Low achromatic contrast sensitivity in birds: a common attribute shared by many phylogenetic orders.

Vision is an important sensory modality in birds, which can outperform other vertebrates in some visual abilities. However, sensitivity to achromatic contrasts - the ability to discern luminance difference between two objects or an object and its background - has been shown to be lower in birds compared with other vertebrates. We conducted a comparative study to evaluate the achromatic contrast sensitivity of 32 bird species from 12 orders using the optocollic reflex technique. We then performed an analysis to test for potential variability in contrast sensitivity depending on the corneal diameter to the axial length ratio, a proxy of the retinal image brightness. To account for potential influences of evolutionary relatedness, we included phylogeny in our analyses. We found a low achromatic contrast sensitivity for all avian species studied compared with other vertebrates (except small mammals), with high variability between species. This variability is partly related to phylogeny but appears to be independent of image brightness.

Responses to novelty in wild insular birds: comparing breeding populations in ecologically contrasting habitats.

Islands have always provided ideal natural laboratories for assessing ecological parameters influencing behaviour. One hypothesis that lends itself well to testing in island habitats suggests that animals frequenting highly variable environments should be motivated to approach and interact with (i.e. explore) novelty. Intra-species comparisons of populations living in ecologically different island habitats may, thus, help reveal the factors that modulate animals' responses to novelty. In this study, we presented novel objects to two geographically isolated breeding populations of the black-faced sheathbill (Chionis minor), a sedentary land-based bird that frequents remote sub-Antarctic islands. In the first population (Chionis minor ssp. crozettensis), the "Crozet group" (Baie du Marin, Ile de la Possession, Crozet Islands), breeding pairs inhabit a variable habitat close to penguin (Aptenodytes patagonicus) colonies. In the second population (Chionis minor ssp. minor), the "Kerguelen group" (île Verte, Morbihan gulf, Kerguelen Islands) breeding pairs live in penguin-free territories. In this latter population, the environment is less variable due to the presence of a broad intertidal zone which ensures year-round food availability. At both Kerguelen and Crozet, at least one breeding partner in all pairs approached at least one of the novel objects, and we found no significant differences in the latency of approach between the two populations. However, sheathbills at Crozet touched objects significantly more than birds at Kerguelen, and were also faster to touch them. We discuss how environmental variability, along with other potential influencing factors, may favour exploration of novelty in this wild insular bird.

Remote islands as natural laboratories: human-food association increases attraction to humans and novelty exploration in a seabird.

Increased attraction to humans and their objects often arises after repeated and positive human-wildlife encounters (e.g. food provided in tourist settings). The causes of this 'over-attraction', which may result from a learned association between humans and food, are still poorly studied in wild animals. Understanding the influence of humans on animals' responses is yet crucial to prevent negative effects (e.g. aggression). We presented three novel objects to two groups of free-ranging brown skuas (Catharacta antarctica ssp. lonnbergi) in the remote sub-Antarctic, where their habitats show no or minimal human disturbance. Skuas in one group (Verte) had previously participated in repeated food-rewarded behavioural and cognitive tasks with a human experimenter; skuas in the other group (Ratmanoff) had never done so. Objects consisted of (i) one natural-food-resembling object (plastic fish), (ii) one anthropogenic food object (real cake slice), and (iii) one anthropogenic non-food object (yellow glove). Verte group skuas approached the human experimenter and pecked significantly more and sooner at novel objects. Human-food association may have thus resulted in increased attraction to humans and novelty exploration in previously naive brown skuas, making this species a useful model for investigating the consequences of experience with humans on wildlife behaviour.

The influence of plant odours on sexual readiness in an insectivorous songbird.

Many organisms rely on environmental cues to predict and anticipate the annual optimal timing of reproduction. In insectivorous birds, preparation for breeding often coincides with the time vegetation starts to develop in spring. Whether there is a direct relationship between the two, and through which mechanisms this link could come about, has rarely been investigated. Plants release herbivore-induced plant volatiles (HIPVs) when they are attacked by insects, and recent studies have shown that birds can detect and orient to those odours when searching for food. Whether those volatiles also stimulate sexual reproductive development and timing of reproduction remains to be discovered. We tested this hypothesis by monitoring gonadal growth in pairs of blue tits (Cyanistes caeruleus) exposed to air from caterpillar-infested oak trees or from a control, in spring. We found that while males and females grew their gonads over time, gonads grew at the same rate in both odour treatments. More exploratory (i.e. a proxy of personality) females did, however, have larger ovarian follicle sizes when exposed to the HIPVs than to the control air, which is consistent with earlier results showing that fast explorers have larger gonads in spring and are more sensitive to HIPVs. If HIPVs constitute powerful attractants in foraging birds, their influence on gonadal development prior to breeding appears to be relatively subtle and to only enhance reproductive readiness in some individuals. These results are nevertheless important as they set olfaction as a new player in the seasonal timing of reproduction in birds.

Wild skuas can follow human-given behavioural cues when objects resemble natural food.

The capacity to follow human cues provides animals with information about the environment and can hence offer obvious adaptive benefits. Most studies carried out so far, however, have been on captive animals with previous experience with humans. Further comparative investigation is needed to properly assess the factors driving the emergence of this capacity under natural conditions, especially in species that do not have longstanding interactions with humans. Wild brown skuas (Catharacta antarctica ssp. lonnbergi) are non-neophobic seabirds that live in human-free habitats. In test 1, we assessed this species' capacity to use human behavioural cues (i.e., pecking at the same object previously picked up and lifted by a human experimenter) when the items presented were food objects: anthropogenic objects (wrapped muffins) and natural-food-resembling objects (plaster eggs). In test 2, we examined the response of another skua population towards non-food objects (sponges). Although all skuas in test 1 pecked at the objects, they pecked significantly more at the same previously handled items when they resembled natural food (plaster eggs). Most skuas in test 2, however, did not approach or peck at the non-food objects presented. Our results lead us to suggest that the use of human behavioural cues may be influenced by skuas' foraging ecology, which paves the way to further field studies assessing whether this capacity is directed specifically towards food objects and/or develops after previous interaction with humans.

Homing and Nest Recognition in Nocturnal Blue Petrels: What Scent May Attract Birds to their Burrows?

Hypogean petrels return to the same nest burrow to breed on remote islands during the summer months. Their nocturnal behavior at the colony, strong musky odor and olfactory anatomy suggest an important role of olfaction in homing behavior and nest recognition. Behavioral experiments showed that olfactory cues are sufficient to allow nest identification, suggesting a stabile chemical signature emanating from burrows and facilitating nest recognition. However, the chemical nature and sources of this odor remain unknown. To better understand the nest odor composition, we analyzed volatile organic compounds (VOCs) of nests of blue petrels (Halobaena caerulea) derived from three different odor sources: nest air, nest material and feather samples. We also compared, during two successive years, VOCs from burrows with an incubating breeder on the nest, and burrows used during the breeding season by blue petrels but shortly temporally unoccupied by breeders. We found that the nest air odor was mainly formed by the owners' odor, which provided an individual chemical label for nests that appeared stabile over the breeding season. These findings, together with the previous homing behavioral studies showing an essential role of the sense of smell in blue petrels, strongly suggest that the scent emanating from burrows of blue petrels provides the information that facilitates nest recognition and homing.

Genome-wide analyses reveal drivers of penguin diversification.

Penguins are the only extant family of flightless diving birds. They currently comprise at least 18 species, distributed from polar to tropical environments in the Southern Hemisphere. The history of their diversification and adaptation to these diverse environments remains controversial. We used 22 new genomes from 18 penguin species to reconstruct the order, timing, and location of their diversification, to track changes in their thermal niches through time, and to test for associated adaptation across the genome. Our results indicate that the penguin crown-group originated during the Miocene in New Zealand and Australia, not in Antarctica as previously thought, and that Aptenodytes is the sister group to all other extant penguin species. We show that lineage diversification in penguins was largely driven by changing climatic conditions and by the opening of the Drake Passage and associated intensification of the Antarctic Circumpolar Current (ACC). Penguin species have introgressed throughout much of their evolutionary history, following the direction of the ACC, which might have promoted dispersal and admixture. Changes in thermal niches were accompanied by adaptations in genes that govern thermoregulation and oxygen metabolism. Estimates of ancestral effective population sizes (Ne ) confirm that penguins are sensitive to climate shifts, as represented by three different demographic trajectories in deeper time, the most common (in 11 of 18 penguin species) being an increased Ne between 40 and 70 kya, followed by a precipitous decline during the Last Glacial Maximum. The latter effect is most likely a consequence of the overall decline in marine productivity following the last glaciation.

Wild skuas can use acoustic cues to locate hidden food.

Among animals, the visual acuity of several predatory bird species is probably the most outstanding. This, and the ease with which visually based tasks are administered, has led researchers to predominantly use the visual modality when studying avian cognition. Some wild skua populations routinely use acoustic cues emitted by their prey during foraging. In this study, we thus assessed whether this species was able to locate hidden food using acoustic cues alone (training phase). During the subsequent test phase, we investigated the capacity of successful individuals to choose the correct baited container in four conditions: (i) baited (shaking the baited container), (ii) full information (shaking both containers), (iii) exclusion (shaking the empty container), and (iv) control (shaking neither container). Four out of ten subjects succeeded in locating the baited container in the training phase. During the test phase, most subjects chose the baited container significantly more than the empty container in the baited and full information condition, while their performance was at chance level in the control condition. When no sound emanated from the empty container in the exclusion condition, one out of four skuas chose the baited container with more accuracy than predicted by chance. As this bird chose correctly on the first trial and during the first five trials, its performance is unlikely due to learning processes (learning to exclude the empty container). Although further tests are necessary to draw firm conclusions, our results open the way for assessing further this species' reasoning abilities in the wild.

Olfactory detection of trace amounts of plant volatiles is correlated with testosterone in a passerine bird.

In response to damage by insects, plants release herbivore-induced plant volatiles (HIPVs) into the air. Insectivorous birds exploit these cues and, consequently, reduce the damages inflicted to the plants. However, little is known about whether they solely use HIPVs as foraging cues, or if they also use them to modulate traits linked to reproduction. As caterpillars are the primary food source required for insectivorous birds to raise offspring, their ability to locate and predict future peaks in caterpillar biomass using olfaction is likely to be advantageous. Therefore, we tested whether an insectivorous songbird that naturally inhabits oak dominated forests can be trained to detect early spring infestation by hatchling caterpillars, at a time when oaks begin bursting, and birds prepare to breed. Tree buds were either infested with caterpillars or left as a control and visually obscured in a Y-Maze choice test. Additionally, we measured testosterone and 17ß-estradiol as they influence olfactory perception in mammals and are linked to reproduction in vertebrates. After being trained to associate the presence of HIPVs with that of food, blue tits spent more time with, were more active around, and more frequently chose to first visit the infested trees, showing that blue tits can smell caterpillar activity. Males with higher testosterone spent more time around infested trees, suggesting that foraging behavior during the pre-breeding season is linked with a major reproductive signal. There was no relationship between foraging and estradiol in females. These results are an important foundation for further investigation of the role of hormones in avian olfaction and how smell may be useful for making breeding decisions that could improve reproductive success.

Exclusion in the field: wild brown skuas find hidden food in the absence of visual information.

Inferential reasoning by exclusion allows responding adaptively to various environmental stimuli when confronted with inconsistent or partial information. In the experimental context, this mechanism involves selecting correctly between an empty option and a potentially rewarded one. Recently, the increasing reports of this capacity in phylogenetically distant species have led to the assumption that reasoning by exclusion is the result of convergent evolution. Within one largely unstudied avian order, i.e. the Charadriiformes, brown skuas (Catharacta antarctica ssp lonnbergi) are highly flexible and opportunistic predators. Behavioural flexibility, along with specific aspects of skuas' feeding ecology, may act as influencing factors in their ability to show exclusion performance. Our study aims to test whether skuas are able to choose by exclusion in a visual two-way object-choice task. Twenty-six wild birds were presented with two opaque cups, one covering a food reward. Three conditions were used: 'full information' (showing the content of both cups), 'exclusion' (showing the content of the empty cup), and 'control' (not showing any content). Skuas preferentially selected the rewarded cup in the full information and exclusion condition. The use of olfactory cues was excluded by results in the control condition. Our study opens new field investigations for testing further the cognition of this predatory seabird.

Plumage microbiota covaries with the major histocompatibility complex in blue petrels.

To increase fitness, a wide range of vertebrates preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC) or that have high MHC diversity. Although MHC often can be assessed through olfactory cues, the mechanism by which MHC genes influence odour remains largely unclear. MHC class IIB molecules, which enable recognition and elimination of extracellular bacteria, have been suggested to influence odour indirectly by shaping odour-producing microbiota, i.e. bacterial communities. However, there is little evidence of the predicted covariation between an animal's MHC genotype and its bacterial communities in scent-producing body surfaces. Here, using high-throughput sequencing, we tested the covariation between MHC class IIB genotypes and feather microbiota in the blue petrel (Halobaena caerulea), a seabird with highly developed olfaction that has been suggested to rely on oduor cues during an MHC-based mate choice. First, we show that individuals with similar MHC class IIB profiles also have similar bacterial assemblages in their feathers. Then, we show that individuals with high MHC diversity have less diverse feather microbiota and also a reduced abundance of a bacterium of the genus Arsenophonus, a genus in which some species are symbionts of avian ectoparasites. Our results, showing that feather microbiota covary with MHC, are consistent with the hypothesis that individual MHC genotype may shape the semiochemical-producing microbiota in birds.

More than the eye can see: Genomic insights into the drivers of genetic differentiation in Royal/Macaroni penguins across the Southern Ocean.

The study of systematics in wide-ranging seabirds can be challenging due to the vast geographic scales involved, as well as the possible discordance between molecular, morphological and behavioral data. In the Southern Ocean, macaroni penguins (Eudyptes chrysolophus) are distributed over a circumpolar range including populations in Antarctic and sub-Antarctic areas. Macquarie Island, in its relative isolation, is home to a closely related endemic taxon - the royal penguin (Eudyptes schlegeli), which is distinguishable from E. chrysolophus mainly by facial coloration. Although these sister taxa are widely accepted as representing distinct species based on morphological grounds, the extent of their genome-wide differentiation remains uncertain. In this study, we use genome-wide Single Nucleotide Polymorphisms to test genetic differentiation between these geographically isolated taxa and evaluate the main drivers of population structure among breeding colonies of macaroni/royal penguins. Genetic similarity observed between macaroni and royal penguins suggests they constitute a single evolutionary unit. Nevertheless, royal penguins exhibited a tendency to cluster only with macaroni individuals from Kerguelen Island, suggesting that dispersal occurs mainly between these neighboring colonies. A stepping stone model of differentiation of macaroni/royal populations was further supported by a strong pattern of isolation by distance detected across its whole distribution range, possibly driven by large geographic distances between colonies as well as natal philopatry. However, we also detected intraspecific genomic differentiation between Antarctic and sub-Antarctic populations of macaroni penguins, highlighting the role of environmental factors together with geographic distance in the processes of genetic differentiation between Antarctic and sub-Antarctic waters.

Sight or smell: which senses do scavenging raptors use to find food?

Raptors are usually considered to be mainly visually dependent, and the use of other sensory modalities has rarely been studied in these birds. Here, we investigated experimentally which senses (vision and/or olfaction) Turkey vultures (Cathartes aura) and Southern caracaras (Caracara plancus) use to find hidden food. First, two identical stainless-steel perforated balls, one containing a putrefied piece of meat and the other an odorless control, were presented to birds in binary choice experiments. Both species interacted more with the smelling ball than with the control, suggesting that they were attracted by the odor of the hidden meat. In a second experiment, individuals were accustomed to eat in one specifically colored ball (blue or green). In the test phase, the meat was hidden in the opposite color with respect to the one each bird had become accustomed to. Vultures still interacted more with the smelly ball disregarding the color, while caracaras interacted equally with the two balls. The prevalence of olfaction in Turkey vultures may partly explain why they are the first raptors to find carcasses in tropical forests. In contrast, caracaras forage on the ground opportunistically, a strategy where both olfaction and sight may be involved. Our experiments suggest that both species are able to use olfactory cues for foraging. However, olfaction could be the predominant sense in Turkey vultures while olfaction and sight could play an equivalent role in Southern caracaras.

Visual field shape and foraging ecology in diurnal raptors.

Birds, particularly raptors, are believed to forage primarily using visual cues. However, raptor foraging tactics are highly diverse - from chasing mobile prey to scavenging - which may reflect adaptations of their visual systems. To investigate this, we studied the visual field configuration of 15 species of diurnal Accipitriformes that differ in such tactics, first focusing on the binocular field and blind area by using a single-traits approach, and then exploring the shape of the binocular field with a morphometric approach. While the maximum binocular field width did not differ between species with different foraging tactics, the overall shape of their binocular fields did. In particular, raptors chasing terrestrial prey (ground predators) had a more protruding binocular field and a wider blind area above the head than did raptors chasing aerial or aquatic prey and obligate scavengers. Ground predators that forage on mammals from above have a wide but short bill - which increases ingestion rate - and a large suborbital ridge to avoid sun glare. This may explain the protruding binocular field and the wide blind area above the head. By contrast, species from the two other groups have long but narrow bills used to pluck, flake or tear food and may need large visual coverage (and reduced suborbital ridges) to increase their foraging efficiency (e.g. using large visual coverage to follow the escaping prey in three dimensions or detect conspecifics). We propose that binocular field shape is associated with bill and suborbital ridge shape and, ultimately, foraging strategies.

Structural organisation and dynamics in king penguin colonies.

During breeding, king penguins do not build nests, however they show strong territorial behaviour and keep a pecking distance to neighbouring penguins. Penguin positions in breeding colonies are highly stable over weeks and appear regularly spaced, but thus far no quantitative analysis of the structural order inside a colony has been performed. In this study, we use the radial distribution function to analyse the spatial coordinates of penguin positions. Coordinates are obtained from aerial images of two colonies that were observed for several years. Our data demonstrate that the structural order in king penguin colonies resembles a 2-dimensional liquid of particles with a Lennard-Jones-type interaction potential. We verify this using a molecular dynamics simulation with thermally driven particles, whereby temperature corresponds to penguin movements, the energy well depth e of the attractive potential corresponds to the strength of the colony-forming behaviour, and the repulsive zone corresponds to the pecking radius. We can recapitulate the liquid disorder of the colony, as measured by the radial distribution function, when the particles have a temperature of several (1.4-10) ε/k B and a normally distributed repulsive radius. To account for the observation that penguin positions are stable over the entire breeding period, we hypothesize that the liquid disorder is quenched during the colony formation process. Quenching requires the temperature to fall considerably below 1 ε/k B, which corresponds to a glass transition, or the repulsion radius to exceed the distance between neighbouring penguins, which corresponds to a jamming transition. Video recordings of a breeding colony together with simulations suggest that quenching is achieved by a behavioural motility arrest akin to a glass transition. We suggest that a liquid disordered colony structure provides an ideal compromise between high density and high flexibility to respond to external disturbances that require a repositioning of penguins.

100 million years of multigene family evolution: origin and evolution of the avian MHC class IIB.

BACKGROUND: Gene duplication has led to a most remarkable adaptation involved in vertebrates' host-pathogen arms-race, the major histocompatibility complex (MHC). However, MHC duplication history is as yet poorly understood in non-mammalian vertebrates, including birds. RESULTS: Here, we provide evidence for the evolution of two ancient avian MHC class IIB (MHCIIB) lineages by a duplication event prior to the radiation of all extant birds >100 million years ago, and document the role of concerted evolution in eroding the footprints of the avian MHCIIB duplication history. CONCLUSIONS: Our results suggest that eroded footprints of gene duplication histories may mimic birth-death evolution and that in the avian MHC the presence of the two lineages may have been masked by elevated rates of concerted evolution in several taxa. Through the presence of a range of intermediate evolutionary stages along the homogenizing process of concerted evolution, the avian MHCIIB provides a remarkable illustration of the erosion of multigene family duplication history.

Odour-based discrimination of similarity at the major histocompatibility complex in birds.

Many animals are known to preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC) in order to maximize the antigen binding repertoire (or disease resistance) in their offspring. Although several mammals, fish or lizards use odour cues to assess MHC similarity with potential partners, the ability of birds to assess MHC similarity using olfactory cues has not yet been explored. Here we used a behavioural binary choice test and high-throughput-sequencing of MHC class IIB to determine whether blue petrels can discriminate MHC similarity based on odour cues alone. Blue petrels are seabirds with particularly good sense of smell, they have a reciprocal mate choice and are known to preferentially mate with MHC-dissimilar partners. Incubating males preferentially approached the odour of the more MHC-dissimilar female, whereas incubating females showed opposite preferences. Given their mating pattern, females were, however, expected to show preference for the odour of the more MHC-dissimilar male. Further studies are needed to determine whether, as in women and female mice, the preference varies with the reproductive cycle in blue petrel females. Our results provide the first evidence that birds can use odour cues only to assess MHC dissimilarity.

Marked phylogeographic structure of Gentoo penguin reveals an ongoing diversification process along the Southern Ocean.

Two main hypotheses have been debated about the biogeography of the Southern Ocean: (1) the Antarctic Polar Front (APF), acting as a barrier between Antarctic and sub-Antarctic provinces, and (2) the Antarctic Circumpolar Current (ACC), promoting gene flow among sub-Antarctic areas. The Gentoo penguin is distributed throughout these two provinces, separated by the APF. We analyzed mtDNA (HVR1) and 12 microsatellite loci of 264 Gentoo penguins, Pygoscelis papua, from 12 colonies spanning from the Western Antarctic Peninsula and the South Shetland Islands (WAP) to the sub-Antarctic Islands (SAI). While low genetic structure was detected among WAP colonies (mtDNA ФST=0.037-0.133; microsatellite FST=0.009-0.063), high differentiation was found between all SAI and WAP populations (mtDNA ФST=0.678-0.930; microsatellite FST=0.110-0.290). These results suggest that contemporary dispersal around the Southern Ocean is very limited or absent. As predicted, the APF appears to be a significant biogeographical boundary for Gentoo penguin populations; however, the ACC does not promote connectivity in this species. Our data suggest demographic expansion in the WAP during the last glacial maximum (LGM, about 20kya), but stability in SAI. Phylogenetic analyses showed a deep divergence between populations from the WAP and those from the SAI. Therefore, taxonomy should be further revised. The Crozet Islands resulted as a basal clade (3.57Mya), followed by the Kerguelen Islands (2.32Mya) as well as a more recent divergence between the Falkland/Malvinas Islands and the WAP (1.27Mya). Historical isolation, local adaptation, and past climate scenarios of those Evolutionarily Significant Units may have led to different potentials to respond to climate changes.

Blue petrels recognize the odor of their egg.

Most studies on avian olfactory communication have focused on mate choice, and the importance of olfaction in subsequent nesting stages has been poorly explored. In particular, the role of olfactory cues in egg recognition has received little attention, despite eggs potentially being spread with parental odorous secretions known to elicit individual discrimination. Here, we used behavioral choice tests to determine whether female blue petrels (Halobaena caerulea) can discriminate the odor of their own egg from the odor of a conspecific egg. Females preferentially approached the odor of their own egg, suggesting that blue petrels can recognize their own egg using odor cues. This finding raises the question of the adaptive value of this mechanism, and may inspire further research on odor-based egg discrimination in species suffering brood parasitism.

Eye Size, Fovea, and Foraging Ecology in Accipitriform Raptors.

Birds with larger eyes are predicted to have higher spatial resolution because of their larger retinal image. Raptors are well known for their acute vision, mediated by their deep central fovea. Because foraging strategies may demand specific visual adaptations, eye size and fovea may differ between species with different foraging ecology. We tested whether predators (actively hunting mobile prey) and carrion eaters (eating dead prey) from the order Accipitriformes differ in eye size, foveal depth, and retinal thickness using spectral domain optical coherence tomography and comparative phylogenetic methods. We found that (1) all studied predators (except one) had a central and a temporal fovea, but all carrion eaters had only the central fovea; (2) eye size scaled with body mass both in predators and carrion eaters; (3) predators had larger eyes relative to body mass and a thicker retina at the edge of the fovea than carrion eaters, but there was no difference in the depth of the central fovea between the groups. Finally, we found that (4) larger eyes generally had a deeper central fovea. These results suggest that the visual system of raptors within the order Accipitriformes may be highly adapted to the foraging strategy, except for the foveal depth, which seems mostly dependent upon the eye size.