American crows that excel at tool use activate neural circuits distinct from less talented individuals.

Tools enable animals to exploit and command new resources. However, the neural circuits underpinning tool use and how neural activity varies with an animal's tool proficiency, are only known for humans and some other primates. We use 18F-fluorodeoxyglucose positron emission tomography to image the brain activity of naïve vs trained American crows (Corvus brachyrhynchos) when presented with a task requiring the use of stone tools. As in humans, talent affects the neural circuits activated by crows as they prepare to execute the task. Naïve and less proficient crows use neural circuits associated with sensory- and higher-order processing centers (the mesopallium and nidopallium), while highly proficient individuals increase activity in circuits associated with motor learning and tactile control (hippocampus, tegmentum, nucleus basorostralis, and cerebellum). Greater proficiency is found primarily in adult female crows and may reflect their need to use more cognitively complex strategies, like tool use, to obtain food.

A global horizon scan for urban evolutionary ecology.

Research on the evolutionary ecology of urban areas reveals how human-induced evolutionary changes affect biodiversity and essential ecosystem services. In a rapidly urbanizing world imposing many selective pressures, a time-sensitive goal is to identify the emergent issues and research priorities that affect the ecology and evolution of species within cities. Here, we report the results of a horizon scan of research questions in urban evolutionary ecology submitted by 100 interdisciplinary scholars. We identified 30 top questions organized into six themes that highlight priorities for future research. These research questions will require methodological advances and interdisciplinary collaborations, with continued revision as the field of urban evolutionary ecology expands with the rapid growth of cities.

The role of urban waterbodies in maintaining bird species diversity within built area of Beijing.

This study aims to provide a comprehensive understanding of the role of urban waterbodies in avian ecology, which is instructive for both biodiversity conservation and urban planning. Based on bird surveys conducted in 41 urban parks in Beijing during the breeding and wintering seasons of 2018-2019, and using standardized regression analyses, we identified the specific effects of waterbody attributes on the full avian community and forest bird guilds. We assessed this at multiple spatial scales, first within the focal parks, and then within buffer zones with radius of 200 m and 1000 m. We found that waterbodies can serve as avian diversity "hotspots" in the urban landscape. More specifically, they support avian diversity in the following ways: (1) Parks with waterbodies maintain a higher number of bird species than parks without waterbodies during the breeding season and attract resident forest birds during the wintering season. (2) When not frozen, waterbodies inside and outside parks contribute equally to resident forest bird species richness, while more individuals were attracted by waterbodies within neighborhoods. (3) In parks without waterbodies, the number of forest bird species significantly increases with the number of waterbody patches within neighborhoods, while the corresponding relationship for parks with waterbodies is insignificant. These findings suggest a preference for habitats nearby waterbodies among forest birds residing highly urbanized areas. This study provides new insights into avian ecology in urban landscapes and scientific support for the idea that creating and maintaining urban waterbodies can conserve biodiversity.

American Crow Brain Activity in Response to Conspecific Vocalizations Changes When Food Is Present.

Social interaction among animals can occur under many contexts, such as during foraging. Our knowledge of the regions within an avian brain associated with social interaction is limited to the regions activated by a single context or sensory modality. We used 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) to examine American crow (Corvus brachyrhynchos) brain activity in response to conditions associated with communal feeding. Using a paired approach, we exposed crows to either a visual stimulus (the sight of food), an audio stimulus (the sound of conspecifics vocalizing while foraging) or both audio/visual stimuli presented simultaneously and compared to their brain activity in response to a control stimulus (an empty stage). We found two regions, the nucleus taenia of the amygdala (TnA) and a medial portion of the caudal nidopallium, that showed increased activity in response to the multimodal combination of stimuli but not in response to either stimulus when presented unimodally. We also found significantly increased activity in the lateral septum and medially within the nidopallium in response to both the audio-only and the combined audio/visual stimuli. We did not find any differences in activation in response to the visual stimulus by itself. We discuss how these regions may be involved in the processing of multimodal stimuli in the context of social interaction.

Brain activity underlying American crow processing of encounters with dead conspecifics.

Animals utilize a variety of auditory and visual cues to navigate the landscape of fear. For some species, including corvids, dead conspecifics appear to act as one such visual cue of danger, and prompt alarm calling by attending conspecifics. Which brain regions mediate responses to dead conspecifics, and how this compares to other threats, has so far only been speculative. Using 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) we contrast the metabolic response to visual and auditory cues associated with a dead conspecific among five a priori selected regions in the American crow (Corvus brachyrhynchos) brain: the hippocampus, nidopallium caudolaterale, striatum, amygdala, and the septum. Using a repeated-measures, fully balanced approach, we exposed crows to four stimuli: a dead conspecific, a dead song sparrow (Melospiza melodia), conspecific alarm calls given in response to a dead crow, and conspecific food begging calls. We find that in response to observations of a dead crow, crows show significant activity in areas associated with higher-order decision-making (NCL), but not in areas associated with social behaviors or fear learning. We do not find strong differences in activation between hearing alarm calls and food begging calls; both activate the NCL. Lastly, repeated exposures to negative stimuli had a marginal effect on later increasing the subjects' brain activity in response to control stimuli, suggesting that crows might quickly learn from negative experiences.

Individual and social factors affecting the ability of American crows to solve and master a string pulling task.

Crows and other birds in the family Corvidae regularly share information to learn the identity and whereabouts of dangerous predators, but can they use social learning to solve a novel task for a food reward? Here we examined the factors affecting the ability of 27 wild-caught American crows to solve a common string-pulling task in a laboratory setting. We split crows into two groups; one group was given the task after repeatedly observing a conspecific model the solution, the other solved in the absence of conspecific models. We recorded the crows' estimated age, sex, size, body condition, level of nervousness, and brain volume using DICOM images from a CT scan. Although none of these variables were statistically significant, crows without a conspecific model and large brain volumes consistently mastered the task in the minimum number of days, whereas those with conspecific models and smaller brain volumes required varying and sometimes a substantial number of days to master the task. We found indirect evidence that body condition might also be important for motivating crows to solve the task. Crows with conspecific models were no more likely to initially solve the task than those working the puzzle without social information, but those that mastered the task usually copied the method most frequently demonstrated by their knowledgeable neighbors. These findings suggest that brain volume and possibly body condition may be factors in learning new tasks, and that crows can use social learning to refine their ability to obtain a novel food source, although they must initially learn to access it themselves.

Population responses of common ravens to reintroduced gray wolves.

Top predators have cascading effects throughout the food web, but their impacts on scavenger abundance are largely unknown. Gray wolves (Canis lupus) provide carrion to a suite of scavenger species, including the common raven (Corvus corax). Ravens are wide-ranging and intelligent omnivores that commonly take advantage of anthropogenic food resources. In areas where they overlap with wolves, however, ravens are numerous and ubiquitous scavengers of wolf-acquired carrion. We aimed to determine whether subsidies provided through wolves are a limiting factor for raven populations in general and how the wolf reintroduction to Yellowstone National Park in 1995-1997 affected raven population abundance and distribution on the Yellowstone's Northern Range specifically. We counted ravens throughout Yellowstone's Northern Range in March from 2009 to 2017 in both human-use areas and wolf habitat. We then used statistics related to the local wolf population and the winter weather conditions to model raven abundance during our study period and predict raven abundance on the Northern Range both before and after the wolf reintroduction. In relatively severe winters with greater snowpack, raven abundance increased in areas of human use and decreased in wolf habitat. When wolves were able to acquire more carrion, however, ravens increased in wolf habitat and decreased in areas with anthropogenic resources. Raven populations prior to the wolf reintroduction were likely more variable and heavily dependent on ungulate winter-kill and hunter-provided carcasses. The wolf recovery in Yellowstone helped stabilize raven populations by providing a regular food supply, regardless of winter severity. This stabilization has important implications for effective land management as wolves recolonize the west and global climate patterns change.

Occurrence and variability of tactile interactions between wild American crows and dead conspecifics.

Observations of some mammals and birds touching their dead provoke questions about the motivation and adaptive value of this potentially risky behaviour. Here, we use controlled experiments to determine if tactile interactions are characteristic of wild American crow responses to dead crows, and what the prevalence and nature of tactile interactions suggests about their motivations. In Experiment 1, we test if food or information acquisition motivates contact by presenting crows with taxidermy-prepared dead crows, and two species crows are known to scavenge: dead pigeons and dead squirrels. In Experiment 2, we test if territoriality motivates tactile interactions by presenting crows with taxidermy crows prepared to look either dead or upright and life-like. In Experiment 1, we find that crows are significantly less likely to make contact but more likely to alarm call and recruit other birds in response to dead crows than to dead pigeons and squirrels. In addition, we find that aggressive and sexual encounters with dead crows are seasonally biased. These findings are inconsistent with feeding or information acquisition-based motivation. In Experiment 2, we find that crows rarely dive-bomb and more often alarm call and recruit other crows to dead than to life-like crows, behaviours inconsistent with responses given to live intruders. Consistent with a danger response hypothesis, our results show that alarm calling and neighbour recruitment occur more frequently in response to dead crows than other stimuli, and that touching dead crows is atypical. Occasional contacts, which take a variety of aggressive and sexual forms, may result from an inability to mediate conflicting stimuli.This article is part of the theme issue 'Evolutionary thanatology: impacts of the dead on the living in humans and other animals'.

Space use of suburban pileated woodpeckers (Dryocopus pileatus): insights on the relationship between home range, core areas, and territory.

Home range, territory, and core areas are concepts that have been used to describe a species' space use. However, little research has been done to understand potential spatial relationships between them. While the relative importance of different areas of the home range has been addressed with utilization distributions, there is a lack of such analysis for territories. We mapped the locations of territorial advertisements (calls and drumming) of the pileated woodpecker in suburban areas to determine a more objective, behavior-based approach to define areas of importance within territories, which we called 'highly-defended areas'. We then analyzed the relationship between such highly-defended areas and a bird's home range and territory. On average, territories represented 69.6 ± 0.06% (mean ± SE) of a woodpecker's home range, and highly-defended areas were 34.3 ± 0.03% of their home range. Highly-defended areas objectively determined the portion of the territory that was important for fitness. For example, they contained a significant proportion of the nests and roost sites of pileated woodpeckers, which are important for reproduction and survivorship. This approach could be useful to further incorporate behavior in the study of the spatial ecology of species.

Genomic evidence of speciation reversal in ravens.

Many species, including humans, have emerged via complex reticulate processes involving hybridisation. Under certain circumstances, hybridisation can cause distinct lineages to collapse into a single lineage with an admixed mosaic genome. Most known cases of such 'speciation reversal' or 'lineage fusion' involve recently diverged lineages and anthropogenic perturbation. Here, we show that in western North America, Common Ravens (Corvus corax) have admixed mosaic genomes formed by the fusion of non-sister lineages ('California' and 'Holarctic') that diverged ~1.5 million years ago. Phylogenomic analyses and concordant patterns of geographic structuring in mtDNA, genome-wide SNPs and nuclear introns demonstrate long-term admixture and random interbreeding between the non-sister lineages. In contrast, our genomic data support reproductive isolation between Common Ravens and Chihuahuan Ravens (C. cryptoleucus) despite extensive geographic overlap and a sister relationship between Chihuahuan Ravens and the California lineage. These data suggest that the Common Raven genome was formed by secondary lineage fusion and most likely represents a case of ancient speciation reversal that occurred without anthropogenic causes.

Global urban signatures of phenotypic change in animal and plant populations.

Humans challenge the phenotypic, genetic, and cultural makeup of species by affecting the fitness landscapes on which they evolve. Recent studies show that cities might play a major role in contemporary evolution by accelerating phenotypic changes in wildlife, including animals, plants, fungi, and other organisms. Many studies of ecoevolutionary change have focused on anthropogenic drivers, but none of these studies has specifically examined the role that urbanization plays in ecoevolution or explicitly examined its mechanisms. This paper presents evidence on the mechanisms linking urban development patterns to rapid evolutionary changes for species that play important functional roles in communities and ecosystems. Through a metaanalysis of experimental and observational studies reporting more than 1,600 phenotypic changes in species across multiple regions, we ask whether we can discriminate an urban signature of phenotypic change beyond the established natural baselines and other anthropogenic signals. We then assess the relative impact of five types of urban disturbances including habitat modifications, biotic interactions, habitat heterogeneity, novel disturbances, and social interactions. Our study shows a clear urban signal; rates of phenotypic change are greater in urbanizing systems compared with natural and nonurban anthropogenic systems. By explicitly linking urban development to traits that affect ecosystem function, we can map potential ecoevolutionary implications of emerging patterns of urban agglomerations and uncover insights for maintaining key ecosystem functions upon which the sustainability of human well-being depends.

Connecting animal and human cognition to conservation.

Expanding human populations favors a few species while extinguishing and endangering many others (Maxwell et al., 2016; Pimm et al., 2014). Understanding how animals perceive and learn about dangers and rewards can aid conservationists seeking to limit abundant or restore rare species (Schakner and Blumstein, 2016; Greggor et al., 2014; Angeloni et al., 2008; Fernández-Juricic and Schulte, 2016). Cognition research is informing conservation science by suggesting how naïve prey learn novel predators (Griffin et al., 2000; Moseby et al., 2015; Schakner et al., 2016; Blumstein, 2016), the mechanisms underlying variation in tolerance of human disturbance (Bostwick et al., 2014), and when natural aversions and fear learning can be leveraged to humanely control predators (Nielsen et al., 2015; Colman et al., 2014; Norbury et al., 2014; Lance et al., 2010; Cross et al., 2013). Insights into the relationships between cognition and adaptability suggest that behavioral inflexibility often presages species rarity (Amiel et al., 2011; Reif et al., 2011; Sol et al., 2008; Zhang et al., 2014; but see Kellert, 1984). Human compassion and restraint are ultimately required to conserve species. Cognitive science can therefore further inform conservation by revealing the complex inner worlds of the animals we threaten and, in partnership with environmental psychologists, explore how such newfound knowledge affects our empathy for other species and ultimately the public's actions on behalf of species in need of conservation (Collado et al., 2013; Zhang et al., 2014).

Breeding Dispersal by Birds in a Dynamic Urban Ecosystem.

Changes in land cover during urbanization profoundly affect the diversity of bird communities, but the demographic mechanisms affecting diversity are poorly known. We advance such understanding by documenting how urbanization influences breeding dispersal-the annual movement of territorial adults-of six songbird species in the Seattle, WA, USA metropolitan area. We color-banded adults and mapped the centers of their annual breeding activities from 2000-2010 to obtain 504 consecutive movements by 337 adults. By comparing movements, annual reproduction, and mate fidelity among 10 developed, 5 reserved, and 11 changing (areas cleared and developed during our study) landscapes, we determined that adaptive breeding dispersal of sensitive forest species (Swainson's Thrush and Pacific wren), which involves shifting territory and mate after reproductive failure, was constrained by development. In changing lands, sensitive forest specialists dispersed from active development to nearby forested areas, but in so doing suffered low annual reproduction. Species tolerant of suburban lands (song sparrow, spotted towhee, dark-eyed junco, and Bewick's wren) dispersed adaptively in changing landscapes. Site fidelity ranged from 0% (Pacific wren in changing landscape) to 83% (Bewick's wren in forest reserve). Mate fidelity ranged from 25% (dark-eyed junco) to 100% (Bewick's wren). Variation in fidelity to mate and territory was consistent with theories positing an influence of territory quality, asynchronous return from migration, prior productivity, and reproductive benefits of retaining a familiar territory. Costly breeding dispersal, as well as reduced reproductive success and lowered survival cause some birds to decline in the face of urbanization. In contrast, the ability of species that utilize edges and early successional habitats to breed successfully, disperse to improve reproductive success after failure, and survive throughout the urban ecosystem enables them to maintain or increase population size.

Vancomycin resistant Enterococcus spp. from crows and their environment in metropolitan Washington State, USA: Is there a correlation between VRE positive crows and the environment?

Vancomycin-resistant enterococci [VRE] have been isolated from municipal, hospital and agricultural wastewater, recreational beaches, wild animals, birds and food animals around the world. In this study, American crows (Corvus brachyrhynchos) from sewage treatment plants (WWTP), dairy farms, and a large roost in a restored wetland with corresponding environmental samples were cultured for VRE. A total of 245 samples [156 crows, 89 environmental] were collected and screened for acquired vanA, vanB and/or intrinsic vanC1 genes. Samples were enriched overnight in BHI supplemented with 20µg/mL aztreonam, 4µg/mL vancomycin and plated on m-Enterococcus agar media supplemented with 6µg/mL vancomycin. Selected colonies were grown on BHI media supplemented with 18µg/mL vancomycin. Of these, 24.5% of the crow and 55% the environmental/cow samples were VRE positive as defined by Enterococcus spp. able to grow on media supplemented with 18µg/mL vancomycin. A total of 122 VRE isolates, 43 crow and 79 environmental isolates were screened, identified to species level using 16S sequencing and further characterized. Four vanA E. faecium and multiple vanC1 E. gallinarum were identified from crows isolated from three sites. E. faecium vanA and E. gallinarum vanC1 along with other Enterococcus spp. carrying vanA, vanB, vanC1 were isolated from three environments. All enterococci were multidrug resistant. Crows were more likely to carry vanA E. faecium than either the cow feces or wetland waters/soils. Comparing E. gallinarum vanC1 from crows and their environment would be useful in determining whether crows share VRE strains with their environment.

Distinct neural circuits underlie assessment of a diversity of natural dangers by American crows.

Social animals encountering natural dangers face decisions such as whether to freeze, flee or harass the threat. The American crow, Corvus brachyrhynchos, conspicuously mobs dangers. We used positron emission tomography to test the hypothesis that distinct neuronal substrates underlie the crow's consistent behavioural response to different dangers. We found that crows activated brain regions associated with attention and arousal (nucleus isthmo-opticus/locus coeruleus), and with motor response (arcopallium), as they fixed their gaze on a threat. However, despite this consistent behavioural and neural response, the sight of a person who previously captured the crow, a person holding a dead crow and a taxidermy-mounted hawk activated distinct forebrain regions (amygdala, hippocampus and portion of the caudal nidopallium, respectively). We suggest that aspects of mobbing behaviour are guided by unique neural circuits that respond to differences in mental processing-learning, memory formation and multisensory discrimination-required to appropriately nuance a risky behaviour to specific dangers.

Brain imaging reveals neuronal circuitry underlying the crow's perception of human faces.

Crows pay close attention to people and can remember specific faces for several years after a single encounter. In mammals, including humans, faces are evaluated by an integrated neural system involving the sensory cortex, limbic system, and striatum. Here we test the hypothesis that birds use a similar system by providing an imaging analysis of an awake, wild animal's brain as it performs an adaptive, complex cognitive task. We show that in vivo imaging of crow brain activity during exposure to familiar human faces previously associated with either capture (threatening) or caretaking (caring) activated several brain regions that allow birds to discriminate, associate, and remember visual stimuli, including the rostral hyperpallium, nidopallium, mesopallium, and lateral striatum. Perception of threatening faces activated circuitry including amygdalar, thalamic, and brainstem regions, known in humans and other vertebrates to be related to emotion, motivation, and conditioned fear learning. In contrast, perception of caring faces activated motivation and striatal regions. In our experiments and in nature, when perceiving a threatening face, crows froze and fixed their gaze (decreased blink rate), which was associated with activation of brain regions known in birds to regulate perception, attention, fear, and escape behavior. These findings indicate that, similar to humans, crows use sophisticated visual sensory systems to recognize faces and modulate behavioral responses by integrating visual information with expectation and emotion. Our approach has wide applicability and potential to improve our understanding of the neural basis for animal behavior.

Social learning spreads knowledge about dangerous humans among American crows.

Individuals face evolutionary trade-offs between the acquisition of costly but accurate information gained firsthand and the use of inexpensive but possibly less reliable social information. American crows (Corvus brachyrhynchos) use both sources of information to learn the facial features of a dangerous person. We exposed wild crows to a novel 'dangerous face' by wearing a unique mask as we trapped, banded and released 7-15 birds at five study sites near Seattle, WA, USA. An immediate scolding response to the dangerous mask after trapping by previously captured crows demonstrates individual learning, while an immediate response by crows that were not captured probably represents conditioning to the trapping scene by the mob of birds that assembled during the capture. Later recognition of dangerous masks by lone crows that were never captured is consistent with horizontal social learning. Independent scolding by young crows, whose parents had conditioned them to scold the dangerous mask, demonstrates vertical social learning. Crows that directly experienced trapping later discriminated among dangerous and neutral masks more precisely than did crows that learned through social means. Learning enabled scolding to double in frequency and spread at least 1.2 km from the place of origin over a 5 year period at one site.

Random interbreeding between cryptic lineages of the Common Raven: evidence for speciation in reverse.

DNA sequence studies frequently reveal evidence of cryptic lineages in morphologically uniform species, many of which turn out to be evolutionarily distinct species. The Common Raven (Corvus corax) includes two deeply divergent mtDNA lineages: one lineage seems restricted to western North America and the other is Holarctic in distribution. These deep clades hint of the possibility of cryptic species in the western United States. We tested this hypothesis in a population consisting of an equal proportion of both mtDNA clades, by quantifying mating patterns and associated fitness consequences with respect to mtDNA. We also tested for morphological, behavioural and ecological correlates of sex and mtDNA clade membership. Mate pairings were random with respect to mtDNA clades, and there were no differences in reproductive success between assortatively and nonassortatively mated pairs. We found no differences in survival or resource use between clades. There were no differences in morphological or behavioural characters between mtDNA clades, except one clade trended towards greater mobility. These results suggest there are no barriers to gene flow between mtDNA clades and argue that the mtDNA clades have remerged in this population, likely due to a lack of ecological or signal differentiation between individuals in each lineage. Hence, in Common Ravens, phylogeographic structure in mtDNA is a reflection of likely past isolation rather than currently differentiated species.

Climatic and landscape correlates for potential West Nile virus mosquito vectors in the Seattle region.

Climatic and landscape patterns have been associated with both relative mosquito abundance and transmission of mosquito-borne illnesses in many parts of the world, especially warm and tropical climes. To determine if temperature, precipitation, or degree of urbanization were similarly important in the number of potential mosquito vectors for West Nile virus in the moderately temperate climate of western Washington, mosquitoes were collected using CDC carbon-dioxide/light traps set throughout the Seattle region during the summers of 2003 and 2004. The type and abundance of recovered species were compared to ecological correlates. Temperature and mosquito abundance were positively correlated, while precipitation was not strongly correlated with numbers of mosquitoes. Potential WNV mosquito vectors were most abundant in urban and suburban sites, including sites near communal roosts of American crows (Corvus brachyrhynchos). Exurban sites had the greatest vector species diversity, and Culex pipiens was the most abundant species throughout the region.