Branislav Igic

Detecting pigments from colourful eggshells of extinct birds

The known chemical basis of diverse avian eggshell coloration is generated by the same two classes of tetrapyrrole pigments in most living birds. We aimed to extend the evolutionary scope of these patterns by detecting pigments from extinct birds’ eggs. In our samples biliverdin was successfully extracted from subfossil shell fragments of the blue-green egg-laying upland moa Megalapteryx didinus, while protoporphyrin was extracted from the beige eggs of two other extinct moa species. Our data on pigment detection from eggshells of other extant paleognath birds, together with published information on other modern lineages, confirm tetrapyrroles as ubiquitous and conserved pigments contributing to diverse eggshell colours throughout avian evolution.

Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wrights (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.

Alternative mechanisms of increased eggshell hardness of avian brood parasites relative to host species

Obligate brood parasitic birds lay their eggs in nests of other species and parasite eggs typically have evolved greater structural strength relative to host eggs. Increased mechanical strength of the parasite eggshell is an adaptation that can interfere with puncture ejection behaviours of discriminating hosts. We investigated whether hardness of eggshells is related to differences between physical and chemical traits from three different races of the parasitic common cuckoo Cuculus canorus, and their respective hosts. Using tools developed for materials science, we discovered a novel correlate of increased strength of parasite eggs: the common cuckoos egg exhibits a greater microhardness, especially in the inner region of the shell matrix, relative to its host and sympatric non-host species. We then tested predictions of four potential mechanisms of shell strength: (i) increased relative thickness overall, (ii) greater proportion of the structurally harder shell layers, (iii) higher concentration of inorganic components in the shell matrix, and (iv) elevated deposition of a high density compound, MgCO3, in the shell matrix. We confirmed support only for hypothesis (i). Eggshell characteristics did not differ between parasite eggs sampled from different host nests in distant geographical sites, suggesting an evolutionarily shared microstructural mechanism of stronger parasite eggshells across diverse host-races of brood parasitic cuckoos.

Size dimorphism and avian‐perceived sexual dichromatism in a New Zealand endemic bird, the whitehead Mohoua albicilla

Sex differences in behavior, morphology, and physiology are common in animals. In many bird species, differences in the feather colors of the sexes are apparent when judged by human observers and using physical measures of plumage reflectance, cryptic (to human) plumage dichromatism has also been detected in several additional avian lineages. However, it remains to be confirmed in almost all species whether sexual dichromatism is perceivable by individuals of the studied species. This latter step is essential because it allows the evaluation of alternative hypotheses regarding the signaling and communication functions of plumage variation. We applied perceptual modeling of the avian visual system for the first time to an endemic New Zealand bird to provide evidence of subtle but consistent sexual dichromatism in the whitehead, Mohoua albicilla. Molecular sexing techniques were also used in this species to confirm the extent of the sexual size dimorphism in plumage and body mass. Despite the small sample sizes, we now validate previous reports based on human perception that in male whiteheads head and chest feathers are physically brighter than in females. We further suggest that the extent of sexual plumage dichromatism is pronounced and can be perceived by these birds. In contrast, although sexual dimorphism was also detectable in the mass among the DNA‐sexed individuals, it was found to be less extensive than previously thought. Sexual size dimorphism and intraspecifically perceivable plumage dichromatism represent reliable traits that differ between female and male whiteheads. These traits, in turn, may contribute to honest communication displays within the complex social recognition systems of communally breeding whitehead and other group‐breeding taxa. J. Morphol., 2010.

Using 3D printed eggs to examine the egg-rejection behaviour of wild birds

The coevolutionary relationships between brood parasites and their hosts are often studied by examining the egg rejection behaviour of host species using artificial eggs. However, the traditional methods for producing artificial eggs out of plasticine, plastic, wood, or plaster-of-Paris are laborious, imprecise, and prone to human error. As an alternative, 3D printing may reduce human error, enable more precise manipulation of egg size and shape, and provide a more accurate and replicable protocol for generating artificial stimuli than traditional methods. However, the usefulness of 3D printing technology for egg rejection research remains to be tested. Here, we applied 3D printing technology to the extensively studied egg rejection behaviour of American robins, Turdus migratorius. Eggs of the robin’s brood parasites, brown-headed cowbirds, Molothrus ater, vary greatly in size and shape, but it is unknown whether host egg rejection decisions differ across this gradient of natural variation. We printed artificial eggs that encompass the natural range of shapes and sizes of cowbird eggs, painted them to resemble either robin or cowbird egg colour, and used them to artificially parasitize nests of breeding wild robins. In line with previous studies, we show that robins accept mimetically coloured and reject non-mimetically coloured artificial eggs. Although we found no evidence that subtle differences in parasitic egg size or shape affect robins’ rejection decisions, 3D printing will provide an opportunity for more extensive experimentation on the potential biological or evolutionary significance of size and shape variation of foreign eggs in rejection decisions. We provide a detailed protocol for generating 3D printed eggs using either personal 3D printers or commercial printing services, and highlight additional potential future applications for this technology in the study of egg rejection.

The cuticle modulates ultraviolet reflectance of avian eggshells

ABSTRACT Avian eggshells are variedly coloured, yet only two pigments, biliverdin and protoporphyrin IX, are known to contribute to the dramatic diversity of their colours. By contrast, the contributions of structural or other chemical components of the eggshell are poorly understood. For example, unpigmented eggshells, which appear white to the human eye, vary in their ultraviolet (UV) reflectance, which may be detectable by birds. We investigated the proximate mechanisms for the variation in UV-reflectance of unpigmented bird eggshells using spectrophotometry, electron microscopy, chemical analyses, and experimental manipulations. We specifically tested how UV-reflectance is affected by the eggshell cuticle, the outermost layer of most avian eggshells. The chemical dissolution of the outer eggshell layers, including the cuticle, increased UV-reflectance for only eggshells that contained a cuticle. Our findings demonstrate that the outer eggshell layers, including the cuticle, absorb UV-light, probably because they contain higher levels of organic components and other chemicals, such as calcium phosphates, compared to the predominantly calcite-based eggshell matrix. These data highlight the need to examine factors other than the known pigments in studies of avian eggshell colour.

Fidelity of vocal mimicry: Identification and accuracy of mimicry of heterospecific alarm calls by the brown thornbill

Avian vocal mimicry has been studied for decades, but little is known about its function or requirements for accurate imitation. Furthermore, progress is hampered by the difficulty in identifying which vocalizations are indeed mimetic. We tested historical claims of vocal mimicry in the brown thornbill, Acanthiza pusilla , using a combination of human and computer methods to identify mimicry, followed by comparisons of acoustic similarity with model vocalizations. We recorded vocalizations of brown thornbills and sympatric heterospecifics while undisturbed and during mist net capture or the presence of natural or model predators. We then cross-validated human classification of mimicry with computer classification based on spectrographic measurements and spectral cross-correlation. Finally, we quantified the accuracy of the most common imitations. Brown thornbills predominantly imitated alarm calls given by heterospecifics towards aerial predators, which function in these models to provoke immediate flight by receivers. Human and computer-based methods produced consistent results when identifying and classifying mimicry. Mimicked aerial alarms were not perfect imitations of their corresponding model alarms, but did retain specific acoustic properties previously shown to be important for provoking immediate alarm responses. Although less accurate mimicry may reflect physiological constraints, we suggest that mimetic function, perhaps startling predators, only requires mimicry to retain features of model alarms that provoke immediate alarm responses by receivers. Understanding what factors influence the acoustic structure of mimetic vocalizations is essential in understanding the evolution of vocal mimicry, particularly with accumulating evidence that mimetic function does not always require perfect resemblance in other sensory modalities.

Sexual plumage dichromatism in a size monomorphic seabird

ABSTRACT Data on the extent to which the sexes may differ in their phenotypes are critical for a full understanding of the biology and management of any species. We previously quantified behavioral differences and vocal similarities between genetically-sexed Australasian Gannets (Morus serrator). Here, we quantify size monomorphism and plumage dichromatism in this socially monogamous, colonial seabird. In comparison with other sulids, the Australasian Gannet is characterized by low sexual dimorphism indices in various size metrics, and most physical dimensions are statistically similar between adult female and male gannets. In contrast, we found indications of sexually dichromatic plumage traits in the melanin-based, rusty head plumage and in the black-and-white tail feathers. To our knowledge, these findings constitute the first evidence of melanin-generated sexual plumage dichromatism in a size monomorphic seabird species. Using opsin-sequencing, we also confirm that the Australasian Gannet is a visually violet-sensitive species, for which the detection of both gross differences in feather reflectance, and long-wavelength based plumage dichromatism, should be perceptually feasible. However, because of the extensive overlap between females and males in the size and chromatic traits detected here, and in the behavioral and vocal displays reported in previous studies, we advocate for the use of genetic techniques for sex identification in this gannet species.

Manakins can produce iridescent and bright feather colours without melanosomes.

ABSTRACT Males of many species often use colourful and conspicuous ornaments to attract females. Among these, male manakins (family: Pipridae) provide classic examples of sexual selection favouring the evolution of bright and colourful plumage coloration. The highly iridescent feather colours of birds are most commonly produced by the periodic arrangement of melanin-containing organelles (melanosomes) within barbules. Melanin increases the saturation of iridescent colours seen from optimal viewing angles by absorbing back-scattered light; however, this may reduce the wide-angle brightness of these signals, contributing to a dark background appearance. We examined the nanostructure of four manakin species (Lepidothrix isidorei, L. iris, L. nattereri and L. coeruleocapilla) to identify how they produce their bright plumage colours. Feather barbs of all four species were characterized by dense and fibrous internal spongy matrices that likely increase scattering of light within the barb. The iridescent, yet pale or whitish colours of L. iris and L. nattereri feathers were produced not by periodically arranged melanosomes within barbules, but by periodic matrices of air and β-keratin within barbs. Lepidothrix iris crown feathers were able to produce a dazzling display of colours with small shifts in viewing geometry, likely because of a periodic nanostructure, a flattened barb morphology and disorder at a microstructural level. We hypothesize that iridescent plumage ornaments of male L. iris and L. nattereri are under selection to increase brightness or luminance across wide viewing angles, which may potentially increase their detectability by females during dynamic and fast-paced courtship displays in dim light environments. Summary: Feathers of two species of Lepidothrix manakin produce iridescence on a pale-coloured background using an inverse opal-like matrix of air and keratin.

A comparison of egg yolk lipid constituents between parasitic Common Cuckoos and their hosts

ABSTRACT Common Cuckoos (Cuculus canorus) are obligate brood parasites that lay their eggs in nests of other species and use these hosts to raise their parasitic offspring. Two key adaptations that increase their reproductive success are (1) the capacity for cuckoos to lay large numbers of eggs and thereby parasitize many nests per year, and (2) the ability of cuckoo eggs to hatch before those of hosts, enabling cuckoo nestlings to evict host eggs and eliminate competition for food. Producing more eggs is generally associated with reduced investment of nutrients and energy reserves per egg, which in turn is associated with shorter incubation periods both within and between species. We hypothesized that Common Cuckoos deposit reduced energy reserves into their eggs than do their hosts to facilitate both (1) and (2). To test these hypotheses, we compared the concentration of yolk lipids (per wet yolk mass) between eggs of 3 cuckoo gentes and their respective host species: Great Reed Warblers (Acrocephalus arundinaceus), Common Redstarts (Phoenicurus phoenicurus), and Reed Warblers (A. scirpaceus). Yolk lipids provide the bulk of energy required for embryonic development and can also serve structural and cell-signalling functions. As a general pattern, cuckoo eggs contained a lower concentration of energy-reserve lipids than eggs of their respective hosts, but not structural or cell-signalling lipids. When controlling for their heavier eggs and yolks, Common Cuckoo eggs had an estimated lower amount of energy reserve lipids for their size than host eggs. Our findings suggest a potential role of yolk lipid composition in facilitating (1) and (2) and advocate the need for further research in this area. We also highlight the potential problems of using either concentration or total yolk mass alone to compare maternal investment across taxa in comparative studies.