Habitat geometry rather than visual acuity limits the visibility of a ground-nesting bird's clutch to terrestrial predators.

The nests of ground-nesting birds rely heavily on camouflage for their survival, and predation risk, often linked to ecological changes from human activity, is a major source of mortality. Numerous ground-nesting bird populations are in decline, so understanding the effects of camouflage on their nesting behavior is relevant to their conservation concerns. Habitat three-dimensional (3D) geometry, together with predator visual abilities, viewing distance, and viewing angle, determine whether a nest is either visible, occluded, or too far away to detect. While this link is intuitive, few studies have investigated how fine-scale geometry is likely to help defend nests from different predator guilds. We quantified nest visibility based on 3D occlusion, camouflage, and predator visual modeling in northern lapwings, Vanellus vanellus, on different land management regimes. Lapwings selected local backgrounds that had a higher 3D complexity at a spatial scale greater than their entire clutches compared to local control sites. Importantly, our findings show that habitat geometry-rather than predator visual acuity-restricts nest visibility for terrestrial predators and that their field habitats, perceived by humans as open, are functionally closed with respect to a terrestrial predator searching for nests on the ground. Taken together with lapwings' careful nest site selection, our findings highlight the importance of considering habitat geometry for understanding the evolutionary ecology and management of conservation sites for ground-nesting birds.

OSpRad: an open-source, low-cost, high-sensitivity spectroradiometer.

Spectroradiometry is a vital tool in a wide range of biological, physical, astronomical and medical fields, yet its cost and accessibility are frequent barriers to use. Research into the effects of artificial light at night (ALAN) further compounds these difficulties with requirements for sensitivity to extremely low light levels across the ultraviolet to human-visible spectrum. Here, I present an open-source spectroradiometry (OSpRad) system that meets these design challenges. The system utilises an affordable miniature spectrometer chip (Hamamatsu C12880MA), combined with an automated shutter and cosine-corrector, microprocessor controller, and graphical user interface 'app' that can be used with smartphones or desktop computers. The system has high ultraviolet sensitivity and can measure spectral radiance at 0.001 cd m-2 and irradiance at 0.005 lx, covering the vast majority of real-world night-time light levels. The OSpRad system's low cost and high sensitivity make it well suited to a range of spectrometry and ALAN research.

Artificial light at night causes conflicting behavioural and morphological defence responses in a marine isopod.

Encroachment of artificial light at night (ALAN) into natural habitats is increasingly recognized as a major source of anthropogenic disturbance. Research focussed on variation in the intensity and spectrum of ALAN emissions has established physiological, behavioural and population-level effects across plants and animals. However, little attention has been paid to the structural aspect of this light, nor how combined morphological and behavioural anti-predator adaptations are affected. We investigated how lighting structure, background reflectance and the three-dimensional properties of the environment combined to affect anti-predator defences in the marine isopod Ligia oceanica. Experimental trials monitored behavioural responses including movement and background choice, and also colour change, a widespread morphological anti-predator mechanism little considered in relation to ALAN exposure. We found that behavioural responses of isopods to ALAN were consistent with classic risk-aversion strategies, being particularly exaggerated under diffuse lighting. However, this behaviour was disconnected from optimal morphological strategies, as diffuse light caused isopods to become lighter coloured while seeking out darker backgrounds. Our work highlights the potential for the structure of natural and artificial light to play a key role in behavioural and morphological processes likely to affect anti-predator adaptations, survival, and ultimately wider ecological effects.

A model of colour appearance based on efficient coding of natural images.

An object's colour, brightness and pattern are all influenced by its surroundings, and a number of visual phenomena and "illusions" have been discovered that highlight these often dramatic effects. Explanations for these phenomena range from low-level neural mechanisms to high-level processes that incorporate contextual information or prior knowledge. Importantly, few of these phenomena can currently be accounted for in quantitative models of colour appearance. Here we ask to what extent colour appearance is predicted by a model based on the principle of coding efficiency. The model assumes that the image is encoded by noisy spatio-chromatic filters at one octave separations, which are either circularly symmetrical or oriented. Each spatial band's lower threshold is set by the contrast sensitivity function, and the dynamic range of the band is a fixed multiple of this threshold, above which the response saturates. Filter outputs are then reweighted to give equal power in each channel for natural images. We demonstrate that the model fits human behavioural performance in psychophysics experiments, and also primate retinal ganglion responses. Next, we systematically test the model's ability to qualitatively predict over 50 brightness and colour phenomena, with almost complete success. This implies that much of colour appearance is potentially attributable to simple mechanisms evolved for efficient coding of natural images, and is a well-founded basis for modelling the vision of humans and other animals.

Combined measures of mimetic fidelity explain imperfect mimicry in a brood parasite-host system.

The persistence of imperfect mimicry in nature presents a challenge to mimicry theory. Some hypotheses for the existence of imperfect mimicry make differing predictions depending on how mimetic fidelity is measured. Here, we measure mimetic fidelity in a brood parasite-host system using both trait-based and response-based measures of mimetic fidelity. Cuckoo finches Anomalospiza imberbis lay imperfectly mimetic eggs that lack the fine scribbling characteristic of eggs of the tawny-flanked prinia Prinia subflava, a common host species. A trait-based discriminant analysis based on Minkowski functionals-that use geometric and topological morphometric methods related to egg pattern shape and coverage-reflects this consistent difference between host and parasite eggs. These methods could be applied to quantify other phenotypes including stripes and waved patterns. Furthermore, by painting scribbles onto cuckoo finch eggs and testing their rate of rejection compared to control eggs (i.e. a response-based approach to quantify mimetic fidelity), we show that prinias do not discriminate between eggs based on the absence of scribbles. Overall, our results support relaxed selection on cuckoo finches to mimic scribbles, since prinias do not respond differently to eggs with and without scribbles, despite the existence of this consistent trait difference.

Artificial lighting affects the landscape of fear in a widely distributed shorebird.

Fear influences almost all aspects of a prey species' behaviour, such as its foraging and movement, and has the potential to cause trophic cascades. The superior low-light vision of many predators means that perceived predation risk in prey is likely to be affected by light levels. The widespread and increasing intensity of artificial light at night is therefore likely to interfere with this nocturnal visual arms race with unknown behavioural and ecological consequences. Here we test how the fear of predation perceived by wintering Eurasian curlew foraging on tidal flats is influenced by lighting. We quantified flight initiation distance (FID) of individuals under varying levels of natural and artificial illumination. Our results demonstrate that FID is significantly and substantially reduced at low light levels and increases under higher intensity illumination, with artificial light sources having a greater influence than natural sources. Contrary to the sensory-limitation hypothesis, the curlews' unwillingness to take flight in low-light appears to reflect the risks posed by low-light flight, and a desire to remain on valuable foraging grounds. These findings demonstrate how artificial light can shape the landscape of fear, and how this interacts with optimal foraging decisions, and the costs of taking flight.

A songbird can detect the eyes of conspecifics under daylight and artificial nighttime lighting.

Eyes convey important information about the external and internal worlds of animals. Individuals can follow the gaze of others to learn about the location of salient objects as well as assess eye qualities to evaluate the health, age or other internal states of conspecifics. Because of the increasing prevalence of artificial lighting at night (ALAN), urbanized individuals can potentially garner information from conspecific eyes under both daylight and ALAN. We tested this possibility using a visual modeling approach in which we estimated the maximum distance at which individuals could detect conspecific eyes under daylight and high levels of ALAN. We also estimated the minimum light level at which individuals could detect conspecific eyes. Great-tailed grackles (Quiscalus mexicanus) were used as our study species because they are highly social and are unusual among birds in that they regularly gather at nocturnal roosts in areas with high levels of ALAN. This visual modelling approach revealed that grackles can detect conspecific eyes under both daylight and ALAN, regardless of iris coloration. The grackles could detect conspecific eyes at farther distances in daylight compared to ALAN. Our results highlight the potential importance of lighting conditions in shaping social interactions.

Nest sanitation as an effective defence against brood parasitism.

Egg rejection is a crucial defence strategy against brood parasitism that requires the host to correctly recognise the foreign egg. Rejection behaviour has, thus, evolved in many hosts, facilitated by the visual differences between the parasitic and host eggs, and driving hosts to rely on colour and pattern cues. On the other hand, the need to recognise non-egg-shaped objects to carry out nest sanitation led birds to evolve the ability to discriminate and eject objects using mainly shape cues. However, little is known regarding the evolutionary significance of rejection behaviour in general and the cognitive processes underlying it. Here, we investigated the response of the barn swallow (Hirundo rustica) during pre-laying and laying stages to four objects types that differed in shape (eggs vs stars) and colour/pattern (mimetic vs non-mimetic) to investigate (1) what cognitive mechanisms are involved in object discrimination and (2) whether egg rejection is a direct defence against brood parasitism, or simply a product of nest sanitation. We found that swallows ejected stars more often than eggs in both stages, indicating that swallows possess a template for the shape of their eggs. Since the effect of colour/pattern on ejection decisions was minor, we suggest that barn swallows have not evolved a direct defence against brood parasitism but instead, egg ejection might be a product of their well-developed nest sanitation behaviour. Nonetheless, the fact that mimetic eggs were ejected especially in the pre-laying stage shows that nest sanitation could be an effective defence against poorly timed brood parasitism.

Chimpanzee (Pan troglodytes) gaze is conspicuous at ecologically-relevant distances.

Chimpanzee (Pan troglodytes) sclera appear much darker than the white sclera of human eyes, to such a degree that the direction of chimpanzee gaze may be concealed from conspecifics. Recent debate surrounding this topic has produced mixed results, with some evidence suggesting that (1) primate gaze is indeed concealed from their conspecifics, and (2) gaze colouration is among the suite of traits that distinguish uniquely social and cooperative humans from other primates (the cooperative eye hypothesis). Using a visual modelling approach that properly accounts for specific-specific vision, we reexamined this topic to estimate the extent to which chimpanzee eye coloration is discriminable. We photographed the faces of captive chimpanzees and quantified the discriminability of their pupil, iris, sclera, and surrounding skin. We considered biases of cameras, lighting conditions, and commercial photography software along with primate visual acuity, colour sensitivity, and discrimination ability. Our visual modeling of chimpanzee eye coloration suggests that chimpanzee gaze is visible to conspecifics at a range of distances (within approximately 10 m) appropriate for many species-typical behaviours. We also found that chimpanzee gaze is discriminable to the visual system of primates that chimpanzees prey upon, Colobus monkeys. Chimpanzee sclera colour does not effectively conceal gaze, and we discuss this result with regard to the cooperative eye hypothesis, the evolution of primate eye colouration, and methodological best practices for future primate visual ecology research.

The gaze of a social monkey is perceptible to conspecifics and predators but not prey.

Eye gaze is an important source of information for animals, implicated in communication, cooperation, hunting and antipredator behaviour. Gaze perception and its cognitive underpinnings are much studied in primates, but the specific features that are used to estimate gaze can be difficult to isolate behaviourally. We photographed 13 laboratory-housed tufted capuchin monkeys (Sapajus [Cebus] apella) to quantify chromatic and achromatic contrasts between their iris, pupil, sclera and skin. We used colour vision models to quantify the degree to which capuchin eye gaze is discriminable to capuchins, their predators and their prey. We found that capuchins, regardless of their colour vision phenotype, as well as their predators, were capable of effectively discriminating capuchin gaze across ecologically relevant distances. Their prey, in contrast, were not capable of discriminating capuchin gaze, even under relatively ideal conditions. These results suggest that specific features of primate eyes can influence gaze perception, both within and across species.

CamoEvo: An open access toolbox for artificial camouflage evolution experiments.

Camouflage research has long shaped our understanding of evolution by natural selection, and elucidating the mechanisms by which camouflage operates remains a key question in visual ecology. However, the vast diversity of color patterns found in animals and their backgrounds, combined with the scope for complex interactions with receiver vision, presents a fundamental challenge for investigating optimal camouflage strategies. Genetic algorithms (GAs) have provided a potential method for accounting for these interactions, but with limited accessibility. Here, we present CamoEvo, an open-access toolbox for investigating camouflage pattern optimization by using tailored GAs, animal and egg maculation theory, and artificial predation experiments. This system allows for camouflage evolution within the span of just 10-30 generations (∼1-2 min per generation), producing patterns that are both significantly harder to detect and that are optimized to their background. CamoEvo was built in ImageJ to allow for integration with an array of existing open access camouflage analysis tools. We provide guides for editing and adjusting the predation experiment and GA as well as an example experiment. The speed and flexibility of this toolbox makes it adaptable for a wide range of computer-based phenotype optimization experiments.

Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space.

Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy (Poecilia reticulata). In guppies, colonisation of low predation habitats is associated with emergence of 'more colourful' phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuousness remains strong. Our study differs from previous investigations in three respects. First, we adopted a multivariate phenotyping approach to characterise parallelism in multitrait space. Second, we used ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e., guppy, predatory cichlid). Third, we estimated population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypic divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model but very limited support for the predicted pattern of greater conspicuousness at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely nonsignificant, and explained little among-population variation. In multitrait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation, potentially by female choice, but suggest that this proceeds in independent directions of multitrait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality, among which some are found in genes contributing to colour pattern variation, presenting opportunities for future genetic study.

Hoverflies use a time-compensated sun compass to orientate during autumn migration.

The sun is the most reliable celestial cue for orientation available to daytime migrants. It is widely assumed that diurnal migratory insects use a 'time-compensated sun compass' to adjust for the changing position of the sun throughout the day, as demonstrated in some butterfly species. The mechanisms used by other groups of diurnal insect migrants remain to be elucidated. Migratory species of hoverflies (Diptera: Syrphidae) are one of the most abundant and beneficial groups of diurnal migrants, providing multiple ecosystem services and undergoing directed seasonal movements throughout much of the temperate zone. To identify the hoverfly navigational strategy, a flight simulator was used to measure orientation responses of the hoverflies Scaeva pyrastri and Scaeva selenitica to celestial cues during their autumn migration. Hoverflies oriented southwards when they could see the sun and shifted this orientation westward following a 6 h advance of their circadian clocks. Our results demonstrate the use of a time-compensated sun compass as the primary navigational mechanism, consistent with field observations that hoverfly migration occurs predominately under clear and sunny conditions.

Artificial nighttime lighting impacts visual ecology links between flowers, pollinators and predators.

The nighttime environment is being altered rapidly over large areas worldwide through introduction of artificial lighting, from streetlights and other sources. This is predicted to impact the visual ecology of many organisms, affecting both their intra- and interspecific interactions. Here, we show the effects of different artificial light sources on multiple aspects of hawkmoth visual ecology, including their perception of floral signals for pollination, the potential for intraspecific sexual signalling, and the effectiveness of their visual defences against avian predators. Light sources fall into three broad categories: some that prevent use of chromatic signals for these behaviours, others that more closely mimic natural lighting conditions, and, finally, types whose effects vary with light intensity and signal colour. We find that Phosphor Converted (PC) amber LED lighting - often suggested to be less harmful to nocturnal insects - falls into this third disruptive group, with unpredictable consequences for insect visual ecology depending on distance from the light source and the colour of the objects viewed. The diversity of impacts of artificial lighting on hawkmoth visual ecology alone argues for a nuanced approach to outdoor lighting in environmentally sensitive areas, employing intensities and spectra designed to limit those effects of most significant concern.

Variable crab camouflage patterns defeat search image formation.

Understanding what maintains the broad spectrum of variation in animal phenotypes and how this influences survival is a key question in biology. Frequency dependent selection - where predators temporarily focus on one morph at the expense of others by forming a "search image" - can help explain this phenomenon. However, past work has never tested real prey colour patterns, and rarely considered the role of different types of camouflage. Using a novel citizen science computer experiment that presented crab "prey" to humans against natural backgrounds in specific sequences, we were able to test a range of key hypotheses concerning the interactions between predator learning, camouflage and morph. As predicted, switching between morphs did hinder detection, and this effect was most pronounced when crabs had "disruptive" markings that were more effective at destroying the body outline. To our knowledge, this is the first evidence for variability in natural colour patterns hindering search image formation in predators, and as such presents a mechanism that facilitates phenotypic diversity in nature.

The evolution of patterning during movement in a large-scale citizen science game.

The motion dazzle hypothesis posits that high contrast geometric patterns can cause difficulties in tracking a moving target and has been argued to explain the patterning of animals such as zebras. Research to date has only tested a small number of patterns, offering equivocal support for the hypothesis. Here, we take a genetic programming approach to allow patterns to evolve based on their fitness (time taken to capture) and thus find the optimal strategy for providing protection when moving. Our 'Dazzle Bug' citizen science game tested over 1.5 million targets in a touch screen game at a popular visitor attraction. Surprisingly, we found that targets lost pattern elements during evolution and became closely background matching. Modelling results suggested that targets with lower motion energy were harder to catch. Our results indicate that low contrast, featureless targets offer the greatest protection against capture when in motion, challenging the motion dazzle hypothesis.

The Size, Symmetry, and Color Saturation of a Male Guppy's Ornaments Forecast His Resistance to Parasites.

AbstractSexually selected ornaments range from highly dynamic traits to those that are fixed during development and relatively static throughout sexual maturity. Ornaments along this continuum differ in the information they provide about the qualities of potential mates, such as their parasite resistance. Dynamic ornaments enable real-time assessment of the bearer's condition: they can reflect an individual's current infection status, or they can reflect resistance to recent infections. Static ornaments, however, are not affected by recent infection but may instead indicate an individual's genetically determined resistance, even in the absence of infection. Given the typically aggregated distribution of parasites among hosts, infection is unlikely to affect the ornaments of the vast majority of individuals in a population: static ornaments may therefore be the more reliable indicators of parasite resistance. To test this hypothesis, we quantified the ornaments of male guppies (Poecilia reticulata) before experimentally infecting them with Gyrodactylus turnbulli. Males with more left-right symmetrical black coloration and those with larger areas of orange coloration, both static ornaments, were more resistant. However, males with more saturated orange coloration, a dynamic ornament, were less resistant. Female guppies often prefer symmetrical males with larger orange ornaments, suggesting that parasite-mediated natural and sexual selection act in concert on these traits.

Multimodal mimicry of hosts in a radiation of parasitic finches.

Brood parasites use the parental care of others to raise their young and sometimes employ mimicry to dupe their hosts. The brood-parasitic finches of the genus Vidua are a textbook example of the role of imprinting in sympatric speciation. Sympatric speciation is thought to occur in Vidua because their mating traits and host preferences are strongly influenced by their early host environment. However, this alone may not be sufficient to isolate parasite lineages, and divergent ecological adaptations may also be required to prevent hybridization collapsing incipient species. Using pattern recognition software and classification models, we provide quantitative evidence that Vidua exhibit specialist mimicry of their grassfinch hosts, matching the patterns, colors and sounds of their respective host's nestlings. We also provide qualitative evidence of mimicry in postural components of Vidua begging. Quantitative comparisons reveal small discrepancies between parasite and host phenotypes, with parasites sometimes exaggerating their host's traits. Our results support the hypothesis that behavioral imprinting on hosts has not only enabled the origin of new Vidua species, but also set the stage for the evolution of host-specific, ecological adaptations.

A Matador-like Predator Diversion Strategy Driven by Conspicuous Coloration in Guppies.

Understanding the adaptive function of conspicuous coloration has been a major focus of evolutionary biology for much of the last century. Although considerable progress has been made in explaining how conspicuous coloration can be used in functions as diverse as sexual and social signaling, startling predators, and advertising toxicity [1], there remain a multitude of species that display conspicuous coloration that cannot be explained by existing theory. Here we detail a new "matador-like" divertive antipredator strategy based on conspicuous coloration in Trinidadian guppies (Poecilia reticulata). Guppies encountering predatory fish rapidly enhance the conspicuousness of their eyes by blackening their irises. By pitting biomimetic robotic guppies against real predatory fish, we show this conspicuous eye coloration diverts attacks away from the guppies' center of mass to their head. To determine the function of this seemingly counterintuitive behavior, we developed a method for simulating escape probabilities when live prey interact with ballistic attacking predators, and find this diversion effect significantly benefits black-eyed guppies because they evade capture by rapidly pivoting away from the predator once it has committed to its attack. Remarkably, this antipredator strategy reverses the commonly observed negative scaling relationship between prey size and evasive ability, with larger fish benefiting most from diverting predators. Taken together, our results introduce a new antipredator divertive strategy that may be widely used by conspicuously colored prey that rely on agility to escape their predators.

Background matching and disruptive coloration as habitat-specific strategies for camouflage.

Camouflage is a key defence across taxa and frequently critical to survival. A common strategy is background matching, resembling the colour and pattern of the environment. This approach, however, may be ineffective in complex habitats where matching one patch may lead to increased visibility in other patches. In contrast, disruptive coloration, which disguises body outlines, may be effective against complex backgrounds. These ideas have rarely been tested and previous work focuses on artificial systems. Here, we test the camouflage strategies of the shore crab (Carcinus maenas) in two habitats, being a species that is highly variable, capable of plastic changes in appearance, and lives in multiple environments. Using predator (bird and fish) vision modelling and image analysis, we quantified background matching and disruption in crabs from rock pools and mudflats, predicting that disruption would dominate in visually complex rock pools but background matching in more uniform mudflats. As expected, rock pool individuals had significantly higher edge disruption than mudflat crabs, whereas mudflat crabs more closely matched the substrate than rock pool crabs for colour, luminance, and pattern. Our study demonstrates facultative expression of camouflage strategies dependent on the visual environment, with implications for the evolution and interrelatedness of defensive strategies.