Pierre-Paul Bitton

pavo: an R package for the analysis, visualization and organization of spectral data

Summary Recent technical and methodological advances have led to a dramatic increase in the use of spectrometry to quantify reflectance properties of biological materials, as well as models to determine how these colours are perceived by animals, providing important insights into ecological and evolutionary aspects of animal visual communication. Despite this growing interest, a unified cross-platform framework for analysing and visualizing spectral data has not been available. We introduce pavo, an R package that facilitates the organization, visualization and analysis of spectral data in a cohesive framework. pavo is highly flexible, allowing users to (a) organize and manipulate data from a variety of sources, (b) visualize data using Rs state-of-the-art graphics capabilities and (c) analyse data using spectral curve shape properties and visual system modelling for a broad range of taxa. In this paper, we present a summary of the functions implemented in pavo and how they integrate in a workflow to explore and analyse spectral data. We also present an exact solution for the calculation of colour volume overlap in colourspace, thus expanding previously published methodologies. As an example of pavos capabilities, we compare the colour patterns of three African glossy starling species, two of which have diverged very recently. We demonstrate how both colour vision models and direct spectral measurement analysis can be used to describe colour attributes and differences between these species. Different approaches to visual models and several plotting capabilities exemplify the packages versatility and streamlined workflow. pavo provides a cohesive environment for handling spectral data and addressing complex sensory ecology questions, while integrating with Rs modular core for a broader and comprehensive analytical framework, automated management of spectral data and reproducible workflows for colour analysis.

How hollow melanosomes affect iridescent colour production in birds

Developmental constraints and trade-offs can limit diversity, but organisms have repeatedly evolved morphological innovations that overcome these limits by expanding the range and functionality of traits. Iridescent colours in birds are commonly produced by melanin-containing organelles (melanosomes) organized into nanostructured arrays within feather barbules. Variation in array type (e.g. multilayers and photonic crystals, PCs) is known to have remarkable effects on plumage colour, but the optical consequences of variation in melanosome shape remain poorly understood. Here, we used a combination of spectrophotometric, experimental and theoretical methods to test how melanosome hollowness—a morphological innovation largely restricted to birds—affects feather colour. Optical analyses of hexagonal close-packed arrays of hollow melanosomes in two species, wild turkeys (Meleagris gallopavo) and violet-backed starlings (Cinnyricinclus leucogaster), indicated that they function as two-dimensional PCs. Incorporation of a larger dataset and optical modelling showed that, compared with solid melanosomes, hollow melanosomes allow birds to produce distinct colours with the same energetically favourable, close-packed configurations. These data suggest that a morphological novelty has, at least in part, allowed birds to achieve their vast morphological and colour diversity.

Uneven Sampling and the Analysis of Vocal Performance Constraints

Studies of trilled vocalizations provide a premiere illustration of how performance constraints shape the evolution of mating displays. In trill production, vocal tract mechanics impose a trade-off between syllable repetition rate and frequency bandwidth, with the trade-off most pronounced at higher values of both parameters. Available evidence suggests that trills that simultaneously maximize both traits are more threatening to males or more attractive to females, consistent with a history of sexual selection favoring high-performance trills. Here, we identify a sampling limitation that confounds the detection and description of performance trade-offs. We reassess 70 data sets (from 26 published studies) and show that sampling limitations afflict 63 of these to some degree. Traditional upper-bound regression, which does not control for sampling limitations, detects performance trade-offs in 33 data sets; yet when sampling limitations are controlled, performance trade-offs are detected in only 15. Sampling limitations therefore confound more than half of all performance trade-offs reported using the traditional method. An alternative method that circumvents this sampling limitation, which we explore here, is quantile regression. Our goal is not to question the presence of mechanical trade-offs on trill production but rather to reconsider how these trade-offs can be detected and characterized from acoustic data.

Assessing Sexual Dicromatism: The Importance of Proper Parameterization in Tetrachromatic Visual Models.

Perceptual models of animal vision have greatly contributed to our understanding of animal-animal and plant-animal communication. The receptor-noise model of color contrasts has been central to this research as it quantifies the difference between two colors for any visual system of interest. However, if the properties of the visual system are unknown, assumptions regarding parameter values must be made, generally with unknown consequences. In this study, we conduct a sensitivity analysis of the receptor-noise model using avian visual system parameters to systematically investigate the influence of variation in light environment, photoreceptor sensitivities, photoreceptor densities, and light transmission properties of the ocular media and the oil droplets. We calculated the chromatic contrast of 15 plumage patches to quantify a dichromatism score for 70 species of Galliformes, a group of birds that display a wide range of sexual dimorphism. We found that the photoreceptor densities and the wavelength of maximum sensitivity of the short-wavelength-sensitive photoreceptor 1 (SWS1) can change dichromatism scores by 50% to 100%. In contrast, the light environment, transmission properties of the oil droplets, transmission properties of the ocular media, and the peak sensitivities of the cone photoreceptors had a smaller impact on the scores. By investigating the effect of varying two or more parameters simultaneously, we further demonstrate that improper parameterization could lead to differences between calculated and actual contrasts of more than 650%. Our findings demonstrate that improper parameterization of tetrachromatic visual models can have very large effects on measures of dichromatism scores, potentially leading to erroneous inferences. We urge more complete characterization of avian retinal properties and recommend that researchers either determine whether their species of interest possess an ultraviolet or near-ultraviolet sensitive SWS1 photoreceptor, or present models for both.

Mimics here and there, but not everywhere: Müllerian mimicry in Ceroglossus ground beetles?

The ground beetle genus Ceroglossus contains co-distributed species that show pronounced intraspecific diversity in the form of geographical colour morphs. While colour morphs among different species appear to match in some geographical regions, in others, there is little apparent colour matching. Mimicry is a potential explanation for covariation in colour patterns, but it is not clear whether the degree of sympatric colour matching is higher than expected by chance given the obvious mismatches among morphs in some regions. Here, we used reflectance spectrometry to quantify elytral coloration from the perspective of an avian predator to test whether colour similarity between species is, indeed, higher in sympatry. After finding no significant phylogenetic signal in the colour data, analyses showed strong statistical support for sympatric colour similarity between species despite the apparent lack of colour matching in some areas. We hypothesize Müllerian mimicry as the responsible mechanism for sympatric colour similarity in Ceroglossus and discuss potential explanations and future directions to elucidate why mimicry has not developed similar levels of interspecific colour resemblance across space.

Analysis of plumage, morphology, and voice reveals species-level differences between two subspecies of Prevost’s Ground-sparrow Melozone biarcuata (Prévost and Des Murs) (Aves: Emberizidae)

Melozone biarcuata (Prevosts Ground-sparrow) has traditionally been divided into two allopatric groups based on differences in vocalizations and plumage characteristics: M. b. cabanisi in Costa Rica and M. b. biarcuata/M. b. hartwegi in northern Central America. However, the relationship between these subspecies has not been studied using a modern taxonomic approach. In this study, our objective was to provide the first detailed taxonomic comparison between these three subspecies using an integrative multi-trait analysis. We analyzed morphometric features, qualitative plumage patterns, and quantitative plumage measurements using spectral reflectance from all three subspecies, and we analyzed vocalizations for subspecies M. b. biarcuata and M. b. cabanisi. Our results show that M. b. cabanisi can be readily distinguished from the two other subspecies on the basis of morphometrics (M. b. cabanisi are smaller), plumage patterns (M. b. cabanisi have different facial markings and plumage patches), color differences (M. b. cabanisi have plumage patches that differ in color and brightness), and vocalizations (M. b. cabanisi have songs and calls that are acoustically distinct from those of M. b. biarcuata). By contrast, the two northern subspecies M. b. biarcuata and M. b. hartwegi were very similar for most traits, supporting previous suggestions that the two northern subspecies should be considered a single subspecies. Our data reveal that the differentiation in phenotypic characteristics between M. b. cabanisi versus M. b. biarcuata and M. b. hartwegi is similar to that reported for other complexes of subspecies where species status has been recognized. We argue that M. b. cabanisi should be treated as a species separate from M. biarcuata and propose that it be called Melozone cabanisi, White-faced Ground-sparrow. Our findings will contribute to the conservation efforts of the White-faced Ground-sparrow, which is endemic to Costa Ricas Central Valley and Turrialba Valley, by bringing focus to conservation policies that preserve ground-sparrow habitat (thickets, shade coffee plantations, and young secondary forest).

Variation and possible function of egg sac coloration in spiders

Abstract Coloration of the egg sacs of spiders varies widely to the human eye, both across and within taxonomic groups. These differences in coloration are expected with differences in the biology and ecology of different species. Here we measure the spectral properties of the egg sacs of 15 species in six families. Ultraviolet chroma, red chroma, and particularly overall brightness vary widely across and within taxonomic groups. We discuss the spectral properties of the silk of the egg sacs in the context of the physical characteristics of the silk, the reflective properties of the background, the environmental illumination, and the natural history and behavior of the spider species. In most cases, the spectral characteristics of the egg sacs seem to reduce their conspicuousness against the background and in those cases in which the coloration does not reduce the contrast in relation to the background, the low environmental light available may help to camouflage the egg sacs.

Sympatric black-headed and elegant trogons focus on different plumage characteristics for species recognition

The ability of individuals to distinguish conspecifics from similar-looking congeners has important evolutionary consequences, yet few studies have determined which specific visual characteristics are used for species recognition, and whether closely related species use the same characteristics. In particular, sympatry with similar-looking congeners may influence which traits are important in species recognition. We presented elegant trogons, Trogon elegans, and black-headed trogons, Trogon melanocephalus, with models that closely resembled conspecifics and models that differed in either the colour of the belly, the colour of the upperparts or the tail-barring pattern, while broadcasting species-specific songs. Elegant trogons showed significantly more aggression towards the conspecific and tail models, suggesting that belly and back colour, but not tail-barring pattern, are important for species recognition in this species. In contrast, the black-headed trogon approached all models very closely, except for the conspecific model. We interpret this counterintuitive behaviour as reluctance to approach an unknown conspecific, suggesting that all three plumage traits are important for species recognition in black-headed trogons. Because the elegant trogon is not sympatric with a similar-looking congener, we argue that they may lack the ability to discriminate fine-barring tail differences or overlook this trait. Sympatry with the similar-looking violaceous trogon may have influenced species recognition in black-headed trogons, favouring the use of all three plumage characteristics, including tail-banding patterns, which differ between these species. Alternatively, it is possible that incongruent stimuli are attended to differently, with elegant trogons focusing on the acoustic traits and black-headed trogons focusing on visual cues. Nevertheless, our study provides the first experimental evidence that specific plumage patches are used for species recognition and that closely related species may use different traits for species recognition. Our findings also suggest that the presence of a similar-looking congener can influence which traits are important in species recognition.

Visual modelling validates prey detection by means of diurnal active photolocation in a small cryptobenthic fish

Active sensing has been well documented in animals that use echolocation and electrolocation. Active photolocation, or active sensing using light, has received much less attention, and only in bioluminescent nocturnal species. However, evidence has suggested the diurnal triplefin Tripterygion delaisi uses controlled iris radiance, termed ocular sparks, for prey detection. While this form of diurnal active photolocation was behaviourally described, a study exploring the physical process would provide compelling support for this mechanism. In this paper, we investigate the conditions under which diurnal active photolocation could assist T. delaisi in detecting potential prey. In the field, we sampled gammarids (genus Cheirocratus) and characterized the spectral properties of their eyes, which possess strong directional reflectors. In the laboratory, we quantified ocular sparks size and their angle-dependent radiance. Combined with environmental light measurements and known properties of the visual system of T. delaisi, we modeled diurnal active photolocation under various scenarios. Our results corroborate that diurnal active photolocation should help T. deia¡s¡ detect gammarids at distances relevant to foraging, 4.5 cm under favourable conditions and up to 2.5 cm under average conditions. Because ocular sparks are widespread across fish species, diurnal active photolocation for micro-prey may be a common predation strategy.

Diurnal active photolocation enhances predator detection in a marine fish

Active sensing by means of light is rare. In vertebrates, it is known only from chemiluminescent fish with light organs below their pupils, an anatomical arrangement that is ideal to generate eyeshine in the pupils of nearby organisms. Here, we test whether diurnal fish can achieve the same by redirecting sunlight through reflection instead. We recently showed that small (A recent study showed that triplefins, small cryptobenthic fish, actively reflect downwelling light sideways using their irides. Here, we investigate whether they do this to break the camouflage of cryptic predators by inducing eyeshine, revealing their presence. We attached mini-shades to triplefins to block light redirection and monitored the distance they kept to a cryptic sit-and-wait predator, a scorpionfish with retroreflective eyes. Shaded triplefins stayed significantly closer than two control treatments in replicate laboratory and field experiments. When confronted with a stone as a control, the treatments did not differ in their behaviour. Visual modelling confirmed that the light redirected by a triplefin is sufficient to increase the brightness of a nearby scorpionfish9s pupil to a degree that can be visually detected by that triplefin. We conclude that small fish detect nearby cryptic predators better when allowed to redirect light from their irides. This new form of active sensing, called diurnal active photolocation, has wide implications for fish eye evolution.Nocturnal and deep-sea fish which possess a chemiluminescent subocular search light to detect prey are currently the only known vertebrates to use light for active sensing1,2. However, recent findings suggest diurnal fish may also benefit from a form of active photolocation3. The triplefin Tripterygion delaisi, a small benthic fish4,5, redirects downwelling sunlight from its irides in a controlled, context-specific manner3. This close arrangement between light source and pupil is analogous to that found in bioluminescent fishes2,6-10 and suggests a specialisation in the induction and detection of retroreflective eyeshine in other organisms1,3,11. However, diurnal active photolocation has never been empirically demonstrated. Here we show that experimentally reducing triplefin iris radiance affects how closely they approach a cryptobenthic sit and wait predator, a scorpionfish with retroreflective eyes12. Triplefins treated with a shading hat, which only prevented iris radiance, approached the predator significantly closer than two controls in replicate laboratory and field experiments. Visual modelling confirmed diurnal active photolocation of scorpionfish is indeed a plausible mechanism under natural light conditions. We conclude that redirection of ambient light can allow a small benthic fish to induce and detect eyeshine in its predator. Given the ubiquity of small fish with light re-directing irides3,13 and cryptobenthic predators with retroreflective eyes, this newly described form of active sensing is likely to be widespread and offers an additional explanation for the evolution of eye-related reflecting structures.