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When senses take flight: the evolution, development, mechanisms and function of avian senses

Event

Starts:

September
042014

09:00

Ends:

September
052014

17:00

Location

Kavli Royal Society Centre, Chicheley Hall, Newport Pagnell, Buckinghamshire, MK16 9JJ

Overview

Theo Murphy international scientific meeting organised by Dr Hannah Rowland, Professor Innes Cuthill and Dr Tom Pike

The unique hearing system of owls allows them to pinpoint the location of even the faintest sounds. Owl’s ears are asymmetrically positioned on the head. The difference in the height of the ears aids prey location because the sounds coming from prey are received by the ears at slightly different times. Image copyright Professor T Birkhead FRS.

Event details

Birds are adapted to a diverse range of habitats, and operate within a broad range of dietary niches. This diversity of life histories has resulted in an equally varied suite of adaptations for acquiring mates, finding food, avoiding predators and for navigation.  In this meeting, a distinguished list of international researchers encompassing avian vision, taste, olfaction, geo-magnetic sense, nociception (pain), tactile sense, and emotion, will be brought together to discuss new and emerging evidence of the evolution, development, mechanisms and function of avian senses.

You can download the draft meeting programme (PDF), and biographies and abstracts of the speakers are available below. Recorded audio of the presentations will be available on this page after the event.

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Schedule of talks

Session 1: Introduction to bird sense

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Bird sense

Professor Tim Birkhead FRS, University of Sheffield, UK

Abstract

Birds are better studied than almost any other group of animals, especially in terms of behavior, yet our understanding of what it is like to be a bird is extremely limited. This lack of understanding limits our ability to interpret behavior, or to put it another way a better understanding of the sensory system of birds will I predict, revolutionise the way we think about behavior. Because birds seem to be like ourselves in relying mainly on vision and hearing, we have studied those senses but tended to ignore and underestimate other senses such as touch, smell and taste, and emotions in particular. There are historical reasons for this narrow view point, but as we will see, this is now beginning to change.

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Session 2: Sensation

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Nociception in birds

Dr Dorothy McKeegan, University of Glasgow, UK

Abstract

Nociceptors are specialised sensory receptors which allow animals to detect noxious, potentially damaging stimuli, and thus are crucial to survival. Birds possess several types of nociceptors, responding to thermal, mechanical or chemical modalities, or combinations of these (polymodal nociceptors such as mechanothermal). Studies of avian nociceptors have focussed on bird welfare, contributing to the ethical debate surrounding poultry production by clarifying to what extent various conditions and practices constitute a welfare insult. Because of the number of animals involved and the range of potential issues, most of this work has been carried out in chickens. Examples of such studies include determining nociceptive thresholds in the tarsometatartsus of the leg to examine whether shackling prior to slaughter is painful, and characterisation of nasal and oral mucosal nociceptors to examine the welfare implications of gas stunning.  Measurements of nociceptor activity related to the long-term welfare implications of infrared beak trimming (partial amputation of the beak to prevent injurious bird-to-bird pecking) directly influenced UK policy debate, preventing a ban on beak trimming. Recently, studies of nociceptor sensitisation (thermal hyperalgesia) have increased our understanding of pain associated with naturally occurring lameness, which is common in broilers (chickens grown for meat).

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Do birds have emotions?

Professor Melissa Bateson, Newcastle University, UK

Abstract

The ease with which we can answer this question depends critically on how emotion is defined. If we define emotions as valenced states associated with actual or expected punishment or reward, then there is ample evidence that birds have negative emotions. Birds will work to reduce negatively-valenced states, they will avoid places where they have experienced negatively-valenced states and they will show a greater expectation of punishment when they are in negatively-valenced states. None of this is surprising given that emotions are adaptive states designed to allocate cognitive and behavioural resources to the most immediately important fitness-relevant priorities. However, for many people emotion implies feeling, and none of this evidence tells us anything about whether birds have feelings associated with their emotional states. Although we do not have access to the subjective experiences of any non-human animals, I will argue that there are techniques available that could be used to reveal more than we currently know about whether there are feelings associated with different emotional states in birds, and, if present, the nature of these feelings. Conducting this research could bring us closer to answering vexed questions such as the severity of the hunger experienced by food-restricted broiler-breeder chickens.

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The sandpiper-type bill-tip organ in birds: who has it and why?

Dr Susan Cunningham, Percy FitzPatrick Institute of African Ornithology, University of Cape Town, South Africa

Abstract

Birds that forage by probing must often rely on senses other than vision to locate food. One such sense is remote-touch, mediated by an organ (the ‘sandpiper-type’ bill-tip organ) consisting of a distinctive honeycomb of sensory pits in the bill-tip, containing mechanoreceptive Herbst corpuscles. This organ was originally described in shorebirds from the family Scolopacidae, and more recently in kiwi (Apterygidae) and ibises (Threskiornithdae). All three groups have been shown experimentally to use remote-touch in foraging. Furthermore, recent work has confirmed that all three possess hypertrophy of brain regions associated with processing tactile information from the trigeminal system, especially the Principal Trigeminal Nucleus (PrV). All of the published comparative work on remote-touch probe-foragers has assumed convergent evolution of this sense in response to similar ecological pressures. However, a new study has provided some anatomical evidence for the existence of a similar bill-tip organ in both ostriches and emus – neither of which have a probe-foraging life-style, or enlarged PrV. Here I present data on how wide-spread this organ is among modern birds; compare the anatomy (using museum skeletal material and microCT scans) and histology of sandpiper-type bill-tip organs across species; and discuss the potential origins and ecological importance of this feature.

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Session 3: Vision

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How visual configuration influences behavior: mechanistic and evolutionary implications

Dr Esteban Fernandez-Juricic, Purdue University, USA

Abstract

Visual physiologists make predictions about bird behavior and behavioral ecologists make assumptions about bird vision that are not generally tested. Bridging the gap between these disciplines requires integrating physiological, behavioral and modeling approaches. I will review some recent research that illustrates how visual perception shapes behavior in birds. There are three main take-home messages. First, retinal configuration (variation in cell density across the retina) varies substantially between species with different types of centers of acute vision, which has important implications for visual exploratory behavior (e.g., binocular vs. foveal vision). Second, there are multiple ways to see like a bird, particularly when considering species that detect prey at close vs. far distances. Third, vigilance behavior as an antipredator strategy may be the result of a trade-off between the biomechanical limitations of moving the visual system (head movements) and the retinal configuration. Overall, understanding the role of the sensory system in behavior can enhance our ability to establish the cues (e.g., chromatic, achromatic) that drive different types visual behaviors (vigilance, foraging), test the assumptions of behavioral models, and make more informed predictions about predator-prey interactions, sociality and mate-choice.

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What drives avian vision?

Professor Graham Martin, University of Birmingham, UK

Abstract

A widely held assumption about birds is that the control of flight is the major perceptual challenge which has shaped their visual abilities. This idea is captured by the phrase “a bird is a wing guided by an eye”. This assumption will be reviewed and it will be argued that a bird is essentially “a bill guided by an eye”. It will be argued that the variation found in the characteristics of all main visual field parameters and retinal structures are associated primarily with perceptual challenges that arise from different modes of foraging or from predator detection. It will also be argued that there is evidence for the fine tuning of vision to these tasks which can be considered analogous to the tuning of bill structures for the exploitation of different food sources. The perceptual requirements for the control of locomotion are met within constraints imposed primarily by a balance between the perceptual requirements for the control bill position and for the detection of predators.

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Using camouflage to investigate avian visual perception

Professor Innes Cuthill, University of Bristol, UK

Abstract

Animal camouflage provides some of the most striking examples of the workings of natural selection. While the general benefits of camouflage are obvious, understanding the precise means by which the viewer is fooled represent a challenge. This is because animal camouflage is an adaptation to the eyes and mind of another animal, often with a visual system different from (and sometimes superior to) that of humans. So, just as perceptual psychologists have used illusions to probe the mechanisms by which the human brain reconstructs the 3D world from a 2D retinal projection, so too can biologists use animal defensive coloration to investigate visual perception in other animals. I review the various forms of camouflage from this perspective, illustrated by the recent upsurge of experimental studies of long-held, but largely untested, theories of defensive coloration. With birds often the main predators that must be deceived, insect camouflage in particular allows us a window on avian visual perception.

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Visual illusions in bowerbirds: the importance of a perceptual perspective

Dr Laura Kelley, University of Cambridge, UK

Abstract

Sexual selection studies normally measure signal strengths, but signal components and sensory processing may interact to create misleading or attention-capturing illusions. Visual illusions may be produced by altering object and scene geometry in ways that trick the viewer when seen from a particular direction. Male great bowerbirds (Ptilonorhynchus nuchalis) build and actively maintain stick structures called bowers that are used by females during mate choice. During courtship displays the female stands inside the bower where she has a fixed and limited view of the male’s display. Males exploit this view by constructing forced perspective illusions, and the quality of illusion is a good predictor of mating success. Males also use other geometrical tricks in bower design that are likely to be important in holding the female’s attention.

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Session 4: Taste and olfaction

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Olfactory experience of chicken embryos influences food preferences after hatching

Dr Aline Bertin, INRA 85 Val de Loire, CNRS-UMR 7247, Université de Tours and IFCE, France

Abstract

In ovo or in utero chemosensory learning has been described in a large range of vertebrate and invertebrate species. However, in birds, very little is known about the effects of early exposure to chemical stimuli on the development of behaviours. Here, we show that exposing the eggs of domestic chicks (Gallus gallus domesticus), the major model for avian development, to chemosensory compounds via air consistently alters the feeding activity of chicks. First, we observed that the concentration of a chemosensory stimulus in the environment surrounding an embryo affects whether hatchlings will approach or avoid foods with or without the same olfactory stimulus. Second, we provided evidence that chicken embryos are able to detect and have a chemosensory memory before breathing in the egg, while still being surrounded by amniotic fluid. Finally, we found that chicks exposed in ovo to menhaden oil via the maternal diet preferentially orient their feeding behaviour towards food containing menhaden oil, when confronted with an unfamiliar food. In ovo chemosensory learning may have evolved to prepare offspring for their environment. This suggests a common principle for embryonic chemosensory learning across vertebrate taxa.

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Nutritional chemosensing and nutrient specific appetite in chickens: the taste of amino acids and calcium

Dr Eugeni Roura, The University of Queensland, Australia

Abstract

The advent of the genomic era has allowed a step forward in the identification and characterization of the chemosensory system linked to dietary nutrients in chickens. The nutrient sensing system consists of a network of sensory cells expressing a wide array of nutrient sensors some related to taste perception in the oral cavity. Thus, taste perception in vertebrate species seems to be related to the adaptation to ecological niches, availability of food and nutrient requirements. Birds have lower taste bud numbers than mammals which has been assumed as a proof of lower taste acuity. However, the number of taste buds relative to the bite size offers chickens a potential oral nutrient sensing capacity similar, if not higher, than mammals. The broad consensus related to the lack of taste sensitivity in birds needs to be reconsidered in the light of emerging data. The seminar will focus on the high sensitivity of birds for dietary amino acids and calcium and other nutrient sensory mechanisms. In addition the presence of taste receptors in the chicken hypothalamus suggests that, in birds as in mammals, they may also play an important role in energy homeostasis and the hunger-satiety cycle. Potential practical applications relevant to avian nutrition will be discussed.

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Chemical communication in birds: petrel seabirds’ olfactory make up

Dr Francesco Bonadonna, CEFE/CNRS, France

Abstract

Chemical cues were probably the first cues ever used to communicate and are still ubiquitous among living organisms. Odours are broadly used in individual, sexual and species recognition in vertebrates and may be reliable signals of quality and compatibility. Yet, chemical signals in birds have rarely been investigated. In fact, birds exhibit a wide array of communication mechanisms (eg colours and calls) but rarely display obvious olfactory-driven behaviours. This is probably why, despite three decades of physiological and behavioural studies establishing the existence of avian olfactory functions, chemical communication has been essentially ignored. In spite of the fact that pheromones have never been highlighted in birds, several species produce characteristic scents that may have a social function. For example, odours seem to contribute to the courtship behaviours of ducks and chickens. In crested auklets, a characteristic citrus odour may act as a sexual olfactory ornament broadcasting resistance to ectoparasites. Eventually, it has been shown that zebra finches (a passerine bird with a very small olfactory apparatus) display olfactory driven behaviours.

Procellariiform seabirds, and burrowing petrels in particular, exhibit acute olfactory abilities, and are thus an excellent model to study avian olfaction. Evidence, which relate to many aspects of petrels’ ecology including homing, foraging, recognition, mate choice, and even interspecific competition for nesting sites, provide a comprehensive case study of avian chemical communication. Using chemical analytical and behavioural methods, it has been evidenced that the preen secretions of these birds contain social information including species, sex and identity (ie a chemical ID). Results further show that some of this information is still present on the plumage, and in the airborne volatiles emitted by birds. Recent experiments further demonstrated the existence of two key olfactory behaviours: individual odour recognition, self, and kin-related odour avoidance. Importantly, such mechanisms are known to mediate mate choice and inbreeding avoidance in other vertebrates (ie mice).  Consequently, we hypothesized that olfactory cues participate to “good genes” mate choice in burrowing petrels. Indeed, the life-history of these birds stresses the importance of optimal mate choice. Their lifelong monogamy implies that a sub-optimal mate choice may result in a lowered inclusive fitness. If evolution has shaped a strong relationship between genes, odours and mate choice in these birds, each individual should exhibit a specific odorous signal, a ‘personal olfactory signature’, reflecting also some genetic characteristics. Together, these results, almost 50 years after the first works on avian olfaction, indicate that chemical signals can contribute, as well as colours, calls and songs, to avian social behaviours; a realisation that has important implications for behavioural processes.

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Avian olfaction in the context of global ocean health: Dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators

Professor Gabrielle Nevitt, University of California, Davis, USA

Abstract

Tritrophic mutualisms have been best studied in plant-insect systems. During these interactions, plants release volatiles in response to herbivore damage, which, in turn, facilitates predation on primary consumers or benefits the primary producer by providing nutrients. Here, we explore a similar interaction in the Southern Ocean food web, where soluble iron limits primary productivity. Dimethyl sulfide (DMS) has been studied in the context of global climate regulation and is an established foraging cue for marine top predators. We present evidence that procellariiform seabird species that use DMS as a foraging cue selectively forage on phytoplankton grazers. Their contribution of beneficial iron recycled to marine phytoplankton via excretion suggests that DMS mediates a link between marine top predators and oceanic primary production. Taken together, our results imply that marine top predators play a critical role in maintaining both ocean health and global climate via this chemically mediated mutualistic interaction with marine phytoplankton.

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Taste perception and its relationships with diet

Dr Gary Beauchamp, Monell Chemical Senses Center, USA

Abstract

Darwin said: “Real taste [in] the mouth, according to my theory must be acquired by certain foods being habitual – [and] hence become hereditary;” As implied, taste provides dramatic examples of coordination between sensory function and diet selection. We have focused on mammals and particularly on the order Carnivora which includes species with a wide range of dietary niches, as is the case for birds, ranging from entirely meat eating (e.g. cats) to monophageous herbivores (e.g. giant pandas). We found a wide-spread, independent loss of functional sweet taste receptors among obligate carnivores probably due to relaxation of selective pressures. Giant pandas, animals that essentially consume a single plant low in simple sugars, have fully functional sweet taste perception. However, genetic evidence suggests they have lost amino acid (“umami”) taste perception. More broadly, many mammalian species that have returned to the sea (e.g. sea lions, dolphins, whales) have lost function for several, perhaps all, taste qualities. These data dramatically illustrate taste plasticity and how it is adapted to diet. In my presentation I will first discuss these mammalian results and then consider how some of the lessons we have learned with mammals may relate to studies of bird taste perception.

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Bitter-bugs: toxin perception and learning

Dr Hannah Rowland, University of Cambridge, UK

Abstract

Many birds consume plants and animals that contain defensive toxins, venoms and stings, urticating hairs, phenolics, and antinutrient factors such as tannins and saponin. Humans report these compounds as tasting intensely bitter and strongly avoid them in preference tests. Solutions that are rated as bitter by humans (e.g., quinine sulfate) also result in rejection by birds. Birds respond to these diverse bitter chemicals with specific rejection responses, which include beak wiping and head shaking, vomiting, and taste-rejection behavior, where birds attack and release prey on the basis of defense chemicals.

These behavioral responses to bitter chemicals are consistent with bioinformatics surveys and direct sequencing, which have shown that turkeys have one bitter taste (Tas2r) gene; emus have two, and chickens have three. These repertoires are low compared with the functional repertoire of Tas2r genes in other sequenced vertebrate genomes, which ranges from 4 in the platypus to 36 in rats, up to 64 in frogs. The range between birds and other species may suggest a reduced ability to detect and discriminate between bitter substances, or fine-tuning of the receptors to the birds’ feeding ecology (specialization), or broad tuning of the receptors allowing many taste chemicals to be perceived by fewer receptors.

I will discuss how birds detect bitter substances, learn about the consequences of ingestion, and discuss if bitter taste is related to diet choice.

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Evolution of sweet taste perception in a nectar-feeding bird

Maude Baldwin, Harvard University, USA

Abstract

Sensory systems are powerful systems for understanding molecular mechanisms underlying phenotypic adaptation: they define an animal's capacity for perception and can evolve to detect different stimuli when species diverge and encounter new selective pressures. In mammals, sweet taste perception is mediated by a G protein-coupled receptor complex; however, the gene encoding one subunit of the mammalian sweet receptor (T1R2) has not been detected in any bird genome, suggesting loss in the avian common ancestor. Nevertheless, many nectar-feeding birds, such as hummingbirds, lorikeets, and honeyeaters display high behavioral affinity for sugars found in nectar. To understand the molecular basis of sugar sensing in hummingbirds, we cloned members of the T1R taste receptor gene family from oral tissue of hummingbirds, swifts, and chickens. Receptor expression studies revealed that the ancestral umami receptor (T1R1-T1R3 heterodimer) was re-purposed in hummingbirds, but not in swifts, their closest relatives, to function as a carbohydrate receptor. Behavioral choice tests and high-speed videography in wild and captive hummingbird populations indicated sweet taste preferences that correlated with in vitro functional studies. This change in taste receptor function may have been one of many key adaptations enabling hummingbirds to detect and utilize nectar, facilitating the radiation of hummingbird species.

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Session 5: Olfactory navigation and geomagnetic sense

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Olfactory navigation in birds: from homing pigeons to wild species

Dr Anna Gagliardo, University of Pisa, Italy

Abstract

Forty years ago Papi and colleagues observed that anosmic pigeons fail to find their way home when released from unfamiliar locations. They explained the dramatic impact on homing by developing the olfactory navigation hypothesis. Pigeons at the home loft learn to associate different odour profiles with the wind direction they arrive from. Once at a release site, they determine the direction of displacement on the basis of the odours perceived locally, and based on that information, compute a homeward bearing. Although forty years of experiments show the specific role of olfaction in pigeon navigation, the question of whether olfactory navigation might be applicable to wild species remains unanswered. Some older research hinted at an important role of olfactory cues for the navigation of nesting swifts and starlings, who displayed homing impairments when made anosmic. More recently, new satellite technologies has allowed us to track wild birds subjected to olfactory manipulation after displacement from their breeding site or from their migratory route. The observed behaviour of displaced birds is consistent with a fundamental role of atmospheric odours and olfaction for navigation in wild birds.

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The magnetic senses of birds: neurobiological evidence and sensitivity to anthropogenic electromagnetic noise

Professor Henrik Mouritsen, Carl-von-Ossietzky Universität Oldenburg, Germany

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The magnetic compass of birds

Professor Roswita Wiltschko, J.W.Goethe-Univeristät Frankfurt am Main, Germany

Abstract

Birds are able to move fast over considerable distances – this requires efficient navigational mechanisms, where their magnetic compass plays a crucial role. Behavioral experiments revealed some unusual characteristics of this compass: (1) it is an ‘inclination compass’, ignoring the polarity of the magnetic field, being based on the axial course of the field lines, (2) it works spontaneously only in a narrow intensity window, but can adapt to other intensities and (3) it requires short-wavelength light from UV to green. The Radical Pair-Model, proposing that the avian magnetic compass is based on spin chemical processes sensitive to the magnetic field, is supported by experimental evidence. The blue-light sensitive photo-pigment cryptochrome has been suggested as receptor molecule. A form of cryptochrome, Cry1a, has been found in the eyes of robins and chickens, where it is located in the retina at the disks of the outer segments of the UV/V-cones. The magnetic compass interacts with the celestial compass mechanisms, forming one integrated system. It is used to locate learned directions within in the home range, in homing to locate courses determined by navigational processes and in migratory orientation, where it serves as a reference for the innate directional information.

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When senses take flight: the evolution, development, mechanisms and function of avian senses Kavli Royal Society Centre, Chicheley Hall Newport Pagnell Buckinghamshire MK16 9JJ