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Our lab has made several contributions to the literature. If you are interested in learning about some of them, there are classified into (1) novel conceptual frameworks, (2) multi-disciplinary contributions, (3) methodological advancements, (4) physiological findings, (5) behavioral findings, (6) vision-behavior relationships, and (7) conservation ecology.
This is a lot of text (with citations of our papers in parentheses), but it is a good source of information to better understand the breath of research in our lab. |
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Relatively little has been done from a conceptual perspective as to how perception shapes behavior in birds. We have proposed some conceptual frameworks to think about how different visual physiological dimensions may influence decision making in the context of predator-prey interactions, social behavior, and mate choice. This theoretical work is relevant because it provides novel hypotheses, predictions, and assumptions that can guide future research endeavors in this area.
There is a high degree of variability in the visual system of birds (see below) but little is known as to how the variability in different visual dimensions (e.g., visual coverage, visual acuity, motion detection, etc.) could affect vigilance behavior, a key component of anti-predator strategies used to enhance the chances of prey detecting predators early, hence enhancing survival. We developed (Behavioural Processes 89: 143-152, 2012) novel hypotheses and predictions as to how this inter-specific variability would lead to different scanning strategies in birds inhabiting open and closed habitats. The rationale is that the visual conditions in these habitats are quite different (i.e., degree of visual obstruction, direction of predator attacks, spectral properties of light, etc.). Consequently, visual systems may have evolved certain visual characteristics to enhance visual performance in each habitat. Given some morphological constraints (e.g., laterally placed eyes, position of the area of acute vision in the retina), these visual specializations are likely to influence the way birds gather information through head and eye movements and influence the relationships between the amount of time invested in vigilance vs. foraging, which has implications for the survival of individuals.
Besides predator-prey interactions, the inter-specific variability in the avian visual system can influence other social behaviors, such as gaze following, which is the ability of individuals to follow the gaze of conspecifics. Gaze following is a fundamental mechanism underlying the coordination of social interactions in humans, and there is evidence that other vertebrates also gaze follow. We collaborated with researchers at University of Cambridge (UK), and published a paper in Animal Behaviour (87:3-15) in which they developed novel predictions as to how variation in the position of the area of acute vision in the retina and the eyes in the skull would influence whether gaze cues (e.g., head and eye movements) would be salient to conspecifics during visual fixation. The implication is that the incidence of gaze following could be a function of how the visual system is configured.
Some of our research shows that avian visual systems vary not only between species, but also within species between individuals. This raises the possibility that variation in visual perception between females may be related to individual variation in mate choice. We made that case in a review/opinion piece (Animal Behaviour 84: 1283-1294, 2012) in relation to multisensory stimuli (i.e., songs and visual displays in birds). We developed novel predictions relative to the direction of mate choice decisions (choosiness, preference functions) based on individual variation in the sensory system caused by ontogenetic factors (development, stress) and condition (resource availability, hormones, age). This work provides a novel conceptual framework for rigorous testing of the relationship between the sensory system and behavior in the context of sexual selection, honest signaling, and mating patterns.
We also contributed to the development of two novel theoretical frameworks to understand and better predict interactions between predators and prey from a sensory perspective (book chapter in Escaping from predators: an integrative view of escape decisions, published by Cambridge University Press) and between vehicles and wildlife (Biological Reviews 90: 60-76.). The first piece develops a sensory approach to establish the probability that prey detect predators with variations in space and time based on the visual system configuration. The second piece establishes the basic behavioral rules that appear to underlie the responses of wildlife to vehicle approaches, and the implications for mortality across different taxa.
There is a high degree of variability in the visual system of birds (see below) but little is known as to how the variability in different visual dimensions (e.g., visual coverage, visual acuity, motion detection, etc.) could affect vigilance behavior, a key component of anti-predator strategies used to enhance the chances of prey detecting predators early, hence enhancing survival. We developed (Behavioural Processes 89: 143-152, 2012) novel hypotheses and predictions as to how this inter-specific variability would lead to different scanning strategies in birds inhabiting open and closed habitats. The rationale is that the visual conditions in these habitats are quite different (i.e., degree of visual obstruction, direction of predator attacks, spectral properties of light, etc.). Consequently, visual systems may have evolved certain visual characteristics to enhance visual performance in each habitat. Given some morphological constraints (e.g., laterally placed eyes, position of the area of acute vision in the retina), these visual specializations are likely to influence the way birds gather information through head and eye movements and influence the relationships between the amount of time invested in vigilance vs. foraging, which has implications for the survival of individuals.
Besides predator-prey interactions, the inter-specific variability in the avian visual system can influence other social behaviors, such as gaze following, which is the ability of individuals to follow the gaze of conspecifics. Gaze following is a fundamental mechanism underlying the coordination of social interactions in humans, and there is evidence that other vertebrates also gaze follow. We collaborated with researchers at University of Cambridge (UK), and published a paper in Animal Behaviour (87:3-15) in which they developed novel predictions as to how variation in the position of the area of acute vision in the retina and the eyes in the skull would influence whether gaze cues (e.g., head and eye movements) would be salient to conspecifics during visual fixation. The implication is that the incidence of gaze following could be a function of how the visual system is configured.
Some of our research shows that avian visual systems vary not only between species, but also within species between individuals. This raises the possibility that variation in visual perception between females may be related to individual variation in mate choice. We made that case in a review/opinion piece (Animal Behaviour 84: 1283-1294, 2012) in relation to multisensory stimuli (i.e., songs and visual displays in birds). We developed novel predictions relative to the direction of mate choice decisions (choosiness, preference functions) based on individual variation in the sensory system caused by ontogenetic factors (development, stress) and condition (resource availability, hormones, age). This work provides a novel conceptual framework for rigorous testing of the relationship between the sensory system and behavior in the context of sexual selection, honest signaling, and mating patterns.
We also contributed to the development of two novel theoretical frameworks to understand and better predict interactions between predators and prey from a sensory perspective (book chapter in Escaping from predators: an integrative view of escape decisions, published by Cambridge University Press) and between vehicles and wildlife (Biological Reviews 90: 60-76.). The first piece develops a sensory approach to establish the probability that prey detect predators with variations in space and time based on the visual system configuration. The second piece establishes the basic behavioral rules that appear to underlie the responses of wildlife to vehicle approaches, and the implications for mortality across different taxa.
We have promoted and further developed the field of conservation behavior (see book published in 2010), which intends to use animal behavior tools and approaches to solve some (not all) conservation problems. Conservation behavior as a multidisciplinary field has blossomed in the last few years. We edited a special issue of the journal Animal Behaviour on this field. We wrote an Editorial piece that set the current context of this field and where it is going (Animal Behaviour 120: 195-196.). Additionally, we co-authored one of the papers in this special issue that shows different examples of how Federal Agencies, like the USDA, have successfully collaborated with academics to solve specific wildlife management problems by using theoretical approaches from animal behavior and sensory ecology (Animal Behaviour 120: 245-254).
One of the challenges of conservation behavior is to allocate the limited funding resources to solving the overwhelmingly large number of conservation problems. To address this issue, a group of scientists from around the world met in San Diego California last year to set the research agenda for conservation behavior. We were invited to participate in this workshop. The outcome was a paper published in a high profile journal (Trends in Ecology and Evolution 31: 953-964). This contribution to the literature is bound to have a widespread impact in policy making and funding decisions throughout the world, as it sets the priorities for research that would affect in major ways the conservation of species and habitats.
Finally, we compiled a large dataset on previously published papers on two key behavioral responses to human disturbance (alert distance and flight initiation distance), which are often used to make policy decisions about the size of protected areas for wildlife conservation. The paper (Journal of Fish and Wildlife Management 7: 181-191) assesses trends in this dataset (e.g., effect of body mass on sensitivity to disturbance) and makes the database available electronically for managers across the world that need to make quick decisions (without the ability to gather empirical data) about the size of protected areas for single-species human-wildlife conflicts.
One of the challenges of conservation behavior is to allocate the limited funding resources to solving the overwhelmingly large number of conservation problems. To address this issue, a group of scientists from around the world met in San Diego California last year to set the research agenda for conservation behavior. We were invited to participate in this workshop. The outcome was a paper published in a high profile journal (Trends in Ecology and Evolution 31: 953-964). This contribution to the literature is bound to have a widespread impact in policy making and funding decisions throughout the world, as it sets the priorities for research that would affect in major ways the conservation of species and habitats.
Finally, we compiled a large dataset on previously published papers on two key behavioral responses to human disturbance (alert distance and flight initiation distance), which are often used to make policy decisions about the size of protected areas for wildlife conservation. The paper (Journal of Fish and Wildlife Management 7: 181-191) assesses trends in this dataset (e.g., effect of body mass on sensitivity to disturbance) and makes the database available electronically for managers across the world that need to make quick decisions (without the ability to gather empirical data) about the size of protected areas for single-species human-wildlife conflicts.
The multidisciplinary study of how visual perception influences behavior in a comparative context requires the development of novel tools and methodological procedures as well as the standardization of techniques to gather data from multiple species to later test hypotheses and predictions in a phylogenetically controlled context. We have embraced this challenge to strengthen the ability of our lab to make these studies possible.
Robotic birds. One of the methodological challenges to study empirically how animals use social information is to manipulate the behavior of group mates and measure the responses of focal individuals. We developed a system to solve this problem by building bird-robots using bird skins and miniature servos (Animal Behaviour 71:901-911). This technique has opened up new opportunities to characterize the mechanistic basis of social information gathering in social as well as territorial species, which can shed light into the evolution of sociality. We used this robotic technique to further study the transmission of social information in species that have different visual acuity (Behavioral Ecology 22: 1304-1311, 2011) and in species with multisensory signals used in anti-predator contexts (Ethology 120: 375-387).
Standardization of retinal wholemounting techniques. Addressing questions related to the evolution of the visual system in vertebrates requires obtaining information from different species with similar methodological procedures in order to make the data comparable. We collaborated with a prestigious group of visual scientists from the University of Western Australia published a paper that presented a set of methodological procedures to standardize the extraction, flattening, and staining of any vertebrate retina as well as visualization of labeled cells and stereological mapping of cell density (Brain, Behavior and Evolution 79: 26-44, 2012). This paper was the Editor’s choice and thus granted open access on the journal website. This an important contribution as it provides the methodological foundations to future studies on the evolution of the vertebrate retina.
Quantifying retinal traits for comparative studies. Modern evolutionary biology tests hypotheses about the evolution of traits using quantitative methods that take into consideration the phylogenetic relationships between species. Comparative visual physiologists have produced a plethora of information on the configuration of the vertebrate retinas based on graphical representations of variations in the density of photoreceptors and retinal ganglion cells across the retina using topographic maps. These topographic maps can help establish the size, position, number, and type of areas of acute vision in the retina (i.e., retinal specializations). Actually, there is large number of retinal topographic maps from diverse vertebrate taxa available in the literature. This valuable comparative resource has been underutilized mostly because of the lack of a method to compare topographic maps from species that differ in eye size. We collaborated with an international group of visual scientists developed a method to quantify several retinal traits using published topographic maps: position of the retinal specialization, gradient in cell density from the retinal specialization to the retinal periphery, and peak and lowest cell density (Journal of Vision 12: 1-24, 2012). These traits are indicators of variations in spatial resolving power within the retina, which can affect the behavioral strategies animals use to gather visual information from their environment (e.g., head and eye movements). This novel method has been used to investigate patterns of retinal configuration in vertebrate retinas with different types of specializations.
Eye-tracker for birds. One of the main challenges to studying avian vision has been to determine which part of their visual fields birds pay attention to under different contexts (e.g.. foraging, predator detection, mate choice). The problem is related to morphology: birds have their eyes approximately laterally placed in the skull. The center of visual attention generally coincides with the projection of the fovea into visual space, which varies because of the movement of eyes. Eye trackers are used in humans to study where they focus their visual attention. We collaborated with a New York based company (http://positivescience.com/) have developed the first eye tracker for small birds with the ability to record both eyes simultaneously. Two infrared cameras are used to track the eyes (one camera per eye) and two additional, full color cameras are positioned above the head so that we can see what the animal can see. The images are integrated through software that requires knowledge on the position of the retinal specialization (e.g., fovea) of the study species. The latter information is also collected in our lab with different physiological techniques. An example of the eye tracker in action is available in this online video (http://www.youtube.com/watch?v=b8pI5O_2UVI&feature=youtu.be) that shows what a European starling pays attention to during a visual attack of a raptor. The video shows the time delay until the starling detects the predator approaching, and how it focuses its visual attention first on the predator’s feet (involved in grabbing the prey) and eventually on the predator’s bill (involved in killing the prey). A paper on this project was published in Methods in Ecology and Evolution (5: 1070-1077). A second paper using this technique was published in the Journal of Experimental Biology (218: 2651-2657) showing that European starlings move both eyes at the same time but not with the same amplitude. More importantly, the direction of eye movement tends to be oblique, which may be related to the need for this species to check the substrate for food and the sky for predators.
Measurement of foveal morphology. We have developed a new piece of software to standardize the measurement of the morphology of the fovea, one of the most common types of centers of acute vision in many vertebrates. This software uses histological cross-sections of the fovea or optical coherence tomography pictures of the fovea to better understand the evolution of the fovea morphology in vertebrates as well as for diagnostic purposes in veterinary pathology. The paper was published in PeerJ (PeerJ 4:e1785).
Robotic birds. One of the methodological challenges to study empirically how animals use social information is to manipulate the behavior of group mates and measure the responses of focal individuals. We developed a system to solve this problem by building bird-robots using bird skins and miniature servos (Animal Behaviour 71:901-911). This technique has opened up new opportunities to characterize the mechanistic basis of social information gathering in social as well as territorial species, which can shed light into the evolution of sociality. We used this robotic technique to further study the transmission of social information in species that have different visual acuity (Behavioral Ecology 22: 1304-1311, 2011) and in species with multisensory signals used in anti-predator contexts (Ethology 120: 375-387).
Standardization of retinal wholemounting techniques. Addressing questions related to the evolution of the visual system in vertebrates requires obtaining information from different species with similar methodological procedures in order to make the data comparable. We collaborated with a prestigious group of visual scientists from the University of Western Australia published a paper that presented a set of methodological procedures to standardize the extraction, flattening, and staining of any vertebrate retina as well as visualization of labeled cells and stereological mapping of cell density (Brain, Behavior and Evolution 79: 26-44, 2012). This paper was the Editor’s choice and thus granted open access on the journal website. This an important contribution as it provides the methodological foundations to future studies on the evolution of the vertebrate retina.
Quantifying retinal traits for comparative studies. Modern evolutionary biology tests hypotheses about the evolution of traits using quantitative methods that take into consideration the phylogenetic relationships between species. Comparative visual physiologists have produced a plethora of information on the configuration of the vertebrate retinas based on graphical representations of variations in the density of photoreceptors and retinal ganglion cells across the retina using topographic maps. These topographic maps can help establish the size, position, number, and type of areas of acute vision in the retina (i.e., retinal specializations). Actually, there is large number of retinal topographic maps from diverse vertebrate taxa available in the literature. This valuable comparative resource has been underutilized mostly because of the lack of a method to compare topographic maps from species that differ in eye size. We collaborated with an international group of visual scientists developed a method to quantify several retinal traits using published topographic maps: position of the retinal specialization, gradient in cell density from the retinal specialization to the retinal periphery, and peak and lowest cell density (Journal of Vision 12: 1-24, 2012). These traits are indicators of variations in spatial resolving power within the retina, which can affect the behavioral strategies animals use to gather visual information from their environment (e.g., head and eye movements). This novel method has been used to investigate patterns of retinal configuration in vertebrate retinas with different types of specializations.
Eye-tracker for birds. One of the main challenges to studying avian vision has been to determine which part of their visual fields birds pay attention to under different contexts (e.g.. foraging, predator detection, mate choice). The problem is related to morphology: birds have their eyes approximately laterally placed in the skull. The center of visual attention generally coincides with the projection of the fovea into visual space, which varies because of the movement of eyes. Eye trackers are used in humans to study where they focus their visual attention. We collaborated with a New York based company (http://positivescience.com/) have developed the first eye tracker for small birds with the ability to record both eyes simultaneously. Two infrared cameras are used to track the eyes (one camera per eye) and two additional, full color cameras are positioned above the head so that we can see what the animal can see. The images are integrated through software that requires knowledge on the position of the retinal specialization (e.g., fovea) of the study species. The latter information is also collected in our lab with different physiological techniques. An example of the eye tracker in action is available in this online video (http://www.youtube.com/watch?v=b8pI5O_2UVI&feature=youtu.be) that shows what a European starling pays attention to during a visual attack of a raptor. The video shows the time delay until the starling detects the predator approaching, and how it focuses its visual attention first on the predator’s feet (involved in grabbing the prey) and eventually on the predator’s bill (involved in killing the prey). A paper on this project was published in Methods in Ecology and Evolution (5: 1070-1077). A second paper using this technique was published in the Journal of Experimental Biology (218: 2651-2657) showing that European starlings move both eyes at the same time but not with the same amplitude. More importantly, the direction of eye movement tends to be oblique, which may be related to the need for this species to check the substrate for food and the sky for predators.
Measurement of foveal morphology. We have developed a new piece of software to standardize the measurement of the morphology of the fovea, one of the most common types of centers of acute vision in many vertebrates. This software uses histological cross-sections of the fovea or optical coherence tomography pictures of the fovea to better understand the evolution of the fovea morphology in vertebrates as well as for diagnostic purposes in veterinary pathology. The paper was published in PeerJ (PeerJ 4:e1785).
Our research has provided new understanding as to how birds perceive their surroundings visually. The results of this work reveal visual configurations unexpected based on previous research.
Many models of the behavioral components of predator-prey interactions are based on assumptions as to how individuals gather information with their sensory systems. One of these assumptions is that scanning and foraging are mutually exclusive activities (e.g., birds cannot gather visual information about predators or conspecifics while head-down seeking food). This mutual exclusivity assumption has framed theoretical and empirical aspects of the fields of anti-predator and foraging behavior, which have often used birds as model species. However, this assumption may not be valid in many bird species with lateral vision, because many species have visual capabilities that may allow them to see not only when head-up (e.g., classic vigilance posture) but also when head-down (Ibis 150: 779-787, 2008; Animal Behaviour 81: 705-713, 2011).
In the predator-prey interaction literature, mammalian predators have generally been associated with having wide binocular fields to detect and track prey (e.g., lions). However, contrary to this paradigm, we found that three avian diurnal predators tend to have relatively narrow binocular fields (PLoS ONE 5(9): e12802, 2010). This may be associated with the configuration of their retina. Avian diurnal predators generally have two retinal areas for acute vision; the fovea with the higher acuity projects into the lateral field and the fovea with lower acuity projects into the binocular field. Avian predators appear to use the binocular field only when they are close to grabbing the prey during an attack. However, they appear to use the lateral field to detect and follow prey over longer distances. Consequently, avian predators have a dual-retinal specialization configuration that divides the detection and catching of prey in different parts of the visual field (lateral and binocular, respectively).
Mammals that tend to be preyed upon (e.g. zebra) have often been associated with narrow binocular fields and narrow blind areas to enhance visual coverage and the early detection of approaching predators. We found in different studies that avian prey tend to have narrow blind areas, but contrary to the mammalian paradigm, they have wide binocular fields (Animal Behaviour 77: 673-684, 2009; Animal Behaviour 81: 705-713, 2011; Journal of Comparative Physiology A 196: 879-888,2010 ; Brain, Behavior and Evolution 83: 181-198). The avian prey retinas have a single fovea configuration where acute vision projects laterally, but a high degree of eye movement that may allow them to have high visual resolution in their binocular fields to detect and grab food items at close distances. Therefore, the binocular field may have an important role in food detection and catching in avian prey.
Vertebrate species living in open habitats have been hypothesized to have a horizontal visual streak in their retinas (a band of high visual acuity across the central part of the retina) that is aligned with the horizon where most of the information about food and predator opportunities is obtained (i.e., terrain hypothesis). We tested whether Canada geese, a species that inhabits open areas in North America, would follow this visual configuration. Canada geese were found to have a visual streak; however, the position of the visual streak was oblique rather than horizontal (Brain, Behavior and Evolution 77: 147-158, 2011). This would allow geese to see with high visual resolution the sky and the ground simultaneously, which could be advantageous while foraging and also flying long distances during their migration. Additionally, the visual streak was found to be associated with both color vision and motion detection (Journal of Experimental Biology 215: 3442-3452, 2012).
Dr. Fernández-Juricic’s team also tested whether another open habitat species that inhabits native prairies in North America would follow the visual configuration proposed by the terrain hypothesis (see previous paragraph). We found that Eastern meadowlarks have a single fovea rather than a visual streak, but interestingly the fovea was placed in the ventral portion of the retina (Scientific Reports 3, Article number: 3231, 2013). The implication is that the area of acute vision in this species would project upwards, possibly to detect and keep track of visual stimuli (predators, conspecifics) as meadowlarks spend a lot of time on the ground. This is the first report of an open habitat avian species having a ventral fovea.
Birds form heterospecific (i.e. multi-species) flocks in tropical and temperate areas. One of the hypotheses explaining heterospecific flocking is that some species (known as satellite species) join other species that initiate flock movements and alarm-call upon detection of predators (known as nuclear species). Therefore, satellite species are expected to benefit by obtaining information about potential predator attacks from nuclear species. One of the key assumptions in this directional transmission of information is that nuclear species have visual systems capable of detecting predators earlier than satellite species. We tested this assumption by studying different visual sensory components and scanning behavior of three species that generally join heterospecific flocks in North America during the non-breeding season: titmice, chickadees, and nuthatches. The results of the study did not support the assumption of the directional transmission of information as the satellite species have higher visual acuity than the nuclear species (Journal of Comparative Physiology A 199: 263–277, 2013). An alternative mechanism for future testing is that satellite species use auditory cues from nuclear species (social information) that are later complemented with their own vigilance behavior (personal information).
Comparative studies on bird vision have generally focused on a single visual dimension (e.g., visual field configuration, distribution and density of ganglion cells/photoreceptors in the retina, sensitivity of visual pigments and oil droplets). However, visual perception involves processing information from multiple dimensions simultaneously. We measured different visual traits (visual field configuration, eye size, retinal configuration, eye movement, visual acuity, position of the retinal specialization, etc.) in nine species of birds belonging to the Emberizidae Family (e.g., sparrows). Even though these species are closely related phylogenetically and are specialized in consuming mostly seeds, this study found that their visual systems differ significantly. One of the main factors associated with this interspecific variation is the size of the pecten, which is a non-sensory and pigmented area of the avian eye that supplies nutrients to the retina. The projection of the pecten into the visual field generates a blind spot from which the animals cannot gather any information. This study also shows that species with wide pectens adjust the visual field configuration by having smaller binocular fields when the eyes are at rest compared to species with narrow pectens. Interestingly, species with wide pectens seem to compensate for this large blind spot by having greater degree of eye movement, leading to an increase in the size of the binocular field when the eyes converged towards the bill, which may be useful when seeking seeds. This study reveals interesting trade-offs in visual field configuration in birds. This study was published in the Journal of Experimental Biology (218:1347-1358).
Besides variation between species, it is possible that there is also variation within a species in visual system configuration based on human studies. However, this level of variation has not been well-documented in non-human vertebrates. In a study published in PLoS One in 2014 (9(11): e111854), we documented for the first time with modern statistical methods intra-population variation in the visual system of birds. More specifically, we found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision in house sparrows (Passer domesticus). Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions. Overall, our findings highlight the need to consider multiple individuals when characterizing sensory traits of a species, and provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities).
Several models have been proposed to explain collective behavior in animals; however, these models often make simplistic assumptions about the sensory systems of the target species. We recently characterized different components of the visual system of two species of cyprinid fish known to engage in visually dependent collective interactions (zebrafish and golden shiners) and derived quantitative predictions about the positioning of individuals within schools based on the configuration of the visual system. Considering between-species differences in the visual system of species exhibiting collective behavior can change the predictions about the positioning of individuals in the group and the shape of the school, which can have implications for group cohesion. This paper was recently published in PeerJ (e1113).
In a follow up study, we considered the effects of these physiological parameters in collective behavior models. Biologists and engineers have been interested in collective animal behavior (i.e., coordinated movements of bird flocks, fish schools, mammal herds, insect swarms) for decades, because establishing the rules animals use to coordinate their behavior with group mates can have multiple applied applications (e.g., unmanned aerial vehicles, disease transmission prevention, etc.). These rules have been incorporated in multiple mathematical models that intend to predict the behavior of these groups. These models make biological assumptions about the individuals interacting in the groups (e.g., interaction distance, number of group mates tracked, etc.). In a recent paper published in Royal Society Open Science (3: 160377), we found that the sensory assumptions often used in these mathematical models do not match with the real sensory configuration of the species studied. More importantly, when considering the realistic sensory assumptions, these mathematical models make very different predictions about collective behavior. These findings have important implications for developing future models that better predict collective animal behavior and establishing the sensory cues animals use to track neighbors.
Many models of the behavioral components of predator-prey interactions are based on assumptions as to how individuals gather information with their sensory systems. One of these assumptions is that scanning and foraging are mutually exclusive activities (e.g., birds cannot gather visual information about predators or conspecifics while head-down seeking food). This mutual exclusivity assumption has framed theoretical and empirical aspects of the fields of anti-predator and foraging behavior, which have often used birds as model species. However, this assumption may not be valid in many bird species with lateral vision, because many species have visual capabilities that may allow them to see not only when head-up (e.g., classic vigilance posture) but also when head-down (Ibis 150: 779-787, 2008; Animal Behaviour 81: 705-713, 2011).
In the predator-prey interaction literature, mammalian predators have generally been associated with having wide binocular fields to detect and track prey (e.g., lions). However, contrary to this paradigm, we found that three avian diurnal predators tend to have relatively narrow binocular fields (PLoS ONE 5(9): e12802, 2010). This may be associated with the configuration of their retina. Avian diurnal predators generally have two retinal areas for acute vision; the fovea with the higher acuity projects into the lateral field and the fovea with lower acuity projects into the binocular field. Avian predators appear to use the binocular field only when they are close to grabbing the prey during an attack. However, they appear to use the lateral field to detect and follow prey over longer distances. Consequently, avian predators have a dual-retinal specialization configuration that divides the detection and catching of prey in different parts of the visual field (lateral and binocular, respectively).
Mammals that tend to be preyed upon (e.g. zebra) have often been associated with narrow binocular fields and narrow blind areas to enhance visual coverage and the early detection of approaching predators. We found in different studies that avian prey tend to have narrow blind areas, but contrary to the mammalian paradigm, they have wide binocular fields (Animal Behaviour 77: 673-684, 2009; Animal Behaviour 81: 705-713, 2011; Journal of Comparative Physiology A 196: 879-888,2010 ; Brain, Behavior and Evolution 83: 181-198). The avian prey retinas have a single fovea configuration where acute vision projects laterally, but a high degree of eye movement that may allow them to have high visual resolution in their binocular fields to detect and grab food items at close distances. Therefore, the binocular field may have an important role in food detection and catching in avian prey.
Vertebrate species living in open habitats have been hypothesized to have a horizontal visual streak in their retinas (a band of high visual acuity across the central part of the retina) that is aligned with the horizon where most of the information about food and predator opportunities is obtained (i.e., terrain hypothesis). We tested whether Canada geese, a species that inhabits open areas in North America, would follow this visual configuration. Canada geese were found to have a visual streak; however, the position of the visual streak was oblique rather than horizontal (Brain, Behavior and Evolution 77: 147-158, 2011). This would allow geese to see with high visual resolution the sky and the ground simultaneously, which could be advantageous while foraging and also flying long distances during their migration. Additionally, the visual streak was found to be associated with both color vision and motion detection (Journal of Experimental Biology 215: 3442-3452, 2012).
Dr. Fernández-Juricic’s team also tested whether another open habitat species that inhabits native prairies in North America would follow the visual configuration proposed by the terrain hypothesis (see previous paragraph). We found that Eastern meadowlarks have a single fovea rather than a visual streak, but interestingly the fovea was placed in the ventral portion of the retina (Scientific Reports 3, Article number: 3231, 2013). The implication is that the area of acute vision in this species would project upwards, possibly to detect and keep track of visual stimuli (predators, conspecifics) as meadowlarks spend a lot of time on the ground. This is the first report of an open habitat avian species having a ventral fovea.
Birds form heterospecific (i.e. multi-species) flocks in tropical and temperate areas. One of the hypotheses explaining heterospecific flocking is that some species (known as satellite species) join other species that initiate flock movements and alarm-call upon detection of predators (known as nuclear species). Therefore, satellite species are expected to benefit by obtaining information about potential predator attacks from nuclear species. One of the key assumptions in this directional transmission of information is that nuclear species have visual systems capable of detecting predators earlier than satellite species. We tested this assumption by studying different visual sensory components and scanning behavior of three species that generally join heterospecific flocks in North America during the non-breeding season: titmice, chickadees, and nuthatches. The results of the study did not support the assumption of the directional transmission of information as the satellite species have higher visual acuity than the nuclear species (Journal of Comparative Physiology A 199: 263–277, 2013). An alternative mechanism for future testing is that satellite species use auditory cues from nuclear species (social information) that are later complemented with their own vigilance behavior (personal information).
Comparative studies on bird vision have generally focused on a single visual dimension (e.g., visual field configuration, distribution and density of ganglion cells/photoreceptors in the retina, sensitivity of visual pigments and oil droplets). However, visual perception involves processing information from multiple dimensions simultaneously. We measured different visual traits (visual field configuration, eye size, retinal configuration, eye movement, visual acuity, position of the retinal specialization, etc.) in nine species of birds belonging to the Emberizidae Family (e.g., sparrows). Even though these species are closely related phylogenetically and are specialized in consuming mostly seeds, this study found that their visual systems differ significantly. One of the main factors associated with this interspecific variation is the size of the pecten, which is a non-sensory and pigmented area of the avian eye that supplies nutrients to the retina. The projection of the pecten into the visual field generates a blind spot from which the animals cannot gather any information. This study also shows that species with wide pectens adjust the visual field configuration by having smaller binocular fields when the eyes are at rest compared to species with narrow pectens. Interestingly, species with wide pectens seem to compensate for this large blind spot by having greater degree of eye movement, leading to an increase in the size of the binocular field when the eyes converged towards the bill, which may be useful when seeking seeds. This study reveals interesting trade-offs in visual field configuration in birds. This study was published in the Journal of Experimental Biology (218:1347-1358).
Besides variation between species, it is possible that there is also variation within a species in visual system configuration based on human studies. However, this level of variation has not been well-documented in non-human vertebrates. In a study published in PLoS One in 2014 (9(11): e111854), we documented for the first time with modern statistical methods intra-population variation in the visual system of birds. More specifically, we found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision in house sparrows (Passer domesticus). Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions. Overall, our findings highlight the need to consider multiple individuals when characterizing sensory traits of a species, and provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities).
Several models have been proposed to explain collective behavior in animals; however, these models often make simplistic assumptions about the sensory systems of the target species. We recently characterized different components of the visual system of two species of cyprinid fish known to engage in visually dependent collective interactions (zebrafish and golden shiners) and derived quantitative predictions about the positioning of individuals within schools based on the configuration of the visual system. Considering between-species differences in the visual system of species exhibiting collective behavior can change the predictions about the positioning of individuals in the group and the shape of the school, which can have implications for group cohesion. This paper was recently published in PeerJ (e1113).
In a follow up study, we considered the effects of these physiological parameters in collective behavior models. Biologists and engineers have been interested in collective animal behavior (i.e., coordinated movements of bird flocks, fish schools, mammal herds, insect swarms) for decades, because establishing the rules animals use to coordinate their behavior with group mates can have multiple applied applications (e.g., unmanned aerial vehicles, disease transmission prevention, etc.). These rules have been incorporated in multiple mathematical models that intend to predict the behavior of these groups. These models make biological assumptions about the individuals interacting in the groups (e.g., interaction distance, number of group mates tracked, etc.). In a recent paper published in Royal Society Open Science (3: 160377), we found that the sensory assumptions often used in these mathematical models do not match with the real sensory configuration of the species studied. More importantly, when considering the realistic sensory assumptions, these mathematical models make very different predictions about collective behavior. These findings have important implications for developing future models that better predict collective animal behavior and establishing the sensory cues animals use to track neighbors.
We have a long tradition of animal behavior work. Here are some examples.
The vertebrate retina has localized areas for acute vision (e.g., fovea) that animals move with their eyes or heads to gather high quality information. We revealed that birds would engage in different visual tasks (e.g., visual search, visual fixation) depending on the position they have in the flock, which could be influenced by the perceived predation risk (higher in the periphery than the center of a flock). When in the center of a group, birds tend to track visually the behavior of group mates, but when in the periphery, they tend to search visually for potential predators (Animal Behaviour 82: 573-577, 2011). This study also proposed sensory mechanisms to support the use of a new metric to study anti-predator behavior in birds by measuring the rates of head movement.
One of the assumptions in the study of animal groups is that information (e.g., about the presence of a predator) flows between group mates with little degradation. We investigated this assumption by assessing the responses of live birds to robotic birds of the same species that mimicked the escape behavior in response to a predator. Contrary to the prediction, information was indeed found to be degraded as it transferred between group mates (Behavioral Ecology 22: 1304-1311, 2011). More importantly, this study shows that the degree of degradation over distance is negatively associated with visual acuity. Species with lower visual acuity have more pronounced levels of information degradation over distance; hence, they are expected to form groups with higher density of individuals to maintain the benefits of joining groups (i.e., collective detection of predators). These findings provide a novel way of looking at how animals establish groups based on their ability to obtain information from group mates.
Animals are exposed to different levels of ambient light during the day (e.g., early morning vs. midday). Previous studies have shown that low light levels can limit the ability to perform certain behaviors (e.g., foraging) because of sensory constraints (e.g., eyes not adapted to low light). We looked at the other side of the ambient light spectrum and asked whether the avian visual system would be somehow constrained under high light levels to perform a key task to ensure survival: predator detection. The findings of this study support the disability glare hypothesis as brown-headed cowbirds responded more slowly to a ground predator in sunlit than in shaded patches (Ethology 188: 341-350, 2012). This is likely the result of excessive ambient light reducing visual contrast and image discrimination due to glare effects. The results also suggest that cowbirds may be using chromatic cues in shaded patches to enhance predator detection. Overall, this study provides evidence that ambient light conditions can affect the probability of predator detection, a key component in predator-prey interactions.
Vision mediates many social behaviors in birds, including one that is also present in humans: gaze following, which is when one individual follows the orientation of the eyes of a conspecific. Gaze following is a mechanism that is expected to facilitate social interactions. We found that European starlings reoriented their attention to follow that of a robot around a barrier more often compared to when the robot oriented its attention elsewhere (Biology Letters 10: 20140665). This is the first empirical evidence of reorienting in response to conspecific attention in a songbird. Birds may use this behavior to obtain fine-tuned spatial information from conspecifics, enhancing group cohesion (e.g., murmurations in starlings).
To understand the mechanisms behind how birds keep attached themselves to a flock, we studied how birds in a group track themselves visually. Humans often use their centers of acute vision (i.e., fovea) to gather high quality information from other humans. Interestingly, starlings perching next to each other keep track of each other’s presence and behavior by using peripheral (i.e., lower quality) rather than high acute vision. Starlings move their heads laterally to scan the environment, and they tend to mimic the neighbor’s timing to move their head while perching in groups (Animal Behaviour 121: 21-31). These strategies can facilitate the spread of social information (i.e., neighbor escaping) within groups.
We examined whether the responses to cowbird songs would be influenced by the sex of the receiver. Our findings supported the motivational structural rule hypothesis as songs directed towards males had higher entropy (i.e., harshness) than the same song type directed towards females. Our results suggest that cowbirds may have evolved the ability to alter multiple dimensions of their singing behavior based on the sex of the receiver (Ethology 121: 1104-1115).
The vertebrate retina has localized areas for acute vision (e.g., fovea) that animals move with their eyes or heads to gather high quality information. We revealed that birds would engage in different visual tasks (e.g., visual search, visual fixation) depending on the position they have in the flock, which could be influenced by the perceived predation risk (higher in the periphery than the center of a flock). When in the center of a group, birds tend to track visually the behavior of group mates, but when in the periphery, they tend to search visually for potential predators (Animal Behaviour 82: 573-577, 2011). This study also proposed sensory mechanisms to support the use of a new metric to study anti-predator behavior in birds by measuring the rates of head movement.
One of the assumptions in the study of animal groups is that information (e.g., about the presence of a predator) flows between group mates with little degradation. We investigated this assumption by assessing the responses of live birds to robotic birds of the same species that mimicked the escape behavior in response to a predator. Contrary to the prediction, information was indeed found to be degraded as it transferred between group mates (Behavioral Ecology 22: 1304-1311, 2011). More importantly, this study shows that the degree of degradation over distance is negatively associated with visual acuity. Species with lower visual acuity have more pronounced levels of information degradation over distance; hence, they are expected to form groups with higher density of individuals to maintain the benefits of joining groups (i.e., collective detection of predators). These findings provide a novel way of looking at how animals establish groups based on their ability to obtain information from group mates.
Animals are exposed to different levels of ambient light during the day (e.g., early morning vs. midday). Previous studies have shown that low light levels can limit the ability to perform certain behaviors (e.g., foraging) because of sensory constraints (e.g., eyes not adapted to low light). We looked at the other side of the ambient light spectrum and asked whether the avian visual system would be somehow constrained under high light levels to perform a key task to ensure survival: predator detection. The findings of this study support the disability glare hypothesis as brown-headed cowbirds responded more slowly to a ground predator in sunlit than in shaded patches (Ethology 188: 341-350, 2012). This is likely the result of excessive ambient light reducing visual contrast and image discrimination due to glare effects. The results also suggest that cowbirds may be using chromatic cues in shaded patches to enhance predator detection. Overall, this study provides evidence that ambient light conditions can affect the probability of predator detection, a key component in predator-prey interactions.
Vision mediates many social behaviors in birds, including one that is also present in humans: gaze following, which is when one individual follows the orientation of the eyes of a conspecific. Gaze following is a mechanism that is expected to facilitate social interactions. We found that European starlings reoriented their attention to follow that of a robot around a barrier more often compared to when the robot oriented its attention elsewhere (Biology Letters 10: 20140665). This is the first empirical evidence of reorienting in response to conspecific attention in a songbird. Birds may use this behavior to obtain fine-tuned spatial information from conspecifics, enhancing group cohesion (e.g., murmurations in starlings).
To understand the mechanisms behind how birds keep attached themselves to a flock, we studied how birds in a group track themselves visually. Humans often use their centers of acute vision (i.e., fovea) to gather high quality information from other humans. Interestingly, starlings perching next to each other keep track of each other’s presence and behavior by using peripheral (i.e., lower quality) rather than high acute vision. Starlings move their heads laterally to scan the environment, and they tend to mimic the neighbor’s timing to move their head while perching in groups (Animal Behaviour 121: 21-31). These strategies can facilitate the spread of social information (i.e., neighbor escaping) within groups.
We examined whether the responses to cowbird songs would be influenced by the sex of the receiver. Our findings supported the motivational structural rule hypothesis as songs directed towards males had higher entropy (i.e., harshness) than the same song type directed towards females. Our results suggest that cowbirds may have evolved the ability to alter multiple dimensions of their singing behavior based on the sex of the receiver (Ethology 121: 1104-1115).
Here are some examples (within and between species) of studies in which we found ways in which vision shapes behavior.
Understanding sex differences in the nervous system and behavior is essential to explain patterns of mate choice and to test the mechanisms behind many hypotheses on sexual selection and animal communication. Unfortunately, we know relatively little about the way in which males and females obtain sensory information. We addressed some of these gaps by characterizing some components of the visual system, modeling visual perception, and assessing the visual exploratory behavior of an avian brood parasite: the brown-headed cowbird. Brood parasites are excellent model systems to study sex differences in the sensory system because males and females are subject to different selection pressures during the breeding season. For instance, in the brown-headed cowbird, males compete against each other to access females, which eventually are the only ones involved in the process of locating hosts to lay their eggs. Cowbird females have been found to have a higher auditory resolution than males (Gall & Lucas 2011 Journal of Comparative Physiology A: 196, 559-567). However, little is known about their visual systems. We found that females have lower visual resolution (both around the fovea and in the retinal periphery) than males. Interestingly, females appear to compensate for this lower visual resolution by exposing both eyes repeatedly on an object to boost the quality of the visual information obtained (PLoS ONE 8(3): e58985, 2013). These results have some important implications. First, individual variation in the configuration of the visual system can affect behavior (i.e., limited visual resolution modifies the behavioral sampling of visual information) within a species. Second, males and females of this brood parasite may invest differently in their sensory systems likely due to the energetic costs of processing sensory information and their different selection pressures. Females have better auditory than visual resolution that may be used in eavesdropping potential hosts at a distance, whereas males have better visual resolution that is likely used in male-male competition for mates.
Along the lines of inter-specific variation in the avian visual system, we quantified the variation in visual spatial resolution across the retina of different species of birds to assess how it could influence visual behavior. The findings were quite surprising and published recently in Scientific Reports (7, Article number: 38406). First, the center of acute vision in birds (i.e., fovea) is not at the center of the retina (as in humans), but displaced to the temporal part of the retina. The implication is that the center of acute vision projects into the fronto-lateral part of the head (but without projecting into the binocular field). Second, species with a greater degree of variation in visual spatial resolution within the retina tended to show a higher degree of eye and head movements. One explanation is that species with lower peripheral visual resolution would rely more on the center of acute vision to gather high quality information and consequently would need to move it more often. Overall, retinal configuration makes birds heads move.
Understanding sex differences in the nervous system and behavior is essential to explain patterns of mate choice and to test the mechanisms behind many hypotheses on sexual selection and animal communication. Unfortunately, we know relatively little about the way in which males and females obtain sensory information. We addressed some of these gaps by characterizing some components of the visual system, modeling visual perception, and assessing the visual exploratory behavior of an avian brood parasite: the brown-headed cowbird. Brood parasites are excellent model systems to study sex differences in the sensory system because males and females are subject to different selection pressures during the breeding season. For instance, in the brown-headed cowbird, males compete against each other to access females, which eventually are the only ones involved in the process of locating hosts to lay their eggs. Cowbird females have been found to have a higher auditory resolution than males (Gall & Lucas 2011 Journal of Comparative Physiology A: 196, 559-567). However, little is known about their visual systems. We found that females have lower visual resolution (both around the fovea and in the retinal periphery) than males. Interestingly, females appear to compensate for this lower visual resolution by exposing both eyes repeatedly on an object to boost the quality of the visual information obtained (PLoS ONE 8(3): e58985, 2013). These results have some important implications. First, individual variation in the configuration of the visual system can affect behavior (i.e., limited visual resolution modifies the behavioral sampling of visual information) within a species. Second, males and females of this brood parasite may invest differently in their sensory systems likely due to the energetic costs of processing sensory information and their different selection pressures. Females have better auditory than visual resolution that may be used in eavesdropping potential hosts at a distance, whereas males have better visual resolution that is likely used in male-male competition for mates.
Along the lines of inter-specific variation in the avian visual system, we quantified the variation in visual spatial resolution across the retina of different species of birds to assess how it could influence visual behavior. The findings were quite surprising and published recently in Scientific Reports (7, Article number: 38406). First, the center of acute vision in birds (i.e., fovea) is not at the center of the retina (as in humans), but displaced to the temporal part of the retina. The implication is that the center of acute vision projects into the fronto-lateral part of the head (but without projecting into the binocular field). Second, species with a greater degree of variation in visual spatial resolution within the retina tended to show a higher degree of eye and head movements. One explanation is that species with lower peripheral visual resolution would rely more on the center of acute vision to gather high quality information and consequently would need to move it more often. Overall, retinal configuration makes birds heads move.
Years ago, we put forward a mechanism to predict human-wildlife interactions based on the relationships between the frequency of human visitation and the frequency of resource use (e.g., foraging, breeding, roosting, etc.) by wildlife (resource-use disturbance trade-off hypothesis; Fernández-Juricic. 2000. Condor 102: 247-255; Fernández-Juricic. 2002. Oecologia 131: 269-278). This hypothesis argues that thresholds in the intensity and spatial and temporal patterns of human activity exist below which animals can continue to meet their feeding and breeding requirements, and above which the availability of resources to animals is diminished. We incorporated the resource-use disturbance trade-off hypothesis into a spatially-explicit simulation that recreates different species foraging and breeding, and recreationists walking along pathways. GIS is used to generate spatially-explicit conditions. This simulation uses species-specific parameters measured in the field to analyze how food consumption rates, habitat use, population size, and the probabilities of persistence can be affected by varying the spatial and temporal distribution of visitors to protected areas. This simulation generates predictions about patterns of habitat selection in response to disturbance that can be tested in the field. The simulation can eventually help managers protect biodiversity by establishing thresholds of visitors and identifying highly sensitive species based on life history traits. This simulation was described in a paper published in Ecological Complexity 6: 113-134, 2009, and tested with empirical data in a study published recently in Ecological Modelling 222: 2770-2779, 2011.
Animals are exposed to stimuli with different levels of risk (predators vs. human recreationists). Overreacting to non-dangerous stimuli can be energetically costly, so animals tend to habituate to these low-level stimuli. We showed that individual lizards differ in their ability to habituate and that this difference is governed by their specific personalities (Proceedings of the Royal Society of London B 278: 266–273, 2010). Less social animals habituate more because they spend less time in the refuge with other lizards and more time exposed to recreationists. Additionally, lizards that tend to explore more than others are more likely to habituate because they can gather more information about risky conditions. The frequency of individuals with these different personalities can influence habituation levels in wild populations, and this can have important consequences for the management of recreational activities in natural areas.
We developed several applied projects based on the the sensory ecology research. Our approach involves tuning stimuli to the visual system of target species and testing the animal responses with behavioral assays in order to manipulate their behavior (described in a chapter in the book Wildlife Management in Airport Environments. The Johns Hopkins University Press, Baltimore, MD, 2013). This approach is intended to save resources by optimizing the development of stimuli to attract or repel species, which to date has generally been done on a trial-and-error basis. This research has direct practical implications for attracting endangered or threatened species to new breeding areas, attracting birds to bird feeders, reducing the frequency of collisions between birds and human objects (e.g., airplanes, buildings, wind turbines, repelling birds from crops, etc.). For instance, we showed that Canada geese, a species with high frequency of damaging bird strikes, detected significantly sooner an aircraft approaching with pulsing lights than with lights off (Journal of Applied Ecology 49: 758-766, 2012). Based on these results, we used perceptual models to predict the wavelengths of light that would be more salient to Canada geese. Additionally, in a study published in 2015, we found that lights tuned to the avian eye sweet-spot enhanced detection and reduced the chances of animals being overwhelmed from a sensory perspective by the high speeds of aircraft (Condor: Ornithological Applications 117: 165–177). This study got a lot of media attention, including a piece in the news section of the journal Science (http://news.sciencemag.org/plants-animals/2015/04/blue-lights-could-prevent-bird-strikes). These findings have direct implications to reduce the frequency of bird-aircraft collisions like the one that happened in January 2009 out of La Guardia Airport with flight 1549.
Along the lines of collisions between wildlife and vehicles, there have been some observational studies suggesting that vehicle speed could influence the risk of collisions. In an effort to address this question from an experimental perspective, we developed a virtual arena for birds similar to the ones used in humans to understand the factors influencing the risk of cars accidents with pedestrians. With video playbacks, we manipulated the speed of vehicle approaches and measured the responses of birds. We found out that birds used a spatial margin of safety (i.e., a threshold distance at which they initiate avoidance behavior). However, the ability to use this behavioral rule breaks down at really high speeds, which could explain wildlife-vehicle collisions in freeways or highways that allow high speeds. This paper was published in the Proceedings of the Royal Society of London (282: 20142188) in 2015. Additionally, using this virtual arena, we asked the question of whether animals exposed repeatedly to a vehicle approach would exhibit sensitization or habituation responses. This is an important question as it can help us explain the risk of animal-vehicle collisions for animals using highways or freeways often. We found that birds became habituated to vehicles over time, which could increase the risk of collision with vehicles in more experienced animals facing traffic. These counter-intuitive findings were published in the Journal of Zoology (301: 17-22).
Within the context of animal-vehicle collisions, there has been some anecdotal evidence suggesting that weather radars could deter birds from aircraft. In a recent study published in Applied Animal Behaviour Science (171: 241-252), we determined whether bird foraging and antipredator behavior is affected by radar. Our findings suggest that birds might avoid stationary radar units, and moving radar units (e.g., aircraft) might enhance escape responses at low vehicle speeds during taxi, but likely not at higher speeds during take-off, landing, and flight.
Finally, Dr. Fernández-Juricic’s expertise in integrating different fields led him to co-author the first primer textbook in the relatively novel discipline of conservation behavior (A Primer of Conservation Behavior, Sinauer Associates, 2010), which is a discipline that uses behavioral approaches to solve some (but not all) conservation biology and wildlife management problems. Additionally, we published review piece on the integration between conservation behavior and conservation physiology, which is an even more recent discipline that uses physiological procedures to establish the biological mechanisms behind conservation problems (Physiological and Biochemical Zoology 87: 1-14).
Animals are exposed to stimuli with different levels of risk (predators vs. human recreationists). Overreacting to non-dangerous stimuli can be energetically costly, so animals tend to habituate to these low-level stimuli. We showed that individual lizards differ in their ability to habituate and that this difference is governed by their specific personalities (Proceedings of the Royal Society of London B 278: 266–273, 2010). Less social animals habituate more because they spend less time in the refuge with other lizards and more time exposed to recreationists. Additionally, lizards that tend to explore more than others are more likely to habituate because they can gather more information about risky conditions. The frequency of individuals with these different personalities can influence habituation levels in wild populations, and this can have important consequences for the management of recreational activities in natural areas.
We developed several applied projects based on the the sensory ecology research. Our approach involves tuning stimuli to the visual system of target species and testing the animal responses with behavioral assays in order to manipulate their behavior (described in a chapter in the book Wildlife Management in Airport Environments. The Johns Hopkins University Press, Baltimore, MD, 2013). This approach is intended to save resources by optimizing the development of stimuli to attract or repel species, which to date has generally been done on a trial-and-error basis. This research has direct practical implications for attracting endangered or threatened species to new breeding areas, attracting birds to bird feeders, reducing the frequency of collisions between birds and human objects (e.g., airplanes, buildings, wind turbines, repelling birds from crops, etc.). For instance, we showed that Canada geese, a species with high frequency of damaging bird strikes, detected significantly sooner an aircraft approaching with pulsing lights than with lights off (Journal of Applied Ecology 49: 758-766, 2012). Based on these results, we used perceptual models to predict the wavelengths of light that would be more salient to Canada geese. Additionally, in a study published in 2015, we found that lights tuned to the avian eye sweet-spot enhanced detection and reduced the chances of animals being overwhelmed from a sensory perspective by the high speeds of aircraft (Condor: Ornithological Applications 117: 165–177). This study got a lot of media attention, including a piece in the news section of the journal Science (http://news.sciencemag.org/plants-animals/2015/04/blue-lights-could-prevent-bird-strikes). These findings have direct implications to reduce the frequency of bird-aircraft collisions like the one that happened in January 2009 out of La Guardia Airport with flight 1549.
Along the lines of collisions between wildlife and vehicles, there have been some observational studies suggesting that vehicle speed could influence the risk of collisions. In an effort to address this question from an experimental perspective, we developed a virtual arena for birds similar to the ones used in humans to understand the factors influencing the risk of cars accidents with pedestrians. With video playbacks, we manipulated the speed of vehicle approaches and measured the responses of birds. We found out that birds used a spatial margin of safety (i.e., a threshold distance at which they initiate avoidance behavior). However, the ability to use this behavioral rule breaks down at really high speeds, which could explain wildlife-vehicle collisions in freeways or highways that allow high speeds. This paper was published in the Proceedings of the Royal Society of London (282: 20142188) in 2015. Additionally, using this virtual arena, we asked the question of whether animals exposed repeatedly to a vehicle approach would exhibit sensitization or habituation responses. This is an important question as it can help us explain the risk of animal-vehicle collisions for animals using highways or freeways often. We found that birds became habituated to vehicles over time, which could increase the risk of collision with vehicles in more experienced animals facing traffic. These counter-intuitive findings were published in the Journal of Zoology (301: 17-22).
Within the context of animal-vehicle collisions, there has been some anecdotal evidence suggesting that weather radars could deter birds from aircraft. In a recent study published in Applied Animal Behaviour Science (171: 241-252), we determined whether bird foraging and antipredator behavior is affected by radar. Our findings suggest that birds might avoid stationary radar units, and moving radar units (e.g., aircraft) might enhance escape responses at low vehicle speeds during taxi, but likely not at higher speeds during take-off, landing, and flight.
Finally, Dr. Fernández-Juricic’s expertise in integrating different fields led him to co-author the first primer textbook in the relatively novel discipline of conservation behavior (A Primer of Conservation Behavior, Sinauer Associates, 2010), which is a discipline that uses behavioral approaches to solve some (but not all) conservation biology and wildlife management problems. Additionally, we published review piece on the integration between conservation behavior and conservation physiology, which is an even more recent discipline that uses physiological procedures to establish the biological mechanisms behind conservation problems (Physiological and Biochemical Zoology 87: 1-14).