Quail taxonomy

Quail belong to two families: Odontophoridae (New World quail) and Phasianidae (including several genera representing Old World species). Both the common quail (Coturnix coturnix), and the Japanese quail (Coturnix japonica) belong to the genus Coturnix and until recently, were believed to be one species. Unlike wild Japanese quail, where no subspecies are existing, Coturnix coturnix has five subspecies: Eurasian subspecies (Coturnix coturnix coturnix, Linneaus, 1758), Azorean Quail (Coturnix coturnix conturbans), Abyssinian quail (Coturnix coturnix erlangeri), African subspecies (Coturnix coturnix africana, Temminck and Schlegel, 1849) and Cape Verde quail (Coturnix coturnix inopinata). The genus Coturnix comprises eight species, two of which are already extinct. All members of the genus are migratory birds, and often their species ranges overlap. This hinders the differentiation of some subspecies (Minvielle, Reference MINVIELLE2009). A serious concern for maintaining genetic purity in wild quail is hybridisation between common and domestic quail by hunters and farmers in the wild (Derégnacourt, 2000; Derégnacourt et al., Reference DERÉGNACOURT, GUYOMARC'H and BELHAMRA2005; Barilani et al., Reference BARILANI, DEREGNACOURT, GALLEGO, GALLI, MUCCI, PIOMBO, PUIGCERVER, RIMONDI, RODRÍGUES-TEIJERO, SPANÒ and RANDI2005; Huisman, Reference HUISMAN2006; Charaza et al., Reference CHARAZA, MINVIELLE, ROUX, BED'HOM, FEVE, COVILLE, KAYANG, LUMINEAU, VIGNAL, BOUTIN and ROGNON2010). Common x domestic quail hybrids are fertile, exhibit the same nesting and brooding behaviour as wild ones (Derégnacourt et al., 2002), but are substantially unstable compared to the wild form, therefore their nests can be exposed to a greater risk of predator attacks (Puigcerver et al., Reference PUIGCERVER, SANCHEZ-DONOSO, VILÀ, SARDÀ-PALOMERA, GARCÍA-GALEA and RODRÍGUEZ-TEIJEIRO2014; Capdevila et al., Reference CAPDEVILA, PUIGCERVER, LÓPEZ, PÉREZ-MASDEU, GARCÍA-GALEA and RODRÍGUEZ-TEIJEIRO2016) and they may lose their migration behaviour (Derégnacourt et al., Reference DERÉGNACOURT, GUYOMARC'H and BELHAMRA2005). A similar crossing has been reported between domestic and wild Japanese quail (Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009), which is not a hybridisation per se, as the species is the same, but results in changes in behavioural and exterior traits compared to the wild Japanese quail population.

Quail domestication

The modern domesticated Japanese quail which are widely used in animal husbandry practice originate from the wild Japanese quail (Coturnix japonica, Temminck and Schlegel, 1849), as confirmed by modern genetic studies (Chang et al., Reference CHANG, CHANG, LIU, ZHAO, JI, MAO, SONG and SHI2007). Rearing wild birds in captivity and their domestication are different things. The analysis of available literature showed that wild quail have been reared as fighting, song and decorative birds from ancient times in East and Southeast Asia, while the real domestication had occurred in Japan within a very short period by the end of the 19^th and beginning of the 20^th century.

According to Mizutani (Reference MIZUTANI2003) first written testimonies about rearing Japanese quail as song birds have been found in Japan and date back to the 18^th century, while other point to the 12^th century (Kovach, Reference KOVACH1974). Other researchers (Chang et al., Reference CHANG, CHANG, LUI, XU, WANG, ZHAO and OLOWOFESO2005) showed that wild quail were reared as song birds in China as far back as 770-476 BC, and were used as sacrificial animals even earlier. Male quail are used for fighting in some parts of Asia (Kuo, Reference KUO1960; Mills et al., Reference MILLS, CRAWFORD, DOJAN and FAURE1997; Chang et al., Reference CHANG, CHANG, LUI, XU, WANG, ZHAO and OLOWOFESO2005), according to a long-standing tradition. There is evidence that this sport has been practiced by ancient Greeks and Romans (Magnin, Reference MAGNIN1838; Brugas and de Witte, Reference BRUGAS and DE WITTE1868; Morgan, Reference MORGAN1975). Most probably, the catching and rearing in captivity of Asian quail occurred in parallel in China and Japan, and possibly in other Asian countries where the birds were distributed. According to Crawford (Reference CRAWFORD1990) quail domestication occurred the 11^th century in Japan, China or Korea and it is generally assumed that already domesticated quail were imported in Japan from China or Korea around that time (Howes, Reference HOWES1964; Wakasugi, Reference WAKASUGI1984; Crawford, Reference CRAWFORD1990; Chang et al., Reference CHANG, CHANG, LUI, XU, WANG, ZHAO and OLOWOFESO2005). There are written testimonies that Japanese quail eggs and meat were used in eastern food and medicine from the 17^th century onward (Genchev, Reference GENCHEV2014). According to Howes (Reference HOWES1964) true domestication has occurred during the last century.

The more serious achievements of selection of Japanese quail as a productive bird species date back to 1910-1941 (Mills et al., Reference MILLS, CRAWFORD, DOJAN and FAURE1997). At that time, a population with substantially better egg-laying and meat traits than other captive quail was created in Japan (Donchev and Angelov, Reference DONCHEV and ANGELOV1971). Quail from this population had a similar appearance to their wild ancestors, but had higher egg production and a lack of brooding instinct. By virtue of purposeful selection of the species, egg production has dramatically increased and now approaches that of chickens.

Prolonged variable selection has resulted in greater genetic distance from wild ancestors. Differences are associated with a number of changes - morphological, behavioural and productive. The main morphological distinctions affect appearance, such as body size and weight (Mills et al., Reference MILLS, CRAWFORD, DOJAN and FAURE1997; Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009), plumage colour (Cheng and Kimura, Reference CHENG and KIMURA1990; Mizutani, Reference MIZUTANI2003; Tsudzuki, Reference TSUDZUKI2008), and other phenotypic traits (Chang et al., Reference CHANG, CHANG and ZHENG2001; Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009). Differences between wild and domestic quail behaviour have been noticed, including their migratory (Derégnacourt et al., Reference DERÉGNACOURT, GUYOMARC'H and BELHAMRA2005), sexual (Mills et al., Reference MILLS, CRAWFORD, DOJAN and FAURE1997; Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009) nesting, brooding (Nichols, Reference NICHOLS1991), and other responses (Nichols, Reference NICHOLS1991; Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009). Prolonged selection on different productive traits in domesticated quail positively affects their egg laying capacity (Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009), sexual maturity (Mizutani, Reference MIZUTANI2003; Cheng et al., Reference CHENG, BENNET and MILLS2010), egg size (Wilson et al., Reference WILSON, ANDERSON and SIOPES1971; Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009), fertilisation and hatchability (Wilson et al., Reference WILSON, ANDERSON and SIOPES1971) compared to those in wild Japanese quail.

Quail in industrial poultry farming

Japanese quail are widely geographically spread as domesticated bird species. They are used in farming systems for production of meat and eggs (Baumgartner, Reference BAUMGARTNER1994; Chang, Reference CHANG1998; Minvielle, Reference MINVIELLE1998; Minvielle, Reference MINVIELLE2004; Vali, Reference VALI2008; Genchev, Reference GENCHEV2014; Lukanov and Genchev, Reference LUKANOV and GENCHEV2018), and, from around 60 years ago, as laboratory animals (Padgett and Ivey, Reference PADGETT and IVEY1959; Reese and Reese, Reference REESE and REESE1962; Kovach, Reference KOVACH1974; Sano et al., Reference SANO, OKAMATO, CHENG and TAKAHASHI1995; Minvielle, Reference MINVIELLE2004; Huss et al., Reference HUSS, POYNTER and LANSFORD2008; Baer et al., Reference BAER, LANSFORD and CHENG2015; Pavlova et al., Reference PAVLOVA, LUKANOV, IVANOV, PETROVA and GENCHEV2018). Last but not least, this is a decorative bird species (both wild and domestic) reared by amateur poultry breeders on a global scale (Lukanov et al., Reference LUKANOV, GENCHEV and KOLEV2018). In some Asian countries (Pakistan, Afghanistan, China etc.) male quail are used for fighting (Mills et al., Reference MILLS, CRAWFORD, DOJAN and FAURE1997).

Worldwide, the main production of quail eggs is concentrated in East Asia and Brazil, and meat in Europe, the USA and China (Baumgartner, Reference BAUMGARTNER1994; Minvielle, Reference MINVIELLE1998; Reference MINVIELLE2004; Bertechini, Reference BERTECHINI2012). Although the estimation of the quail population involved in industrial farming is difficult, it has progressively increased over the last few decades. At the beginning of the millennium, about 1 billion Japanese quail were reared globally (Xu et al., Reference XU, CHANG, WANG, CHANG, DU, LU, YI, XU and WANG2003; Chang et al., Reference CHANG, CHANG, LIU, ZHAO, JI, MAO, SONG and SHI2007). According to Duval et al. (Reference DUVAL, CASSEY, DESAIVRE, REYNOLDS and SPENCER2012) over nine billion quail are produced each year in East Asia (China, Japan, Hong Kong). China is the biggest producer of quail meat and eggs producing 146,000 to 190,000 tonnes of meat and about 90 billion eggs on an annual basis (da Cunha, Reference DA CUNHA2009). For comparison, in the early 1990s, China produced about seven billion eggs annually, and Chinese quail meat production was behind Spain, France and the USA (Minvielle, Reference MINVIELLE2004). Another serious player on the world's quail retail market is the European Union (mainly Spain, France, Italy and Portugal) with about 100 million reared quail (www.ciwf.org.uk), mainly used for meat production. The USA dominates meat-type quail farming with about 19 million fattening birds (da Cunha, Reference DA CUNHA2009). The continuously increasing production of eggs and meat in Brazil with more than 11.5 million quail should not be underestimated (Bertechini, Reference BERTECHINI2012). By the early 2000s, the industrial quail farming population in Japan decreased to seven million layers (Mizutani, Reference MIZUTANI2003), that, according to Minvielle (Reference MINVIELLE2004) produce yearly about 1.8 billion quail eggs. Despite the serious increase in the number of quail reared in Australia in 2001-2002 up to 6.5 million (da Cunha, Reference DA CUNHA2009), in 2010 the population decreased to 3.5 million birds (Department of Agriculture, Australia, 2010, cited by Farooq, Reference FAROOQ2014). Other countries with well-developed quail production are Canada, Egypt, Saudi Arabia, India, Estonia, Russia, Singapore, Venezuela, Peru, Columbia and Bolivia. It can be summed up that the global production of quail meat and eggs is concentrated in several countries - China, Spain, France, Italy, Brazil, the USA and Japan. Quail produce about 10% of all table eggs in the world, or around 1.2-1.3 million tonnes, leaving chickens as a dominating species with production of about 72 million tonnes eggs in 2016 (Conway, Reference CONWAY2017). On the basis of available data, world quail meat production is estimated to be 200,000 to 240,000 tonnes, that is, about 0.2% of the world poultry meat produce (Figure 1).

Despite the large number of reared birds, the small size of quail and their eggs negatively influences quantitative parameters for production. The FAO database contains data on chickens, turkeys, ducks, geese and guineafowl, pigeons and others. According to FAOSTAT the global numbers of pigeons and other birds for 2016 was about 28.5 million (FAOSTAT, 2018). Taking into account the estimated number of quail reared in the world, it is clear that quail were not included at all in the statistics, despite being included in the list of domestic animals (FAO, 2000). There was a statement that, in 2016, chickens accounted for some 91% of the world's poultry population, followed by ducks (5%), turkeys (2%), other poultry, such as geese and guineafowl, made up the remaining 2% (FAO, 2018). The lack of exact data for production from domestic quail as a farmed bird species neglected its role in poultry farming. The available data suggested that the domestic quail population involved in global production of poultry meat and eggs comes second after that of domestic chickens (Figure 2). This clearly confirms the role of domestic quail for human consumption and the need for throwing more light on this avian species.

Figure 1

Global poultry meat production by species (FAOSTAT, 2018 and estimated data for quail).

Figure 2

Average share of the domestic birds, slaughtered annually worldwide (FAOSTAT, 2018 and estimated data for quail).

Quail as a laboratory animal model, pet and show bird

Domesticated Japanese quail are often used as laboratory animals (Huss et al., Reference HUSS, POYNTER and LANSFORD2008; Cheng et al., Reference CHENG, BENNET and MILLS2010; Andraszek et al., Reference ANDRASZEK, GRYZIŃSKA, WÓJCIK, KNAGA and SMALEC2014; Baer et al., Reference BAER, LANSFORD and CHENG2015). Due to its small body size, robustness, fast maturation, laying ability and cage adaptive housing, they are known as the ‘Drosophila of the avian laboratory’ (Padgett and Ivey, Reference PADGETT and IVEY1959; Reese and Reese, Reference REESE and REESE1962). Their genome has been fully sequenced (Nishibori et al., Reference NISHIBORI, HAYASHI, TSUDZUKI, YAMAMOTO and YASUE2001; Kawahara-Miki et al., Reference KAWAHARA-MIKI, SANO, NUNOME, SHIMMURA, KUWAYAMA, TAKAHASHI, KAWASHIMA, MATSUDA, YOSHIMURA and KONO2013), which makes them suitable for genetic studies, replacing the domestic chicken (Andraszek et al., Reference ANDRASZEK, GRYZIŃSKA, WÓJCIK, KNAGA and SMALEC2014). Domesticated Japanese quail are used as laboratory animal models for studies in developmental biology, animal science, veterinary and human medicine (Huss et al., Reference HUSS, POYNTER and LANSFORD2008; Tserveni-Goussi and Fortomaris, Reference TSERVENI-GOUSSI and FORTOMARIS2011) and genetic and epigenetic investigations (Minvielle, Reference MINVIELLE2004; Huss et al., Reference HUSS, POYNTER and LANSFORD2008; Andraszek et al., Reference ANDRASZEK, GRYZIŃSKA, WÓJCIK, KNAGA and SMALEC2014; Baer et al., Reference BAER, LANSFORD and CHENG2015), including as a transgenic bird model (Shin et al., Reference SHIN, KIM, KIM, SEO, LEE, KWON, LEE, KIM, LIM and HAN2008; Poyntner et al., Reference POYNTNER, HUSS and LANSFORD2009). All this put them on the top of the bird laboratory list.

Domesticated Japanese quail are popular as an ornamental, exhibition and pet bird in many areas in the world (Lukanov et al., Reference LUKANOV, GENCHEV and KOLEV2018). Their small size, fast growing and maturing, easy care, taming and different plumage coloration makes them preferable for a lot of poultry fans. Some quail breeder associations and clubs have been established in Europe, such as Sondervereines der Japanischen Legewachteln (Germany), DFKP-Club (The Netherlands), improving their potential as a show bird. The European association of poultry, pigeon, cage bird, rabbit and cavy breeders separate the domesticated Japanese quail from the wild ones, naming them ‘laying quail’, and are preparing a European standard (ESC-P, 2018).

Poultry or game bird, where is the Japanese quails place?

In poultry farming, several species are reared as productive fowl, for example chicken (Gallus gallus domesticus, Linnaeus, 1758), turkey (Meleagris gallopavo, Linnaeus, 1758), geese (Anser anser domesticus, and Anser cygnoides domesticus, Linnaeus, 1758), duck (Anas platyrhynchos domesticus, Linnaeus, 1758), Muscovy duck (Cairina moschata domestica), pigeon (Columba livia domestica), Japanese quail (Coturnix japonica, Temminck and Schlegel, 1849), guineafowl (Numida meleagris, Linnaeus, 1758), as well as ostriches (Struthio camelus domesticus, Linnaeus, 1758), the common pheasant (Phasianus colchicus, Linnaeus, 1758) and Virginia quail (Colinus virginianus, Linnaeus, 1758). Less important, from economical point of view, are the other ratites reared in farms - emus, rheas and cassowaries (FAO, 2000). As can be seen from species’ names, three domestic bird species are implemented in industrial production of meat and/or eggs without a clear distinction between them and their respective ancestors. These include Japanese quail, guineafowl and turkeys. Similarly, in species designated as semi-domesticated (e.g. the common pheasant and the Virginia quail), no differentiation exists between captive and wild birds, which is logical as no major differences are present. Unlike these, domestic quail, turkeys and guineafowl are unlikely survive in the wild because of physiological, morphological and ethological changes occurring consequently to domestication and selection for productive traits. In the scientific literature, a clear distinction from the wild form is made only with respect to turkeys by adding the adjective ‘domestic’ (Hart et al., Reference HART, PARTRIDGE and CUTHILL1999; Radzimirska, Reference RADZIMIRSKA2003; Maxwell, Reference MAXWELL2008; Paździor et al., Reference PAŹDZIOR, SZWEDA, OTROCKA-DOMAGAŁA and ROTKIEWICZ2012; Dalloul et al., Reference DALLOUL, LONG, ZIMIN, ASLAM, BEAL and BLOMBERG2010) and/or using a trinomen Meleagris gallopavo domesticus/domestica (Hejlicek and Treml, Reference HEJLICEK and TREML1995; Radzimirska, Reference RADZIMIRSKA2003; Paździor et al., Reference PAŹDZIOR, SZWEDA, OTROCKA-DOMAGAŁA and ROTKIEWICZ2012; Olias et al., Reference OLIAS, ADAM, MEYER, SCHARFF and GRUBER2014). In some sources, including those referring for other domestic fowl species, the terms ‘variety’ and ‘forma’ are used to designate the subspecies, similar to the botanical trinomial nomenclature, but this is not considered proper for zoological use (ICZN, 2000). While there are no serious taxonomical changes in the name of guineafowl, the name for Japanese quail was changed from Coturnix coturnix japonica to Coturnix japonica, placing the bird in a different species from the common quail Coturnix coturnix (McGowan, Reference MCGOWAN1994; Clements, Reference CLEMENTS2002). Even some modern literature sources still mention the bird as Coturnix coturnix japonica (Kul and Seker, Reference KUL and SEKER2004; Antarasena et al., Reference ANTARASENA, SIRIMUJALIN, PROMMUANG, BLACKSELL, PROMKUNTOD and PROMMUANG2006; Scholtz et al., Reference SCHOLTZ, HALLE, FLACHOWSKY and SAUERWEIN2009; Alkan et al., Reference ALKAN, KARABAC, GALIC, KARSLI and BALCIOGLU2010; Duval et al., Reference DUVAL, CASSEY, MIKSIK, REYNOLDS and SPENCER2013; Franqueza et al., Reference FRANQUEZA, RIBEIRO, PEREIRA, FERNANDES, FERNANDES and BARRETO2016; Akdemir et al., Reference AKDEMIR, BAYRIL, BARAN, YILDIZ, KAHRAMAN, ORHAN and SAHIN2018), and domesticated Japanese quail is reported as Coturnix coturnix (Orsi et al., Reference ORSI, SIMOES, STEFANINI and VIOTTO2017; Cox et al., Reference COX, COSBY, THIPPAREDDI, RITZ, BERRANG and JACKSON2018). Another serious concern is the free usage of the word combination ‘Japanese quail’ without specifying whether the wild or domesticated Japanese quail was meant. This, of course, does not decrease the worth of cited reports, but the lack of a uniform term is confusing for readers. Regardless of abovementioned, there is a positive tendency for increasing use of the term ‘domestic quail’ or ‘domestic Japanese quail’ in the scientific literature (Mills et al., Reference MILLS, CRAWFORD, DOJAN and FAURE1997; FAO, 2000; Chang et al., Reference CHANG, LIU, CHANG, CHEN, ZHAO, JI, CHEN, QIN, SHI and HU2009; Orsi et al., Reference ORSI, SIMOES, STEFANINI and VIOTTO2017; Nunome et al., Reference NUNOME, NAKANO, TADANO, KAWAHARA-MIKI, KONO, TAKAHASHI, KAWASHIMA, FUJIWARA, NIRASAWA, MIZUTANI and MATSUDA2017; Sun et al., Reference SUN, LIU, LI, XU and YANG2017; Shalini et al., Reference SHALINI, MEHTA and SINHA2018).

Quail farming in EU and its legislation

Another interesting point is the lack of clear regulations pertaining to the production and quality of domestic quail meat and eggs in the European Union. This is probably due to an existing discrepancy about the designation of the domestic quail - both farm or game species. The following fowl species are included in Commission Regulation No 543/2008 (EC, 2008a): domestic fowl (Gallus domesticus), turkeys (Meleagris gallopavo dom.), ducks (Anas platyrhynchos dom.), Muscovy ducks (Cairina muschata), Mallard ducks (Cairina muschata x Anas platyrhynchos), geese (Anser anser dom.) and guinea fowl (Numida meleagris domesticus). According to the definition of EC No 798/2008 (EC, 2008b) and EC No 158/2009 (EC, 2009), ‘poultry’ refers to fowl, turkeys, guinea fowl, ducks, geese, quail, pigeons, pheasants, partridges and ratites (ratitae), reared or kept in captivity for breeding, the production of meat or eggs for consumption, or for restocking supplies of game. This definition encompasses other game species, such as partridges and pheasants. A similar situation exists for stock egg production, quality evaluation, storage and marketing. In the existing regulations, only chicken eggs are considered, omitting the fact that there are other species producing eggs for consumption, e.g. the domestic quail. EC No 589/2008 (EC, 2008c) defines the term ‘eggs’ as ‘eggs in shell i.e. other than broken, incubated or cooked eggs, that are produced by hens of the species Gallus gallus and are fit for direct human consumption or for the preparation of egg products’. Despite the lack of clear regulations on quail eggs, they partly follow the rules applied for chicken stock eggs. Quail eggs, however, are not subject to grading by weight, marking is impossible due to specific coloration of the eggshell, candling and exact determination of the air cell size are impossible. The widescale introduction of domestic quail in industrial poultry breeding should be reflected in such legislation and the latter should take account of the specific features of the product, its production, quality evaluation, storage, packaging and marketing. Only a comprehensible legal base referring to this bird species will prevent a double standard among producers and will largely avoid the possibility of subjective interpretation of existing legislation on the part of controlling bodies.