Responses of Young Red Jungle Fowl (Gallus gallus) and White Leghorn Layers to Familiar and Unfamiliar Social Stimuli

Responses of Young Red Jungle Fowl (Gallus gallus) and White Leghorn Layers to Familiar and Unfamiliar Social Stimuli J. Va¨isa¨nen and P. Jensen1 Department of Biology, IFM, University of Linko¨ping, SE-581 83 Linko¨ping, Sweden were observed in an open field for 10 min (pair test). In the first runway test, clear preference for familiar chicks and avoidance of unfamiliar social stimuli was found only in Leghorns, whereas both breeds showed a preference for their own breed members in the second runway test. Affiliation to the familiar breed, however, was more pronounced in Leghorns. In the pair test, Leghorns were significantly more involved in agonistic interactions than wild-type chicks. Avoidance of unfamiliar and preference for familiar conspecifics might suggest a weaker capacity of Leghorns to cope with novel social and environmental stimuli, which might have implications for the welfare of the birds in production environments when encountering unfamiliar individuals.

ABSTRACT Social preferences of familiar over unfamiliar social stimuli in chicks may be used to measure sociality, a characteristic important for the welfare of poultry in commercial production. We studied social preferences and reaction to strangers in young White Leghorns and red jungle fowl (Gallus gallus) in 3 tests. All chicks were raised and housed in 2 groups of 34 individuals per breed. At 24 to 29 d of age 38 chicks per breed were tested in 2 runway tests. In the first, chicks had a free choice between familiar and unfamiliar breed members, and in the second the choice was between unfamiliar chicks of their own breed and the other breed. On d 41 to 42, spacing and agonistic interactions of 28 pairs of chicks per breed (in half of the pairs, chicks were unfamiliar to each other)

(Key words: coping, jungle fowl, layer, production, social preference) 2004 Poultry Science 83:335–343

Social motivation in fowl is sensitive to genetic selection (Jones and Mills, 1999). It is thought to influence all aspects of social cognition and interaction processes, such as cohesion, affiliation, attachment, aggression, and behavioral responses to disruption of social environment. Thus, individual variation in social motivation and social discrimination capacity may have important implications for the welfare of fowl in the production environments. Comparisons of social behavior and social discrimination among different lines of fowl may give more insight into the internal and external factors behind the elicitation and reduction of social stress (Jones et al., 1996). These comparisons might further be helpful in determining if selection for appropriate social characteristics in breeding could alleviate harmful effects of exposure to certain social stressors present in modern housing systems. A recent study carried out by Va¨isa¨nen and Jensen (2003) revealed that intensive selection for production seems to have influenced interaction between coping capacity and social motivation in chicks of a modern layer strain. When White Leghorn chicks were compared with red jungle fowl, the ancestor of all modern domestic poultry breeds (Fumihito et al., 1994), it was found that in a

INTRODUCTION In domestic fowl (Gallus gallus) social bonding to flock members and establishment of a rank order is based on recognition and discrimination (Guhl, 1962; Syme et al., 1983; Doyen, 1987; Zayan, 1987; Jones et al., 1996). However, laying hens kept in intensive production are often imposed to social environments differing greatly from the relatively stable, small groups with an elaborate hierarchical social organization found in wild and feral conspecifics (McBride et al., 1969; Collias and Collias, 1996; Jones et al., 1996). Crowding, alteration of group membership, and large stocks exceeding the social recognition capacity often disturb or completely prevent natural social relationships between the birds and cause potentially harmful effects (Jones et al., 1996; Hughes et al., 1997). For instance, group disruptions increase aggressive encounters (Wood-Gush, 1989; Cloutier and Newberry, 2002) and cause a high degree of social stress in fowl (Candland et al., 1969; Gross and Siegel, 1983; Anthony et al., 1988).

2004 Poultry Science Association, Inc. Received for publication April 24, 2003. Accepted for publication October 13, 2003. 1 To whom correspondence should be addressed: per.jensen@ifm. liu.se

Abbreviation Key: F = familiar chicks; O = other breed; S = same breed; SLU13 = White Leghorn strain; U = unfamiliar chicks.

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short (5 min) runway test, jungle fowl chicks were more prone to stay near conspecifics. However, in behavioral tests of a longer duration wild-type chicks were better able to adapt to stressful elements such as environmental novelty and food deprivation. They, for instance, performed more exploration and foraging out of sight of companion birds, whereas Leghorns responded more passively. Leghorn chicks also showed greater social aggregation with a higher level of immobilization than jungle fowl in an open field. After regrouping adult birds of the same 2 genetic strains with unfamiliar breed members, Va¨isa¨nen et al. (2003) found increased and prolonged levels of aggression among Leghorns, suggesting they have poorer ability to cope with group disruptions than jungle fowl. Hens kept in relatively small groups discriminate between members of their own social group and unfamiliar individuals (Dawkins, 1982; Bradshaw, 1991; Grigor et al., 1995) and show a strong preference for own group members in a free-choice situation (Hughes, 1977; Bradshaw, 1992). Social discrimination is present already in very young chicks before the ages of 6 to 10 wk when pecking orders are established (Guhl, 1958; Rushen, 1982; Vallortigara, 1992; Marin et al., 2001). In domestic chicks preferences over familiar vs. unfamiliar social stimuli have been proposed to reflect an underlying level of social motivation and a degree of attachment to conspecifics (Cailotto, 1989; Vallortigara et al., 1990; Jones et al., 1996), features that can further be affected by stress (Marin et al., 2001). Nevertheless, studies comparing social discrimination and preferences between different breeds are scarce in fowl. Earlier studies have mainly focused on a related species, Japanese quail (Corturnix japonica) (Jones et al., 1996; Carmichael, 1998; Franc¸ois et al., 2000). The aim of this study was to investigate differences in social preferences between red jungle fowl and White Leghorn layer chicks from 24 to 42 d of age. Chicks of each breed were subjected to 2 runway tests. In the first, they were simultaneously exposed to familiar vs. unfamiliar breed members and, in the second, to unfamiliar breed members vs. unfamiliar chicks from the other breed as 2 alternatives of free choice. In addition, chicks were introduced to an open field in the presence of a familiar or an unfamiliar bird of the same breed. In light of the previous studies, Leghorn chicks were predicted to affiliate more to the familiar social stimuli in novel test environments, whereas the jungle fowl were expected to be more explorative toward unfamiliar social companions and the environment.

MATERIALS AND METHODS

2002). The present study was a part of the phenotypic characterization of these stocks. The red jungle fowl descended from a Swedish zoo population originating from Thailand (Schu¨tz et al., 2001). The White Leghorn strain (SLU13) is a result of a Scandinavian selection and crossbreeding experiment with a well-defined breeding background (Liljedahl and Weyde, 1980). SLU13 has a long history of simultaneous selection for high number of eggs and egg mass under suboptimal nutrition conditions that favor effective feed utilization. With these same constant selection criteria, SLU13 is presently maintained at the Swedish University of Agricultural Sciences.

Rearing and Housing of Birds Eggs from both breeds were artificially incubated and hatched simultaneously under identical conditions at Go¨tala research station in Skara, Sweden. At 4 d of age, chicks were randomly assigned to 2 experimental groups per breed labeled as JF1 and JF2 (jungle fowl) and WL1 and WL2 (White Leghorn), each consisting of 34 nonsexed individuals. All 4 groups of chicks were reared identically on wood shavings. They had audible but no visual contact with birds in the other groups. Until the 19th day of age, each group was kept in circular brooders measuring 93 × 62 cm (diameter × height), after which they were kept in pens measuring 1.5 × 1.5 m (width × length). The chicks were maintained on commercial chick starter food and fresh water ad libitum and exposed to a light cycle of 13L:11D. Additional heat was provided up to 7 wk of age, and perches were available from 32 d of age onward.

Experimental Procedures Pretest Treatment. All chicks were marked individually with plastic identity labels (3.6-cm length × 1.5-cm width × 0.3-mm thickness) at 6 d of age. The labels were attached carefully through the neck skin with a plastic thread (0.5 mm thick) that caused no obvious discomfort to the chicks. Within each experimental group, 15 chicks were randomly assigned to be used as stimulus chicks in the forthcoming runway tests. Within each group stimulus chicks were divided randomly into five trios; to facilitate their identification, they were marked with leg bands of 5 different colors before each runway test. All chicks were sexed at the age of 40 d. The sex ratios (females per males) of test chicks and stimulus chicks were 20/18 and 16/14 for Leghorns and 22/16 and 20/ 10 for jungle fowl.

Preference of Familiar Vs. Unfamiliar Chicks

Birds In the present study birds from 2 different breeds of poultry, a White Leghorn layer and red jungle fowl, were used. Only 1 strain of Leghorn and 1 population of jungle fowl were used because these particular stocks are a target of a large-scale molecular genetics study (Schu¨tz et al.,

Test Arena. The purpose of this test was to measure the birds’ degrees of preference for familiar vs. unfamiliar chicks of the same breed. This measurement was done by recording the behavior in a runway where the opposite ends were connected to cages containing familiar or unfamiliar chicks. The runway was situated in a separate room

SOCIAL PREFERENCES OF WILD- AND LAYER-TYPE FOWL

with a constant temperature of 24°C and a light intensity above the test arena of 120 lx. The runway was a straight corridor (2.1-m length × 0.5-m width × 0.5-m height) made of 5 mm thick solid plywood walls and a floor. The corridor was divided, by solid sliding doors on either side of the start zone, into a 50 cm long midsection (start zone) and 2 side sections. Each section was roofed with a wire mesh lid. Wire mesh screens separated stimulus bird boxes (both measuring 0.5 × 0.5 × 0.5 m) from the corridor at opposite ends of the runway. Otherwise, the boxes consisted of solid plywood and were equipped with wire mesh lids. The floors of the boxes were covered with a 3 cm thick layer of clean wood shavings. The borders outlining the start zone as well as 25 cm wide areas (close zones) at both ends of the corridor in front of the stimulus bird boxes were marked with black adhesive tape stripes. Except on the marking stripes, the whole runway corridor was covered with a 2.5-cm layer of clean wood shavings. Test Procedure. At 24 to 26 d of age 19 chicks per experimental group (38 chicks per breed), were tested individually and once only in the runway. The tests took 3 d and were evenly spread out between 0715 and 1600 h every day. In the beginning of each block of 2 tests, a stimulus chick trio from each experimental group of the same breed was gently placed into the opposing stimulus bird boxes and allowed a 2-min acclimatization period. Before each test the stimulus chicks were activated by moving a hand carefully among them a few seconds. Right after this, a randomly chosen test chick from either of the experimental groups of the particular breed was placed in the start zone, and the sliding doors were removed. Timing started when the doors were fully opened. Each test lasted for 10 min and was recorded on video, from which the following measures were taken: initial direction of travel [familiar stimulus chicks (F); unfamiliar stimulus chicks (U)] defined as an entry to either of the side sections, the latencies to enter zones close to familiar and unfamiliar chicks (chicks that did not enter a particular zone during the test were assigned a latency of 600 s for that variable), number of entries into each close zone, cumulative time spent in the zone, and number of transitions from one zone to another. In addition, the percentage of time spent in zones close to familiar chicks and unfamiliar was calculated in percentage of test time left after the first entry to a zone (later referred to as tendency to stay in zones F and U). The runway was cleaned after each test, and the tested chick was marked with a leg band before returning it to the home pen. The second test chick of the test block was selected from the other experimental group of the same breed. After each block of 2 tests, the stimulus chick trios were returned to their home pens and two chicks from the other breed were tested. Stimulus chicks were reused in a systematic order over the whole course of testing.

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Microsoft Corp., Redmond, WA.

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The testing procedure as well as the use of stimulus bird boxes was fully balanced between experimental groups within and between the breeds.

Preference of Own Vs. Other Breed Test Procedure. The purpose of this test was to measure the chicks’ preferences for birds of the same breed over birds of another breed. This test was done by recording the behavior in a runway where the opposite ends were connected to cages containing unfamiliar chicks of the same breed as the test bird or of the other breed. The chicks were tested at the age of 27 to 29 d in the same runway and under conditions as described above. The test procedure was identical to that of the first runway test with the exception that both stimulus chick trios used in each block of 2 tests came from experimental groups other than the test chicks. The 2 test chicks within each test block always represented both breeds. Same breed is later referred to with S and the other breed with O.

Data Treatment and Analyses The Kolmogorov-Smirnov test of normality was used to test the normality of the distribution of all data from both runway tests. The preference for initial direction of travel (F or U and S or O) was compared within breeds with a binomial test and between breeds using a χ2 test (Minitab 12.21).2 The other variables, which were not normally distributed, were subjected to nonparametric Kruskal-Wallis test for analyses of the breed effects and within-breed sex effects. In addition, within each breed the nonparametric Mann-Whitney U-test was used to examine the effect of familiarity vs. unfamiliarity or own breed vs. other breed on latency to enter zones F and U or S and O as well as on time spent, tendency to stay, and times visited in each zone. Results are presented as mean ± standard error of the mean (SEM).

Pair Test Test Arena. The purpose of this test was to measure the behavior of chicks in a large novel arena where they were allowed to roam freely in the companionship of a familiar or an unfamiliar chick of the same breed. The arena was a 3.0- × 3.5-m pen, which was situated in a separate test room where light intensity was 40 to 45 lx, and temperature was 23°C. The pen had solid plywood walls as short sides, concrete wall as one long side, and wire mesh as the other. To aid in recordings, the floor of the pen was divided into 6 zones (50 cm wide) marked with black adhesive tape stripes parallel to the short sides. The floor was covered with a thin layer of clean wood shavings except on the marking stripes. Test Procedure. At 41 to 42 d of age, 16 female and 12 male pairs per breed were tested over 2 d in the test pen. Each bird was tested once only. Half of the pairs per each sex within each breed consisted of chicks from the

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same experimental group, and the other pairs consisted of birds from different experimental groups. Within this limitation, the selection of the test pairs was randomized. The tests were evenly spread out between 0700 and 1700 h, and the pairs were tested in a balanced manner with respect to breed, sex, experimental group, and familiarity vs. nonfamiliarity. At the beginning of each test, a chick pair was placed in the middle of the test pen at 20 cm from each other, and direct behavioral recordings started 20 s later. During a 10-min test period the distance between the 2 chicks was recorded with instantaneous sampling (Martin and Bateson, 1993) at 10-s intervals. At less than 1 m, distances were estimated to the nearest 10 cm, and distances over 1 m were estimated to the nearest 0.5 m up to 2 m, beyond which no further estimation was done. The occurrence of distress calls (Kruijt, 1964) was recorded by 1/0 sampling (Martin and Bateson, 1993) at pair level during each 10 s bout between instantaneous observation points. In addition, each occurrence of the following social behaviors was recorded using behavioral and continuous sampling methods (Martin and Bateson, 1993): 1. Aggressive peck: fast vigorous peck directed to an anterior part of another bird (Kruijt, 1964). 2. Nonaggressive peck: pecking or manipulating gently at other bird’s feathers. 3. Leap: jumps at another bird; may kick the other bird simultaneously (Kruijt, 1964). 4. Threat: stiff body posture in front of another bird less than 25 cm away with neck feathers lifted (Kruijt, 1964). 5. Attack: moves rapidly toward another bird preceding a leap or an aggressive peck. Neck feathers may be lifted. 6. Chase: follows another bird. Both birds are running. After each test, the tested pair was marked with colored leg bands before returning them to their home groups, and the test arena was cleaned.

Data Treatment and Analyses The results were analyzed at the pair level so that each pair constituted one statistical unit (28 pairs/breed). The distance data were pooled in the following categories: <10 cm, 10 to 40 cm, 40 to 100 cm, and >100 cm to facilitate the statistical analyses. All data were tested for normal distribution using Kolmogorov-Smirnov test. Arcsinesquare root transformation was applied to distance variable >100 cm and square root transformation to all social behavior variables to allow a parametric analysis by ANOVA (general linear model, Minitab 12.21). The model analyzed the main effects of breed, familiarity, and sex as well as the interactive effects of familiarity and sex with breed on all variables. Moreover, within each breed the effects of familiarity and sex were examined. All deviations from mean values are given as standard error of the mean.

Ethical Note The present study was approved by the local Ethical Committee of the Swedish National Board of Laboratory Animals. The Committee assesses the welfare of the animals in relation to the purpose of the study and the possibility for the problem to be solved without the use of experimental animals and ascertains that the experiment is not an unnecessary repetition of previous experiments. No adverse effects on the welfare of the chicks were observed to result from marking or behavioral test procedures.

RESULTS Preference of Familiar Vs. Unfamiliar Chicks In Leghorns there was a clear preference for zone F (close to familiar chicks) compared with zone U (close to unfamiliar chicks). Leghorn chicks spent significantly more time in total in zone F (Figure 1), and their tendency to stay in zone F after the first entry was much greater compared with zone U (Figure 2). A tendency among Leghorn chicks to make more entries into zone F than zone U was also found (1.90 ± 0.36 vs. 1.26 ± 0.29 entries per test in F vs. U; P = 0.089). No preference for either of the zones was found in jungle fowl chicks (P > 0.05). Compared with jungle fowl, Leghorn chicks spent more time in zone F (Figure 1) and entered zone F earlier and more frequently (1.90 ± 0.36 vs. 1.21 ± 1.30 entries per test; P = 0.05). There was no difference between or within breeds in the preference of initial direction of travel (P > 0.05). A nonsignificant tendency for more transitions from one end of the runway to another was found for Leghorns compared with jungle fowl chicks (1.47 ± 0.40 vs. 0.61 ± 0.19 transitions per test, P = 0.097). Leghorn females entered earlier and stayed longer in zone U than the males of this breed (Figure 1). In contrast, jungle fowl females had a longer latency to reach zone U than the males. Sex did not affect any other variables studied.

Preference of Own Vs. Other Breed The preference for initial direction of travel did not differ between the breeds (P > 0.05). In Leghorns, direction S (own breed) was highly preferred to O (other breed) (S = 25 choices vs. O = 5 choices; P < 0.001), and jungle fowl showed a similar trend (S = 18 choices vs. O = 9 choices; P = 0.122). Chicks from both breeds preferred zone S to O. They entered zone S earlier and spent more time in there compared with zone O (Figure 3). Leghorn chicks had a significantly stronger tendency to remain in zone S after the first entrance compared to zone O (Figure 4). A similar trend, although not significant, was observable also in jungle fowl chicks across these variables. The latency to reach zone S was lower for the Leghorns (Figure 3), and they spent more time in zone S in comparison with jungle fowl chicks.

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FIGURE 1. Latencies to enter familiar (F) and unfamiliar (U) zones as well as times spent in zones F and U in the first runway test by female (n = 20/22; Leghorn/jungle fowl) and male chicks (n = 18/16; Leghorn/jungle fowl) of each breed (mean number of s ± SEM). Comparison between breeds (dashed lines) and within breeds (solid lines) include all chicks/breed (n = 38), comparison between sexes (bars) is within each breed. Significances (aKruskal-Wallis test , bMann-Whitney U-test), *P < 0.05, **P < 0.01.

The latency to enter zone O was influenced by sex for both breeds (Figure 4). Leghorn males entered zone O later than females, which was opposite to what was found with jungle fowl. Leghorn females and jungle fowl males also spent more time in zone O than the respective sexes of these breeds. No effect of sex was found on the other variables.

FIGURE 2. Tendency to stay in familiar (F) and unfamiliar (U) zones in the first runway test by Leghorn and jungle fowl chicks (n = 38) (mean % ± SEM). Comparison within breeds with Mann-Whitney Utest. Significances **P < 0.01.

Pair Test Results from the ANOVA are shown in Table 1. In comparison with jungle fowl, Leghorn chicks emitted significantly more aggressive pecks and performed more leaps, threats, attacks, and chases. Leghorn chicks were also found significantly more often at distances >100 cm from one another than jungle fowl. Furthermore, there was a trend for Leghorn chicks to spend more time at distances 40 to 100 cm compared with wild-type chicks. Familiarity did not influence any of the studied variables in overall, but within-breed analysis revealed a nonsignificant tendency for familiar pairs of Leghorns to stay more at distances >100 cm from each other compared with unfamiliar pairs (18.7 ± 3.3 vs. 13.3 ± 3.5% of observations). Jungle fowl chicks familiar to each other showed significantly more chasing (0.36 ± 0.17 vs. 0.00 ± 0.00 chases per test) and had a tendency to perform more attacks (0.93 ± 0.37 vs. 0.43 ± 0.23 attacks per test) compared with unfamiliar pairs. Breed and familiarity interaction tended to influence the occurrence of threats (11.86 ± 3.99 vs. 5.36 ± 2.22 and 1.14 ± 0.52 vs. 2.14 ± 0.83 threats per test in unfamiliar vs. familiar pairs of Leghorns and jungle fowl, respectively). Males gave more aggressive pecks (2.50 ± 0.92 vs. 0.63 ± 0.30 and 0.42 ± 0.23 vs. 0.00 ± 0.00 aggressive pecks per test in male vs. female pairs of Leghorn and jungle fowl, respectively) than females (Table 1). Likewise, males from both breeds threatened more (16.42 ± 4.13 vs. 2.75 ± 1.52 and 3.58 ± 0.87 vs. 0.19 ± 0.14 threats per test in male vs. female pairs of Leghorn and jungle fowl, respectively),

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FIGURE 3. Latencies to enter zones with the same (S) breed and with the other (O) breed as well as times spent in zones S and O in the second runway test by female (n = 20/22; Leghorn/jungle fowl) and male chicks (n = 18/16; Leghorn/jungle fowl) of each breed (mean time in s ± SEM). Comparison between breeds (dashed lines) and within breeds (solid lines) include all chicks/breed (n = 38), comparison between sexes (bars) is within each breed. Significances (aKruskal-Wallis test, bMann-Whitney U-test), *P < 0.05, ***P ≤ 0.001, ****P < 0.0001.

attacked more (8.75 ± 2.32 vs. 3.56 ± 0.96 and 1.33 ± 0.43 vs. 0.19 ± 0.10 attacks per test in male vs. female pairs of Leghorn and jungle fowl, respectively), and chased more (4.83 ± 1.81 vs. 1.00 ± 0.34 and 0.42 ± 0.19 vs. 0.00 ± 0.00 chases per test in male vs. female pairs of Leghorn and jungle fowl, respectively) than females. Furthermore, in

Leghorn chicks, but not jungle fowl, leaping was significantly more frequent among male than female pairs (3.58 ± 1.33 vs. 0.44 ± 0.32 leaps per test). Jungle fowl males tended to deliver nonaggressive pecks more than females (5.50 ± 1.39 vs. 3.06 ± 1.36 nonaggressive pecks per test), which was not the case with Leghorns. Among Leghorn pairs, a trend for more distress calls were found for females compared with males (75.0 ± 5.9% vs. 57.4 ± 7.9% of observation bouts).

DISCUSSION

FIGURE 4. Tendency to stay in zones with the same (S) breed and with the other (O) breed in the second runway test by Leghorn and jungle fowl chicks (n = 38) (mean % ± SEM). Comparison within breeds with Mann-Whitney U-test. Significances ****P < 0.0001.

Social preferences for familiar vs. unfamiliar breed members and the degree of attachment to familiar vs. unfamiliar social companions differed notably between the breeds in the runway tests. This finding might be explained by possible differences in their social discrimination ability. On the other hand, the stronger affiliation to familiar and avoidance of unfamiliar social stimuli shown by Leghorns could indicate a poorer ability to cope with stressful events such as novelty of social companions and environment. Jungle fowl, instead, might have a greater tendency to explore new environmental and social stimuli in general. Moreover, in the pair test Leghorns preferred social interaction under novel circumstances, whereas jungle fowl perhaps devoted more time to exploration. In the present study each breed was represented by only one genetic strain or population, thus we cannot generalize the results to other populations of these breeds.

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TABLE 1. The main effects of breed (BM), familiarity (FM), sex (SM); interactive effects of breed × familiarity (BM × FM) and breed × sex (BM × SM) as well as within breed effects of sex (SWL , Leghorn; SJF, jungle fowl) and familiarity (FWL, Leghorn; FJF , jungle fowl) on the variables (mean ± SE % of observations done or number of occurrences per test) recorded in the pair test1 Variable < 10 cm (%) 10–40 cm (%) 40–100 cm (%) > 100 cm (%) Aggressive pecks (n) Other pecks (n) Leaps (n) Threats (n) Attacks (n) Chasing (n) Distress calls

Leghorn Mean ± SE 28.13 36.34 19.50 16.03 1.43 2.93 1.79 8.61 5.79 2.64 67.44

± ± ± ± ± ± ± ± ± ± ±

4.01 2.57 1.70 2.41 0.46 0.88 0.66 2.32 1.22 0.86 4.96

Jungle fowl Mean ± SE

BM

FM

FWL

FJF

BM × FM

SM

SWL

SJF

BM × SM

± ± ± ± ± ± ± ± ± ± ±

NS NS 0.063 <0.05 <0.01 NS <0.001 <0.001 <0.001 <0.001 NS

NS NS NS NS NS NS NS NS NS NS NS

NS NS NS 0.077 NS NS NS NS NS NS NS

NS NS NS NS NS NS NS NS 0.067 <0.01 NS

NS NS NS NS NS NS NS 0.088 0.099 NS NS

0.072 NS NS NS <0.05 NS <0.01 <0.001 <0.01 <0.01 NS

NS NS NS NS 0.072 NS <0.01 0.001 0.052 <0.05 0.072

NS NS NS NS <0.05 0.081 NS <0.001 0.001 <0.01 NS

NS NS NS NS NS NS <0.01 NS NS NS NS

35.83 42.20 13.10 8.87 0.18 4.11 0.04 1.64 0.68 0.18 58.81

5.86 4.32 2.79 2.50 0.10 0.99 0.04 0.49 0.22 0.09 6.46

Significances (ANOVA: general linear model) are shown when P < 0.05 and trends for differences when P < 0.01.

1

Social motivation already differs between layer populations (Hocking et al., 2001) so variation in social preferences is likely to exist among different breeds. The jungle fowl used here may not exactly represent the ancestral type of the species due to, for instance, potential effects of genetic drift commonly occurring in small populations (Price, 1998). However, because the origins of this particular stock can be dated to Thailand only a few generations back (Schu¨tz, 2002), we consider it to be the most suitable of the available captive jungle fowl populations to suffice in behavioral comparisons with modern breeds. It is possible that the recorded behavioral differences between the layer and the wild-type chicks have arisen as side effects of intense selection for egg production in the Leghorns. Runway tests, commonly used to measure social reinstatement tendency in young domestic fowl and Japanese quail, are applicable also to social preference and discrimination studies (Vallortigara, 1992; Mills et al., 1995; Carmichael et al., 1998; Marin et al., 2001). It is known that encountering strangers is an aversive experience for chickens (Rajecki et al., 1977; Grigor et al., 1995), and in a novel, fear-eliciting environment, birds are attracted to familiar stimuli (Jones, 1987; Jones and Mills, 1999). Marin et al. (2001) reported that broilers as young as 10 d old show more pronounced social affiliation to familiar chicks than to strange chicks of the same breed in a runway. This finding is in agreement with our results for Leghorn chicks. The avoidance vs. affiliation reaction (measured as tendency to stay in each close zone), which is based on social discrimination, however, was clear only when the chick had once approached the social stimuli. Distinguishing the identity of the companions might have been difficult for the chicks from the start zone of the runway, as visual recognition of other hens is possible only at very close distances of 8 to 30 cm (Dawkins, 1995). Although visual cues are important for social recognition in hens (D’Eath and Stone, 1999), olfactory cues and inaudible sounds may also be essential in early attachments in chicks (Vallortigara and Andrew, 1994; Dawkins, 1995; Jones and Carmichael, 1999). Instead of individual recognition, the chicks might also rely on some unidentified general characteristics of their own social group (perhaps scent) when making social discriminations in a runway.

Sexually mature jungle fowl appear to have a generally better learning ability than Leghorns (Lindqvist et al., 2002) with some indications of faster social learning as well (Va¨isa¨nen et al., 2003). Nevertheless, in the first runway test, jungle fowl chicks did not prefer either of the stimulus bird groups. This result could be a sign of a poorer social discrimination capacity of subadult jungle fowl. Jungle fowl and Leghorn chicks might have differed in their stages of neurological development connected to the sensory functions, hence contributing to the social discrimination ability or preferences. It should be noted, however, that a free-choice test situation such as the runway used here exposes birds to a balance between preferences for familiarity and novelty (Carmichael et al., 1998). Thus, it might alternatively be possible that the absence of social preferences in jungle fowl could have resulted from a greater motivation to explore the novel environmental and social stimuli. This would be plausible from an evolutionary point of view, because the behavioral strategies of jungle fowl are likely to be close to those adaptive in the wild, such as for instance exploration of new environments (Murphy and Wood-Gush, 1978; Schu¨tz, 2002). Indeed, jungle fowl show more pronounced exploration in familiar and novel circumstances compared with Leghorns according to previous studies in chicks and adult birds from these same strains (Schu¨tz, 2002; Va¨isa¨nen and Jensen, 2003). Stress before a runway test has been found to increase affiliation to cage mates but not to strangers (Marin et al., 2001). The greater affiliation to and motivation to establish a contact with the familiar social stimuli shown by Leghorns in both runway tests might therefore result from a more pronounced fear response to the test situation. This finding would coincide with those of several previous studies done with the same 2 strains. Jungle fowl chicks, for instance, have been found to move and disperse in novel test arenas more, whereas Leghorns tend to immobilize and flock together (Va¨isa¨nen and Jensen). In addition, Schu¨tz et al. (2001) have shown that adult Leghorns respond more passively in acute feareliciting situations and adopt tonic immobility, a common measure of fear in poultry (Jones, 1996), more readily than jungle fowl. Furthermore, Va¨isa¨nen et al. (2003) have

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reported adult Leghorns to show higher and prolonged aggression than jungle fowl when mixed with unfamiliar birds. Thus, Leghorns of this genetic strain might also have a weaker ability to cope with encountering strangers than wild-type birds. The differences between sexes in the behavioral responses to familiar vs. unfamiliar social stimuli in the runway tests were opposite in the 2 breeds. Jungle fowl males showed a greater interest in unfamiliar social stimuli than females. This sexual dimorphism of behavior may be associated with the behavioral organization of adult fowl in the nature (Vallortigara, 1992; Vallortigara and Andrew, 1994). Territoriality might favor increased responsiveness to strangers in males and strong social bonding in females. In Leghorns, selection for egg production might have influenced the natural behavioral dimorphism between the sexes, and sex-specific behavioral strategies might have lost their adaptive value in an artificial environment or have been modified due to genetic correlations with selected production traits. Leghorns kept longer interindividual distances than jungle fowl in the pair test. This was not the case in an earlier study of a similar kind, in which test time was much longer (30 min) (Va¨isa¨nen and Jensen, 2003). Introduction of chicks in pairs in an open field therefore caused different responses during a short interval (10 min). Agonistic behavior was more frequent in Leghorn pairs, which is likely to cause avoidance reactions contributing to looser spacing. The breeds differ remarkably in their sexual maturation rate, and Leghorns start to lay eggs several weeks earlier than jungle fowl (Schu¨tz et al., 2002). Hormonal effects associated with sexual maturity are important for the onset of aggressive behavior (Guhl, 1958; Craig, 1992), which increases before the establishment of dominance relationships (Guhl, 1958; Rushen, 1982; Wood-Gush, 1989; Craig, 1992). This could perhaps account for increased aggressiveness in subadult Leghorns and thus contribute to the breed differences. The low number of agonistic interactions in jungle fowl could partially be influenced because they might have devoted more time to exploration. Dominance hierarchy is established earlier in males (Guhl, 1958; Rushen, 1982), which coincides with the sex differences in agonistic activity in both breeds. Besides runway tests, social pecking (Rajecki et al., 1976; Vallortigara, 1992), open field responses in presence of familiar or unfamiliar social partner (Jones, 1984), and interindividual distances (Franc¸ois et al., 2000) have been used to measure social discrimination in domestic and Japanese quail chicks. However, in the pair test, we found no consistent effects of familiarity in either breed. It is possible that the birds were not able to recognize the identity of their test companions. Although this is unlikely, as shown by the unexpected tendency for greater spacing distances in Leghorn and the higher frequency of chasing and attacks in jungle fowl pairs from the same experimental groups. These effects of familiarity were contrary to expected, and at present we have no plausible explanation for this result. As such these findings do

not appear to support the runway test results. The faster sexual maturation rate of Leghorns at the time of the pair test might be one factor contributing to this discrepancy. In conclusion, Leghorn but not jungle fowl affiliated more strongly with familiar than unfamiliar conspecifics when given a free choice in a runway. This result might have been caused by differences in social discrimination ability or developmental state between the 2 breeds of chicks. However, avoidance of unfamiliar and strong preference for familiar birds could also indicate a poorer ability of Leghorn chicks to cope with novel social stimuli. Agonistic interactions were more frequent in pairs of Leghorn chicks than jungle fowl. Found breed differences may constitute side effects of increased production. This in turn might have implications for the welfare of birds in production environments by affecting their ability to cope with group disruptions.

ACKNOWLEDGMENTS The authors sincerely thank Anette Wichman and Alf Blomqvist for excellent technical assistance during the study. Tommaso Pizzari provided valuable scientific input and comments. The study was supported by grants from MISTRA (Food 21), Formas and Wallenberg Consortium North, Stockholm, Sweden.

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