Sensory pollutants alter bird phenology and fitness across a continent.

Expansion of anthropogenic noise and night lighting across our planet1,2 is of increasing conservation concern3-6. Despite growing knowledge of physiological and behavioural responses to these stimuli from single-species and local-scale studies, whether these pollutants affect fitness is less clear, as is how and why species vary in their sensitivity to these anthropic stressors. Here we leverage a large citizen science dataset paired with high-resolution noise and light data from across the contiguous United States to assess how these stimuli affect reproductive success in 142 bird species. We find responses to both sensory pollutants linked to the functional traits and habitat affiliations of species. For example, overall nest success was negatively correlated with noise among birds in closed environments. Species-specific changes in reproductive timing and hatching success in response to noise exposure were explained by vocalization frequency, nesting location and diet. Additionally, increased light-gathering ability of species' eyes was associated with stronger advancements in reproductive timing in response to light exposure, potentially creating phenological mismatches7. Unexpectedly, better light-gathering ability was linked to reduced clutch failure and increased overall nest success in response to light exposure, raising important questions about how responses to sensory pollutants counteract or exacerbate responses to other aspects of global change, such as climate warming. These findings demonstrate that anthropogenic noise and light can substantially affect breeding bird phenology and fitness, and underscore the need to consider sensory pollutants alongside traditional dimensions of the environment that typically inform biodiversity conservation.

Artificial night light and anthropogenic noise interact to influence bird abundance over a continental scale.

The extent of artificial night light and anthropogenic noise (i.e., "light" and "noise") impacts is global and has the capacity to threaten species across diverse ecosystems. Existing research involving impacts of light or noise has primarily focused on noise or light alone and single species; however, these stimuli often co-occur and little is known about how co-exposure influences wildlife and if and why species may vary in their responses. Here, we had three aims: (1) to investigate species-specific responses to light, noise, and the interaction between the two using a spatially explicit approach to model changes in abundance of 140 prevalent bird species across North America, (2) to investigate responses to the interaction between light exposure and night length, and (3) to identify functional traits and habitat affiliations that explain variation in species-specific responses to these sensory stimuli with phylogenetically informed models. We found species that responded to noise exposure generally decreased in abundance, and the additional presence of light interacted synergistically with noise to exacerbate its negative effects. Moreover, the interaction revealed negative emergent responses for several species that only reacted when light and noise co-occurred. Additionally, an interaction between light and night length revealed 47 species increased in abundance with light exposure during longer nights. In addition to modifying behavior with optimal temperature and potential foraging opportunities, birds might be attracted to light, yet suffer inadvertent physiological consequences. The trait that most strongly related to avian response to light and noise was habitat affiliation. Specifically, species that occupy closed habitat were less tolerant of both sensory stressors compared to those that occupy open habitat. Further quantifying the contexts and intrinsic traits that explain how species respond to noise and light will be fundamental to understanding the ecological consequences of a world that is ever louder and brighter.

The Hawk-Eyed Songbird: Retinal Morphology, Eye Shape, and Visual Fields of an Aerial Insectivore.

Swallows are a unique group of songbirds because they are active-pursuit predators that execute all aspects of hunting prey in flight: search, detection, pursuit, and capture. We show that swallows have evolved a visual system that is unlike that of any other studied songbird. Swallows have a bifoveate retina that provides sharp lateral and frontal vision, an unusually long eye that enhances spatial resolution, a large posterior blind area, and a narrow binocular field. We also show that swallows and diurnal raptors (hawks and falcons) have converged on a similar visual configuration but that, interestingly, predatory songbirds that ambush prey (flycatchers) have not converged on the same suite of traits. Despite the commonly held belief that predators rely on binocular vision, the temporal (frontally projecting) fovea present in swallows-but not present in other songbirds-is likely not involved in binocular vision. Instead, swallows have four nonoverlapping foveae in a 100° arc around the beak, which can improve the tracking of frontally located aerial prey that are engaging in evasive maneuvers. Overall, vision in pursuit predators reflects the complex sensory demands of hunting in the air at high speeds and emphasizes the importance of acute frontal vision in predators.

Oculomotor strategy of an avian ground forager: tilted and weakly yoked eye saccades.

Many bird species are capable of large saccadic eye movements that can result in substantial shifts in gaze direction and complex changes to their visual field orientation. In the absence of visual stimuli, birds make spontaneous saccades that follow an endogenous oculomotor strategy. We used new eye-tracking technology specialized for small birds to study the oculomotor behavior of an open-habitat, ground-foraging songbird, the European starling (Sturnus vulgaris). We found that starlings primarily move their eyes along a tilted axis 13.46 deg downwards anteriorly and upwards posteriorly, which differs from the axis parallel to the horizon employed by other species. This tilted axis could enhance foraging and anti-predator strategies while starlings are head-down looking for food, allowing them to direct vision between the open mandibles to visually inspect food items, and above and behind the head to scan areas where predators are more likely to attack. We also found that starlings have neither fully conjugate saccades (as in humans, for example) nor independent saccades (as in chameleons, for example). Rather, they exhibit weakly yoked saccades where the left and right eyes move at the same time but not at the same magnitude. Functionally, weakly yoked saccades may be similar to independent saccades in that they allow the two eyes to concomitantly perform different tasks. The differences between the oculomotor strategies of studied species suggest eye movements play variable but important roles across bird species with different ecological niches.

Vision in avian emberizid foragers: maximizing both binocular vision and fronto-lateral visual acuity.

Avian species vary in their visual system configuration, but previous studies have often compared single visual traits between two to three distantly related species. However, birds use different visual dimensions that cannot be maximized simultaneously to meet different perceptual demands, potentially leading to trade-offs between visual traits. We studied the degree of inter-specific variation in multiple visual traits related to foraging and anti-predator behaviors in nine species of closely related emberizid sparrows, controlling for phylogenetic effects. Emberizid sparrows maximize binocular vision, even seeing their bill tips in some eye positions, which may enhance the detection of prey and facilitate food handling. Sparrows have a single retinal center of acute vision (i.e. fovea) projecting fronto-laterally (but not into the binocular field). The foveal projection close to the edge of the binocular field may shorten the time to gather and process both monocular and binocular visual information from the foraging substrate. Contrary to previous work, we found that species with larger visual fields had higher visual acuity, which may compensate for larger blind spots (i.e. pectens) above the center of acute vision, enhancing predator detection. Finally, species with a steeper change in ganglion cell density across the retina had higher eye movement amplitude, probably due to a more pronounced reduction in visual resolution away from the fovea, which would need to be moved around more frequently. The visual configuration of emberizid passive prey foragers is substantially different from that of previously studied avian groups (e.g. sit-and-wait and tactile foragers).

Genome sequence of Microbacterium foliorum phage CandC.

We report the discovery and genome sequence of CandC, a lytic bacteriophage with siphovirus morphology. CandC was isolated from a soil sample from Plattsburgh, NY, USA (Fall 2021). It has a genome size of 62,344 bp with 106 predicted protein-encoding genes, 30 of which are assigned putative functions.

Why conservation biology can benefit from sensory ecology.

Global expansion of human activities is associated with the introduction of novel stimuli, such as anthropogenic noise, artificial lights and chemical agents. Progress in documenting the ecological effects of sensory pollutants is weakened by sparse knowledge of the mechanisms underlying these effects. This severely limits our capacity to devise mitigation measures. Here, we integrate knowledge of animal sensory ecology, physiology and life history to articulate three perceptual mechanisms-masking, distracting and misleading-that clearly explain how and why anthropogenic sensory pollutants impact organisms. We then link these three mechanisms to ecological consequences and discuss their implications for conservation. We argue that this framework can reveal the presence of 'sensory danger zones', hotspots of conservation concern where sensory pollutants overlap in space and time with an organism's activity, and foster development of strategic interventions to mitigate the impact of sensory pollutants. Future research that applies this framework will provide critical insight to preserve the natural sensory world.

A novel cellular structure in the retina of insectivorous birds.

The keen visual systems of birds have been relatively well-studied. The foundations of avian vision rest on their cone and rod photoreceptors. Most birds use four cone photoreceptor types for color vision, a fifth cone for achromatic tasks, and a rod for dim-light vision. The cones, along with their oil droplets, and rods are conserved across birds - with the exception of a few shifts in spectral sensitivity - despite taxonomic, behavioral and ecological differences. Here, however, we describe a novel photoreceptor organelle in a group of New World flycatchers (Empidonax spp.) in which the traditional oil droplet is replaced with a complex of electron-dense megamitochondria surrounded by hundreds of small, orange oil droplets. The photoreceptors with this organelle were unevenly distributed across the retina, being present in the central region (including in the fovea), but absent from the retinal periphery and the area temporalis of these insectivorous birds. Of the many bird species with their photoreceptors characterized, only the two flycatchers described here (E. virescens and E. minimus) possess this unusual retinal structure. We discuss the potential functional significance of this unique sub-cellular structure, which might provide an additional visual channel for these small predatory songbirds.

The Orientation of Visual Space from the Perspective of Hummingbirds.

Vision is a key component of hummingbird behavior. Hummingbirds hover in front of flowers, guide their bills into them for foraging, and maneuver backwards to undock from them. Capturing insects is also an important foraging strategy for most hummingbirds. However, little is known about the visual sensory specializations hummingbirds use to guide these two foraging strategies. We characterized the hummingbird visual field configuration, degree of eye movement, and orientation of the centers of acute vision. Hummingbirds had a relatively narrow binocular field (~30°) that extended above and behind their heads. Their blind area was also relatively narrow (~23°), which increased their visual coverage (about 98% of their celestial hemisphere). Additionally, eye movement amplitude was relatively low (~9°), so their ability to converge or diverge their eyes was limited. We confirmed that hummingbirds have two centers of acute vision: a fovea centralis, projecting laterally, and an area temporalis, projecting more frontally. This retinal configuration is similar to other predatory species, which may allow hummingbirds to enhance their success at preying on insects. However, there is no evidence that their temporal area could visualize the bill tip or that eye movements could compensate for this constraint. Therefore, guidance of precise bill position during the process of docking occurs via indirect cues or directly with low visual acuity despite having a temporal center of acute vision. The large visual coverage may favor the detection of predators and competitors even while docking into a flower. Overall, hummingbird visual configuration does not seem specialized for flower docking.

Avian binocular vision: It's not just about what birds can see, it's also about what they can't.

With the exception of primates, most vertebrates have laterally placed eyes. Binocular vision in vertebrates has been implicated in several functions, including depth perception, contrast discrimination, etc. However, the blind area in front of the head that is proximal to the binocular visual field is often neglected. This anterior blind area is important when discussing the evolution of binocular vision because its relative length is inversely correlated with the width of the binocular field. Therefore, species with wider binocular fields also have shorter anterior blind areas and objects along the mid-sagittal plane can be imaged at closer distances. Additionally, the anterior blind area is of functional significance for birds because the beak falls within this blind area. We tested for the first time some specific predictions about the functional role of the anterior blind area in birds controlling for phylogenetic effects. We used published data on visual field configuration in 40 species of birds and measured beak and skull parameters from museum specimens. We found that birds with proportionally longer beaks have longer anterior blind areas and thus narrower binocular fields. This result suggests that the anterior blind area and beak visibility do play a role in shaping binocular fields, and that binocular field width is not solely determined by the need for stereoscopic vision. In visually guided foragers, the ability to see the beak-and how much of the beak can be seen-varies predictably with foraging habits. For example, fish- and insect-eating specialists can see more of their own beak than birds eating immobile food can. But in non-visually guided foragers, there is no consistent relationship between the beak and anterior blind area. We discuss different strategies-wide binocular fields, large eye movements, and long beaks-that minimize the potential negative effects of the anterior blind area. Overall, we argue that there is more to avian binocularity than meets the eye.

Does retinal configuration make the head and eyes of foveate birds move?

Animals move their heads and eyes to compensate for movements of the body and background, search, fixate, and track objects visually. Avian saccadic head/eye movements have been shown to vary considerably between species. We tested the hypothesis that the configuration of the retina (i.e., changes in retinal ganglion cell density from the retinal periphery to the center of acute vision-fovea) would account for the inter-specific variation in avian head/eye movement behavior. We characterized retinal configuration, head movement rate, and degree of eye movement of 29 bird species with a single fovea, controlling for the effects of phylogenetic relatedness. First, we found the avian fovea is off the retinal center towards the dorso-temporal region of the retina. Second, species with a more pronounced rate of change in ganglion cell density across the retina generally showed a higher degree of eye movement and higher head movement rate likely because a smaller retinal area with relatively high visual acuity leads to greater need to move the head/eye to align this area that contains the fovea with objects of interest. Our findings have implications for anti-predator behavior, as many predator-prey interaction models assume that the sensory system of prey (and hence their behavior) varies little between species.

FOVEA: a new program to standardize the measurement of foveal pit morphology.

The fovea is one of the most studied retinal specializations in vertebrates, which consists of an invagination of the retinal tissue with high packing of cone photoreceptors, leading to high visual resolution. Between species, foveae differ morphologically in the depth and width of the foveal pit and the steepness of the foveal walls, which could influence visual perception. However, there is no standardized methodology to measure the contour of the foveal pit across species. We present here FOVEA, a program for the quantification of foveal parameters (width, depth, slope of foveal pit) using images from histological cross-sections or optical coherence tomography (OCT). FOVEA is based on a new algorithm to detect the inner retina contour based on the color variation of the image. We evaluated FOVEA by comparing the fovea morphology of two Passerine birds based on histological cross-sections and its performance with data from previously published OCT images. FOVEA detected differences between species and its output was not significantly different from previous estimates using OCT software. FOVEA can be used for comparative studies to better understand the evolution of the fovea morphology in vertebrates as well as for diagnostic purposes in veterinary pathology. FOVEA is freely available for academic use and can be downloaded at: http://estebanfj.bio.purdue.edu/fovea.

Vision in two cyprinid fish: implications for collective behavior.

Many species of fish rely on their visual systems to interact with conspecifics and these interactions can lead to collective behavior. Individual-based models have been used to predict collective interactions; however, these models generally make simplistic assumptions about the sensory systems that are applied without proper empirical testing to different species. This could limit our ability to predict (and test empirically) collective behavior in species with very different sensory requirements. In this study, we characterized components of the visual system in two species of cyprinid fish known to engage in visually dependent collective interactions (zebrafish Danio rerio and golden shiner Notemigonus crysoleucas) and derived quantitative predictions about the positioning of individuals within schools. We found that both species had relatively narrow binocular and blind fields and wide visual coverage. However, golden shiners had more visual coverage in the vertical plane (binocular field extending behind the head) and higher visual acuity than zebrafish. The centers of acute vision (areae) of both species projected in the fronto-dorsal region of the visual field, but those of the zebrafish projected more dorsally than those of the golden shiner. Based on this visual sensory information, we predicted that: (a) predator detection time could be increased by >1,000% in zebrafish and >100% in golden shiners with an increase in nearest neighbor distance, (b) zebrafish schools would have a higher roughness value (surface area/volume ratio) than those of golden shiners, (c) and that nearest neighbor distance would vary from 8 to 20 cm to visually resolve conspecific striping patterns in both species. Overall, considering between-species differences in the sensory system of species exhibiting collective behavior could change the predictions about the positioning of individuals in the group as well as the shape of the school, which can have implications for group cohesion. We suggest that more effort should be invested in assessing the role of the sensory system in shaping local interactions driving collective behavior.

Looking above the prairie: localized and upward acute vision in a native grassland bird.

Visual systems of open habitat vertebrates are predicted to have a band of acute vision across the retina (visual streak) and wide visual coverage to gather information along the horizon. We tested whether the eastern meadowlark (Sturnella magna) had this visual configuration given that it inhabits open grasslands. Contrary to our expectations, the meadowlark retina has a localized spot of acute vision (fovea) and relatively narrow visual coverage. The fovea projects above rather than towards the horizon with the head at rest, and individuals modify their body posture in tall grass to maintain a similar foveal projection. Meadowlarks have relatively large binocular fields and can see their bill tips, which may help with their probe-foraging technique. Overall, meadowlark vision does not fit the profile of vertebrates living in open habitats. The binocular field may control foraging while the fovea may be used for detecting and tracking aerial stimuli (predators, conspecifics).