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
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.
Nutritional chemosensing and nutrient specific appetite in chickens: the taste of amino acids and calcium
Dr Eugeni Roura, The University of Queensland, Australia
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.
Chemical communication in birds: petrel seabirds’ olfactory make up
Dr Francesco Bonadonna, CEFE/CNRS, France
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.
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
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.
Taste perception and its relationships with diet
Dr Gary Beauchamp, Monell Chemical Senses Center, USA
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.
Bitter-bugs: toxin perception and learning
Dr Hannah Rowland, University of Cambridge, UK
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.
Evolution of sweet taste perception in a nectar-feeding bird
Maude Baldwin, Harvard University, USA
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.