The Evolution of Multiple Color Mechanisms Is Correlated with Diversification in Sunbirds (Nectariniidae).

How and why certain groups become speciose is a key question in evolutionary biology. Novel traits that enable diversification by opening new ecological niches are likely important mechanisms. However, ornamental traits can also promote diversification by opening up novel sensory niches and thereby creating novel inter-specific interactions. More specifically, ornamental colors may enable more precise and/or easier species recognition and may act as key innovations by increasing the number of species-specific patterns and promoting diversification. While the influence of coloration on diversification is well-studied, the influence of the mechanisms that produce those colors (e.g., pigmentary, nanostructural) is less so, even though the ontogeny and evolution of these mechanisms differ. We estimated a new phylogenetic tree for 121 sunbird species and combined color data of 106 species with a range of phylogenetic tools to test the hypothesis that the evolution of novel color mechanisms increases diversification in sunbirds, one of the most colorful bird clades. Results suggest that: (1) the evolution of novel color mechanisms expands the visual sensory niche, increasing the number of achievable colors, (2) structural coloration diverges more readily across the body than pigment-based coloration, enabling an increase in color complexity, (3) novel color mechanisms might minimize trade-offs between natural and sexual selection such that color can function both as camouflage and conspicuous signal, and (4) despite structural colors being more colorful and mobile, only melanin-based coloration is positively correlated with net diversification. Together, these findings explain why color distances increase with an increasing number of sympatric species, even though packing of color space predicts otherwise.

Living fast, dying young: Anthropogenic habitat modification influences the fitness and life history traits of a cooperative breeder.

Anthropogenic habitat modification can indirectly effect reproduction and survival in social species by changing the group structure and social interactions. We assessed the impact of habitat modification on the fitness and life history traits of a cooperative breeder, the Arabian babbler (Argya squamiceps). We collected spatial, reproductive and social data on 572 individuals belonging to 21 social groups over 6 years and combined it with remote sensing to characterize group territories in an arid landscape. In modified resource-rich habitats, groups bred more and had greater productivity, but individuals lived shorter lives than in natural habitats. Habitat modification favoured a faster pace-of-life with lower dispersal and dominance acquisition ages, which might be driven by higher mortality providing opportunities for the dominant breeding positions. Thus, habitat modification might indirectly impact fitness through changes in social structures. This study shows that trade-offs in novel anthropogenic opportunities might offset survival costs by increased productivity.

Performative Manipulation of the Environment by Displaying Albert's Lyrebirds.

AbstractWhere dramatic sexual displays are involved in attracting a mate, individuals can enhance their performances by manipulating their physical environment. Typically, individuals alter their environment either in preparation for a performance by creating a "stage" or during the display itself by using discrete objects as "props." We examined an unusual case of performative manipulation of an entire stage by male Albert's lyrebirds (Menura alberti) during their complex song and dance displays. We found that males from throughout the species' range shake the entangled forest vegetation of their display platforms, creating a highly conspicuous and stereotypical movement external to their bodies. This "stage shaking" is performed in two different rhythms, with the second rhythm an isochronous beat that matches the beat of the coinciding vocalizations. Our results provide evidence that stage shaking is an integral, and thus likely functional, component of male Albert's lyrebird sexual displays and so highlight an intriguing but poorly understood facet of complex communication.

Aggressive interactions influence cognitive performance in Western Australian magpies.

Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.

The evolution and ecology of gigantism in terror birds (Aves, Phorusrhacidae).

Terror birds (Aves, Phorusrhacidae) were large flightless apex predators in South America during the Cenozoic. Here, we estimate a new phylogeny for phorusrhacids using Bayesian inference. We demonstrate phylogenetic evidence for a monophyletic Patagornithinae and find significant support for a distinct crown group associated with the quintessential 'terror bird' characteristics. We use this phylogeny to analyse the evolution of body size and cursoriality. Our results reveal that size overlap was rare between co-occurring subfamilies, supporting the hypothesis that these traits were important for niche partitioning. We observe that gigantism evolved in a single clade, containing Phorusrhacinae and Physornithinae. The members of this lineage were consistently larger than all other phorusrhacids. Phorusrhacinae emerged following the extinction of Physornithinae, suggesting the ecological succession of the apex predator niche. The first known phorusrhacine, Phorusrhacos longissimus, was gigantic but significantly smaller and more cursorial than any physornithine. These traits likely evolved in response to the expansion of open environments. Following the Santacrucian SALMA, phorusrhacines increased in size, further converging on the morphology of Physornithinae. These findings suggest that the evolution and displacement of body size drove terror bird niche partitioning and competitive exclusion controlled phorusrhacid diversity.

Odours of caterpillar-infested trees increase testosterone concentrations in male great tits.

Trees release Herbivore-Induced Plant Volatiles (HIPVs) into the air in response to damage inflicted by insects. It is known that songbirds use those compounds to locate their prey, but more recently the idea emerged that songbirds could also use those odours as cues in their reproductive decisions, as early spring HIPVs may contain information about the seasonal timing and abundance of insects. We exposed pre-breeding great tits (Parus major) to the odours of caterpillar-infested trees under controlled conditions, and monitored reproduction (timing of egg laying, number of eggs, egg size) and two of its main hormonal drivers (testosterone and 17ß-estradiol in males and females, respectively). We found that females exposed to HIPVs did not advance their laying dates, nor laid larger clutches, or larger eggs compared to control females. 17ß-estradiol concentrations in females were also similar between experimental and control birds. However, males exposed to HIPVs had higher testosterone concentrations during the egg-laying period. Our study supports the hypothesis that insectivorous songbirds are able to detect minute amounts of plant odours. The sole manipulation of plant scents was not sufficient to lure females into a higher reproductive investment, but males increased their reproductive effort in response to a novel source of information for seasonal breeding birds.

Biomechanics of biting in loggerhead shrikes: jaw-closing force, velocity and an argument for power.

Differences in the physical and behavioral attributes of prey are likely to impose disparate demands of force and speed on the jaws of a predator. Because of biomechanical trade-offs between force and speed, this presents an interesting conundrum for predators of diverse prey types. Loggerhead shrikes (Lanius ludovicianus) are medium-sized (∼50 g) passeriform birds that dispatch and feed on a variety of arthropod and vertebrate prey, primarily using their beaks. We used high-speed video of shrikes biting a force transducer in lateral view to obtain corresponding measurements of bite force, upper and lower bill linear and angular displacements, and velocities. Our results show that upper bill depression (about the craniofacial hinge) is more highly correlated with bite force, whereas lower bill elevation is more highly correlated with jaw-closing velocity. These results suggest that the upper and lower jaws might play different roles for generating force and speed (respectively) in these and perhaps other birds as well. We hypothesize that a division of labor between the jaws may allow shrikes to capitalize on elements of force and speed without compromising performance. As expected on theoretical grounds, bite force trades-off against jaw-closing velocity during the act of biting, although peak bite force and jaw-closing velocity across individual shrikes show no clear signs of a force-velocity trade-off. As a result, shrikes appear to bite with jaw-closing velocities and forces that maximize biting power, which may be selectively advantageous for predators of diverse prey that require both jaw-closing force and speed.

Investigating the relationship between physical cognitive tasks and a social cognitive task in a wild bird.

Despite considerable research into the structure of cognition in non-human animal species, there is still much debate as to whether animal cognition is organised as a series of discrete domains or an overarching general cognitive factor. In humans, the existence of general intelligence is widely accepted, but less work has been undertaken in animal psychometrics to address this question. The relatively few studies on non-primate animal species that do investigate the structure of cognition rarely include tasks assessing social cognition and focus instead on physical cognitive tasks. In this study, we tested 36 wild Western Australian magpies (Gymnorhina tibicen dorsalis) on a battery of three physical (associative learning, spatial memory, and numerical assessment) and one social (observational spatial memory) cognitive task, to investigate if cognition in this species fits a general cognitive factor model, or instead one of separate physical and social cognitive domains. A principal component analysis (PCA) identified two principal components with eigenvalues exceeding 1; a first component onto which all three physical tasks loaded strongly and positively, and a second component onto which only the social task (observational spatial memory) loaded strongly and positively. These findings provide tentative evidence for separate physical and social cognitive domains in this species, and highlight the importance of including tasks assessing both social and physical cognition in cognitive test batteries.

Proto-tool use for food processing in wild Arabian babblers: matching processing methods, substrates and prey types.

Cognition is a powerful adaptation, enabling animals to utilise resources that are unavailable without manipulation. Tool use and food processing are examples of using cognition to overcome the protective mechanisms of food resources. Here, we describe and examine the flexibility of proto-tool use (defined as the alteration of an object through object-substrate manipulation) for food processing in a cooperatively breeding bird, the Arabian babbler (Argya squamiceps). Field observations demonstrate that the birds transport different caterpillar species to different substrate types depending on the processing method needed to prepare the caterpillar for eating. Species with toxic setae (e.g. Casama innotata) are transported to be rubbed on rough substrates (e.g. sand) before consumption, while other species (e.g. Hyles livornica) are transported to be pounded against hard substrates until their inner organs are removed and only their external body part is consumed. These results are among the few to describe flexible proto-tool use for food processing in wild animals. They thereby contribute to the taxonomic mapping of proto-tool use and food processing in non-human species, which is a fundamental step to advance comparative studies on the evolution of these behaviours and their underlying cognitive mechanisms.

Are comparable studies really comparable? Suggestions from a problem-solving experiment on urban and rural great tits.

Performance in tests of various cognitive abilities has often been compared, both within and between species. In intraspecific comparisons, habitat effects on cognition has been a popular topic, frequently with an underlying assumption that urban animals should perform better than their rural conspecifics. In this study, we tested problem-solving ability in great tits Parus major, in a string-pulling and a plug-opening test. Our aim was to compare performance between urban and rural great tits, and to compare their performance with previously published problem solving studies. Our great tits perfomed better in string-pulling than their conspecifics in previous studies (solving success: 54%), and better than their close relative, the mountain chickadee Poecile gambeli, in the plug-opening test (solving success: 70%). Solving latency became shorter over four repeated sessions, indicating learning abilities, and showed among-individual correlation between the two tests. However, the solving ability did not differ between habitat types in either test. Somewhat unexpectedly, we found marked differences between study years even though we tried to keep conditions identical. These were probably due to small changes to the experimental protocol between years, for example the unavoidable changes of observers and changes in the size and material of test devices. This has an important implication: if small changes in an otherwise identical set-up can have strong effects, meaningful comparisons of cognitive performance between different labs must be extremely hard. In a wider perspective this highlights the replicability problem often present in animal behaviour studies.

Auditory risk recognition is socially transmitted across territory borders in wild birds.

Prey species commonly assess predation risk based on acoustic signals, such as predator vocalizations or heterospecific alarm calls. The resulting risk-sensitive decision-making affects not only the behavior and life-history of individual prey, but also has far-reaching ecological consequences for population, community, and ecosystem dynamics. Although auditory risk recognition is ubiquitous in animals, it remains unclear how individuals gain the ability to recognize specific sounds as cues of a threat. Here, it has been shown that free-living birds (Wood Warblers Phylloscopus sibilatrix) can learn to recognize unfamiliar, complex sounds (samples of punk rock songs) as cues of a threat from conspecifics holding adjacent territories during the spring breeding season. In a playback experiment, Wood Warblers initially ignored the unfamiliar sounds, but after repeatedly hearing that these sounds trigger alarm calling reaction of neighbors, most individuals showed an anti-predator response to them. Moreover, once learned soon after nestlings hatching, the anti-predator response of parents toward previously unfamiliar sounds was then retained over the entire nestlings rearing period. These results demonstrate that social learning via the association of unfamiliar sounds with known alarm signals enables the spread of anti-predator behavior across territory borders and provides a mechanism explaining the widespread abilities of animals to assess predation risk based on acoustic cues.

The flashy escape: support for dynamic flash coloration as anti-predator defence.

Dynamic flash coloration is a type of antipredator coloration where intermittently appearing colour patterns in moving animals misdirect predator attacks by obscuring the precise location and trajectory of the moving prey. Birds and butterflies with differing dorsoventral wing coloration or iridescent surface structures may potentially benefit from such effects. However, we lack an understanding of what makes for an effective dynamic flash colour design and how much it benefits the carrier. Here, we test the effect of colour flashing using small passerine birds preying upon colourful, moving, virtual 'prey' stimuli on a touchscreen. We show that at fast speeds, green-to-blue flashing colour patterns can reduce the likelihood of pecks hitting the target, induce greater error in targeting accuracy and increase the number of pecks at a stimulus relative to similarly coloured non-flashing targets. Our results support the idea that dynamic flash coloration can deflect predatory attacks at fast speeds, but the effect may be the opposite when moving slowly.

Infection risk associated with carnivore carcasses may govern trophic interactions between maggots and insectivorous passerine birds.

Infection risk by pathogenic agents motivates hosts to avoid using resources with high risks. This, in turn, results in increased availability of these resources for other species that are more tolerant of infections. For instance, carcasses of mammalian carnivores are frequently avoided by conspecific or closely related carnivores, allowing them to be almost exclusively used by maggots. This may lead to novel interactions with other species. This study investigated the consumption of maggots from carnivore carcasses by non-corvid passerines. We successfully monitored 66 raccoon carcasses in Hokkaido, Japan, from 2016 to 2019. Vertebrates only scavenged 14 carcasses before maggot dispersal; the other 52 carcasses produced abundant maggots that regularly fed at least 12 species of non-corvid passerines. Surprisingly, predation occurred at a distance from the carcasses, mainly after maggot dispersal for pupation, despite the higher efficiency of feeding on maggot masses on the carcasses. Birds are likely to reduce the potential risk of infection from the carcass and/or from maggots on the carcasses. Overall, only 1% of maggots were consumed. Our results suggest that necrophagous flies could benefit from the infection risk associated with carnivore carcasses, which may decrease scavenging by other carnivores and constrain maggot consumption by insectivorous birds.

Noise constrains heterospecific eavesdropping more than conspecific reception of alarm calls.

Many vertebrates eavesdrop on alarm calls of other species, as well as responding to their own species' calls, but eavesdropping on heterospecific alarm calls might be harder than conspecific reception when environmental conditions make perception or recognition of calls difficult. This could occur because individuals lack hearing specializations for heterospecific calls, have less familiarity with them, or require more details of call structure to identify calls they have learned to recognize. We used a field playback experiment to provide a direct test of whether noise, as an environmental perceptual challenge, reduces response to heterospecific compared to conspecific alarm calls. We broadcast superb fairy-wren (Malurus cyaneus) and white-browed scrubwren (Sericornis frontalis) flee alarm calls to each species with or without simultaneous broadcast of ambient noise. Using two species allows isolation of the challenge of heterospecific eavesdropping independently of any effect of call structure on acoustic masking. As predicted, birds were less likely to flee to heterospecific than conspecific alarm calls during noise. We conclude that eavesdropping was harder in noise, which means that noise could disrupt information on danger in natural eavesdropping webs and so compromise survival. This is particularly significant in a world with increasing anthropogenic noise.

Winter-ground microhabitat use by differently coloured phenotypes affects return rate in a long-distance migratory bird.

Migratory bird populations are declining globally at alarming rates. Non-breeding site conditions affect breeding populations, but generalising non-breeding habitat conditions over large spatial regions cannot address potential fine-scale differences across landscapes or local populations. Plumage characteristics can mediate the effects of environmental conditions on individual fitness. However, whether different phenotypes use distinctive non-breeding sites, and whether they respond to non-breeding site conditions differently remains largely unknown. Stable isotopes (δ13C, δ15N, δ2H) of inert tissues are useful to infer habitat characteristics and geographic origins where those tissues were grown. We collected winter-grown feathers from pied flycatchers (Ficedula hypoleuca) on their breeding grounds over several years from males whose dorsal plumage colouration ranged continuously from brown to black and assessed their stable isotope values as proxies of local habitat conditions. Based on feather δ2H profiles we found that browner males spent their non-breeding season in drier habitats than black males. Assignment to origin analysis shows potential regional non-breeding ground separation between differently coloured males. High within-individual repeatability of both δ13C and δ15N indicate the pied flycatcher males return yearly to similar areas. Blacker males were more likely to return to the breeding grounds after dry years compared with brown males. The opposite was found in wet years. Our study demonstrates that different phenotypes are exposed to different non-breeding site conditions which can differentially affect individual survivorship. This has important ramifications for population dynamics under predicted climate change scenarios where especially brown phenotype pied flycatcher males may be under a risk of decreasing.

Nightly reductions in body temperature and effect of transmitter attachment method in free-living welcome swallows (Hirundoneoxena).

Small birds and mammals face similar energetic challenges, yet use of torpor to conserve energy while resting is considered less common among birds, especially within the most specious order Passeriformes. We conducted the first study to record the natural thermoregulatory physiology of any species from the family Hirundinidae, which we predicted would use torpor because of their specialised foraging by aerial pursuit of flying insects, that are less active during cold or windy weather. We used temperature telemetry on wild-living welcome swallows (Hirundo neoxena, 13 to 17 g) and found that skin temperature declined during nightly resting by an average by 5 °C, from daytime minima of 41.0 ± 0.8 °C to nightly minima of 36.3 ± 0.8 °C, and by a maximum of 8 °C to a minimum recorded skin temperature of 32.0 °C. The extent of reduction in skin temperature was greater on cold nights and following windy daytime (foraging) periods. Further, we found that transmitters glued directly to the skin between feather tracts (i.e., an apterium) provided a less variable and probably also more accurate reflection of body temperature than transmitters applied over closely trimmed feathers. A moderate decrease in skin temperature, equivalent to shallow torpor, would provide energy savings during rest. Yet, deeper torpor was not observed, despite a period of extreme rainfall that presumedly decreased foraging success. Further studies are needed to understand the resting thermoregulatory energetics of swallows under different environmental conditions. We advocate the importance of measuring thermal biology in wild-living birds to increase our knowledge of the physiology and ecological importance of torpor among passerine birds.

Increased density of conspecifics caused niche contraction in a multispecific passerine assemblage.

Competition is a prominent mechanism driving population dynamics and structuring community assemblage, which can be investigated by linking shifts in species' ecological niche and the densities of sympatric species because the ecological release from competitive constraints is a density-dependent process. In this work we determine how a steppe passerine community segregates their ecological niches and evaluate the role of competition in inducing changes in the ecological niche of species. We built multidimensional ecological niches (with Gaussian kernel density estimators) using data on the habitat features used by 10 bird species collected from seven sites in the natural steppes of Central Spain over 2 consecutive years. We computed distance and niche similarity metrics to explore the ecological niche partitioning of the bird community. Next, we ran multivariate linear regression models to evaluate the effects of conspecific and heterospecific density (as proxies of intraspecific and interspecific competition, respectively) on niche breadth and/or position of the three most abundant species. We found low niche overlap in the community assemblage but varying levels of niche similarity among pairs of species, which could increase the likelihood of current competition operating in the community. However, we found no effect of heterospecific density on niche breadth or position, although conspecific density was negatively related to niche breadth. Contrary to predictions of competition theory, increased density of conspecifics caused niche contraction. Our results from a multispecies system contribute to advanced knowledge of the biotic mechanisms structuring wildlife communities within the framework of ecological niche theory.

Eurasian jays (Garrulus glandarius) show episodic-like memory through the incidental encoding of information.

Episodic memory describes the conscious reimagining of our memories and is often considered to be a uniquely human ability. As these phenomenological components are embedded within its definition, major issues arise when investigating the presence of episodic memory in non-human animals. Importantly, however, when we as humans recall a specific experience, we may remember details from that experience that were inconsequential to our needs, thoughts, or desires at that time. This 'incidental' information is nevertheless encoded automatically as part of the memory and is subsequently recalled within a holistic representation of the event. The incidental encoding and unexpected question paradigm represents this characteristic feature of human episodic memory and can be employed to investigate memory recall in non-human animals. However, without evidence for the associated phenomenology during recall, this type of memory is termed 'episodic-like memory'. Using this approach, we tested seven Eurasian jays (Garrulus glandarius) on their ability to use incidental visual information (associated with observed experimenter made 'caches') to solve an unexpected memory test. The birds performed above chance levels, suggesting that Eurasian jays can encode, retain, recall, and access incidental visual information within a remembered event, which is an ability indicative of episodic memory in humans.

Episodic-like memory in wild free-living blue tits and great tits.

Episodic-like memory in non-human animals represents the behavioral characteristics of human episodic memory-the ability to mentally travel backward in time to "re-live" past experiences. A focus on traditional model species of episodic-like memory may overlook taxa possessing this cognitive ability and consequently its evolution across species. Experiments conducted in the wild have the potential to broaden the scope of episodic-like memory research under the natural conditions in which they evolved. We combine two distinct yet complementary episodic-like memory tasks (the what-where-when memory and incidental encoding paradigms), each targeting a different aspect of human episodic memory, namely the content (what-where-when) and process (incidental encoding), to comprehensively test the memory abilities of wild, free-living, non-caching blue tits (Cyanistes caeruleus) and great tits (Parus major). Automated feeders with custom-built programs allowed for experimental manipulation of spatiotemporal experiences on an individual-level basis. In the what-where-when memory experiment, after learning individualized temporal feeder rules, the birds demonstrated their ability to recall the "what" (food type), "where" (feeder location), and "when" (time since their initial visit of the day) of previous foraging experiences. In the incidental encoding experiment, the birds showed that they were able to encode and recall incidental spatial information regarding previous foraging experiences ("where" test), and juveniles, but not adults, were also able to recall incidentally encoded visual information ("which" test). Consequently, this study presents multiple lines of converging evidence for episodic-like memory in a wild population of generalist foragers, suggesting that episodic-like memory may be more taxonomically widespread than previously assumed.

Expression patterns of heat-shock genes during stopover and the trade-off between refueling and stress response in a passerine migrant.

Migrating birds are often exposed to variable environments and face a multitude of stress exposures along their long-distance flights. During stopover refueling, migratory birds must balance the need to accumulate energy reserves to continue their migration with the need to respond to environmental and physiological stressors. We examined the gene expression patterns of different Heat Shock Proteins (HSPs) in migrating birds during stopover at different body condition states (lean vs. fat), to provide some first insights on the role of HSPs in bird migration and explore the concept of a trade-off between refueling and stress response. Our results showed upregulation of HSP expression at release that could be associated with muscle growth and increased cholesterol and lipid synthesis needed for birds to fuel their upcoming migration. On the other hand, during capture, upregulation of HSP5 could be attributed to physiological recovery from the non-stop endurance flight when crossing the Sahara Desert-Mediterranean Sea ecological barrier. All birds significantly increased their fuel loads up to 48% of lean body mass and we provide evidence for muscle rebuilding during stopover as flight muscle mass increased by 10%, highlighting the fact that stopover sites can play a major role in the physiological recovery of migrants.