Applied Animal Behaviour Science 94 (2005) 303–318
www.elsevier.com/locate/applanim
Behavioural evidence of hybridization
(Japanese European) in domestic quail
released as game birds
S. Derégnaucourt a,b,*, J.-C. Guyomarc’h a, S. Spanò c
a
b
UMR CNRS 6552, ‘Ethologie Evolution Ecologie’, University of Rennes, France
Department of Biology, City College, City University of New York, 138th Street and Convent Avenue,
NY 10031, New York, USA
c
DIP.TE.RIS, University of Genova, Italy
Accepted 8 March 2005
Available online 23 May 2005
Abstract
The European quail is a partial migrant bird considered ‘vulnerable’ by the European community.
The decline of this subspecies has spurred an annual release of large numbers of domestic Japanese
quail. Prezygotic and postzygotic isolating mechanisms have not been established between these two
subspecies, enhancing the risk of hybridization. In addition, anecdotal reports suggest that hybridization is commonly practiced in game farms of domestic quails. In this article, we present the
results of behavioural characterization of the quails produced by two European game farms: one
French and one Italian. First, we looked for evidences of hybridization in both game farms. Using
actographic methods, we measured migratory tendency. Birds, hatched in summer, were submitted in
autumn to an artificial increase of daylength (LD 14:10) for 60 days. In quails, the length of the
cloacal vent which is a good indicator of sexual development, was monitored every 10 days. We noted
the appearance of cloacal foam in males and egg-laying activity in females. In addition, mating calls
produced by the males when sexually mature were recorded and analyzed using spectrographic
methods. Seventeen males of 27 from the French game farm exhibited nocturnal restlessness. Most of
the birds of the Italian game farm (40/44) developed sexually without showing any migratory activity.
Since Japanese quail has lost its migratory impulse during the domestication process, the presence of
migratory activity in quails of both game farms clearly demonstrated the introduction of wild
European quail. Spectrographic analysis of male mating calls confirmed this assumption: some males
* Corresponding author. Tel.: +1 212 650 8608; fax: +1 212 650 8959.
E-mail address: [email protected] (S. Derégnaucourt).
0168-1591/$ – see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2005.03.002
304
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
in both game farms (21/27 in the French game farm, 5/22 in the Italian game farm) produced calls
similar to those produced by control lines of hybrid quails (Japanese European). In an additional
experiment, we report the results of encounters between males of the French game farm and males of
European quail. One bird of each strain were put together on day 1 and on day 3, we introduced in the
pen a female European quail. In 11 cases out of 11, the male of the French game farm dominated the
male European quail and monopolized the female. These results imply that releasing hybrid and
Japanese quails in the wild could rapidly lead to widespread genetic pollution of the western
Palaearctic populations of the European quail.
# 2005 Elsevier B.V. All rights reserved.
Keywords: Game bird; Genetic pollution; Hybridization; European quail; Japanese quail
1. Introduction
The European quail (Coturnix c. coturnix) is a small-sized migratory phasianid with a
geographic range extending from the British Isles to Lake Baı̈kal and from the polar circle
to the tropics (Johnsgard, 1988; Del Hoyo et al., 1994; Guyomarc’h et al., 1998;
Guyomarc’h, 2003). The wintering area extends between the latitudes of 10–128N and 38–
398N and the breeding one between the latitudes of 288N and 55–608N. These two areas
therefore overlap in North Africa, the Nile and Jordan valleys, the new irrigated area of
Northern Arabia, and the Indus basin (Guyomarc’h, 2003). Since the 1970s, there has been
a decline in western Palaearctic populations of European quail, which has led to the listing
of this subspecies in the Bonn convention (June 23, 1979; annexe II: migrant species not
protected, but in an unfavourable state of conservation) and Berne convention (September
19, 1979; annexe III: game bird under regulated exploitation). Changes in agricultural
practices and development of pesticide treatments have noticeably affected reproduction in
Europe. At the same time, the number of wintering quails in Sahelian countries has
dramatically decreased with the persistent drought which has affected these areas since the
early 1970s (Guyomarc’h et al., 1998; Guyomarc’h, 2003). This selective environmental
pressure against long distance migratory phenotypes may have induced micro-evolutionary
processes in favour of short-distance migrating quails (Guyomarc’h and Belhamra, 1998).
The populations of European quail became mainly wintering and sexually precocious (with
a low migratory drive) in the countries between 288 and 388LN: south of Portugal to the
south of Morocco (Guyomarc’h et al., 1998; Guyomarc’h, 2003).
The decline of the European quail populations has spurred an annual release of domestic
Japanese quail (Coturnix c. japonica) as a game bird in France, Spain, Italy (Guyomarc’h
et al., 1998) and probably in other European countries. Although the Japanese quail still
lives in the wild in Asia (Johnsgard, 1988; Del Hoyo et al., 1994), it is better known in its
domestic form in Europe, Asia, North America and India, where it is farmed for meat and
egg production (Mills et al., 1997). The migratory impulse of the Japanese quail has been
counterselected during the domestication process (Derégnaucourt, 2000; Derégnaucourt
et al., 2005). This was known by the breeders in the 1970s (Rizzoni and Lucchetti, 1972).
Their goal was to develop sedentary populations of quails, mimicking the case of the
Chuckar partridge, Alectoris chuckar (Potts, 1988). Attempts to establish Japanese quail in
North America in the 1950s by releasing domestic birds were not successful (Wetherbee
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
305
and Jacobs, 1961; Labisky, 1961; Howes, 1964), as opposed to those in Hawaii where feral
populations have gotten established (Schwartz and Schwartz, 1949; Nichols, 1991). In
Europe, the releases may have begun in the 1970s (Rizzoni and Lucchetti, 1972; Lucotte,
1977).
Both subspecies are sympatric in Mongolia, but so far, there has been no report of
natural hybridization (Del Hoyo et al., 1994). Initial reports suggested that hybridization
between the two subspecies did not extend beyond the first generation (Lepori, 1964; Pala
and Lissia-Frau, 1966), however recent data show that productivity of hybrid combinations
(F1, F2 and backcrosses) do not differ from those of European quail pairs bred under the
same conditions (Derégnaucourt et al., 2002). In addition, prezygotic mechanisms such as
sexual mate selection may not be strong enough to prevent hybridization (Derégnaucourt
and Guyomarc’h, 2003). Similar cases of hybridization caused by human disturbance
following the introduction of a foreign species have been reported (Rhymer and
Simberloff, 1996; Duncan et al., 2003) for fishes (Echelle and Connor, 1989; Verspoor and
Hammar, 1991; Youngson et al., 1993), amphibians (Haffner, 1997), mammals (Thulin
et al., 1997; Goodman et al., 1999) and birds (Potts, 1988; Hughes, 1996; Hoysak and
Ankney, 1996; Rhymer et al., 1994). Interbreeding between domestic Japanese quail and
European quail potentially constitutes another example. Furthermore, some naturalists and
hunters reported that the introduction of European quail in breedings of domestic Japanese
quail is a practice commonly used by game bird breeders. Domestic quails selected for
meat and egg production reach sexual maturity early and exhibit a growth rate that leads to
a progressive increase in both size and weight (Mills et al., 1997). Consequently,
introduction of wild birds may improve the flight qualities of game birds provided to
hunters (Nadal, 1992).
In the first part of this study, we checked whether European quails had been introduced
in game farms of two independent breeders, one French and one Italian. The two
subspecies are morphologically similar in appearance, and there is no way to distinguish
them from hybrids unambiguously based on plumage and skeletal characteristics
(Derégnaucourt, 2000). On the contrary, behavioural analysis can give us clear evidence of
the introduction of wild European quail in game farms, and subsequent hybridization. First,
using actographic methods, we measured migratory tendencies of these quails. Since the
domestic Japanese quail has lost its migratory impulse (Derégnaucourt et al., 2005),
presence of nocturnal restlessness in birds raised in game farms could reveal the
introduction of European quail. Second, we analyzed the structure of male mating calls
using spectrographic methods. Both subspecies share the same vocal repertoire except for
male mating call (Guyomarc’h and Guyomarc’h, 1996) that may be used in sexual
selection (Derégnaucourt and Guyomarc’h, 2003). The presence of mating calls similar to
those produced by European quail or control lines of hybrid (European Japanese) quail
(Guyomarc’h and Guyomarc’h, 1996; Derégnaucourt et al., 2001) would reveal
unambiguously the introgression of European genes in domestic Japanese quail strains.
Additional behavioural selection may improve the quality of the birds supplied to
hunters (Rizzoni and Lucchetti, 1972). The French breeder told us that his strain has been
selected for some characteristics of ‘nervousness’ (‘nervousness’ is the term that the
breeder used to describe his selection) that might stimulate flight take off. The genetic
determinism of such behaviours (i.e., fearfulness, stress, emotivity, etc.) has been
306
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
demonstrated in agronomical research whose goal is to improve the welfare of poultry in
breeding (Mills and Faure, 1991; Jones et al., 1994; Marin and Satterlee, 2003). Our
assumption was that selection of such behavioural characteristics could enhance the
dominance of these individuals over European quails. So, in the second part of this article,
we present the results of encounters between males of the french breeding farm and males
of European quail in the presence of a female European quail.
2. Methods
2.1. Subspecific status of the quails
2.1.1. Birds and housing
Twenty-two males and 22 females were purchased from a commercial breeder in Italy
(Italian Breeding: ITB). Twenty-seven males were purchased from a commercial breeder
in the south-west of France (French Breeding: FRB). These birds hatched in summer and
were held under the natural photoperiod prior to purchase.
At their arrival in our laboratory, quails were maintained under the natural photoperiod
of the autumn. They were placed in individual cages (25 cm 20 cm 15 cm) in which
water and food (vitamin-supplemented pellets and wheat seeds) were provided ad libitum.
All birds were in sexual rest.
2.1.2. Migratory restlessness (‘zugunruhe’)
The quail is a nocturnal migrant bird (Guyomarc’h et al., 1998) and nocturnal
restlessness is the activity performed by captive birds during the migratory seasons
(Berthold, 1973). Since the domestic Japanese quail has lost its migratory impulse
(Derégnaucourt et al., 2005), presence of nocturnal activity characteristic of migrant quails
would reveal the introduction of European quails in game farms. Both subspecies of quail
and their hybrids can be photostimulated by long days at any time of the year (Follett and
Maung, 1978; Guyomarc’h et al., 1990; Derégnaucourt et al., 2005). In order to evaluate
the migratory impulse of the quails in these two groups, we transferred them to an artificial
photoperiod of LD 14:10 for 60 days. Temperature was maintained at 20 8C (2 8C) during
this period.
In quails, the length of the cloacal vent is a good indicator of sexual development
(Sachs, 1969). It was monitored by measuring at 10-day intervals, with callipers to the
nearest 0.1 mm. In addition, we noted the appearance of cloacal foam in males and egglaying activity in females.
Throughout the experiments, the activity of each bird was recorded using an infrared
beam placed on the upper part of the front of the cage. This beam was interrupted each time
the bird passed his head through the bars of its cage trying to take off (Guyomarc’h and
Guyomarc’h, 1992). After analysis by home made software, we obtained some actograms
which represent the daily profile of activity of each bird day after day. We classified ethophysiological phenotypes using the sexual state of the birds and their daily patterns of
activity. Typology of daily profiles has been previously described (Derégnaucourt et al.,
2005). Briefly, levels of activity for each bird were measured during different parts of the
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
307
daily cycle for each day. If the level of activity (beam cuts) was below 200 during the night,
the bird was considered as diurnal. If the level of activity was above 200, the sexual status
of the bird (based on the cloacal length measure) and the repartition of the activity during
the night (i.e., maximal at the beginning, middle, or end of the night) were taken into
account to determine if the bird presented a nocturnal activity characteristic of a migrant
bird, or an anticipation to sunrise characteristic of sexually developed individuals. Each
individual could show different daily profiles during the experiment. Therefore, based on
previous experiments performed with European, domestic Japanese and hybrid quails
under the same conditions (Derégnaucourt et al., 2005), we defined a hierarchical
classification of the responses to increasing day length. We expected three types of
response (Derégnaucourt et al., 2005). (1) Birds that showed nocturnal activity during
sexual quiescence (length of clocal vent <4 mm): ‘migrant birds’ (Fig. 1A). Some of the
males classified as ‘migrant birds’ could maintain a migratory restlessness as they sexually
develop. (2) Birds that presented a nocturnal activity only when they were sexually mature
(length of cloacal vent >4 mm), we called them ‘nomads’ (Fig. 1B). This phenotype is only
represented by some males and never observed in females (Derégnaucourt et al., 2005). In
the field, this activity may be associated with a search for a suitable sexual mate
(Puigcerver et al., 1989). (3) Birds that developed sexually and never exhibited nocturnal
activity: ‘sedentary birds’ (Fig. 1C).
Fig. 1. Three actograms from three different individuals representing the main daily profiles of activity observed
in quail. (A) Typical profile of a ‘migrant’ quail; (B) typical profile of a ‘nomad’ quail (only observed in males);
(C) profile of a sedentary quail. D1–D7: seven successive days. The numbers on the right of the actogram indicate
the level of activity (total number of beam cuts) during the night.
308
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
In addition to this classification, we counted the number of nights of migratory
restlessness during the 60 days of the experiment for each bird.
2.1.3. Spectrographic analysis of male mating calls
The European quail and the Japanese quail share the same vocal repertoire. The only
difference lies in the structure of male mating calls (Fig. 2; Guyomarc’h and Guyomarc’h,
1996) that may act as a behavioural reproductive isolating mechanism in quails
(Derégnaucourt and Guyomarc’h, 2003). In Galliform species, learning has no influence on
vocal development and therefore, male mating call structure reflects a strong genetic
determinism (Konishi and Nottebohm, 1969; Baptista, 1996). Consequently, the presence
of hybrid mating calls would reveal unambiguously the introduction of the European quail
in game farms.
Males of European quail produce two different mating calls (Fig. 2A and B named
‘wawa’ and ‘triplet’ respectively), whereas males of the Japanese subspecies produce only
one (Fig. 2C; Guyomarc’h and Guyomarc’h, 1996). Hybrids produce all the intermediaries
between the three types of parental forms (Fig. 2D–G, Guyomarc’h and Guyomarc’h,
1996; Derégnaucourt et al., 2001). Male mating calls were recorded after the end of the 60day experiment. Each male was placed in a sound-proof box (75 cm 50 cm 30 cm,
with a frontal window that permits direct observation of the bird) at dawn when vocal
activity is maximal (Guyomarc’h and Thibout, 1969). After few minutes to few hours, the
bird started spontaneously to produce mating calls. An observer was present during the
whole session to control the recorder. Some birds that did not call during the first session
were tested again the following days.
All recordings were made with a Marantz CP270 recorder equipped with a dynamic
Sennheiser MD 41 microphone. Spectrograms (graphic representation of the sounds
produced; x-axis: time, y-axis: frequency) were obtained using Sound Analysis 3.0
software (Tchernichovski et al., 2000). Two observers visually classified the spectrograms
in three categories: ‘European-like’, ‘Japanese-like’ and ‘Hybrid-like’. Both observers
reached a 100% agreement in their classification. This result was not surprising since the
different categories are well defined and a similar classification would be even expected
from a naı̈ve observer not familiar with spectrographic analysis.
2.2. Male–male encounters
2.2.1. Birds
Eleven FRB males and 11 males and 11 females of European quail were used for this
experiment. The founders of the strain of European quail (EUR), maintained in our
laboratory, were wild migratory birds caught in France (1983–1984), Spain (1992) and
Portugal (1997).
2.2.2. Experimental procedure
Eleven encounters were performed. Each encounter lasted 4 days. On the first day,
single sexually mature males (cloacal gland developed with foam production) from each
breeding group were placed in an indoor terrarium (2 m 1 m 1.5 m). The ground was
covered with sand and two tufts of grass were provided so that the subordinate male could
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
309
Fig. 2. Spectrograms (spectral derivatives) of male quail mating calls. Each letter indicates the spectrogram of a
different mating call. A and B: ‘wawa’ and ‘triplet’ respectively produced by European quail; C: Japanese quail;
D–G: spectrograms of mating calls produced by four different hybrid males F1; H–K: spectrograms of mating calls
produced by four different quails of the French breeding (FRB); L–O: spectrograms of mating calls produced by
four different quails of the Italian breeding (ITB).
310
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
hide from the aggressor. Natural lighting was supplied through a window. Temperature was
25 8C (2 8C) during this period. Food and water were provided ad libitum. On the third
day, a sexually mature female European quail (length of cloacal vent >5 mm) was
introduced into the terrarium. After the observations on the fourth day, the three birds were
removed from the terrarium and returned to their individual cages. None of the subjects was
injured during these experiments.
2.2.3. Behavioural sampling and notation methods
Observations were performed every day, 2 h after sunrise. Based on previous observations
(Frigola, 1982), it appeared that the period that follows the sunrise is characterized by a high
amount of activity. We used instantaneous and scan sampling (Martin and Bateson, 1993).
The 100 min observation session was divided up into 1 min sample intervals giving 100
sample points. We monitored different behaviours in males and females described elsewhere
(Guyomarc’h and Guyomarc’h, 1996) and classified as: (1) aggressive behaviours: chasing,
the aggressor runs toward the opponent; pecking, aggression with the bill and mounting (in
male–male interaction); (2) defensive behaviours: running away; moving away; ruffling, an
individual swells its feathers when another approaches him; (3) sexual displays: mounting (in
male–female interactions); waltzing, the male lowers one wing and circles around the
female; side display, repeated down-up head movements.
In addition, the position of each individual was noted every 5 min, resulting in 20
measures of inter-individual distance (male–male from day 1 to day 4; male EUR-female and
male FRB-female for day 3 and day 4) per day scored as follows: score 1: 0–0.5 m; score 2:
0.5–1 m; score 3: 1–1.5 m; score 4: 1.5 m (maximal distance was 2.2 m). A mean score of
inter-individual distance per day was obtained by averaging the 20 scores from a session.
2.2.4. Statistical analysis
We used the Wilcoxon non-parametric test (Siegel and Castellan, 1988) to compare (1)
behavioural differences between the males of the two strains; (2) their respective distance
to the female. If data were used for more than one test, then the probability was Bonferroni
adjusted according to the number of tests used (Sokal and Rohlf, 1995). Based on our
behavioural analysis, we appointed a dominant male and a subordinate male for each pair.
The male showing more aggressive behaviour and, after the introduction of the female,
monopolizing her, was designated as the dominant male. The other one, which usually
showed different forms of avoidance was designated as the subordinate one. A Binomial
test was calculated to compare the two strains regarding the difference in their dominance.
The statistical packages Statview 4.0 and Statistica 2.0 were used for all analyses.
3. Results
3.1. Subspecific status of the quails
3.1.1. Nocturnal restlessness
Seventeen males of 27 FRB exhibited nocturnal restlessness. Two of them were
considered as ‘nomads’ as they showed nocturnal restlessness only when they were
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
311
sexually developed. Seven males classified as ‘migrant birds’ showed less than 10 nights of
migratory restlessness. But 6 males out of the 15 ‘migrants’ presented more than 40 nights
of ‘zugunruhe’ during the experiment.
Two male and two female ITB showed nocturnal restlessness and were classified as
‘migrant’ birds. They exhibited 8, 29, 17 and 18 nights of migratory activity respectively.
The others (n = 40) were classified as ‘sedentary’ birds.
3.1.2. Spectrographic analysis of male mating calls
We observed a great inter-individual variability in male mating calls produced by the
FRB quails (Fig. 2H–K). Six males produced mating calls similar to those of the
European quail: five looked like the ‘triplet’ (Fig. 2H; three of them were preceded by a
‘wawa’) and one of them produced only the ‘wawa’. The remaining 21 males produced
hybrid mating calls (Fig. 2I–K). None produced mating calls similar to those of the
Japanese subspecies.
Seventeen male ITB produced mating calls similar to those of the Japanese quail, in
which no trace of introgression of European quail could be found (Fig. 2L). The last five
males produced hybrid mating calls (Fig. 2M–O). It is worth noting that the two ITB males
that showed migratory restlessness produced hybrid mating calls.
3.2. Male–male encounters
Spectrographic analysis of mating calls ensured that the FRB birds we used were
hybrids.
3.2.1. Before the introduction of a female in the terrarium
In 10 cases out of the 11 encounters, the FRB males exhibited more aggressive
behaviours than the EUR males (Fig. 3A, Wilcoxon, z = 2.8, P = 0.004). The latter showed
more defensive postures than their opponents (Fig. 3B, Wilcoxon, z = 2.8, P = 0.004). In
fivr encounters, we observed some sexual displays: four cases involving a FRB male
(circling and side displays) and one case involving a EUR male (side displays). In all cases,
the dominance was established on the first day of the meeting. FRB males dominated EUR
males in 10 out of 11 cases (Binomial test, P = 0.008).
3.2.2. After the introduction of the female
As previously, FRB males were more aggressive than EUR males (Fig. 3A; Wilcoxon,
z = 2.93, P = 0.003), and dominated the latter in all cases. Male European quails exhibited
more defensive behaviours than their opponents (Fig. 3B; Wilcoxon, z = 2.66, P = 0.007).
In addition, the inter-individual distance increased between the males in 7 cases out of 11
after the introduction of the female, but the difference was not significant (Fig. 4A;
comparison between day 2 and day 3, Wilcoxon, z = 0.6, P = 0.11).
In all the encounters, the FRB males presented more sexual displays to the female
than the EUR males (Fig. 5; Wilcoxon, z = 2.93, P = 0.003). Copulation attempts were
observed in nine different pens. In three of them, both EUR males and their respective
FRB counterpart attempted to mount the female on day 3; only the three FRB males
exhibited this behaviour on day 4. In addition, the FRB males were closer to the
312
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
Fig. 3. Aggressive (A) and defensive (B) behaviours exhibited by males (n = 11 encounters) before and after the
introduction of a female in the terrarium (box and whisker plots: median, quartiles, min, max). FRB: hybrid quails
from the French breeding; EUR: European quails. P-values: results of the Wilcoxon test.
females than the EUR males (Fig. 4B; Wilcoxon, z = 2.71, P = 0.007). In seven pens out
of nine, we observed copulation acceptation by the female. Even if some females
showed different forms of avoidance behaviour, none of them was aggressive towards
the males.
Fig. 4. Box and whisker plots (median, quartiles, min, max) of inter-individual distances. (A) Distance between
the male of the French breeding (FRB) and the male of European quail (EUR), before and after the introduction of
a female in the terrarium (n = 11 encounters). (B) Distance between both males and the female of European quail.
P-values: results of the Wilcoxon test.
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
313
Fig. 5. Sexual behaviours exhibited by males towards the female (median, quartiles, min, max). FRB: hybrid
quails form the French breeding; EUR: European quails (n = 11 pairs). P-value: results of the Wilcoxon test.
4. Discussion
Our results demonstrate that hybridization between domestic Japanese quail and
European quail is a practice used in European game farms. Hybridization was
unambiguously revealed by spectrographic analysis of male mating calls. Some males
produced mating calls similar to those of hybrid quails from laboratory bred strains
(Guyomarc’h and Guyomarc’h, 1996; Derégnaucourt, 2000; Derégnaucourt et al.,
2001). Based on spectrographic analysis, we could think that hybridization is
statistically higher in the French breeding (FRB) than in the Italian breeding (ITB) (21/
27 males FRB and 5/22 males ITB produced hybrid mating calls). But based on other
observations (Derégnaucourt, 2000; Derégnaucourt et al., 2001), we know that hybrid
quails can produce mating calls similar to those produced by both parental subspecies.
Thus, mating calls classified as ‘European-like’ or ‘Japanese-like’ could have been
produced by hybrid quails.
Several birds in both samples (15/27 FRB, 4/44 ITB) exhibited migratory impulse. As
this characteristic has been counterselected during the domestication process of the
Japanese quail (Derégnaucourt et al., 2005), its expression clearly demonstrates the
introduction of wild European quails in game farms. Migrant birds presented a great interindividual variability in the number of active nights: from four nights to more than 40
during the 60-day experiment.
It appeared that a majority of the birds of the Italian breeding farm presented
characteristics of the Japanese quail and some of them could be considered as pure ones.
Nevertheless, we revealed some traces of hybridization of Japanese quail with the
314
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
European subspecies. These traces were more apparent in the French breeding, and based
on our behavioural analysis, some of the quails analyzed may be pure European quails
although there was no evidence for this in the Italian sample.
Hybridization of domestic quail with wild European quail may constitute the only step
to improve the quality of birds supplied to hunters. In addition to hybridization, selection of
behavioural characteristics could be practiced, as is the case for the French breeding. Birds
of this strain dominated the males in our breeding of European quail in all the encounters.
Even though we observed an unambiguous dominance of these birds over the European
quails, we cannot claim that this is a direct result of selection of behavioural characteristics
by the breeder. First, it may be due to domestication. Hypersexuality is well known in
domestic birds, expressed as precocious maturation as well as an extended breeding season
and increased number of eggs in females (Sossinka, 1982). This hypersexuality is
accompanied by high levels of aggressive behaviour in male quail (Ishii, 1984). In addition,
a genetic basis of dominance has been shown in Galliforms (Craig et al., 1965; Boag and
Alway, 1981; Nol et al., 1986). Second, there is perhaps a natural tendency of one species
(or subspecies) to dominate the other one (Brodsky et al., 1988). Even though the European
quail and the Japanese quail are sympatric in Mongolia (Kentei Area), there is currently no
data available about hybridization or progression of the breeding range of one subspecies
over the other one (Del Hoyo et al., 1994). Third, the dominance observed here may be the
results of hybridization that may improve the vigour of hybrids (heterosis effect) and
facilitate their dominance (Nadal, 1992). For example, a behavioural heterosis for fear of
man has been evidenced in hybrid duck (muscovy drake Cairina moschata Mallard Anas
platyrhynchos; Faure et al., 2003). Further experiments are required to address these
different hypotheses that are not mutually exclusive. Nevertheless, the FRB birds that we
tested belong to the same pool of birds released in the wild, and we can claim that if they
had been in competition with European quail on their reproductive areas, they would have
dominated them. These released males might monopolize females available in the wild.
Female animals in the presence of conspecific males generally, however, do not accept
allospecific males; a surplus of males would not cause hybridization unless unpaired males
resort to sneak fertilizations and forced copulations with females of other species (Wirtz,
1999). A study on Japanese quail has shown that forced copulations have equivalent
reproductive success to other copulations and so could be a successful male strategy
(Adkins-Regan, 1995). Despite the monogamous mating system of the species
(Guyomarc’h et al., 1998), polypaternity has been observed in the wild (Puigcerver,
1990; Rodriguez-Teijeiro et al., 2003) and may result from forced fertilizations. Moreover,
since some hybrids exhibit characteristics of European quail and may be in some cases
indistinguishable from them (Derégnaucourt et al., 2001), it may increase their likelihood
to attract European females and thenceforth to facilitate the introgression of Japonica
genes into the natural populations. These observations and results of previous experiments
at both prezygotic (sexual selection; Derégnaucourt and Guyomarc’h, 2003) and
postzygotic (hybrid fecundity and viability; Derégnaucourt et al., 2002) levels highlight the
risks of hybridization in the wild.
The development of hybridization in game farms could be for two reasons. First, the
legislation does not clearly authorize the breeding of the European quail in the European
community (Guyomarc’h, 2003). Second, there is a perception among hunters that captive-
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
315
bred individuals are of inferior quality to wild ones, particularly in terms of vigour, antipredatory or mating behaviour (Nadal, 1992).
Large numbers of domestic quails are released in Europe each year. Released quails
could mate with the rare long migrant that still arrives north of the 40th parallel. Moreover,
they may have contributed to the development of sedentary western populations
(Guyomarc’h, 2003; Derégnaucourt et al., 2005). Hybrid quails that show migratory
activity might be able to leave the spots of release and may reach other areas where such
releases are not practiced, especially favourable habitats in Maghreb that constitute for the
time being the ‘natural reservoir’ of the European quail. These hypotheses are a strong
invitation to tighten up the controls of game farms and stop the releasing of domestic quails
in the field.
5. Conclusion
Our results show that wild European quails have been introduced in domestic Japanese
quail game farms in Europe. This was demonstrated unambiguously by the presence of
hybrid male mating calls in one French and one Italian game farm. Expression of migratory
activity in birds raised in game farms is another evidence of the introgression of European
quail genes in the domestic strains. Moreover, in male–male encounters in the presence of a
female European quail, hybrid males from the French game farm always dominated the
male of European quail. This superiority may be a consequence of hybridization,
domestication, or the result of a selective process of behavioural characteristics by the
breeders to improve the quality of game birds released in the wild.
Acknowledgements
This project was supported by the Office National de la Chasse et de la Faune Sauvage
(convention 97/27). We thank Thierry Lints and Olga Fehér for reviewing our English
manuscript.
References
Adkins-Regan, E., 1995. Predictors of fertilization in the Japanese quail, Coturnix japonica. Anim. Behav. 50,
1405–1415.
Baptista, L.F., 1996. Nature and its nurturing in avian vocal development. In: Kroodsma, D.E., Miller, E.H.
(Eds.), Ecology and Evolution of Acoustic Communication in Birds. Cornell University Press, Ithaca, pp.
39–60.
Berthold, P., 1973. Relationships between migratory restlessness and migration distance in six Sylvia species. Ibis
115, 594–599.
Boag, D.A., Alway, J.H., 1981. Heritability of dominance status among Japanese quail: a preliminary report. Can.
J. Zool. 59, 441–444.
Brodsky, L.M., Ankney, C.D., Dennis, D.G., 1988. The influence of male dominance on social interactions in
black ducks and mallards. Anim. Behav. 36, 1371–1378.
316
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
Craig, J.V., Ortman, L.L., Guhl, A.M., 1965. Genetic selection for social dominance ability in chickens. Anim.
Behav. 13, 114–131.
Del Hoyo, J., Elliott, A., Sargatal, J., 1994. Handbook of the Birds of the World, vol.2. Lynx Edicions, Barcelona.
Derégnaucourt, S., 2000. Hybridation entre la Caille des blés (Coturnix coturnix coturnix) et la Caille japonaise
(Coturnix coturnix japonica). Mise en évidence des risques de pollution génétique des populations naturelles
par les cailles domestiques. Ph.D. Thesis. University of Rennes.
Derégnaucourt, S., Guyomarc’h, J.-C., 2003. Mating call discrimination in female European (Coturnix c. coturnix)
and Japanese quail (Coturnix c. japonica) Ethology 109, 107–119.
Derégnaucourt, S., Guyomarc’h, J.-C., Aebischer, N., 2002. Hybridization between European quail (Coturnix c.
coturnix) and Japanese quail (Coturnix c. japonica) Ardea 90, 15–21.
Derégnaucourt, S., Guyomarc’h, J.-C., Belhamra, M., 2005. Comparison of migratory tendency in European
Quail Coturnix c. coturnix, domestic Japanese Quail Coturnix c japonica and their hybrids. Ibis 147,
25–36.
Derégnaucourt, S., Guyomarc’h, J.-C., Richard, V., 2001. Classification of hybrid crows in Quail using Artificial
Neural Networks. Behav. Proc. 56, 103–112.
Duncan, R.P., Blackburn, T.M., Sol, D., 2003. The ecology of bird introductions. Annu. Rev. Ecol. Evol. Syst. 34,
71–98.
Echelle, A.A., Connor, P.J., 1989. Rapid, geographically extensive genetic introgression after secondary contact
between two pupfish species (Cyprinodon, Cyprinodontidae). Evolution 43, 717–727.
Faure, J.M., Val-Laillet, D., Guy, G., Bernadet, M.-D., Guémené, D., 2003. Fear and stress reactions in two species
of duck and their hybrid. Horm. Behav. 43, 568–572.
Follett, B.K., Maung, S.L., 1978. Rate of testicular maturation in relation to gonadotrophin and testosterone
levels in quail exposed to various artificial photoperiods and to natural daylengths. J. Endocrinol. 78,
267–280.
Frigola, P., 1982. Etude quantitative au laboratoire de comportements liés à la territorialité chez la Caille:
distance inter-individuelle et forme d’expression du chant au début de la reproduction. Graduate
Report.
Goodman, S.J., Barton, N.H., Swanson, G., Abernethy, K., Pemberton, J.M., 1999. Introgression through rare
hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland.
Genetics 152, 355–371.
Guyomarc’h, C., Guyomarc’h, J.-C., 1992. Sexual development and free running period in quail kept in constant
darkness. Gen. Comp. Endocrinol. 86, 103–110.
Guyomarc’h, C., Guyomarc’h, J.-C., Saint Jalme, M., 1990. Potentialités reproductrices chez les jeunes cailles des
blés Coturnix coturnix coturnix. Cahiers d’Ethologie Appliquée 10, 125–142.
Guyomarc’h, J.-C., 2003. Elements for a Common Quail (Coturnix c. coturnix) management plan. Game Wildl.
Sci. 20, 1–92.
Guyomarc’h, J.-C., Belhamra, M., 1998. Effets de la sélection sur l’expression des tendances sexuelles et
migratoires chez une population captive de caille des blés (Coturnix c. coturnix L.) Cahiers d’Ethologie 18, 1–
16.
Guyomarc’h, J.-C., Guyomarc’h, C., 1996. Vocal communication in European quail; comparison with Japanese
quail. C. R. Acad. Sci. Paris 319, 827–834.
Guyomarc’h, J.-C., Thibout, E., 1969. Rythmes et cycles dans l’émission du chant chez la Caille japonaise
(Coturnix c. japonica) Revue de Comportement Animal 3, 37–49.
Guyomarc’h, J.-C., Combreau, O., Puigcerver, M., Fontoura, P., Aebischer, N., 1998. Coturnix coturnix Quail.
Birds of Western Palaearctic Update 2. Oxford University Press, Oxford, pp. 27–46.
Haffner, P., 1997. Bilan des introductions récentes d’Amphibiens et de Reptiles dans les milieux aquatiques
continentaux de France métropolitaine. Bull. Fr. Pêche Piscic. 344, 155–163.
Howes, J.R., 1964. Japanese quail as found in Japan. Quail Quat. 1, 19–30.
Hoysak, D.J., Ankney, D., 1996. Correlates of behavioural dominance in Mallards and American Black Ducks.
Anim. Behav. 51, 409–419.
Hughes, B., 1996. The Ruddy Duck (Oxyura jamaicensis) in Europe and the threat to the White-headed Duck
(Oxyura leucocephala): a review, an evaluation and conservation actions. Gibier Faune Sauvage 13, 1127–
1141.
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
317
Ishii, S., 1984. Endocrine control of aggressive behavior in male and female Japanese quail. In: Aoki, K., Ishii,
S., Morita, H. (Eds.), Animal Behavior: Neurophysiological and Ethological Approaches. Japan Scientific
Societies Press, Tokyo, pp. 22–234.
Johnsgard, P.A., 1988. The Quails, Partridges and Francolins of the World. Oxford University Press,
Oxford.
Jones, R.B., Mills, A.D., Faure, J.M., Williams, J.B., 1994. Restraint, fear and distress in Japanese quail selected
for long or short tonic immobility reactions. Physiol. Behav. 56, 529–534.
Konishi, M., Nottebohm, F., 1969. Experimental studies in the ontogeny of avian vocalizations. In: Hinde, R.A.
(Ed.), Bird Vocalizations. Cambridge University Press, Cambridge, pp. 29–48.
Labisky, R.F., 1961. Report of attempts to establish Japanese quail in Illinois. J. Wildl. Manage. 25, 290–
295.
Lepori, N.G., 1964. Primi dati sugli ibridi di Coturnix c. japonica Coturnix c. coturnix ottenuti in allevamento.
Rivu Italian Ornithologica 2, 192–198.
Lucotte, G., 1977. La caille de tir. Crépin-Leblond, Paris.
Marin, R.H., Satterlee, D.G., 2003. Selection for contrasting adrenocortical responsiveness in
Japanese quail (Coturnix japonica) influences sexual behaviour in males. Appl. Anim. Behav. Sci. 83,
187–199.
Martin, P., Bateson, P., 1993. Measuring Behaviour: An Introductory Guide, 2nd ed. Cambridge University Press,
Cambridge.
Mills, A.D., Faure, J.M., 1991. Divergent selection for duration of tonic immobility and social reinstatement
behaviour in Japanese quail (Coturnix coturnix japonica) chicks. J. Comp. Psychol. 105, 25–38.
Mills, A.D., Crawford, L.L., Domjan, M., Faure, J.M., 1997. The behavior of the Japanese or Domestic Quail
(Coturnix japonica). Neurosc. Biobehav. Rev. 21, 261–281.
Nadal, J., 1992. Problemàticas de las poblaciones de perdiz roja, bases ecoetologicas para tener exito con las
repoblaciones. Fundacion la Caixa, editorial Aedos, Barcelona.
Nichols, C.R., 1991. A comparison of the reproductive and behavioural differences in feral and domestic Japanese
quail. Ph.D. Thesis. University of British Columbia.
Nol, E., Cheng, K., Nichols, C., 1986. Heritability and phenotypic correlations of behaviour and dominance rank
of Japanese quail. Anim. Behav. 52, 813–820.
Pala, M., Lissia-Frau, A.M., 1966. Ricerche sulla sterilita degli ibridi tra la quaglia giaponese (Coturnix c.
japonica) e la quaglia europea (Coturnix c. coturnix) Rivu Italian Ornithologica 2, 4–9.
Potts, D., 1988. The impact of releasing hybrid Partridges on wild Red-Legged populations. The Game
Conservancy Review of 1988, pp. 81–85.
Puigcerver, M., 1990. Contribucion al conocimiento de la bioilogia y ecotologia de la Codurniz (Coturnix
coturnix). Ph.D. Thesis. University of Barcelona.
Puigcerver, M., Rodriguez-Teijeiro, J.D., Gallego, S., 1989. Migracion y/o nomadismo en la codorniz (Coturnix
coturnix). Etologia 1, 39–45.
Rhymer, J.M., Simberloff, D., 1996. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27, 83–
109.
Rhymer, J.M., Williams, M.J., Braun, M.J., 1994. Mitochondrial analysis of gene flow between New Zealand
Mallards (Anas platyrhynchos) and Grey Ducks (A. superciliosa) Auk 111, 970–978.
Rizzoni, R., Lucchetti, L., 1972. Elevage et utilisation de la Caille domestique. La Maison Rustique, Paris.
Rodriguez-Teijeiro, J.D., Puigcerver, M., Gallego, S., Cordero, P.J., Parkin, D.T., 2003. Pair bonding and multiple
paternity in the polygamous Common Quail Coturnix coturnix. Ethology 109, 291–302.
Sachs, B.D., 1969. Photoperiodic control of reproductive behavior and physiology of reproductive behavior and
physiology of the male Japanese quail. Horm. Behav. 1, 7–24.
Schwartz, C.W., Schwartz, E.R., 1949. A Reconnaissance of Game Birds in Hawaii. Hawaii Board of Commissioners of Agriculture and Forestry, Hawaii.
Siegel, S., Castellan, N.J., 1988. Nonparametric Statistics for the Behavioral Sciences, 2nd ed. McGraw-Hill
Book Company, New York.
Sokal, R.R., Rohlf, F.J., 1995. Biometry, 2nd ed. W.H. Freeman and Company, New York.
Sossinka, R., 1982. Domestication in birds. In: Farner, D.S., King, J.R., Parkes, K.C. (Eds.), Avian Biology.
Academic Press, New York, pp. 373–403.
318
S. Derégnaucourt et al. / Applied Animal Behaviour Science 94 (2005) 303–318
Tchernichovski, O., Nottebohm, F., Ho, C.E., Pesaran, B., Mitra, P.P., 2000. A procedure for an automated
measurement of song similarity. Anim. Behav. 59, 1167–1176.
Thulin, C.-G., Jaarola, M., Tegelström, H., 1997. The occurrence of mountain hare mitochondrial DNA in wild
brown hares. Mol. Ecol. 6, 463–467.
Verspoor, E., Hammar, J., 1991. Introgressive hybridization in fishes: the biochemical evidence. J. Fish Biol. 39,
309–334.
Wetherbee, D., Jacobs, K.F., 1961. Migration of the common Coturnixin North America. Bird Banding 32, 85–91.
Wirtz, P., 1999. Mother species–father species: unidirectional hybridization in animals with female choice. Anim.
Behav. 58, 1–12.
Youngson, A.F., Webb, J.H., Thompson, C.E., Knox, D., 1993. Spawning of escaped farmed Atlantic Salmon
(Salmo salar): hybridization of females with brown trout (Salmo trutta). Can. J. Fish. Aqua. Sci. 1980–1990.