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Nutrient sensing, taste and feed intake in avian species

Published online by Cambridge University Press:  11 June 2018

Shahram Niknafs  and
Eugeni Roura
Shahram Niknafs
Affiliation:
Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD 4072, Australia
Eugeni Roura*
Affiliation:
Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD 4072, Australia
*
*Corresponding author: Associate Professor Eugeni Roura, fax +61 7 3365 1188, email e.roura@uq.edu.au
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Abstract

The anatomical structure and function of beaks, bills and tongue together with the mechanics of deglutition in birds have contributed to the development of a taste system denuded of macrostructures visible to the human naked eye. Studies in chickens and other birds have revealed that the avian taste system consists of taste buds not clustered in papillae and located mainly (60 %) in the upper palate hidden in the crevasses of the salivary ducts. That explains the long delay in the understanding of the avian taste system. However, recent studies reported 767 taste buds in the oral cavity of the chicken. Chickens appear to have an acute sense of taste allowing for the discrimination of dietary amino acids, fatty acids, sugars, quinine, Ca and salt among others. However, chickens and other birds have small repertoires of bitter taste receptors (T2R) and are missing the T1R2 (related to sweet taste in mammals). Thus, T1R2-independent mechanisms of glucose sensing might be particularly relevant in chickens. The chicken umami receptor (T1R1/T1R3) responds to amino acids such as alanine and serine (known to stimulate the umami receptor in rodents and fish). Recently, the avian nutrient chemosensory system has been found in the gastrointestinal tract and hypothalamus related to the enteroendocrine system which mediates the gut–brain dialogue relevant to the control of feed intake. Overall, the understanding of the avian taste system provides novel and robust tools to improve avian nutrition.

Keywords

ChickensFeed intakeGrowthNutrient sensingRegulatory genesTaste
Type
Review Article
Information
Nutrition Research Reviews , Volume 31 , Issue 2 , December 2018 , pp. 256 - 266
Copyright
© The Authors 2018 

Introduction

Optimising the consumption of balanced diets is critical to the welfare, development, health and productivity of animals, particularly when raised or kept in captivity. In non-forced animal feeding scenarios, dietary choices are a result of the preference for available feeds or ingredients and the motivation to eat which, in turn, reflects the innate drive of preserving or achieving nutritional homeostasis( Reference Roura and Navarro 1 ). The maintenance of the nutritional balance (or homeostasis) is a dynamic process that implies the existence of a network of nutrient sensors covering critical physiological functions. Thus, the term nutritional chemosensing was coined to describe studies on the sensing of nutrients in biological systems including the molecular mechanisms related to changes in genomic, metabolic, physiological and behavioural parameters( Reference Roura, Koopmans and Lallès 2 ). In mammals and birds, dietary nutrients are perceived in the oral cavity mainly through the taste system which has evolved to differentiate nutrients from toxins( Reference Glendinning 3 , Reference Herness and Gilbertson 4 ). Taste sensory cells form the taste buds in the oral cavity and translate nutrient sensing into neuronal signals (through cranial nerves) to the primary gustatory cortex of the brain. Chickens seem to have developed an acute sense of taste which enables them to distinguish at least five of the six primary tastes including fatty, umami, salty, sour and bitter (it is noted that the acceptance of fatty acid sensing as a differential taste type is still controversial particularly in chickens)( Reference El Boushy and van der Poel 5 , Reference Roura, Baldwin and Klasing 6 ). In addition, the existence (or lack) of sweet taste linked to carbohydrate sensing in chickens remains unclear and will be further discussed in the ‘Nutritional chemosensing in chickens: the molecular inside to taste’ section( Reference Roura, Baldwin and Klasing 6 – Reference Higashida, Kawabata and Kawabata 8 ).

Similar to mammals, birds integrate gustatory perception with post-ingestive events, particularly originating in the gastrointestinal system, to control feed intake( Reference Werner and Provenza 9 ). In this context, extra-oral sensing of nutrients has been recently attracting a lot of attention, collating the importance of nutrient receptors (including taste receptors) and related downstream pathways on the control of feed intake( Reference Roura, Koopmans and Lallès 2 , Reference Roura, Baldwin and Klasing 6 , Reference Buchan 10 – Reference Foster, Roura and Thomas 14 ). The existence of this network of nutrient sensors outside the oral cavity implies that behavioural studies assessing the effect of taste in the control of feed intake need to be assessed with caution since pre- and post-ingestive nutrient sensing can be easily confounded. In the following sections, the present review will outline the main scientific findings covering oral and extra-oral nutrient sensing (but not always discerning which one of the two or both are the main drivers) relevant to chicken diet selection, feeding behaviour, oral/tongue anatomy, and nutritional genetics and genomics organised in a chronological order (Table 1).

Table 1 Chronological accountancy of the main peer-reviewed publications on taste and nutrient sensing and feed intake in poultry grouped by scientific discipline

TR, taste receptor; AA, amino acid; MCT, medium-chain TAG; T2R, taste receptor family 2; T1R, taste receptor family 1; GLP, glucagon-like peptide; GPR, G-protein receptor; CD36, cluster of differentiation 36; GIT, gastrointestinal; CaSR, Ca sensing receptor.

* These reports are in German and have been reviewed by Berkhoudt (1992)( Reference Berkhoudt 20 ).

The avian taste and nutrient-sensing system: research highlights

Table 1 represents a chronogram of the avian taste and feed intake research featuring the highlights of what has been published to date. The first traceable studies on the avian taste system refer back to more than 130 years ago and consisted of an anatomical examination of the avian oral cavity by Merkel (1880)( Reference Merkel 15 ) who failed to find taste buds. Botezat and Bath( Reference Botezat 16 – Reference Botezat 19 ) were the first to report taste buds on palatal and mandibular areas of the oral cavity in several bird species. All these early reports were published in German and were reviewed in a book chapter by Berkhoudt (1992)( Reference Berkhoudt 20 ).

Chicken taste buds were shown to have common morphological and anatomical features together with some cellular and developmental differences compared with other vertebrates( Reference Gentle 21 – Reference Ganchrow, Ganchrow and Royer 23 ). Based on a few bird species studied to date (i.e. chicken, turkey, pigeon, etc.), it seems that taste buds are located mainly in the posterior tongue and pharynx as well as in the upper palate and base of the tongue, but not in the highly keratinised anterior and central tongue as is the case in mammals( Reference Roura, Baldwin and Klasing 6 , Reference Kitchell, Ström and Zotterman 24 ). The most recent studies using molecular biology techniques showed that broiler chickens had 507 taste buds in the palate and 260 in the base of the oral cavity( Reference Rajapaksha, Wang and Venkatesan 25 ). Ganchrow & Ganchrow (1985)( Reference Ganchrow and Ganchrow 26 ) reported only a total of 316 taste buds in chickens, a number which has been used as a reference until recently as it appears to have underestimated the density of the avian taste sensory network. The palate of chickens has the highest number of taste buds compared with the other regions of the oral cavity, while broiler chickens have higher numbers than the egg-laying breeds( Reference Rajapaksha, Wang and Venkatesan 25 , Reference Kudo, Nishimura and Tabata 27 , Reference Kudo, Shiraishi and Nishimura 28 ). Finally on anatomic structures, the chorda tympani nerve has been identified to be involved in chicken taste bud innervation( Reference Gentle 29 , Reference Ganchrow, Ganchrow and Oppenheimer 30 ).

The taste sense of the chicken plays a key role in the initial choice of feed and the level of feed consumption and growth( Reference Kare and Pick 31 – Reference Barbato, Siegel and Cherry 33 ). Skelhorn & Rowe (2010)( Reference Skelhorn and Rowe 34 ) showed that bitter taste-driven dietary selection in European starlings was essential in maximising nutrient while minimise toxin ingestion. Taste perception has been frequently targeted to try to improve feed intake, growth performance, mortality and feed conversion ratio in poultry( Reference El Boushy and van der Poel 5 , Reference McNaughton, Deaton and Reece 35 – Reference Mabayo, Okumura and Hirao 37 ) (Table 1). Additionally, taste-driven behaviours have also been studied to prevent economic losses in agricultural production due to birds damaging cereal and fruit production( Reference Mason, Adams and Clark 38 , Reference Clark, Hagelin and Werner 39 ). For example, fruits have been successfully protected against bird damage by increased sucrose content or by using coniferyl benzoate, a compound known to be bitter to avian species( Reference Brugger and Nelms 40 – Reference Brugger, Nol and Phillips 42 ). Furthermore, compounds known to be bitter to humans (quinine, garlic oil, almond oil, clove oil, magnesium chloride) have been successfully used to reduce feather pecking incidence in laying hens( Reference Harlander Matauschek, Beck and Rodenburg 43 – Reference Harlander-Matauschek and Rodenburg 45 ). A decreased feed intake was also observed by adding jojoba oilseed to the diet, presumably caused by bitter taste aversion( Reference Vermaut, De Coninck and Flo 46 ).

On the other hand, water deprivation of 2–6 h decreased the averseness to a quinine solution in chickens which was related to changes in taste sensitivity due to dry mouth( Reference Gentle 47 , Reference Gentle 48 ). It is tempting to speculate that under water scarcity (drought) the abundance of foods available may decrease and birds may need to be more tolerant to low-quality grains and fruits.

Other main taste-related events found in chicken literature include amino acid (AA) sensing. Initial work showing AA sensing in chickens studied AA preferences of limiting essential AA. A maize–soyabean meal diet supplemented with 4 % lysine was preferred over the same supplementation of methionine, threonine and arginine( Reference Edmonds and Baker 49 ). Similarly, broiler chicks were found to prefer a balanced diet containing synthetic AA compared with a similar diet deficient in lysine, methionine and tryptophan( Reference Picard, Uzu and Dunnington 50 ). In addition, glutamic acid (l-Glu) received considerable attention as well, potentially related to umami taste. For example, l-Glu increased feed intake and growth in broiler chickens fed a low-crude protein diet( Reference Moran and Stilborn 51 ). However, excess dietary l-Glu may decrease appetite( Reference Kerr and Kidd 52 ). Recently, Niknafs et al. (2017)( Reference Niknafs, Kim and Roura 53 ) reported that AA preference was related to the rate of growth in broiler chickens: slow-growing broilers consumed 64 % more of a non-essential AA (alanine/aspartic acid/asparagine)-supplemented diet compared with fast-growing broilers( Reference Niknafs, Kim and Roura 53 ). In addition, broiler chickens lowered their feed intake when the diet was supplemented with synthetic AA compared with a diet containing soya protein isolate( Reference Siegert 54 ). The authors speculated that taste played a major role explaining this behaviour but post-ingestive effects were not properly considered.

Some studied avian species have shown preference for Ca-rich feed ingredients such as bones, shells and grit, which are rich in Ca( Reference Reynolds and Perrins 55 ). Both broiler and laying chickens have a specific appetite for Ca, and they can meet their Ca requirement by consuming from a separate source in a choice feeding scenario( Reference Leeson and Summers 56 – Reference Wilkinson, Selle and Bedford 58 ). Such specific appetite was also reported to be associated with the level of dietary non-phytate P( Reference Wilkinson, Bradbury and Bedford 59 ). Taste cues may play a key role in recognising Ca-deficient and -supplemented diets by chickens, and it has been reported that Ca-deficient chicks rejected calcium lactate solution due to aversive taste( Reference Wood‐Gush and Kare 60 , Reference Hughes and Wood-Gush 61 ).

Finally, fat perception and consumption may have strong implications in poultry nutrition. Chickens were shown to increase feed intake of a high-added fat compared with a low-fat isoenergetic diet( Reference Roura, Baldwin and Klasing 6 , Reference Klasing 62 ). In addition, chickens showed a higher intake of a long-chain TAG compared with a medium-chain TAG-supplemented diet. Interestingly, such preference was inhibited after tongue paralysis, suggesting the role of oral gustation in dietary fat preferences( Reference Furuse, Mabayo and Okumura 36 ). Similarly, chickens were also reported to prefer oleic and linoleic acids from a maize oil-rich diet following a double-choice paradigm( Reference Sawamura, Kawabata and Kawabata 63 ). However, these results need to be interpreted with caution because of the long-term assay (7 h) together with the use of mineral oil (potentially toxic at high inclusion levels) in the reference diet.

In summary, the chronological review of the taste-related anatomy and feeding behaviour in chickens shows a long delay (50 years) in the discovery of the taste system (taste buds) in birds compared with mammals, probably related to the lack of taste papillae and to the initial focus on the bird tongue which is mostly deprived of taste-related anatomical structures( Reference Berkhoudt 20 ). However, in recent years research highlighting the association between taste-related feeding behaviour and cellular mechanisms in chicken has been abundant( Reference Cheled-Shoval, Behrens and Korb 64 – Reference Dey, Kawabata and Kawabata 66 ). On the other hand, the advent of the sequencing of the red jungle fowl genome in 2004 introduced a new area, genetics and genomics, which has significantly changed the profile of research on avian chemosensory science ever since( Reference Hillier, Miller and Birney 67 ). Thus, novel research tools have been applied to chicken chemosensory research including RT-PCR, functional heterologous expression assays, immunohistochemistry combined with scanning electron microscopy, and three-dimensional image reconstruction, which has allowed improving our understanding of the molecular mechanisms of chicken taste.

Nutritional chemosensing in chickens: the molecular inside to taste

The availability of the chicken genome as a model opened up the research field of avian taste and nutrient sensing to the molecular underpinnings (Table 1). Lagerström et al. ( Reference Lagerström, Hellström and Gloriam 68 ) identified 557 G protein–coupled receptor (GPCR) genes forming part of the chicken genome of which more than forty might be directly related to taste and nutrient sensing, as summarised in Table 2 ( Reference Roura, Baldwin and Klasing 6 , Reference Lagerström, Hellström and Gloriam 68 – Reference Schioth 70 ). Some of the early works involved the downstream taste cellular signalling using vimentin and α-gustducin as molecular biomarkers for labelling and visualising chicken taste sensory cells( Reference Rajapaksha, Wang and Venkatesan 25 , Reference Kudo, Wakamatsu and Nishimura 71 – Reference Witt, Reutter and Ganchrow 73 ). Studies on the early development of taste buds showed profound differences between human subjects and chickens. Human taste bud cells originate from epithelial cells while in chickens they are of mesenchymal origin( Reference Witt, Reutter and Ganchrow 73 ). Interestingly, based on their unique migratory properties, mesenchymal cells play a fundamental role in embryonic development. Thus, it is tempting to speculate that taste sensory cells in chickens have the potential to spread, reaching a wider distribution in body tissues than in humans or mice (see the ‘Extra-oral taste receptors mediating feed intake in poultry’ section of the present review).

Table 2 Chicken nutrient-sensing genes (G protein-coupled receptors; GPR) identified based on homology with mammalian genes and mRNA expression data

T1R, taste receptor family 1; SGLT1, sodium–glucose cotransporter 1; CaSR, Ca sensing receptor; mGluR, metabotropic glutamate receptor; eNaC, epithelial sodium channel; PKD1L3, (protein coding), polycystin 1 like 3; PKD2L1, (protein coding), polycystin 2 like 1; HCN, hyperpolarisation-activated cyclic nucleotide-gated.

* These receptors have been defined as membrane channels and do not belong to the GPCR super-family.

Generally speaking, bird species that have been studied so far have shown a lower number of bitter taste receptors (T2R) than some other vertebrates studied to date( Reference Roura, Baldwin and Klasing 6 ). Chickens have only three bitter taste receptor genes: T2R1, T2R2 and T2R7( Reference Cheled-Shoval, Behrens and Korb 64 , Reference Lagerström, Hellström and Gloriam 68 , Reference Behrens, Korsching and Meyerhof 74 ). Using heterologous cell expression systems and in vivo double-choice trials, specific agonist and antagonist ligands of the three chicken genes have been confirmed( Reference Cheled-Shoval, Behrens and Korb 64 , Reference Dey, Kawabata and Kawabata 66 , Reference Behrens, Korsching and Meyerhof 74 ). In particular, caffeine was shown to stimulate the T2R2 chicken receptor and elicit a negative preference in chickens at 10 mm or higher, but potential confounding stimulation of other receptors was not assessed( Reference Lagerström, Hellström and Gloriam 68 ). In addition, the results reported by Dey et al. ( Reference Dey, Kawabata and Kawabata 66 ) showing no preferences for 3 mm-caffeine suggest that the affinity for the chicken T2R2 may be relatively low or that the gene may not be fully functional in chickens. Moreover, there is a wide variation in the number of bitter taste receptors (T2R) between avian species, varying from one reported for domestic pigeons to eighteen for the white-throated sparrow( Reference Davis, Lowman and Thomas 75 , Reference Wang and Zhao 76 ). Such diversity in the T2R repertoire in birds has been related to reflect species differences in nutritional needs and the adaptation to ecological niches( Reference Dong, Jones and Zhang 77 , Reference Li and Zhang 78 ). Despite having only three bitter taste receptors in chickens, there is no evidence of an evolutionary contraction of the gene pool( Reference Dong, Jones and Zhang 77 ). In addition, the relatively low number of taste receptors in chickens did not result in a decreased functionality and relevance of bitter taste since these receptors were shown to be widely tuned( Reference Behrens, Korsching and Meyerhof 74 ). Hirose et al. (2015)( Reference Hirose, Kawabata and Kawabata 65 ) showed a direct association between behavioural responses to bitter tastants and the level of activity of the T2R1. Furthermore, before and/or after hatching exposure to bitterness altered the expression of bitter taste receptor genes in the palate of chickens, leading to decreased feed intake( Reference Cheled-Shoval, Behrens and Meyerhof 79 ).

In vitro studies using cell reporter systems expressing chicken T1R1 and T1R3 receptors confirmed that these receptors respond to umami agonists to a similar extent seen in mice( Reference Baldwin, Toda and Nakagita 7 , Reference Kudo, Kawabata and Nomura 80 ). In contrast, chickens lack T1R2, one of the dimers of the sweet taste receptor gene in mammals( Reference Lagerström, Hellström and Gloriam 68 , Reference Shi and Zhang 81 ). The latter seems to explain the lack of response to sweet tastants in several studies conducted in chickens( Reference Ganchrow, Steiner and Bartana 82 , Reference Halpern 83 ). However, preference for carbohydrates including sugar in poultry has been reported in many studies( Reference Brindley 84 – Reference Kare and Medway 87 ). In the mouse, a T1R2-independent pathway involving oligosaccharidases and the glucose transporter SGLT-1 in taste buds has been recently described( Reference Sukumaran, Yee and Iwata 88 ). A similar mechanism may be hypothesised in chickens( Reference Higashida, Kawabata and Kawabata 8 ). Alternatively, it has been shown that some birds, such as the hummingbird, have adapted the umami receptor T1R1 to mainly perceive carbohydrates (and presumably sweetness)( Reference Baldwin, Toda and Nakagita 7 ).

Table 2 summarises the array of mammalian nutrient sensors found to be expressed in the oral cavity of chickens (T1R1/3, Ca sensing receptor (CaSR), G-protein receptor (GPR) 120, T2R and cluster of differentiation 36 (CD36)). For example, the taste system seems to play a role in the regulation of Ca intake which is probably mediated by the CaSR and T1R3 in several mammals and chickens( Reference Conigrave and Brown 89 – Reference Tordoff, Shao and Alarcón 92 ). Finally, the long-chain fatty acid receptor GPR120 was found expressed in the palate of chickens which is speculated to be associated to oleic and linoleic acid sensing( Reference Sawamura, Kawabata and Kawabata 63 ). In addition, the fatty acid transporter CD36 has also been reported to sense fatty acids in the oral cavity of chickens( Reference Kawabata, Mizobuchi and Kawabata 93 ). However, to date, taste perception of fatty acids in chickens has not been clearly demonstrated and requires further investigations.

Overall, the nutrient receptor gene repertoire in the chicken highly resembles those of the human and mouse with a few important exceptions such as the low number of T2R and the absence of the T1R2. However, the widely tuned nature of the T2R genes advocates for a fully functional sense in the chicken to a similar relevance than in some mammals. In contrast, the lack of the sweet receptor in the chicken may indicate that T1R2-independent pathways exist to monitor simple carbohydrates such as glucose. Chemosensory science in avian species is only an emerging discipline and is lagging behind the knowledge in mammals. Given their implication in feed intake and nutrient appetite, there is an increasing need for studying and understanding the regulatory network and co-expression analysis of nutrient sensors. Finally, since avian taste sensory cells are of mesenchymal origin which, in turn, is related to a higher capacity to migrate during development than epithelial cells (the origin of mammalian taste sensory cells) it would be interesting to study if the avian sensory cells are more abundant than mammalian sensory cells outside the oral cavity.

Extra-oral taste receptors mediating feed intake in poultry

The expression of taste receptors and nutrient sensors in extra-oral tissues, such as the gastrointestinal tract (GIT), has been found to play key roles in food intake and appetite control. They have been involved in responses to the luminal content involving the secretion of hunger–satiety hormones such as glucagon-like peptide (GLP)-1, ghrelin and cholecystokinin (CCK)( Reference Behrens and Meyerhof 13 , Reference San Gabriel 94 – Reference Janssen and Depoortere 96 ). Chickens under feed restriction had higher numbers of GLP-1-containing intestinal L cells compared with unrestricted birds( Reference Monir, Hiramatsu and Yamasaki 97 ). Similarly, a lower number of GLP-1-immunoreactive cells were found in chickens fed a methionine/lysine-supplemented diet compared with the control non-supplemented group( Reference Nishimura, Hiramatsu and Watanabe 98 ), whereas in ovo injection of arginine increased the secretion of jejunal ghrelin and GLP-2( Reference Gao, Zhao and Zhang 99 ). In addition, dietary supplementation with medium-chain TAG increased CCK secretion and decreased feed intake in chickens( Reference Furuse, Mabayo and Choi 100 ). Taste receptors and nutrient sensors expressed in the GIT have been related to sensing nutrients in luminal contents, resulting in the secretion of gut peptides mediating food appetite in some mammalian species. The main outcomes have been recently reviewed( Reference San Gabriel 94 – Reference Janssen and Depoortere 96 , Reference Breer, Eberle and Frick 101 – Reference Wauson, Lorente-Rodríguez and Cobb 103 ).

In an early work in chickens, Byerly et al. (2010)( Reference Byerly, Simon and Cogburn 104 ) demonstrated the presence of the umami taste receptor (T1R1) in the hypothalamus. The chicken T1R1 was expressed at higher levels in fat compared with lean broiler lines. Cheled-Shoval et al. (2014( Reference Cheled-Shoval, Behrens and Meyerhof 79 ) and 2015( Reference Cheled-Shoval, Druyan and Uni 105 )) reported the expression of both chicken T1R and T2R subfamilies in the GIT. The presence of umami taste receptors in the chicken’s GIT was also cofirmed by Yoshida et al. (2015)( Reference Yoshida, Kawabata and Kawabata 106 ). In addition, the expression of fatty acid receptors GPR43, GPR120 and CD36 were also reported in the chicken’s intestine( Reference Kawabata, Mizobuchi and Kawabata 93 , Reference Meslin, Desert and Callebaut 107 ). Finally, α-gustducin and α-transducin cells have also been reported in the chicken’s GIT( Reference Mazzoni, Bombardi and Vallorani 108 ).

Unpublished results from our group (S Niknafs and E Roura, unpublished results) targeted extra-oral AA sensors (T1R1/T1R3, CaSR, GPR92 and GPR139) and showed that they are significantly expressed in the chicken’s GIT, being a higher expression of CaSR and GPR139 associated with higher feed intake and growth rate in broiler chickens. In addition, intestinal nutrient transporters have also been reported to sense nutrients( Reference Hyde, Taylor and Hundal 109 ). In poultry, transporters for peptides, AA, glucose and fructose have been extensively studied( Reference Awad, Aschenbach and Ghareeb 110 – Reference Zhang, Zhang and Wan 119 ). However, their role as chemosensory mediators has yet to be fully described.

The role of nutrient sensors in the GIT has been unveiled in the mouse, rat and humans but current knowledge in avian species is scarce. The scenario depicted in the Introduction where the anatomy (and perhaps the function) of the chicken taste system is fundamentally different from in some studied mammals may be repeated regarding the role of taste receptors in the GIT. The existence of a network of sensory cells related to the enteroendocrine system underlines the relevance of nutrient sensors in the secretion of gut peptides. However, the hormonal control of appetite related to the gut–brain axis based on gut peptides has been shown to feature major differences between the chicken and mouse. For example, although ghrelin in humans and the mouse is an orexigenic hormone( Reference Vancleef, Van Den Broeck and Thijs 120 ), it has been well documented to be anorexigenic in the chicken( Reference Furuse, Tachibana and Ohgushi 121 – Reference Ocłoń and Pietras 127 ). In contrast, peptide YY (PYY) and GLP-1 have an anorexigenic role in humans and the mouse, whereas in the chicken they seem to stimulate appetite( Reference Richards and Proszkowiec-Weglarz 69 , Reference Monir, Hiramatsu and Yamasaki 97 , Reference Nishimura, Hiramatsu and Watanabe 98 , Reference Kuenzel, Douglass and Davison 128 , Reference Ando, Kawakami and Bungo 129 ). Overall, what has been learned so far on chicken nutritional chemosensing shows an area with potentially profound implications in avian nutrition that needs further investigation, particularly regarding gut mechanisms and their functionality related to gut peptides and the hunger–satiety cycle.

Conclusion

The present review of the avian taste-related literature dismounts the long-sustained dogma that birds have a minor level of taste sensing. Chickens, and the other avian species studied so far, seem to taste different (not less) from mammalian species. The anatomical features reveal an evolution of the taste system in harmony with an oral cavity and deglutition mechanics requiring a slim long keratinised tongue incompatible with a sensing system on it (such as in mammals) which, in turn, found its place in the upper palate. The essential role of taste as the nutrient-sensing machinery in chickens seems to be close to the mammalian system except for carbohydrates (sweet in mammals) since the T1R2 gene was lost in evolution. Similarly, compared with mammals and most amphibians, chickens and the other avian species studied to date appear to have a smaller bitter taste receptor (T2R) repertoire. However, the low number of T2R genes may be compensated by their nature, tuned to sense a wide array of chemicals. Thus, AA and fatty acid sensing (and possibly Ca) seems to take the lead in nutrient appetites in chickens. However, the relevance of carbohydrates (i.e. glucose) should not be discarded in birds since chickens show an active T1R2-independent pathway and the umami gene T1R1 in some mammals responds to sugars in hummingbirds. The change in molecular roles from mammals to some bird species like the hummingbird does not seem to be an isolated occurrence. On the contrary, gut peptides with appetite-enhancing properties in well-studied mammals like mice may suppress the appetite of birds and the other way around such as in the case of ghrelin, PYY and GLP-1. However, there is a lack of data regarding the regulatory genes and pathways orchestrating the control of feed intake in chickens. Studying the molecular and regulatory networks involved in nutrient-sensing mechanisms across the GIT and the central nervous system can partially explain the variation in feed intake within strains with the same genetics. In addition, little is known about genetic polymorphisms in taste receptors, nutrient sensors and their downstream effects that may affect feed intake regulation mechanisms in chickens, warranting further investigation.

Acknowledgements

S. N. wrote the paper. E. R. designed, edited and revised the paper.

There are no conflicts of interest.

References

1. Roura, E & Navarro, M (2018) Physiological and metabolic control of diet selection. Anim Prod Sci 58, 613–626.Google Scholar
2. Roura, E, Koopmans, S-J, Lallès, J-P, et al. (2016) Critical review evaluating the pig as a model for human nutritional physiology. Nutr Res Rev 29, 60–90.Google Scholar
3. Glendinning, JI (1994) Is the bitter rejection response always adaptive? Physiol Behav 56, 1217–1227.Google Scholar
4. Herness, MS & Gilbertson, TA (1999) Cellular mechanisms of taste transduction. Annu Rev Physiol 61, 873–900.Google Scholar
5. El Boushy, ARY & van der Poel, AFB (editors) (2000) Palatability and feed intake regulations. In Handbook of Poultry Feed from Waste: Processing and Use, pp. 348–397. Dordrecht: Springer Netherlands.Google Scholar
6. Roura, E, Baldwin, MW & Klasing, KC (2013) The avian taste system: potential implications in poultry nutrition. Anim Feed Sci Technol 180, 1–9.Google Scholar
7. Baldwin, MW, Toda, Y, Nakagita, T, et al. (2014) Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345, 929–933.Google Scholar
8. Higashida, M, Kawabata, Y, Kawabata, F, et al. (2016) Preferences for sugars and T1r2-independent sweet taste molecules in chickens. Abstract from 17th International Symposium on Olfaction and Taste (ISOT2016) PACIFICO Yokohama, Yokohama, Japan, June 5–9, 2016 President: Yuzo Nimoniya. Chem Senses 41, e274–e275.Google Scholar
9. Werner, SJ & Provenza, FD (2011) Reconciling sensory cues and varied consequences of avian repellents. Physiol Behav 102, 158–163.Google Scholar
10. Buchan, AMJ (1999) III. Endocrine cell recognition of luminal nutrients. Am J Physiol Gastrointest Liver Physiol 277, G1103–G1107.Google Scholar
11. Furness, JB, Kunze, WAA & Clerc, N (1999) II. The intestine as a sensory organ: neural, endocrine, and immune responses. Am J Physiol Gastrointest Liver Physiol 277, G922–G928.Google Scholar
12. Sternini, C, Anselmi, L & Rozengurt, E (2008) Enteroendocrine cells: a site of ‘taste’ in gastrointestinal chemosensing. Curr Opin Endocrinol Diabetes Obes 15, 73–78.Google Scholar
13. Behrens, M & Meyerhof, W (2011) Gustatory and extragustatory functions of mammalian taste receptors. Physiol Behav 105, 4–13.Google Scholar
14. Foster, SR, Roura, E & Thomas, WG (2014) Extrasensory perception: odorant and taste receptors beyond the nose and mouth. Pharmacol Ther 142, 41–61.Google Scholar
15. Merkel, F (1880) Über die Endigungen der sensiblen Nerven in der Haut der Wirbeltiere (About the endings of sensitive nerves in the skin of vertebrates). Leipzig: Fues’s Verlag.Google Scholar
16. Botezat, E (1904) Geschmacksorgane und andere nervose Endapparate im Schnabel der Vogel (vorlaufige Mitteilung) (Taste organs and other nerve endings in the beak of birds (preliminary communication)). Biol Zbl 24, 722–736.Google Scholar
17. Bath, W (1906) Die Geschmacksorgane der Vogel und Krokodile (Taste organs in birds and crocodiles). Arch Biontologie 1, 5–47.Google Scholar
18. Botezat, E (1906) Die Nervenendapparate in den Mundteilen der Vogel und die einheitliche Endigungsweise der peripheren Nerven bei den Wirbeltieren (Nerve endings in mouth parts of birds and uniformity of termination types of peripheral nerves in vertebrates). Z Wiss Zool 84, 205–360.Google Scholar
19. Botezat, E (1910) Morphologie, Physiologie, und physiogenetische Bedeutung der Geschmacksorgane der Vogel (Morphology, physiology, and physiogenetic importance of the taste organs in birds). Anat Anz 36, 428–461.Google Scholar
20. Berkhoudt, H (1992) Avian taste buds: topography, structure and function. In Chemical Signals in Vertebrates 6, pp. 15–20 [RL Doty and D Müller-Schwarze, editors]. Boston, MA: Springer US.Google Scholar
21. Gentle, MJ (1975) Gustatory hyposensitivity to quinine hydrochloride following diencephalic lesions in Gallus domesticus . Physiol Behav 14, 265–270.Google Scholar
22. Ganchrow, JR & Ganchrow, D (1987) Taste bud development in chickens (Gallus gallus domesticus). Anat Rec 218, 88–93.Google Scholar
23. Ganchrow, JR, Ganchrow, D, Royer, SM, et al. (1993) Aspects of vertebrate gustatory phylogeny: morphology and turnover of chick taste bud cells. Microsc Res Tech 26, 106–119.Google Scholar
24. Kitchell, RL, Ström, L & Zotterman, Y (1959) Electrophysiological studies of thermal and taste reception in chickens and pigeons. Acta Physiol Scand 46, 133–151.Google Scholar
25. Rajapaksha, P, Wang, Z, Venkatesan, N, et al. (2016) Labeling and analysis of chicken taste buds using molecular markers in oral epithelial sheets. Sci Rep 6, 37247.Google Scholar
26. Ganchrow, D & Ganchrow, JR (1985) Number and distribution of taste buds in the oral cavity of hatchling chicks. Physiol Behav 34, 889–894.Google Scholar
27. Kudo, K-i, Nishimura, S & Tabata, S (2008) Distribution of taste buds in layer-type chickens: scanning electron microscopic observations. Anim Sci J 79, 680–685.Google Scholar
28. Kudo, K-i, Shiraishi, J-i, Nishimura, S, et al. (2010) The number of taste buds is related to bitter taste sensitivity in layer and broiler chickens. Anim Sci J 81, 240–244.Google Scholar
29. Gentle, MJ (1984) Sensory functions of the chorda tympani nerve in the chicken. Experientia 40, 1253–1255.Google Scholar
30. Ganchrow, JR, Ganchrow, D & Oppenheimer, M (1986) Chorda tympani innervation of anterior mandibular taste buds in the chicken (Gallus gallus domesticus). Anat Rec 216, 434–439.Google Scholar
31. Kare, MR & Pick, HL (1960) The influence of the sense of taste on feed and fluid consumption. Poult Sci 39, 697–706.Google Scholar
32. Gentle, MJ (1972) ) Taste preference in the chicken (Gallus domesticus L.). Br Poult Sci 13, 141–155.Google Scholar
33. Barbato, GF, Siegel, PB & Cherry, JA (1982) Genetic analyses of gustation in the fowl. Physiol Behav 29, 29–33.Google Scholar
34. Skelhorn, J & Rowe, C (2010) Birds learn to use distastefulness as a signal of toxicity. Proc R Soc Lond B Biol Sci 277, 1729–1734.Google Scholar
35. McNaughton, JL, Deaton, JW & Reece, FN (1978) Effect of sucrose in the initial drinking water of broiler chicks on mortality and growth. Poult Sci 57, 985–988.Google Scholar
36. Furuse, M, Mabayo, RT & Okumura, J-i (1996) The role of gustation in oil preference in the chicken. Jpn Poult Sci 33, 256–260.Google Scholar
37. Mabayo, RT, Okumura, J-I, Hirao, A, et al. (1996) The role of olfaction in oil preference in the chicken. Physiol Behav 59, 1185–1188.Google Scholar
38. Mason, JR, Adams, MA & Clark, L (1989) Anthranilate repellency to starlings: chemical correlates and sensory perception. J Wildlife Manage 53, 55–64.Google Scholar
39. Clark, L, Hagelin, J & Werner, S (2014) The chemical senses in birds. In Sturkie’s Avian Physiology, 6th ed., pp. 89–111 [[C Scanes, editor]. Boston, MA: Academic Press.Google Scholar
40. Brugger, KE & Nelms, CO (1991) Sucrose avoidance by American robins (Turdus migratorius): implications for control of bird damage in fruit crops. Crop Prot 10, 455–460.Google Scholar
41. Jakubas, WJ, Shah, PS, Mason, JR, et al. (1992) Avian repellency of coniferyl and cinnamyl derivatives. Ecol Appl 2, 147–156.Google Scholar
42. Brugger, KE, Nol, P & Phillips, CI (1993) Sucrose repellency to European starlings: will high-sucrose cultivars deter bird damage to fruit? Ecol Appl 3, 256–261.Google Scholar
43. Harlander Matauschek, A, Beck, P & Rodenburg, TB (2010) Effect of an early bitter taste experience on subsequent feather-pecking behaviour in laying hens. Appl Anim Behav Sci 127, 108–114.Google Scholar
44. Harlander-Matauschek, A, Beck, P & Piepho, H-P (2009) Taste aversion learning to eliminate feather pecking in laying hens, Gallus gallus domesticus . Anim Behav 78, 485–490.Google Scholar
45. Harlander-Matauschek, A & Rodenburg, TB (2011) Applying chemical stimuli on feathers to reduce feather pecking in laying hens. Appl Anim Behav Sci 132, 146–151.Google Scholar
46. Vermaut, S, De Coninck, K, Flo, G, et al. (1997) Effect of deoiled jojoba meal on feed intake in chickens: satiating or taste effect? J Agric Food Chem 45, 3158–3163.Google Scholar
47. Gentle, MJ (1976) Quinine hydrochloride acceptability after water deprivation in Gallus domesticus . Chem Senses 2, 121–128.Google Scholar
48. Gentle, MJ (1985) Sensory involvement in the control of food intake in poultry. Proc Nutr Soc 44, 313–321.Google Scholar
49. Edmonds, MS & Baker, DH (1987) Comparative effects of individual amino acid excesses when added to a corn–soybean meal diet: effects on growth and dietary choice in the chick. J Anim Sci 65, 699–705.Google Scholar
50. Picard, ML, Uzu, G, Dunnington, EA, et al. (1993) Food intake adjustments of chicks: short term reactions to deficiencies in lysine, methionine and tryptophan. Br Poult Sci 34, 737–746.Google Scholar
51. Moran, ET & Stilborn, HL (1996) Effect of glutamic acid on broilers given submarginal crude protein with adequate essential amino acids using feeds high and low in potassium. Poult Sci 75, 120–129.Google Scholar
52. Kerr, BJ & Kidd, MT (1999) Amino acid supplementation of low-protein broiler diets: 1. glutamic acid and indispensable amino acid supplementation. J Appl Poult Res 8, 298–309.Google Scholar
53. Niknafs, S, Kim, JM & Roura, E (2017) Fast and slow-growing broiler chickens show different appetite for limiting and non-essential amino acids. In Proceedings of the 28th Australian Poultty Science Symposium, Sydney, New South Wales, p. 222. http://sydney.edu.au/vetscience/apss/documents/2017/APSS%20Proceedings%202017.pdf (accessed May 2018).Google Scholar
54. Siegert, W (2016) Factors influencing the response of broiler chicken to glycine supplements in low crude protein diets. PhD Thesis, University of Hohenheim.Google Scholar
55. Reynolds, SJ & Perrins, CM (2010) Dietary calcium availability and reproduction in birds. In Current Ornithology vol. 17, pp. 31–74 [CF Thompson, editor]. New York: Springer Science.Google Scholar
56. Leeson, S & Summers, JD (1978) Voluntary food restriction by laying hens mediated through dietary self‐selection. Br Poult Sci 19, 417–424.Google Scholar
57. Joshua, IG & Mueller, WJ (1979) The development of a specific appetite for calcium in growing broiler chicks. Br Poult Sci 20, 481–490.Google Scholar
58. Wilkinson, SJ, Selle, PH, Bedford, MR, et al. (2011) Exploiting calcium-specific appetite in poultry nutrition. Worlds Poult Sci J 67, 587–598.Google Scholar
59. Wilkinson, SJ, Bradbury, EJ, Bedford, MR, et al. (2014) Effect of dietary nonphytate phosphorus and calcium concentration on calcium appetite of broiler chicks. Poult Sci 93, 1695–1703.Google Scholar
60. Wood‐Gush, DGM & Kare, MR (1966) The behaviour of calcium‐deficient chickens. Br Poult Sci 7, 285–290.Google Scholar
61. Hughes, BO & Wood-Gush, DGM (1971) A specific appetite for calcium in domestic chickens. Anim Behav 19, 490–499.Google Scholar
62. Klasing, KC (1998) Lipids. In Comparative Avian Nutrition, pp. 171–200 [KC Klasing, editor]. Wallingford: CAB International.Google Scholar
63. Sawamura, R, Kawabata, Y, Kawabata, F, et al. (2015) The role of G-protein-coupled receptor 120 in fatty acids sensing in chicken oral tissues. Biochem Biophys Res Commun 458, 387–391.Google Scholar
64. Cheled-Shoval, S, Behrens, M, Korb, A, et al. (2017) From cell to beak: in-vitro and in-vivo characterization of chicken bitter taste thresholds. Molecules 22, E821.Google Scholar
65. Hirose, N, Kawabata, Y, Kawabata, F, et al. (2015) Bitter taste receptor T2R1 activities were compatible with behavioral sensitivity to bitterness in chickens. Biochem Biophys Res Commun 460, 464–468.Google Scholar
66. Dey, B, Kawabata, F, Kawabata, Y, et al. (2017) Identification of functional bitter taste receptors and their antagonist in chickens. Biochem Biophys Res Commun 482, 693–699.Google Scholar
67. Hillier, LW, Miller, W, Birney, E, et al. (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432, 695–716.Google Scholar
68. Lagerström, MC, Hellström, AR, Gloriam, DE, et al. (2006) The G protein-coupled receptor subset of the chicken genome. PLoS Comput Biol 2, e54.Google Scholar
69. Richards, MP & Proszkowiec-Weglarz, M (2007) Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult Sci 86, 1478–1490.Google Scholar
70. Schioth, HB (2006) G protein-coupled receptors in regulation of body weight. CNS Neurol Disord Drug Targets 5, 241–249.Google Scholar
71. Kudo, K-i, Wakamatsu, K-i, Nishimura, S, et al. (2010) Gustducin is expressed in the taste buds of the chicken. Anim Sci J 81, 666–672.Google Scholar
72. Venkatesan, N, Rajapaksha, P, Payne, J, et al. (2016) Distribution of α-gustducin and vimentin in premature and mature taste buds in chickens. Biochem Biophys Res Commun 479, 305–311.Google Scholar
73. Witt, M, Reutter, K, Ganchrow, D, et al. (2000) Fingerprinting taste buds: intermediate filaments and their implication for taste bud formation. Philos Trans R Soc Lond B Biol Sci 355, 1233–1237.Google Scholar
74. Behrens, M, Korsching, SI & Meyerhof, W (2014) Tuning properties of avian and frog bitter taste receptors dynamically fit gene repertoire sizes. Mol Biol Evol 31, 3216–3227.Google Scholar
75. Davis, JK, Lowman, JJ, Thomas, PJ, et al. (2010) Evolution of a bitter taste receptor gene cluster in a new world sparrow. Genome Biol Evol 2, 358–370.Google Scholar
76. Wang, K & Zhao, H (2015) Birds generally carry a small repertoire of bitter taste receptor genes. Genome Biol Evol 7, 2705–2715.Google Scholar
77. Dong, D, Jones, G & Zhang, S (2009) Dynamic evolution of bitter taste receptor genes in vertebrates. BMC Evol Biol 9, 12.Google Scholar
78. Li, D & Zhang, J (2014) Diet shapes the evolution of the vertebrate bitter taste receptor gene repertoire. Mol Biol Evol 31, 303–309.Google Scholar
79. Cheled-Shoval, SL, Behrens, M, Meyerhof, W, et al. (2014) Perinatal administration of a bitter tastant influences gene expression in chicken palate and duodenum. J Agric Food Chem 62, 12512–12520.Google Scholar
80. Kudo, K-i, Kawabata, F, Nomura, T, et al. (2014) Isolation of chicken taste buds for real-time Ca2+ imaging. Anim Sci J 85, 904–909.Google Scholar
81. Shi, P & Zhang, J (2006) Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 23, 292–300.Google Scholar
82. Ganchrow, JR, Steiner, JE & Bartana, A (1990) Behavioral reactions to gustatory stimuli in young chicks (Gallus gallus domesticus). Dev Psychobiol 23, 103–117.Google Scholar
83. Halpern, BP (1962) Gustatory nerve responses in the chicken. Am J Physiol 203, 541–544.Google Scholar
84. Brindley, LD (1965) Taste discrimination in bobwhite and Japanese quail. Anim Behav 13, 507–512.Google Scholar
85. Harriman, AE & Milner, JS (1969) Preference for sucrose solutions by Japanese quail (Coturnix coturnix japonica) in two-bottle drinking tests. Am Midl Nat 81, 575–578.Google Scholar
86. Jacobs, HL & Scott, ML (1957) Factors mediating food and liquid intake in chickens: 1. Studies on the preference for sucrose or saccharine solutions. Poult Sci 36, 8–15.Google Scholar
87. Kare, MR & Medway, W (1959) Discrimination between carbohydrates by the fowl. Poult Sci 38, 1119–1127.Google Scholar
88. Sukumaran, SK, Yee, KK, Iwata, S, et al. (2016) Taste cell-expressed α-glucosidase enzymes contribute to gustatory responses to disaccharides. Proc Nat Acad Sci U S A 113, 6035–6040.Google Scholar
89. Conigrave, AD & Brown, EM (2006) Taste receptors in the gastrointestinal tract II. l-Amino acid sensing by calcium-sensing receptors: implications for GI physiology. Am J Physiol Gastrointest Liver Physiol 291, G753–G761.Google Scholar
90. Omori, H, Kawabata, Y, Kawabata, F, et al. (2016) Functional analysis of the extracellular calcium-sensing receptor (CaSR) in chicken oral tissue. Abstract from 17th International Symposium on Olfaction and Taste (ISOT2016) PACIFICO Yokohama, Yokohama, Japan, June 5–9, 2016 President: Yuzo Nimoniya. Chem Senses 41, e260.Google Scholar
91. Tordoff, MG (2001) Calcium: taste, intake, and appetite. Physiol Rev 81, 1567–1597.Google Scholar
92. Tordoff, MG, Shao, H, Alarcón, LK, et al. (2008) Involvement of T1R3 in calcium–magnesium taste. Physiol Genomics 34, 338–348.Google Scholar
93. Kawabata, Y, Mizobuchi, M, Kawabata, F, et al. (2016) Expression patterns and functional analysis of GPR120 and CD36 in oral and gastrointestinal tissues of chicks. Abstract from 17th International Symposium on Olfaction and Taste (ISOT2016) PACIFICO Yokohama, Yokohama, Japan, June 5–9, 2016 President: Yuzo Nimoniya. Chem Senses 41, e273.Google Scholar
94. San Gabriel, A (2015) Taste receptors in the gastrointestinal system. Flavour 4, 14.Google Scholar
95. Efeyan, A, Comb, WC & Sabatini, DM (2015) Nutrient-sensing mechanisms and pathways. Nature 517, 302–310.Google Scholar
96. Janssen, S & Depoortere, I (2013) Nutrient sensing in the gut: new roads to therapeutics? Trends Endocrinol Metab 24, 92–100.Google Scholar
97. Monir, MM, Hiramatsu, K, Yamasaki, A, et al. (2014) The influence of restricted feeding on glucagon-like peptide-1 (GLP-1)-containing cells in the chicken small intestine. Anat Histol Embryol 43, 153–158.Google Scholar
98 Nishimura, K, Hiramatsu, K, Watanabe, T, et al. (2015) Amino acid supplementation to diet influences the activity of the L cells in chicken small intestine. J Poult Sci 52, 221–226.Google Scholar
99. Gao, T, Zhao, M, Zhang, L, et al. (2017) Effect of in ovo feeding of l-arginine on the hatchability, growth performance, gastrointestinal hormones, and jejunal digestive and absorptive capacity of posthatch broilers. J Anim Sci 95, 3079–3092.Google Scholar
100. Furuse, M, Mabayo, RT, Choi, YH, et al. (1993) Feeding behaviour in chickens given diets containing medium chain triglyceride. Br Poult Sci 34, 211–217.Google Scholar
101. Breer, H, Eberle, J, Frick, C, et al. (2012) Gastrointestinal chemosensation: chemosensory cells in the alimentary tract. Histochem Cell Biol 138, 13–24.Google Scholar
102. Geraedts, MCP, Troost, FJ & Saris, WHM (2011) Gastrointestinal targets to modulate satiety and food intake. Obes Rev 12, 470–477.Google Scholar
103. Wauson, EM, Lorente-Rodríguez, A & Cobb, MH (2013) Minireview: nutrient sensing by G protein-coupled receptors. Mol Endocrinol 27, 1188–1197.Google Scholar
104. Byerly, MS, Simon, J, Cogburn, LA, et al. (2010) Transcriptional profiling of hypothalamus during development of adiposity in genetically selected fat and lean chickens. Physiol Genomics 42, 157–167.Google Scholar
105. Cheled-Shoval, SL, Druyan, S & Uni, Z (2015) Bitter, sweet and umami taste receptors and downstream signaling effectors: expression in embryonic and growing chicken gastrointestinal tract. Poult Sci 94, 1928–1941.Google Scholar
106. Yoshida, Y, Kawabata, Y, Kawabata, F, et al. (2015) Expressions of multiple umami taste receptors in oral and gastrointestinal tissues, and umami taste synergism in chickens. Biochem Biophys Res Commun 466, 346–349.Google Scholar
107. Meslin, C, Desert, C, Callebaut, I, et al. (2015) Expanding duplication of free fatty acid receptor-2 (GPR43) genes in the chicken genome. Genome Biol Evol 7, 1332–1348.Google Scholar
108. Mazzoni, M, Bombardi, C, Vallorani, C, et al. (2016) Distribution of α-transducin and α-gustducin immunoreactive cells in the chicken (Gallus domesticus) gastrointestinal tract. Poult Sci 95, 1624–1630.Google Scholar
109. Hyde, R, Taylor, PM & Hundal, HS (2003) Amino acid transporters: roles in amino acid sensing and signalling in animal cells. Biochem J 373, 1–18.Google Scholar
110. Awad, WA, Aschenbach, JR, Ghareeb, K, et al. (2014) Campylobacter jejuni influences the expression of nutrient transporter genes in the intestine of chickens. Vet Microbiol 172, 195–201.Google Scholar
111. Chen, H, Pan, Y, Wong, EA, et al. (2005) Dietary protein level and stage of development affect expression of an intestinal peptide transporter (cPepT1) in chickens. J Nutr 135, 193–198.Google Scholar
112. Dong, XY, Wang, YM, Yuan, C, et al. (2012) The ontogeny of nutrient transporter and digestive enzyme gene expression in domestic pigeon (Columba livia) intestine and yolk sac membrane during pre- and posthatch development. Poult Sci 91, 1974–1982.Google Scholar
113. Garriga, C, Hunter, RR, Amat, C, et al. (2006) Heat stress increases apical glucose transport in the chicken jejunum. Am J Physiol Regul Integr Comp Physiol 290, R195–R201.Google Scholar
114. Garriga, C, Rovira, N, Moretó, M, et al. (1999) Expression of Na-d-glucose cotransporter in brush-border membrane of the chicken intestine. Am J Physiol Regul Integr Comp Physiol 276, R627–R631.Google Scholar
115. Gilbert, ER, Li, H, Emmerson, DA, et al. (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult Sci 86, 1739–1753.Google Scholar
116. Madsen, SL & Wong, EA (2011) Expression of the chicken peptide transporter 1 and the peroxisome proliferator-activated receptor α following feed restriction and subsequent refeeding. Poult Sci 90, 2295–2300.Google Scholar
117. Mott, CR, Siegel, PB, Webb, KE, et al. (2008) Gene expression of nutrient transporters in the small intestine of chickens from lines divergently selected for high or low juvenile body weight. Poult Sci 87, 2215–2224.Google Scholar
118. Zeng, PL, Li, XG, Wang, XQ, et al. (2011) The relationship between gene expression of cationic and neutral amino acid transporters in the small intestine of chick embryos and chick breed, development, sex, and egg amino acid concentration. Poult Sci 90, 2548–2556.Google Scholar
119. Zhang, XY, Zhang, NN, Wan, XP, et al. (2017) Gene expression of amino acid transporter in pigeon (Columbia livia) intestine during post-hatch development and its correlation with amino acid in pigeon milk. Poult Sci 96, 1120–1131.Google Scholar
120. Vancleef, L, Van Den Broeck, T, Thijs, T, et al. (2015) Chemosensory signalling pathways involved in sensing of amino acids by the ghrelin cell. Sci Rep 5, 15725.Google Scholar
121. Furuse, M, Tachibana, T, Ohgushi, A, et al. (2001) Intracerebroventricular injection of ghrelin and growth hormone releasing factor inhibits food intake in neonatal chicks. Neurosci Lett 301, 123–126.Google Scholar
122. Kaiya, H, van der Geyten, S, Kojima, M, et al. (2002) Chicken ghrelin: purification, cDNA cloning, and biological activity. Endocrinology 143, 3454–3463.Google Scholar
123. Saito, E-S, Kaiya, H, Tachibana, T, et al. (2005) Inhibitory effect of ghrelin on food intake is mediated by the corticotropin-releasing factor system in neonatal chicks. Regul Pept 125, 201–208.Google Scholar
124. Saito, E-S, Kaiya, H, Takagi, T, et al. (2002) Chicken ghrelin and growth hormone-releasing peptide-2 inhibit food intake of neonatal chicks. Eur J Pharmacol 453, 75–79.Google Scholar
125. Geelissen, SME, Swennen, Q, van der Geyten, S, et al. (2006) Peripheral ghrelin reduces food intake and respiratory quotient in chicken. Domest Anim Endocrinol 30, 108–116.Google Scholar
126. Buyse, J, Janssen, S, Geelissen, S, et al. (2009) Ghrelin modulates fatty acid synthase and related transcription factor mRNA levels in a tissue-specific manner in neonatal broiler chicks. Peptides 30, 1342–1347.Google Scholar
127. Ocłoń, E & Pietras, M (2011) Peripheral ghrelin inhibits feed intake through hypothalamo–pituitary–adrenal axis-dependent mechanism in chicken. J Anim Feed Sci 20, 118–130.Google Scholar
128. Kuenzel, WJ, Douglass, LW & Davison, BA (1987) Robust feeding following central administration of neuropeptide Y or peptide YY in chicks, Gallus domesticus . Peptides 8, 823–828.Google Scholar
129. Ando, R, Kawakami, S-i, Bungo, T, et al. (2001) Feeding responses to several neuropeptide Y receptor agonists in the neonatal chick. Eur J Pharmacol 427, 53–59.Google Scholar
130. Moore, CA & Elliott, R (1946) Numerical and regional distribution of taste buds on the tongue of the bird. J Comp Neurol 84, 119–131.Google Scholar
131. Hamrum, CL (1953) Experiments on the senses of taste and smell in the bob-white quail (Colinus virginianus virginianus). Am Midl Nat 49, 872–877.Google Scholar
132. Kare, MR, Black, R & Allison, EG (1957) The sense of taste in the fowl. Poult Sci 36, 129–138.Google Scholar
133. Lindenmaier, P & Kare, MR (1959) The taste end-organs of the chicken. Poult Sci 38, 545–550.Google Scholar
134. Duncan, CJ (1960) Preference tests and the sense of taste in the feral pigeon (Columba livia var gmelin). Anim Behav 8, 54–60.Google Scholar
135. Capretta, PJ (1961) An experimental modification of food preference in chickens. J Comp Physiol Psychol 54, 238–242.Google Scholar
136. Duncan, CJ (1962) Salt preferences of birds and mammals. Physiol Zool 35, 120–132.Google Scholar
137. Fuerst, WF & Kare, MR (1962) The influence of pH on fluid tolerance and preferences. Poult Sci 41, 71–77.Google Scholar
138. Herbert, L, Pick, J & Kare, RM (1962) The effect of artificial cues on the measurement of taste preference in the chicken. J Comp Physiol Psychol 55, 342–345.Google Scholar
139. Kare, MR & Maller, O (1967) Taste and food intake in domesticated and jungle fowl. J Nutr 92, 191–196.Google Scholar
140. Vince, MA (1977) Taste sensitivity in the embryo of the domestic fowl. Anim Behav 25, 797–805.Google Scholar
141. Gentle, MJ (1978) Extra-lingual chemoreceptors in the chicken (Gallus domesticus). Chem Senses 3, 325–329.Google Scholar
142. Summers, JD & Leeson, S (1978) Dietary selection of protein and energy by pullets and broilers. Br Poult Sci 19, 425–430.Google Scholar
143. Kaufman, LW, Collier, G & Squibb, RL (1978) Selection of an adequate protein–carbohydrate ratio by the domestic chick. Physiol Behav 20, 339–344.Google Scholar
144. Gentle, MJ & Harkin, C (1979) The effect of sweet stimuli on oral behaviour in the chicken. Chem Senses 4, 183–190.Google Scholar
145. Gentle, MJ (1983) The chorda tympani nerve and taste in the chicken. Experientia 39, 1002–1003.Google Scholar
146. Werner, S (1983) Responses to sugars and their behavioural mechanisms in the starling (Sturnus vulgaris L.). Behav Ecol Sociobiol 13, 243–251.Google Scholar
147. Kurosawa, T, Niimura, S, Kusuhara, S, et al. (1983) Morphological studies of taste buds in chickens. Nihon Chikusan Gakkaiho 54, 502–510.Google Scholar
148. Cheeke, PR, Powley, JS, Nakaue, HS, et al. (1983) Feed preference responses of several avian species fed alfalfa meal, high- and low-saponin alfalfa, and quinine sulfate. Can J Anim Sci 63, 707–710.Google Scholar
149. Gillette, K, Thomas, DK & Bellingham, WP (1983) A parametric study of flavoured food avoidance in chicks. Chem Senses 8, 41–57.Google Scholar
150. Taher, AI, Gleaves, EW & Beck, M (1984) Special calcium appetite in laying hens. Poult Sci 63, 2261–2267.Google Scholar
151. Rio, CMd, Stevens, BR, Daneke, DE, et al. (1988) Physiological correlates of preference and aversion for sugars in three species of birds. Physiol Zool 61, 222–229.Google Scholar
152. Balog, JM & Millar, RI (1989) Influence of the sense of taste on broiler chick feed consumption. Poult Sci 68, 1519–1526.Google Scholar
153. James, EE & Mason, JR (1990) Differences in taste preference between red-winged blackbirds and European starlings. Wilson Bull 102, 292–299.Google Scholar
154. Noble, DO, Picard, ML, Dunnington, EA, et al. (1993) Food intake adjustments of chicks: short term reactions of genetic stocks to deficiencies in lysine, methionine or tryptophan. Br Poult Sci 34, 725–735.Google Scholar
155. Choi, YH, Asakura, K, Okumura, J, et al. (1996) Repulsive effect and palatability of dietary phenylalanine in laying hens. Asian Australas J Anim Sci 9, 159–164.Google Scholar
156. Mabayo, RT, Okumura, J-I & Furuse, M (1996) Dietary flavor modifies oil preferences in the chicken. Appl Anim Behav Sci 49, 213–221.Google Scholar
157. Burne, THJ & Rogers, LJ (1997) Relative importance of odour and taste in the one-trial passive avoidance learning bead task. Physiol Behav 62, 1299–1302.Google Scholar
158. Marples, NM & Roper, TJ (1997) Response of domestic chicks to methyl anthranilate odour. Anim Behav 53, 1263–1270.Google Scholar
159. Sneddon, H, Hadden, R & Hepper, PG (1998) Chemosensory learning in the chicken embryo. Physiol Behav 64, 133–139.Google Scholar
160. Richard, S & Davies, DC (2000) Comparison of methyl anthranilate and denatonium benzoate as aversants for learning in chicks. Physiol Behav 70, 521–525.Google Scholar
161. Matson, KD, Millam, JR & Klasing, KC (2001) Thresholds for sweet, salt, and sour taste stimuli in cockatiels (Nymphicus hollandicus). Zoo Biol 20, 1–13.Google Scholar
162. Zuberbuehler, CA, Messikommer, RE & Wenk, C (2002) Choice feeding of selenium-deficient laying hens affects diet selection, selenium intake and body weight. J Nutr 132, 3411–3417.Google Scholar
163. Matson, KD, Millam, JR & Klasing, KC (2004) Cockatiels (Nymphicus hollandicus) reject very low levels of plant secondary compounds. Appl Anim Behav Sci 85, 141–156.Google Scholar
164. Hile, AG, Shan, Z, Zhang, S-Z, et al. (2004) Aversion of European starlings (Sturnus vulgaris) to garlic oil treated granules: garlic oil as an avian repellent. Garlic oil analysis by nuclear magnetic resonance spectroscopy. J Agric Food Chem 52, 2192–2196.Google Scholar
165. Skelhorn, J & Rowe, C (2005) Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey. Biol Lett 1, 500–503.Google Scholar
166. Ueda, H & Kainou, S (2005) Aversion to quinine is associated with taste sensation in chicks. J Poult Sci 42, 254–262.Google Scholar
167. Skelhorn, J, Griksaitis, D & Rowe, C (2008) Colour biases are more than a question of taste. Anim Behav 75, 827–835.Google Scholar
168. Werner, SJ, Kimball, BA & Provenza, FD (2008) Food color, flavor, and conditioned avoidance among red-winged blackbirds. Physiol Behav 93, 110–117.Google Scholar
169. Di Pizio, A & Niv, MY (2015) Promiscuity and selectivity of bitter molecules and their receptors. Bioorg Med Chem 23, 4082–4091.Google Scholar
170. Skelhorn, J (2016) Bitter tastes can influence birds’ dietary expansion strategies. Behav Ecol 27, 725–730.Google Scholar
Figure 0

Table 1 Chronological accountancy of the main peer-reviewed publications on taste and nutrient sensing and feed intake in poultry grouped by scientific discipline

Figure 1

Table 2 Chicken nutrient-sensing genes (G protein-coupled receptors; GPR) identified based on homology with mammalian genes and mRNA expression data