sampled species with ventral photophores capable of counterillumination possess an eye-facing photophore that is pigmented on the anterior and lateral sides, thus preventing its use as a laterally directed signal, lure or searchlight. The two species that are incapable of counterillumination, Cyclothone obscura and Sigmops bathyphilus, lack an eye-facing photophore. After determining the phylogenetic distribution of eye-facing photophores, we used histology to examine the morphology of the cranial tissue in Argyropelecus aculeatus and determined that light from the eye-facing photophore passes through a transparent layer of tissue, then the lens, and finally strikes the accessory retina. Additionally, eight of the 14 species for which fresh specimens were available had an aphakic gap that aligned with the path of emitted light from the eye-facing photophore, while the remaining six had no aphakic gap. These findings, combined with records of eye-facing photophores from distantly related taxa, strongly suggest that eye-facing photophores serve as a reference for counterillumination in these fishes.

Pulse magnetization elicits differential gene expression in the central nervous system of the Caribbean spiny lobster, Panulirus argus.

Diverse animals use Earth's magnetic field to guide their movements, but the neural and molecular mechanisms underlying the magnetic sense remain enigmatic. One hypothesis is that particles of the mineral magnetite (Fe3O4) provide the basis of magnetoreception. Here we examined gene expression in the central nervous system of a magnetically sensitive invertebrate, the Caribbean spiny lobster (Panulirus argus), after applying a magnetic pulse known to alter magnetic orientation behavior. Numerous genes were differentially expressed in response to the pulse, including 647 in the brain, 1256 in the subesophageal ganglion, and 712 in the thoracic ganglia. Many such genes encode proteins linked to iron regulation, oxidative stress, and immune response, consistent with possible impacts of a magnetic pulse on magnetite-based magnetoreceptors. Additionally, however, altered expression also occurred for numerous genes with no apparent link to magnetoreception, including genes encoding proteins linked to photoreception, carbohydrate and hormone metabolism, and other physiological processes. Overall, the results are consistent with the magnetite hypothesis of magnetoreception, yet also reveal that in spiny lobsters, a strong pulse altered expression of > 10% of all expressed genes, including many seemingly unrelated to sensory processes. Thus, caution is required when interpreting the effects of magnetic pulses on animal behavior.

Animal navigation: a noisy magnetic sense?

Diverse organisms use Earth's magnetic field as a cue in orientation and navigation. Nevertheless, eliciting magnetic orientation responses reliably, either in laboratory or natural settings, is often difficult. Many species appear to preferentially exploit non-magnetic cues if they are available, suggesting that the magnetic sense often serves as a redundant or 'backup' source of information. This raises an interesting paradox: Earth's magnetic field appears to be more pervasive and reliable than almost any other navigational cue. Why then do animals not rely almost exclusively on the geomagnetic field, while ignoring or downplaying other cues? Here, we explore a possible explanation: that the magnetic sense of animals is 'noisy', in that the magnetic signal is small relative to thermal and receptor noise. Magnetic receptors are thus unable to instantaneously acquire magnetic information that is highly precise or accurate. We speculate that extensive time-averaging and/or other higher-order neural processing of magnetic information is required, rendering the magnetic sense inefficient relative to alternative cues that can be detected faster and with less effort. This interpretation is consistent with experimental results suggesting a long time course for magnetic compass and map responses in some animals. Despite possible limitations, magnetoreception may be maintained by natural selection because the geomagnetic field is sometimes the only source of directional and/or positional information available.

Genomic signatures of G-protein-coupled receptor expansions reveal functional transitions in the evolution of cephalopod signal transduction.

Coleoid cephalopods show unique morphological and neural novelties, such as arms with tactile and chemosensory suckers and a large complex nervous system. The evolution of such cephalopod novelties has been attributed at a genomic level to independent gene family expansions, yet the exact association and the evolutionary timing remain unclear. In the octopus genome, one such expansion occurred in the G-protein-coupled receptors (GPCRs) repertoire, a superfamily of proteins that mediate signal transduction. Here, we assessed the evolutionary history of this expansion and its relationship with cephalopod novelties. Using phylogenetic analyses, at least two cephalopod- and two octopus-specific GPCR expansions were identified. Signatures of positive selection were analysed within the four groups, and the locations of these sequences in the Octopus bimaculoides genome were inspected. Additionally, the expression profiles of cephalopod GPCRs across various tissues were extracted from available transcriptomic data. Our results reveal the evolutionary history of cephalopod GPCRs. Unexpanded cephalopod GPCRs shared with other bilaterians were found to be mainly nervous tissue specific. By contrast, duplications that are shared between octopus and the bobtail squid or specific to the octopus' lineage generated copies with divergent expression patterns devoted to tissues outside of the brain. The acquisition of novel expression domains was accompanied by gene order rearrangement through either translocation or duplication and gene loss. Lastly, expansions showed signs of positive selection and some were found to form tandem clusters with shared conserved expression profiles in cephalopod innovations such as the axial nerve cord. Altogether, our results contribute to the understanding of the molecular and evolutionary history of signal transduction and provide insights into the role of this expansion during the emergence of cephalopod novelties and/or adaptations.

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.

Polarisation signals: a new currency for communication.

Most polarisation vision studies reveal elegant examples of how animals, mainly the invertebrates, use polarised light cues for navigation, course-control or habitat selection. Within the past two decades it has been recognised that polarised light, reflected, blocked or transmitted by some animal and plant tissues, may also provide signals that are received or sent between or within species. Much as animals use colour and colour signalling in behaviour and survival, other species additionally make use of polarisation signalling, or indeed may rely on polarisation-based signals instead. It is possible that the degree (or percentage) of polarisation provides a more reliable currency of information than the angle or orientation of the polarised light electric vector (e-vector). Alternatively, signals with specific e-vector angles may be important for some behaviours. Mixed messages, making use of polarisation and colour signals, also exist. While our knowledge of the physics of polarised reflections and sensory systems has increased, the observational and behavioural biology side of the story needs more (and more careful) attention. This Review aims to critically examine recent ideas and findings, and suggests ways forward to reveal the use of light that we cannot see.

Orienting to polarized light at night - matching lunar skylight to performance in a nocturnal beetle.

For polarized light to inform behaviour, the typical range of degrees of polarization observable in the animal's natural environment must be above the threshold for detection and interpretation. Here, we present the first investigation of the degree of linear polarization threshold for orientation behaviour in a nocturnal species, with specific reference to the range of degrees of polarization measured in the night sky. An effect of lunar phase on the degree of polarization of skylight was found, with smaller illuminated fractions of the moon's surface corresponding to lower degrees of polarization in the night sky. We found that the South African dung beetle Escarabaeus satyrus can orient to polarized light for a range of degrees of polarization similar to that observed in diurnal insects, reaching a lower threshold between 0.04 and 0.32, possibly as low as 0.11. For degrees of polarization lower than 0.23, as measured on a crescent moon night, orientation performance was considerably weaker than that observed for completely linearly polarized stimuli, but was nonetheless stronger than in the absence of polarized light.

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.

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.

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.

De novo transcriptomics reveal distinct phototransduction signaling components in the retina and skin of a color-changing vertebrate, the hogfish (Lachnolaimus maximus).

Across diverse taxa, an increasing number of photoreceptive systems are being discovered in tissues outside of the eye, such as in the skin. Dermal photoreception is believed to serve a variety of functions, including rapid color change via specialized cells called chromatophores. In vitro studies of this system among color-changing fish have suggested the use of a phototransduction signaling cascade that fundamentally differs from that of the retina. Thus, the goal of this study was to identify phototransduction genes and compare their expression in the retina and skin of a color-changing fish, the hogfish Lachnolaimus maximus. De novo transcriptomics revealed the expression of genes that may underlie distinct, yet complete phototransduction cascades in L. maximus retina and skin. In contrast to the five visual opsin genes and cGMP-dependent phototransduction components expressed in the retina of L. maximus, only a single short-wavelength sensitive opsin (SWS1) and putative cAMP-dependent phototransduction components were expressed in the skin. These data suggest a separate evolutionary history of phototransduction in the retina and skin of certain vertebrates and, for the first time, indicate an expression repertoire of genes that underlie a non-retinal phototransduction pathway in the skin of a color-changing fish.