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Response of male and female domestic chicks to change in the number (quantity) of imprinting objects

Response of male and female domestic chicks to change in the number (quantity) of imprinting objects When facing two sets of imprinting objects of different numerousness, domestic chicks prefer to approach the larger one. Given that choice for familiar and novel stimuli in imprinting situations is known to be affected by the sex of the animals, we investigated how male and female domestic chicks divide the time spent in the proximity of a familiar versus an unfamiliar number of objects, and how animals interact (by pecking) with these objects. We confirmed that chicks discriminate among the different numerousnesses, but we also showed that females and males behave differently, depending on the degree of familiarity of the objects. When objects in the testing sets were all familiar, females equally explored both sets and pecked at all objects individually. Males instead selectively approached the familiar numerousness and pecked more at it. When both testing sets comprised familiar as well as novel objects, both males and females approached the larger numerousness of familiar objects. However, chicks directed all their pecks toward the novel object within the set. Differences in the behavior of males and females can be accounted for in terms of sex difference in the motivation to reinstate social contact with the familiar objects and to explore novel ones, likely associated with the ecology and the social structure of the species before domestication. . . . Keywords Filial imprinting Domestic chicks Numerical discrimination Sex differences Introduction (Nieder, 2020). While foraging, animals from various taxa show a spontaneous preference for more food items (Bogale, The investigation of numerical cognition in animals has been Aoyama, & Sugita, 2014; Gazzola, Vallortigara, & Pellitteri- challenging. Scientists have been taking advantage of sponta- Rosa, 2018; Hauser, Carey, & Hauser, 2000; Hunt, Low, & neous choice tasks (where the animals are expected to choose Burns, 2008; Lucon-Xiccato et al., 2015; Rodríguez et al., the preferred or the most advantageous option) as well as 2015;Rugani etal., 2013a, b; Yang & Chiao, 2016). While operant conditioning tasks (Nieder, 2019). Spontaneous pref- defending their territory, animals assess the strength of the erence allows for the investigation of relative numerosity opponents by estimating their number prior to engaging in judgments (“more than” or “less than”). Using such proce- defensive displays (Benson-Amram et al., 2011; Bonanni dures, the ability to discriminate between different numerous- et al., 2011; Cassidy et al., 2015; McComb, Packer & Pusey, nesses has been described in several ecological contexts 1994; Van Belle & Scarry, 2015; Wilson et al., 2012). While escaping from predators or looking for sexual partners, fishes prefer to join larger groups of conspecifics (Agrillo, Dadda & Electronic supplementary material The online version of this article (https://doi.org/10.3758/s13420-020-00446-1) contains supplementary Bisazza, 2006; Hager & Helfman, 1991;Mehliset al., 2015; material, which is available to authorized users. Potrich et al., 2015). Overall, this evidence shows that animals spontaneously * Bastien S. Lemaire (in the absence of any numerical training) discriminate be- [email protected] tween numerousnesses to deal with various circumstances in their everyday life. Therefore, animal brains seem to be natu- Center for Mind/Brain Sciences, University of Trento, Piazza della rally equipped to use simple numerical cues (Nieder, 2019; Manifaturra 1, 38068 Rovereto, TN, Italy Rugani, 2018; Vallortigara, 2015, 2017). Using operant con- Department of General Psychology, University of Padova, ditioning, several animal species have learned to distinguish Padova, Italy stimuli based on the absolute number of items (Bogale et al., Department of Psychology, University of Pennsylvania, 2011;Bortot etal., 2019; Ditz & Nieder, 2016;Pepperberg, Philadelphia, PA, USA Learn Behav (2021) 49:54–66 55 2010; Smirnova, Lazareva, & Zorina, 2000; Xia et al., 2001). range (1 vs. 4 and 2 vs. 5; Rugani et al., 2013a). The upper By training animals, numerical achievements can reach a high limit of this kind of numerical discrimination is 3 versus 4. level of abstraction. Beyond numerical discrimination, ani- Nevertheless, this limit can be exceeded by the use of cogni- mals can learn to match symbols to specific numerosities tive strategies as grouping (Rugani, Loconsole, & Regolin, (Biro & Matsuzawa, 2001; Boysen & Berntson, 1989; 2017) and by adding to each object individually distinctive Olthof, Iden, & Roberts, 1997; Pepperberg & Gordon, features, allowing for individual processing (Rugani et al., in 2005), perform simple mathematical operations with those press). symbols (Boysen & Berntson, 1989;Olthof et al., 1997), sym- In 2010, by taking advantage of filial imprinting, it was bolically label subsets of items embedded within heteroge- demonstrated that young domestic chicks, when presented neous arrays (Pepperberg & Gordon, 2005) and master the with two sets of objects, prefer to approach the larger one precursors of a zero-like concept (Howard et al., 2018; (Rugani et al., 2010b). The choice for familiar or novel stimuli Merritt, Rugani & Brannon, 2009; Pepperberg, 1988; in imprinting situations is known to be affected by the sex of Pepperberg & Brezinsky, 1991; Pepperberg & Gordon, the animals. When exposed to familiar and unfamiliar individ- 2005). Sophisticated and abstract numerical concepts can be uals, males and females of domestic chicks behave differently mastered by both primates and birds (Pepperberg, 2009; (Vallortigara & Andrew, 1991; Vallortigara, 1992a, b). Rugani, Vallortigara, & Regolin, 2016b), indicating that bird Females spend more time close to familiar individuals, where- brains, though characterized by a different pallial organization as males spend more time close to unfamiliar ones. (Güntürkün & Bugnyar, 2016), should not be neglected in Furthermore, both sexes pecked more at unfamiliar than at studying high cognition (Gibbs et al., 2008;Matsushima familiar individuals, and overall males pecked more than fe- et al., 2003;Pepperberg, 2017). males. These differences are probably the result of different To investigate the ontogenetic origins of numerical knowl- levels of attachment to conspecifics following imprinting edge, the domestic chick (Gallus gallus) is an ideal animal (Vallortigara, Cailotto, & Zanforlin, 1990). Females seem to model (Rugani, 2018; Versace & Vallortigara, 2015). Unlike develop stronger attachment to their fellows than males studies on adult animals, chicks can be tested very early in life, (McBride & Foenander, 1962; McBride, Parer, & allowing for the discovery of the origins of numerical com- Foenander, 1969; Vallortigara et al., 1990;Workman & prehension. Young chicks can learn to solve different numer- Andrew, 1989). ical problems, ranging from numerical discrimination The aim of this study was to investigate how male and (Rugani, Vallortigara, & Regolin, 2013b)to the useof ordinal female chicks respond to familiar and unfamiliar objects in a cues (Rugani, Regolin, & Vallortigara, 2007), arithmetic cal- number (quantity) discrimination test. Considering the differ- culation (Rugani et al., 2009), comprehension of proportion ent motivation of male and female chicks in approaching their (Rugani, Vallortigara, & Regolin, 2015b), and abstract ratios artificial social companion (Regolin et al., 2005), we expected (Rugani et al., 2016a). a different behavior depending on the sex of the animals. Exploiting chicks’ memories for their imprinting objects Using the original method developed by Rugani et al. allows one to assess whether chicks discriminate between dif- (2010b), we investigated not only how male and female do- ferent numbers of artificial social companions (i.e., objects mestic chicks divided their time in the proximity of a familiar they were exposed to soon after hatching; Rugani, Regolin, versus an unfamiliar number of objects, but also how they & Vallortigara, 2008, 2010b). Filial imprinting is a well- interacted (by social pecking) with familiar and novel objects known phenomenon (Bolhuis, 1991; McCabe, 2019; at test. This new measure allowed us to better understand the Vallortigara & Versace, 2018), allowing the young birds to factors underlying the intrinsic motivation to join the larger learn the characteristics of an object they have been exposed to number of artificial social companions. and to develop a robust social attachment toward it in the first few days of life (Bolhuis, 1991; Yamaguchi et al., 2012). Once imprinted, chicks regard their imprinting objects as so- cial companions (Regolin et al., 2005) and can generalize their Experiment 1 filial behaviors toward similar objects (Bolhuis & Horn, 1992; Versace et al., 2017). Previous studies have exploited chicks’ In this experiment, we applied the experimental procedure of memories for their artificial social companions (object they the first experiment by Rugani et al. (2010b) to test the dis- were reared with) to test their numerical abilities, which range crimination between 1 and 3 imprinting objects in 3-day-old from numerical discrimination (Rugani, Regolin, & domestic chicks. Here we determined the sex of the animal to Vallortigara, 2010b) to proto-arithmetic calculations in the assess any difference in the time spent at test by male versus range of small numbers, up to 3 (Rugani et al., 2009), in the female chicks near the numerically familiar versus numerical- large-number range (6 vs. 9 and 5 vs. 10; Rugani, Regolin & ly novel objects. Moreover, we introduced a novel measure Vallortigara, 2011a) and between the small- and large-number (spontaneous pecking) to assess the level of interaction of 56 Learn Behav (2021) 49:54–66 each sex based on the scoring of spontaneous pecking toward per cylinder). Half of the chicks were imprinted to one cylin- familiar versus unfamiliar objects at test. der, and the other half were imprinted to three cylinders (Table 1). Food (chick starter crumbs) and water were avail- able ad libitum. Ethics statement After 2 days spent under this rearing conditions (from Tuesday 9:00 am to Thursday 1:00 pm), chicks were individ- The study was performed in compliance with the European ually placed for 6 min in the testing apparatus where they were Union and the Italian laws on the treatment of animals. The free to choose and approach either their familiar numerosity procedures were approved by the Ethics Committee of the set or an unfamiliar numerosity set. University of Trento and licensed by the Italian Health Ministry (permit number 53/2020). Test Subjects For testing, animals were moved in a room adjacent to the rearing room and placed into the testing apparatus. This The number of chicks required in each group was a priori consisted of a short runway (45 × 20 × 30 cm, Fig. 1B), determined with a power analysis (Champely, 2020)with an illuminated by two LED lamps (12 V). The behavior of each effect size (d) of .65, and an alpha of .05. Results showed that animal was recorded using a Microsoft Life Camera located 20 individuals were required per group to achieve a power of 70 cm above the apparatus. .80. Overall, we used 147 chicks (75 females) of the strain Depending on the experimental condition, two different Ross 308 (Table 1). The eggs were obtained from a commer- sets of stimuli were located at either end of the runway (Fig. cial hatchery (Azienda Agricola Crescenti) and were incubat- 1B). Testing stimuli consisted of same size cylinders (5 cm ed in our laboratory under controlled conditions (37.7 °C and high, 2 cm diameter per cylinder) colored red or blue. Each 40% humidity). Three days before hatching, eggs were moved bird underwent a single test, which could be either an Absolute into opaque black boxes within a hatching chamber at 37.7 °C Discrimination or a Relative Discrimination test. The position and 60% of humidity. of each set in the runway was balanced across animals Soon after hatching, chicks were sexed (this chicken strain (Table 1). exhibits a sexual dimorphism on the wing feathers) and were In the Absolute Discrimination test, chicks were presented singly housed into rectangular cages (22 × 30 × 40 cm, Fig. with one versus three objects, which were identical to the 1A). Cages were illuminated by 30 W fluorescent lights in a imprinting objects (red cylinders, Table 1). In the Relative controlled temperature environment (30 °C). Chicks were Discrimination task, chicks were presented with two compos- reared together with an artificial stimulus (or set of stimuli) ite sets of four objects. One set comprised one red cylinder suspended 1 cm above the floor by a transparent thread in the (familiar object) and three blue cylinders (unfamiliar objects), centre of the cage. By exposing the animals to a set of stimuli while the other set comprised three red cylinders (familiar in their rearing cages, filial imprinting occurred, leading objects) and one blue cylinder (unfamiliar object, Table 1). chicks to develop a strong attachment toward those objects. The positions of the objects within the sets were fixed (such Stimuli consisted of red cylinders (5 cm high, 2 cm diameter as presented in Table 1). In the original study, the Relative Discrimination test was performed to check whether chicks Table 1 Number of animals and sets of stimuli used in the Absolute and would respond to the actual number of familiar objects within Relative Discrimination tests (chicks that did not respond were excluded a set of larger numerosity (composed of unfamiliar objects from the analysis and therefore are not included in this table). In the too). Relative Discrimination test, the position of the objects within the sets was fixed Data analysis To assess the preference toward a set of stimuli, the time spent by the chicks near each set (within a 15-cm area close to it, Fig. 1B) was automatically scored using Ethovision (version 13). A preference for the imprinting numerosity (%) was then calculated using the following formula: Preference for imprinting numerosity time spent close to the familiar imprinting numerosity ¼ x100: time spent close to both sets of stimuli Learn Behav (2021) 49:54–66 57 Fig. 1 Three-dimensional representation of the rearing cage (A) and the by a transparent thread. Dashed-lines in B delimited the zones (left, center testing apparatus (B). B shows an example of the Absolute and right) in which the time spent by the animal was scored (the zones Discrimination test. The stimuli were suspended 1 cm above the floor were defined computationally using Ethovision) Post hoc Tukey tests were performed when required using A value higher than 50% indicated a preference for the fa- miliar imprinting numerosity (if imprinted with 1, a preference Bonferroni’scorrection. All the statistical analyses were performed using RStudio for 1). A value lower than 50% indicated a preference for the unfamiliar numerosity set (if imprinted with 1, a preference for v1.1 (RStudio Team, 2015) with the following packages: goftest (Faraway et al., 2019), nlme (Pinheiro et al., 2020), 3). A score of 50% indicated no preference (chance level). As pecking is a behavior expressed during social exploration lme (Bates et al., 2015), tidyr (Wickham & Lionel, 2020), and recognition in domestic chicks (Gottier, 1968;Nicol, 2015; plyr (Wickham, 2011), dplyr (Wickham et al., 2020), reshape (Wickham, 2007), lsr (Navarro, 2015), ggplot2 (Wickham, Schjelderup-Ebbe, 1922; Vallortigara, 1992a), we also scored the number of pecks assigned by the animals to each stimulus 2016), pwr (Champely, 2020). within each set. Manual scoring was made by a scorer blind to the experimental conditions. The coding reliability of the pecks Results was assessed by re-coding 21 chicks randomly selected (Pearson’s correlation test showed a high correlation between Absolute Discrimination the two codings, r = 0.99). Pecking analysis was performed once the videorecordings were already archived. Preference for the imprinting numerosity The results are Unfortunately, while uploading the videos, a folder got showninFig. 2A. There was a significant effect of Sex corrupted and prevented us from coding the pecking behaviour of 21 chicks (12 females) in the Relative Discrimination test. (F(1, 66) = 6.73, p < 0.05), but not of Imprinting Numerosity (F(1, 66) = 0.20, p = 0.66) or interaction (F(1, Chicks that did not respond (one female and two males) were removed from the analysis as they did not score any 66) = 1.69, p =0.20). Overall, the preference for the imprinting numerosity set preference during the entire testing duration. was significantly different from chance level for males (t(33) = 2.50, p < 0.05, Cohen’s d = 0.42, Bonferroni correction), but Statistical analysis not for females (t(35) = -0.54, p = 0.59, Cohen’sd=0.090, Bonferroni correction). Males spent on average 66% (± 5.89 To determine whether animals showed preferences for the sets SEM) of their time close to the imprinting numerosity set, while females spent on average 47% (± 6.42 SEM) of their of objects differing across Sex (female, male) and Imprinting time close to it. Numerosity (1, 3), we performed an ANOVA for each dis- crimination task (Absolute, Relative). To meet parametric as- Pecks The results are shown in Fig. 2B. When imprinted with 1, sumptions, we arcsine-transformed the data. To check wheth- er chicks had a significant preference for the imprinting there was a significant effect of Object (F(3, 132) = 6.46, p < 0.01) and of the interaction between Object and Sex (F(3, 132) numerosity, we performed two-tailed one-sample t-tests against chance level (50%). = 6.36, p < 0.01) but a non-significant effect of Sex (F(1, 132) = 0.86, p = 0.36). While females pecked similarly at each object, To determine whether animals were pecking at the stimuli (each cylinder within a set of stimuli) differently across Sex the post hoc analysis revealed that males pecked significantly more at the single object in comparison to the central (t(132) = (female, male), we performed an ANOVA for each discrimina- tion task (Absolute, Relative) and Imprinting Numerosity (1, 3). 4.10, p < 0.01, Cohen’s d = 1.41) and right-most (t(132) = 3.50, p < 0.05, Cohen’s d = 1.19) objects within the set of three. To meet parametric assumptions, we log-transformed the data. 58 Learn Behav (2021) 49:54–66 Fig. 2 Graph (A) represents the time spent by the chicks during testing (females in red and males in light-blue) and Imprinting Numerosity (* p close to their imprinting numerosity between Imprinting Numerosity and < 0.05; ** p < 0.01). Light blue asterisks show the statistical difference in Sex (p < 0.05, *). Graph (B) represents the number of pecks made toward males; black asterisks show the statistical differences in both males and each stimulus composing the different set of stimuli between Sex females When imprinted with 3, there was a significant effect of Sex significant effect of Sex (F(1, 70) = 0.19, p =0.67) norof the (F(1, 132) = 4.12, p < 0.05) and Object (F(3, 132) = 3.99, p < interaction (F(1, 70) = 0.00, p =0.99). 0.01), but no interaction (F(3, 132) = 0.30, p = 0.82). As revealed Overall, the preference for the imprinting numerosity set by the ANOVA, males (mean = 9.90, SEM = 2.27) pecked was significantly different from chance level for the chicks significantly more than females (mean = 5.31, SEM = 1.25) at imprinted with 1 (t(35) = -4.74, p <0.001, Cohen’sd= the objects, a difference that seems to mainly be driven by the 0.79, Bonferroni correction) and 3 (t(37) = 5.32, p < 0.001, number of pecks made at the left-most object within the set of Cohen’s d = 0.86, Bonferroni correction). Nevertheless, the three. Males pecked on average 15 times (SEM = 4.79) at it, preferences between these two groups were the opposite. while females pecked on average five times (SEM = 1.76) at it. Chicks imprinted with 1 spent on average 23% (±5.64 SEM) Overall, the post hoc analysis revealed that chicks pecked of their time close to the imprinting numerosity set while significantly more at the single stimulus in comparison to the chicks imprinted with 3 spent on average 79% (±5.36 SEM) central object composing the set of three stimuli (t(132) = close to it. This indicates that, independently of rearing con- 3.05, p < 0.05, Cohen’s d =0.73). ditions and sex, chicks approached the larger set of familiar objects. Relative Discrimination Pecks The results are shown in Fig. 3B. When imprinted on 1 Preference for the imprinting numerosity The results are or 3, there was a significant effect of Object (imprinted with 1: showninFig. 3A. There was a significant effect of F(7, 184) = 11.48, p < 0.001; imprinted with 3: F(7, 208) = Imprinting Numerosity (F(1, 70) = 53.16, p < 0.001) but no 7.75, p < 0.001), but not a significant effect of Sex (imprinted Learn Behav (2021) 49:54–66 59 Fig. 3 (A) The time spent by the chicks during testing close to the object different set of stimuli between Imprinting Numerosity (females and set containing the number of familiar objects experienced during males grouped; *** p < 0.001). Black asterisks show the statistical imprinting between Imprinting Numerosity and Sex (p < 0.001, ***). differences in both males and females (B) The number of pecks made toward each stimulus composing the with 1: F(1, 184) = 0.01, p = 0.92; imprinted with 3: F(1, 208) motivation of male and female birds in exploring a novel =1.10, p = 0.30) or of the interaction (imprinted with 1: F(7, numerousness of familiar objects. Males seemed more in- 184) = 0.36, p = 0.93; imprinted with 3: F(7, 208) = 0.71, p = clined to spend time close to the familiar numerousness, 0.66). while females seemed equally motivated in joining the fa- No matter whether they had been imprinted on 1 or 3, the miliar group or exploring the novel one. When tested in the post hoc analysis revealed that chicks pecked significantly presence of familiar and unfamiliar objects (Relative more at the single blue object in the set in comparison to all Discrimination), both sexes used the relative numerical other objects (statistics are detailed in the Online information available concerning the subset of familiar ob- Supplemental Material table). jects present within each set and chose to associate with the larger set of familiar objects as described in the original study by Rugani et al. (2010a, b). Thepresenceofnovel Experiment 2 objects seems to play a relevant role in the choice to ap- proach the larger number of familiar objects, or in avoiding In the first experiment, chicks behaved differently in the the larger number of unfamiliar ones. Support for the latter two discrimination tests. When only exposed to familiar hypothesis comes from the analyses of the pecks, which objectsattest(Absolute Discrimination), males consistently highlight an increased number of pecks at the approached the familiar numerousness, whereas females single novel object in the group comprising three familiar did not show any preference. This may indicate a different objects and an unfamiliar one. 60 Learn Behav (2021) 49:54–66 To investigate the importance of unfamiliarity, we conduct- 1.96, p = 0.12). As revealed by the ANOVA, males were ed a second experiment in which we manipulated the degree pecking (mean = 8.80, SEM = 1.40) significantly more than of unfamiliarity. females (mean = 6.21, SEM = 1.39) at the objects. Furthermore, the post hoc analysis revealed that males pecked significantly more at the left-most object (mean = Methods 11.16, SEM = 2.39) in the set of three objects in comparison to the single object (mean = 8.21, SEM = 4.67; t(144) = -3.45, The general procedure was the same as in the first experiment. p < 0.05, Cohen’s d = -1.12). The opposite tendency was The same number of objects as in the Absolute Discrimination observed in females although not revealed by the post hoc was used (Table 2), but this time we slightly modified the analysis as the variability of the pecks to the single object appearance of the stimuli during testing. Chicks at test were seemed quite high (mean = 13.42, SEM = 5.84) in comparison offered a choice between one or three objects, but a small to that of the left-most object within the set of three objects yellow dot (diameter of 5 mm) was added on the central object (mean = 5.79, SEM = 1.61). of the set corresponding to the original imprinting numerosity When imprinted with 3, there was a significant effect of (Table 2). For the chicks that had been imprinted to one object, Object (F(3, 144) = 6.92, p < 0.001) but no significant effects the yellow dot was placed on the single object during testing. of Sex (F(1, 144) = 0.46, p = 0.50) nor of the interaction (F(3, For the chicks that had been imprinted to three objects, the 144) = 0.23, p =0.87). yellow dot was placed on the central object composing the set The post hoc analysis revealed that chicks pecked signifi- of three during testing. cantly more at the single stimulus in comparison to the left- We used 79 chicks (40 females) of the strain Ross 308 most one (t(144) = 3.48, p < 0.01, Cohen’s d = 0.80) or to the (Table 2). Chicks that did not respond (two females and one right-most one (t(144) = 4.10, p <0.001, Cohen’s d =0.94) in male) were removed from the analysis as they did not score the set of three objects . any preference during the entire testing duration. Results General discussion Preference for the imprinting numerosity The results are Number cognition in birds has been widely investigated. showninFig. 4A. There was a significant effect of Studies performed by Pepperberg on Alex the parrot illustrat- Imprinting Numerosity (F(1, 72) = 7.43, p < 0.01) but no ed the impressive numerical competences owned by avian significant effects of Sex (F(1, 72) = 0.075, p = 0.79) or of species (Pepperberg, 2009). Alex was able to quantify up to the interaction (F(1, 72) = 1.87, p =0.18). six-item sets using English labels with an accuracy of 80%, Overall, the preference for the imprinting numerosity was and remaining unaffected by array quantity, mass, or contour significantly different from chance level for the chicks (Pepperberg, 1994; Pepperberg & Gordon, 2005). The imprinted to 1 (t(37) = -5.86, p <0.001, Cohen’s d =0.97, achievement of a high level of abstraction in numerical com- Bonferroni correction) but not for the chicks imprinted to 3 prehension suggests that birds may naturally deal with numer- (t(37) = -0.83, p = 0.41, Cohen’s d = 0.14, Bonferroni correc- ical information in everyday life. In our study, instead of fo- tion). Chicks imprinted to 1 spent on average 20% (±4.98 cusing on the symbolic use of numbers as Pepperberg did, we SEM) of their time close to the familiar numerosity, while studied a much simpler numerical ability (numerousness dis- chicks imprinted to 3 spent on average 44% (±6.62 SEM) crimination), exploiting a paradigm that allows one to test close to it. numerical comprehension in the absence of any numerical training. This allows for the understanding of how birds can Pecks The results are shown in Fig. 4B. Whenimprintedwith spontaneously deal with numerical cues. 1, there was a significant effect of Sex (F(1, 144) = 5.51, p < As in previous studies (Rugani et al., 2008, 2010b), our 0.05) and an interaction between Object and Sex (F(3, 144) = results showed that chicks could use numerical/quantity infor- 4.23, p < 0.01), but no significant effect of Object (F(3, 144) = mation to discriminate between different sets of objects. As we did not control for the role of continuous physical vari- Table 2 Number of animals and sets of stimuli used in the second ables, we cannot disentangle whether chicks used numerical experiment (chicks that did not respond were excluded from the and/or continuous quantities to discriminate. However, previ- analysis and therefore are not included in this table) ous work has shown that chicks, depending on the available cues, could use both sources of information (Rugani et al., 2010b). Moreover, several sources of supporting evidence points to the existence of a general magnitude system in hu- man and non-human species that comprises both discrete Learn Behav (2021) 49:54–66 61 Fig. 4 Graph (A) represents the time spent by the chicks during testing between Sex (females in red and males in light-blue) and Imprinting close to their imprinting numerosity set between Imprinting Numerosity Numerosity (* p < 0.05; ** p < 0.01; *** p < 0.001). Light blue asterisk and Sex (*** p < 0.015). Graph (B) represents the number of pecks shows the statistical difference in males; black asterisks show the statis- assigned to each stimulus composing the different sets of stimuli tical differences for both males and females (countable) and continue quantities (Bortot, Stancher & and had a strong preference to associate with the set composed Vallortigara, 2020; De Corte, Navarro & Wasserman, 2017; of more familiar objects (three red objects and one blue ob- Di Giorgio et al., 2019;Gallistel, 1989;Merritt, Casasanto, & ject). Motivational differences may support chicks’ tendency Brannon, 2010;Walsh, 2003). to approach the larger group of social companions: the larger In our study, we focused on whether males and females group can guarantee more protection toward potential preda- used numerical/quantities cues similarly. We found that males tors, higher level of social interaction, a richer environment, and females make different use of numerical cues depending and in the natural situation more heat (Pulliam, 1973;Roberts, on the context (familiar, in the Absolute Discrimination task, 1996). Furthermore, the experimental procedure used in our or familiar and unfamiliar in the Relative Discrimination task). study exploits the chick’s memory for its imprinting object (or The Absolute Discrimination task showed that males prefer set of objects). As a result of filial imprinting, an increase in to associate with the familiar numerosity set, while females fear is observed when exposed to novel stimuli (Bolhuis, 1991). This leads the young animals to avoid proximity with showed no preference. This may indicate that in a novel envi- ronment, as the testing apparatus was, males are motivated to novel objects, which therefore could explain why chicks tend approach the familiar numerosity sets, while females are to associate with the set composed of the largest number of equally motivated to explore the two sets. The Relative familiar objects and the fewest number of unfamiliar objects. Discrimination task revealed a completely different pattern The number of pecks here is not to be interpreted as a of results, but this time more similar to what Rugani et al. feeding behavior. Instead, it likely reflects a social, either (2010b) described initially. Males and females behaved alike affiliative or aggressive, behavior toward familiar or 62 Learn Behav (2021) 49:54–66 unfamiliar objects (Vallortigara, 1992a), providing inter- 1992a, b). Hence, it is possible that chicks used esting cues as to the possible nature of sex differences. numerical/quantitative information available to determine While affiliative pecks are usually equally distributed which object was more likely to be unfamiliar. across time among familiar individuals, aggressive pecks A similar interpretation can be made by looking at the are reiterated toward unfamiliar individuals/objects results obtained in the Relative Discrimination task. Chicks (Schjelderup-Ebbe, 1935). Pecking behavior may, there- repeatedly pecked at the blue object incorporating the larger fore, reveal lack of recognition when intensively exhibited set of familiar objects (three red objects), demonstrating that toward an individual (Guhl & Ortman, 1953; Vallortigara, they recognized the blue object as being unfamiliar within a 1992a, b). In the Absolute Discrimination task, males familiar set. pecked more at the familiar numerosity set. This measure Our results suggest that male and female domestic correlates with the time spent near the familiar numerous- chicks use numerical/quantity information slightly differ- ness and shows a preference of male chicks to interact ently depending on the familiarity of the objects. In a more with the familiar set rather than with the novel familiar context, males tend to use numerical/quantity in- one. A peculiar behavior emerged from the analysis of formation to discriminate between two sets of familiar the distribution of pecks toward the array of three objects: objects, while females focus on each familiar object indi- males seemed to peck more at the left object than at the vidually. Interestingly, in a context composed of unfamil- central or at the right one. This left-sided preference could iar objects, males and females expressed similar behaviors be related to a general bias in the allocation of spatial and chose to associate with the set containing less unfa- attention (Diekamp et al., 2005; Regolin, 2006; Rugani miliar objects. In the previous study (Rugani et al., et al., 2011b). Day-old domestic chicks, in fact, associate 2010b), no difference was found between the Absolute numbers with space in different contexts. Chicks trained and Relative Discrimination tasks. Therefore, the authors to respond to a certain numerical value spontaneously concluded that chicks mainly use the number of familiar associated a smaller number with the left side and a larger objects to discriminate between two sets of stimuli and number with the right side of space (Rugani et al., 2020, that they choose to associate with the larger set of familiar 2015a). Chicks, trained to identify a target element (e.g., objects. Our data instead support the idea that chicks the fourth) in a sagitally oriented series of identical ele- mainly rely on the number of unfamiliar objects instead ments, when required to react to an identical series but of the number of familiar ones. This difference could be rotated by 90°, identified most often the left target than possibly explained by the colors used: yellow and light the right one (Rugani et al., 2010a, 2015a). A lateral bias pink in the study by Rugani et al. (2010b), versus red has also been found in a numerical task which required to and blue in the present study. The relevance of the unfa- discriminate between two groups of artificial social com- miliar object may have been emphasized using novel blue panions. Female chicks were reared with a set of identical objects instead of light pink ones. Even if different strat- objects. At test, the objects disappeared one at a time egies seem to be at the basis of the current study (avoid behind one of two identical screens, one on the left and the larger number of unfamiliar objects) and in the previ- one on the right. On a free-choice test, chicks showed a ous study (approach the larger number of familiar objects), preference for the larger group. Nevertheless, their perfor- nevertheless both studies converge in demonstrating that mance was higher when the larger group was hidden on day-old chicks do discriminate numerousness in the ab- the right side (Rugani, Rosa Salva, & Regolin, 2014). sence of any numerical training. Differences in strains This evidence suggests that also in a spontaneous search should also be considered. for social companions a tendency can emerge to associate To better understand to which degree unfamiliarity influ- numbers and space. The latter evidence is also in line with ences chicks’ behaviors, we conducted a second experiment. our new findings in which male chicks tend to explore the The task in this second experiment shared properties with the smaller numbers of social companions on the left side. Absolute and Relative Discrimination tasks. During testing, Going back to our current study, females, in contrast, chicks were offered a choice between a set of one or three visited and pecked at all objects individually, which can objects (suchasinthe Absolute condition). However, we probably explain why they did not express any preference slightly changed the appearance of the familiar numerosity in the time spent analysis (females were at chance-level). set so that it neither appeared completely familiar nor Curiously, when imprinted with the set composed of three completely unfamiliar, by adding a small yellow dot on one objects, both sexes significantly pecked more at the single of the objects of the familiar numerosity set (for the stimulus as if they were treating it as a less familiar indi- discriminability of imprinting object based on individual vidual. Indeed, pecking can also demonstrate a lack of features depicted on them, see Fontanari et al., 2011). recognition when it is repeatedly directed toward a spe- In the second experiment, chicks tended to explore the cific individual (Guhl & Ortman, 1953; Vallortigara, unfamiliar numerosity set. This demonstrates that even a slight Learn Behav (2021) 49:54–66 63 change in the appearance of one object influences the chick’s a context, using numerical abilities would be an efficient strat- decision to associate with either set. Although no sex differ- egy, as has been shown to occur in several other species ence was observed in terms of time spent close to either set, (Benson-Amram et al., 2011; Bonanni et al., 2011; Cassidy the pecking analysis revealed that males and females behaved et al., 2015; McComb, Packer, & Pusey, 1994;Van Belle & differently. When imprinted with one, females pecked more at Scarry, 2015; Wilson et al., 2012). the single object (with the yellow dot) than at the other objects In conclusion, our results show that young and almost (set of three, where they spent 72% of their time). As in the naïve domestic chicks rely on numerical information to make Absolute Discrimination task, females seem to focus more on social decisions. They first discriminate between familiar ver- individual recognition, which suggests that they do not treat sus unfamiliar objects based on their perceptual features, and the single stimulus (with the yellow dot) as entirely unfamiliar. then they estimate the numerousness of both sets to avoid the In contrast, males completely avoided the single stimulus larger number of unfamiliar objects. Moreover, the degree of (with the yellow dot) and pecked more at the set of three. novelty of the unfamiliar objects seems to correlate with the The results of this second experiment appear to be in agree- avoidance of the unfamiliar set. Numerousness is, therefore, a ment with the study by Rugani, Regolin and Vallortigara relevant information animals can spontaneously use in a social (2010b) and with our first experiment, suggesting that chicks context to optimize their fitness. firstly discriminate between familiar and unfamiliar objects Acknowledgements We are grateful to Elif Karakoç for helping to test before making a decision based on their numerousness. the animals, and to Nicholas Zampiero and Chiara Eccher for assisting in Our study provides additional information concerning the the coding of the chicks’ behaviors. use of numerical or quantitative information by young domes- This project was supported by funding from the European Research tic chicks in the specific context of filial imprinting. Taken Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No. 833504 SPANUMBRA) to together, our results confirm that chicks can use numerousness GV. The project also received funding from the European Union’s to discriminate between different set of objects. It also dem- Horizon 2020 research and innovation program under the Marie onstrates that male and female domestic chicks do not always Sklodowska-Curie (grant agreement No. 795242 SNANeB) to RR; and use available numerical cues similarly, and that, instead, they from a PRIN 2017 ERC-SH4–A (2017PSRHPZ) to LR and GV. might prefer to use different strategies depending on the fa- Funding Open access funding provided by Università degli Studi di miliarity of the objects. Overall, females seem more flexible in Trento within the CRUI-CARE Agreement. the use of numerical/quantitative cues depending on the con- text. In a familiar context, females perform individual recog- Data availability The datasets (.csv) are available on Fig Share (10.6084/ nition rather than using numerical/quantitative information to m9.figshare.12336140). make a decision. In an environment composed of familiar as Open Access This article is licensed under a Creative Commons well as unfamiliar objects, females used numerical informa- Attribution 4.0 International License, which permits use, sharing, tion to discriminate between two sets of objects. In contrast, adaptation, distribution and reproduction in any medium or format, as males tend to rely upon numerical information either by ap- long as you give appropriate credit to the original author(s) and the proaching the familiar numerosity set when exposed to famil- source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article iar objects or the larger set of familiar objects when exposed to are included in the article's Creative Commons licence, unless indicated sets of familiar and unfamiliar objects. otherwise in a credit line to the material. If material is not included in the Likely the sex difference we observed may derive from the article's Creative Commons licence and your intended use is not natural history of feral birds. Adult fowls are organized in permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a groups comprising a dominant rooster and many hens copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. (Queiroz & Cromberg, 2006). Males are more solitary as they spend most of their time maintaining and patrolling their ter- ritory, whereas females tend to live in strict hierarchies that they develop and maintain through time (Gottier, 1968; References McBride & Foenander, 1962; McBride et al., 1969; Schjelderup-Ebbe, 1922). Such organization may favor the Agrillo, C., Dadda, M., & Bisazza, A. (2006). 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Response of male and female domestic chicks to change in the number (quantity) of imprinting objects

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10.3758/s13420-020-00446-1
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Abstract

When facing two sets of imprinting objects of different numerousness, domestic chicks prefer to approach the larger one. Given that choice for familiar and novel stimuli in imprinting situations is known to be affected by the sex of the animals, we investigated how male and female domestic chicks divide the time spent in the proximity of a familiar versus an unfamiliar number of objects, and how animals interact (by pecking) with these objects. We confirmed that chicks discriminate among the different numerousnesses, but we also showed that females and males behave differently, depending on the degree of familiarity of the objects. When objects in the testing sets were all familiar, females equally explored both sets and pecked at all objects individually. Males instead selectively approached the familiar numerousness and pecked more at it. When both testing sets comprised familiar as well as novel objects, both males and females approached the larger numerousness of familiar objects. However, chicks directed all their pecks toward the novel object within the set. Differences in the behavior of males and females can be accounted for in terms of sex difference in the motivation to reinstate social contact with the familiar objects and to explore novel ones, likely associated with the ecology and the social structure of the species before domestication. . . . Keywords Filial imprinting Domestic chicks Numerical discrimination Sex differences Introduction (Nieder, 2020). While foraging, animals from various taxa show a spontaneous preference for more food items (Bogale, The investigation of numerical cognition in animals has been Aoyama, & Sugita, 2014; Gazzola, Vallortigara, & Pellitteri- challenging. Scientists have been taking advantage of sponta- Rosa, 2018; Hauser, Carey, & Hauser, 2000; Hunt, Low, & neous choice tasks (where the animals are expected to choose Burns, 2008; Lucon-Xiccato et al., 2015; Rodríguez et al., the preferred or the most advantageous option) as well as 2015;Rugani etal., 2013a, b; Yang & Chiao, 2016). While operant conditioning tasks (Nieder, 2019). Spontaneous pref- defending their territory, animals assess the strength of the erence allows for the investigation of relative numerosity opponents by estimating their number prior to engaging in judgments (“more than” or “less than”). Using such proce- defensive displays (Benson-Amram et al., 2011; Bonanni dures, the ability to discriminate between different numerous- et al., 2011; Cassidy et al., 2015; McComb, Packer & Pusey, nesses has been described in several ecological contexts 1994; Van Belle & Scarry, 2015; Wilson et al., 2012). While escaping from predators or looking for sexual partners, fishes prefer to join larger groups of conspecifics (Agrillo, Dadda & Electronic supplementary material The online version of this article (https://doi.org/10.3758/s13420-020-00446-1) contains supplementary Bisazza, 2006; Hager & Helfman, 1991;Mehliset al., 2015; material, which is available to authorized users. Potrich et al., 2015). Overall, this evidence shows that animals spontaneously * Bastien S. Lemaire (in the absence of any numerical training) discriminate be- [email protected] tween numerousnesses to deal with various circumstances in their everyday life. Therefore, animal brains seem to be natu- Center for Mind/Brain Sciences, University of Trento, Piazza della rally equipped to use simple numerical cues (Nieder, 2019; Manifaturra 1, 38068 Rovereto, TN, Italy Rugani, 2018; Vallortigara, 2015, 2017). Using operant con- Department of General Psychology, University of Padova, ditioning, several animal species have learned to distinguish Padova, Italy stimuli based on the absolute number of items (Bogale et al., Department of Psychology, University of Pennsylvania, 2011;Bortot etal., 2019; Ditz & Nieder, 2016;Pepperberg, Philadelphia, PA, USA Learn Behav (2021) 49:54–66 55 2010; Smirnova, Lazareva, & Zorina, 2000; Xia et al., 2001). range (1 vs. 4 and 2 vs. 5; Rugani et al., 2013a). The upper By training animals, numerical achievements can reach a high limit of this kind of numerical discrimination is 3 versus 4. level of abstraction. Beyond numerical discrimination, ani- Nevertheless, this limit can be exceeded by the use of cogni- mals can learn to match symbols to specific numerosities tive strategies as grouping (Rugani, Loconsole, & Regolin, (Biro & Matsuzawa, 2001; Boysen & Berntson, 1989; 2017) and by adding to each object individually distinctive Olthof, Iden, & Roberts, 1997; Pepperberg & Gordon, features, allowing for individual processing (Rugani et al., in 2005), perform simple mathematical operations with those press). symbols (Boysen & Berntson, 1989;Olthof et al., 1997), sym- In 2010, by taking advantage of filial imprinting, it was bolically label subsets of items embedded within heteroge- demonstrated that young domestic chicks, when presented neous arrays (Pepperberg & Gordon, 2005) and master the with two sets of objects, prefer to approach the larger one precursors of a zero-like concept (Howard et al., 2018; (Rugani et al., 2010b). The choice for familiar or novel stimuli Merritt, Rugani & Brannon, 2009; Pepperberg, 1988; in imprinting situations is known to be affected by the sex of Pepperberg & Brezinsky, 1991; Pepperberg & Gordon, the animals. When exposed to familiar and unfamiliar individ- 2005). Sophisticated and abstract numerical concepts can be uals, males and females of domestic chicks behave differently mastered by both primates and birds (Pepperberg, 2009; (Vallortigara & Andrew, 1991; Vallortigara, 1992a, b). Rugani, Vallortigara, & Regolin, 2016b), indicating that bird Females spend more time close to familiar individuals, where- brains, though characterized by a different pallial organization as males spend more time close to unfamiliar ones. (Güntürkün & Bugnyar, 2016), should not be neglected in Furthermore, both sexes pecked more at unfamiliar than at studying high cognition (Gibbs et al., 2008;Matsushima familiar individuals, and overall males pecked more than fe- et al., 2003;Pepperberg, 2017). males. These differences are probably the result of different To investigate the ontogenetic origins of numerical knowl- levels of attachment to conspecifics following imprinting edge, the domestic chick (Gallus gallus) is an ideal animal (Vallortigara, Cailotto, & Zanforlin, 1990). Females seem to model (Rugani, 2018; Versace & Vallortigara, 2015). Unlike develop stronger attachment to their fellows than males studies on adult animals, chicks can be tested very early in life, (McBride & Foenander, 1962; McBride, Parer, & allowing for the discovery of the origins of numerical com- Foenander, 1969; Vallortigara et al., 1990;Workman & prehension. Young chicks can learn to solve different numer- Andrew, 1989). ical problems, ranging from numerical discrimination The aim of this study was to investigate how male and (Rugani, Vallortigara, & Regolin, 2013b)to the useof ordinal female chicks respond to familiar and unfamiliar objects in a cues (Rugani, Regolin, & Vallortigara, 2007), arithmetic cal- number (quantity) discrimination test. Considering the differ- culation (Rugani et al., 2009), comprehension of proportion ent motivation of male and female chicks in approaching their (Rugani, Vallortigara, & Regolin, 2015b), and abstract ratios artificial social companion (Regolin et al., 2005), we expected (Rugani et al., 2016a). a different behavior depending on the sex of the animals. Exploiting chicks’ memories for their imprinting objects Using the original method developed by Rugani et al. allows one to assess whether chicks discriminate between dif- (2010b), we investigated not only how male and female do- ferent numbers of artificial social companions (i.e., objects mestic chicks divided their time in the proximity of a familiar they were exposed to soon after hatching; Rugani, Regolin, versus an unfamiliar number of objects, but also how they & Vallortigara, 2008, 2010b). Filial imprinting is a well- interacted (by social pecking) with familiar and novel objects known phenomenon (Bolhuis, 1991; McCabe, 2019; at test. This new measure allowed us to better understand the Vallortigara & Versace, 2018), allowing the young birds to factors underlying the intrinsic motivation to join the larger learn the characteristics of an object they have been exposed to number of artificial social companions. and to develop a robust social attachment toward it in the first few days of life (Bolhuis, 1991; Yamaguchi et al., 2012). Once imprinted, chicks regard their imprinting objects as so- cial companions (Regolin et al., 2005) and can generalize their Experiment 1 filial behaviors toward similar objects (Bolhuis & Horn, 1992; Versace et al., 2017). Previous studies have exploited chicks’ In this experiment, we applied the experimental procedure of memories for their artificial social companions (object they the first experiment by Rugani et al. (2010b) to test the dis- were reared with) to test their numerical abilities, which range crimination between 1 and 3 imprinting objects in 3-day-old from numerical discrimination (Rugani, Regolin, & domestic chicks. Here we determined the sex of the animal to Vallortigara, 2010b) to proto-arithmetic calculations in the assess any difference in the time spent at test by male versus range of small numbers, up to 3 (Rugani et al., 2009), in the female chicks near the numerically familiar versus numerical- large-number range (6 vs. 9 and 5 vs. 10; Rugani, Regolin & ly novel objects. Moreover, we introduced a novel measure Vallortigara, 2011a) and between the small- and large-number (spontaneous pecking) to assess the level of interaction of 56 Learn Behav (2021) 49:54–66 each sex based on the scoring of spontaneous pecking toward per cylinder). Half of the chicks were imprinted to one cylin- familiar versus unfamiliar objects at test. der, and the other half were imprinted to three cylinders (Table 1). Food (chick starter crumbs) and water were avail- able ad libitum. Ethics statement After 2 days spent under this rearing conditions (from Tuesday 9:00 am to Thursday 1:00 pm), chicks were individ- The study was performed in compliance with the European ually placed for 6 min in the testing apparatus where they were Union and the Italian laws on the treatment of animals. The free to choose and approach either their familiar numerosity procedures were approved by the Ethics Committee of the set or an unfamiliar numerosity set. University of Trento and licensed by the Italian Health Ministry (permit number 53/2020). Test Subjects For testing, animals were moved in a room adjacent to the rearing room and placed into the testing apparatus. This The number of chicks required in each group was a priori consisted of a short runway (45 × 20 × 30 cm, Fig. 1B), determined with a power analysis (Champely, 2020)with an illuminated by two LED lamps (12 V). The behavior of each effect size (d) of .65, and an alpha of .05. Results showed that animal was recorded using a Microsoft Life Camera located 20 individuals were required per group to achieve a power of 70 cm above the apparatus. .80. Overall, we used 147 chicks (75 females) of the strain Depending on the experimental condition, two different Ross 308 (Table 1). The eggs were obtained from a commer- sets of stimuli were located at either end of the runway (Fig. cial hatchery (Azienda Agricola Crescenti) and were incubat- 1B). Testing stimuli consisted of same size cylinders (5 cm ed in our laboratory under controlled conditions (37.7 °C and high, 2 cm diameter per cylinder) colored red or blue. Each 40% humidity). Three days before hatching, eggs were moved bird underwent a single test, which could be either an Absolute into opaque black boxes within a hatching chamber at 37.7 °C Discrimination or a Relative Discrimination test. The position and 60% of humidity. of each set in the runway was balanced across animals Soon after hatching, chicks were sexed (this chicken strain (Table 1). exhibits a sexual dimorphism on the wing feathers) and were In the Absolute Discrimination test, chicks were presented singly housed into rectangular cages (22 × 30 × 40 cm, Fig. with one versus three objects, which were identical to the 1A). Cages were illuminated by 30 W fluorescent lights in a imprinting objects (red cylinders, Table 1). In the Relative controlled temperature environment (30 °C). Chicks were Discrimination task, chicks were presented with two compos- reared together with an artificial stimulus (or set of stimuli) ite sets of four objects. One set comprised one red cylinder suspended 1 cm above the floor by a transparent thread in the (familiar object) and three blue cylinders (unfamiliar objects), centre of the cage. By exposing the animals to a set of stimuli while the other set comprised three red cylinders (familiar in their rearing cages, filial imprinting occurred, leading objects) and one blue cylinder (unfamiliar object, Table 1). chicks to develop a strong attachment toward those objects. The positions of the objects within the sets were fixed (such Stimuli consisted of red cylinders (5 cm high, 2 cm diameter as presented in Table 1). In the original study, the Relative Discrimination test was performed to check whether chicks Table 1 Number of animals and sets of stimuli used in the Absolute and would respond to the actual number of familiar objects within Relative Discrimination tests (chicks that did not respond were excluded a set of larger numerosity (composed of unfamiliar objects from the analysis and therefore are not included in this table). In the too). Relative Discrimination test, the position of the objects within the sets was fixed Data analysis To assess the preference toward a set of stimuli, the time spent by the chicks near each set (within a 15-cm area close to it, Fig. 1B) was automatically scored using Ethovision (version 13). A preference for the imprinting numerosity (%) was then calculated using the following formula: Preference for imprinting numerosity time spent close to the familiar imprinting numerosity ¼ x100: time spent close to both sets of stimuli Learn Behav (2021) 49:54–66 57 Fig. 1 Three-dimensional representation of the rearing cage (A) and the by a transparent thread. Dashed-lines in B delimited the zones (left, center testing apparatus (B). B shows an example of the Absolute and right) in which the time spent by the animal was scored (the zones Discrimination test. The stimuli were suspended 1 cm above the floor were defined computationally using Ethovision) Post hoc Tukey tests were performed when required using A value higher than 50% indicated a preference for the fa- miliar imprinting numerosity (if imprinted with 1, a preference Bonferroni’scorrection. All the statistical analyses were performed using RStudio for 1). A value lower than 50% indicated a preference for the unfamiliar numerosity set (if imprinted with 1, a preference for v1.1 (RStudio Team, 2015) with the following packages: goftest (Faraway et al., 2019), nlme (Pinheiro et al., 2020), 3). A score of 50% indicated no preference (chance level). As pecking is a behavior expressed during social exploration lme (Bates et al., 2015), tidyr (Wickham & Lionel, 2020), and recognition in domestic chicks (Gottier, 1968;Nicol, 2015; plyr (Wickham, 2011), dplyr (Wickham et al., 2020), reshape (Wickham, 2007), lsr (Navarro, 2015), ggplot2 (Wickham, Schjelderup-Ebbe, 1922; Vallortigara, 1992a), we also scored the number of pecks assigned by the animals to each stimulus 2016), pwr (Champely, 2020). within each set. Manual scoring was made by a scorer blind to the experimental conditions. The coding reliability of the pecks Results was assessed by re-coding 21 chicks randomly selected (Pearson’s correlation test showed a high correlation between Absolute Discrimination the two codings, r = 0.99). Pecking analysis was performed once the videorecordings were already archived. Preference for the imprinting numerosity The results are Unfortunately, while uploading the videos, a folder got showninFig. 2A. There was a significant effect of Sex corrupted and prevented us from coding the pecking behaviour of 21 chicks (12 females) in the Relative Discrimination test. (F(1, 66) = 6.73, p < 0.05), but not of Imprinting Numerosity (F(1, 66) = 0.20, p = 0.66) or interaction (F(1, Chicks that did not respond (one female and two males) were removed from the analysis as they did not score any 66) = 1.69, p =0.20). Overall, the preference for the imprinting numerosity set preference during the entire testing duration. was significantly different from chance level for males (t(33) = 2.50, p < 0.05, Cohen’s d = 0.42, Bonferroni correction), but Statistical analysis not for females (t(35) = -0.54, p = 0.59, Cohen’sd=0.090, Bonferroni correction). Males spent on average 66% (± 5.89 To determine whether animals showed preferences for the sets SEM) of their time close to the imprinting numerosity set, while females spent on average 47% (± 6.42 SEM) of their of objects differing across Sex (female, male) and Imprinting time close to it. Numerosity (1, 3), we performed an ANOVA for each dis- crimination task (Absolute, Relative). To meet parametric as- Pecks The results are shown in Fig. 2B. When imprinted with 1, sumptions, we arcsine-transformed the data. To check wheth- er chicks had a significant preference for the imprinting there was a significant effect of Object (F(3, 132) = 6.46, p < 0.01) and of the interaction between Object and Sex (F(3, 132) numerosity, we performed two-tailed one-sample t-tests against chance level (50%). = 6.36, p < 0.01) but a non-significant effect of Sex (F(1, 132) = 0.86, p = 0.36). While females pecked similarly at each object, To determine whether animals were pecking at the stimuli (each cylinder within a set of stimuli) differently across Sex the post hoc analysis revealed that males pecked significantly more at the single object in comparison to the central (t(132) = (female, male), we performed an ANOVA for each discrimina- tion task (Absolute, Relative) and Imprinting Numerosity (1, 3). 4.10, p < 0.01, Cohen’s d = 1.41) and right-most (t(132) = 3.50, p < 0.05, Cohen’s d = 1.19) objects within the set of three. To meet parametric assumptions, we log-transformed the data. 58 Learn Behav (2021) 49:54–66 Fig. 2 Graph (A) represents the time spent by the chicks during testing (females in red and males in light-blue) and Imprinting Numerosity (* p close to their imprinting numerosity between Imprinting Numerosity and < 0.05; ** p < 0.01). Light blue asterisks show the statistical difference in Sex (p < 0.05, *). Graph (B) represents the number of pecks made toward males; black asterisks show the statistical differences in both males and each stimulus composing the different set of stimuli between Sex females When imprinted with 3, there was a significant effect of Sex significant effect of Sex (F(1, 70) = 0.19, p =0.67) norof the (F(1, 132) = 4.12, p < 0.05) and Object (F(3, 132) = 3.99, p < interaction (F(1, 70) = 0.00, p =0.99). 0.01), but no interaction (F(3, 132) = 0.30, p = 0.82). As revealed Overall, the preference for the imprinting numerosity set by the ANOVA, males (mean = 9.90, SEM = 2.27) pecked was significantly different from chance level for the chicks significantly more than females (mean = 5.31, SEM = 1.25) at imprinted with 1 (t(35) = -4.74, p <0.001, Cohen’sd= the objects, a difference that seems to mainly be driven by the 0.79, Bonferroni correction) and 3 (t(37) = 5.32, p < 0.001, number of pecks made at the left-most object within the set of Cohen’s d = 0.86, Bonferroni correction). Nevertheless, the three. Males pecked on average 15 times (SEM = 4.79) at it, preferences between these two groups were the opposite. while females pecked on average five times (SEM = 1.76) at it. Chicks imprinted with 1 spent on average 23% (±5.64 SEM) Overall, the post hoc analysis revealed that chicks pecked of their time close to the imprinting numerosity set while significantly more at the single stimulus in comparison to the chicks imprinted with 3 spent on average 79% (±5.36 SEM) central object composing the set of three stimuli (t(132) = close to it. This indicates that, independently of rearing con- 3.05, p < 0.05, Cohen’s d =0.73). ditions and sex, chicks approached the larger set of familiar objects. Relative Discrimination Pecks The results are shown in Fig. 3B. When imprinted on 1 Preference for the imprinting numerosity The results are or 3, there was a significant effect of Object (imprinted with 1: showninFig. 3A. There was a significant effect of F(7, 184) = 11.48, p < 0.001; imprinted with 3: F(7, 208) = Imprinting Numerosity (F(1, 70) = 53.16, p < 0.001) but no 7.75, p < 0.001), but not a significant effect of Sex (imprinted Learn Behav (2021) 49:54–66 59 Fig. 3 (A) The time spent by the chicks during testing close to the object different set of stimuli between Imprinting Numerosity (females and set containing the number of familiar objects experienced during males grouped; *** p < 0.001). Black asterisks show the statistical imprinting between Imprinting Numerosity and Sex (p < 0.001, ***). differences in both males and females (B) The number of pecks made toward each stimulus composing the with 1: F(1, 184) = 0.01, p = 0.92; imprinted with 3: F(1, 208) motivation of male and female birds in exploring a novel =1.10, p = 0.30) or of the interaction (imprinted with 1: F(7, numerousness of familiar objects. Males seemed more in- 184) = 0.36, p = 0.93; imprinted with 3: F(7, 208) = 0.71, p = clined to spend time close to the familiar numerousness, 0.66). while females seemed equally motivated in joining the fa- No matter whether they had been imprinted on 1 or 3, the miliar group or exploring the novel one. When tested in the post hoc analysis revealed that chicks pecked significantly presence of familiar and unfamiliar objects (Relative more at the single blue object in the set in comparison to all Discrimination), both sexes used the relative numerical other objects (statistics are detailed in the Online information available concerning the subset of familiar ob- Supplemental Material table). jects present within each set and chose to associate with the larger set of familiar objects as described in the original study by Rugani et al. (2010a, b). Thepresenceofnovel Experiment 2 objects seems to play a relevant role in the choice to ap- proach the larger number of familiar objects, or in avoiding In the first experiment, chicks behaved differently in the the larger number of unfamiliar ones. Support for the latter two discrimination tests. When only exposed to familiar hypothesis comes from the analyses of the pecks, which objectsattest(Absolute Discrimination), males consistently highlight an increased number of pecks at the approached the familiar numerousness, whereas females single novel object in the group comprising three familiar did not show any preference. This may indicate a different objects and an unfamiliar one. 60 Learn Behav (2021) 49:54–66 To investigate the importance of unfamiliarity, we conduct- 1.96, p = 0.12). As revealed by the ANOVA, males were ed a second experiment in which we manipulated the degree pecking (mean = 8.80, SEM = 1.40) significantly more than of unfamiliarity. females (mean = 6.21, SEM = 1.39) at the objects. Furthermore, the post hoc analysis revealed that males pecked significantly more at the left-most object (mean = Methods 11.16, SEM = 2.39) in the set of three objects in comparison to the single object (mean = 8.21, SEM = 4.67; t(144) = -3.45, The general procedure was the same as in the first experiment. p < 0.05, Cohen’s d = -1.12). The opposite tendency was The same number of objects as in the Absolute Discrimination observed in females although not revealed by the post hoc was used (Table 2), but this time we slightly modified the analysis as the variability of the pecks to the single object appearance of the stimuli during testing. Chicks at test were seemed quite high (mean = 13.42, SEM = 5.84) in comparison offered a choice between one or three objects, but a small to that of the left-most object within the set of three objects yellow dot (diameter of 5 mm) was added on the central object (mean = 5.79, SEM = 1.61). of the set corresponding to the original imprinting numerosity When imprinted with 3, there was a significant effect of (Table 2). For the chicks that had been imprinted to one object, Object (F(3, 144) = 6.92, p < 0.001) but no significant effects the yellow dot was placed on the single object during testing. of Sex (F(1, 144) = 0.46, p = 0.50) nor of the interaction (F(3, For the chicks that had been imprinted to three objects, the 144) = 0.23, p =0.87). yellow dot was placed on the central object composing the set The post hoc analysis revealed that chicks pecked signifi- of three during testing. cantly more at the single stimulus in comparison to the left- We used 79 chicks (40 females) of the strain Ross 308 most one (t(144) = 3.48, p < 0.01, Cohen’s d = 0.80) or to the (Table 2). Chicks that did not respond (two females and one right-most one (t(144) = 4.10, p <0.001, Cohen’s d =0.94) in male) were removed from the analysis as they did not score the set of three objects . any preference during the entire testing duration. Results General discussion Preference for the imprinting numerosity The results are Number cognition in birds has been widely investigated. showninFig. 4A. There was a significant effect of Studies performed by Pepperberg on Alex the parrot illustrat- Imprinting Numerosity (F(1, 72) = 7.43, p < 0.01) but no ed the impressive numerical competences owned by avian significant effects of Sex (F(1, 72) = 0.075, p = 0.79) or of species (Pepperberg, 2009). Alex was able to quantify up to the interaction (F(1, 72) = 1.87, p =0.18). six-item sets using English labels with an accuracy of 80%, Overall, the preference for the imprinting numerosity was and remaining unaffected by array quantity, mass, or contour significantly different from chance level for the chicks (Pepperberg, 1994; Pepperberg & Gordon, 2005). The imprinted to 1 (t(37) = -5.86, p <0.001, Cohen’s d =0.97, achievement of a high level of abstraction in numerical com- Bonferroni correction) but not for the chicks imprinted to 3 prehension suggests that birds may naturally deal with numer- (t(37) = -0.83, p = 0.41, Cohen’s d = 0.14, Bonferroni correc- ical information in everyday life. In our study, instead of fo- tion). Chicks imprinted to 1 spent on average 20% (±4.98 cusing on the symbolic use of numbers as Pepperberg did, we SEM) of their time close to the familiar numerosity, while studied a much simpler numerical ability (numerousness dis- chicks imprinted to 3 spent on average 44% (±6.62 SEM) crimination), exploiting a paradigm that allows one to test close to it. numerical comprehension in the absence of any numerical training. This allows for the understanding of how birds can Pecks The results are shown in Fig. 4B. Whenimprintedwith spontaneously deal with numerical cues. 1, there was a significant effect of Sex (F(1, 144) = 5.51, p < As in previous studies (Rugani et al., 2008, 2010b), our 0.05) and an interaction between Object and Sex (F(3, 144) = results showed that chicks could use numerical/quantity infor- 4.23, p < 0.01), but no significant effect of Object (F(3, 144) = mation to discriminate between different sets of objects. As we did not control for the role of continuous physical vari- Table 2 Number of animals and sets of stimuli used in the second ables, we cannot disentangle whether chicks used numerical experiment (chicks that did not respond were excluded from the and/or continuous quantities to discriminate. However, previ- analysis and therefore are not included in this table) ous work has shown that chicks, depending on the available cues, could use both sources of information (Rugani et al., 2010b). Moreover, several sources of supporting evidence points to the existence of a general magnitude system in hu- man and non-human species that comprises both discrete Learn Behav (2021) 49:54–66 61 Fig. 4 Graph (A) represents the time spent by the chicks during testing between Sex (females in red and males in light-blue) and Imprinting close to their imprinting numerosity set between Imprinting Numerosity Numerosity (* p < 0.05; ** p < 0.01; *** p < 0.001). Light blue asterisk and Sex (*** p < 0.015). Graph (B) represents the number of pecks shows the statistical difference in males; black asterisks show the statis- assigned to each stimulus composing the different sets of stimuli tical differences for both males and females (countable) and continue quantities (Bortot, Stancher & and had a strong preference to associate with the set composed Vallortigara, 2020; De Corte, Navarro & Wasserman, 2017; of more familiar objects (three red objects and one blue ob- Di Giorgio et al., 2019;Gallistel, 1989;Merritt, Casasanto, & ject). Motivational differences may support chicks’ tendency Brannon, 2010;Walsh, 2003). to approach the larger group of social companions: the larger In our study, we focused on whether males and females group can guarantee more protection toward potential preda- used numerical/quantities cues similarly. We found that males tors, higher level of social interaction, a richer environment, and females make different use of numerical cues depending and in the natural situation more heat (Pulliam, 1973;Roberts, on the context (familiar, in the Absolute Discrimination task, 1996). Furthermore, the experimental procedure used in our or familiar and unfamiliar in the Relative Discrimination task). study exploits the chick’s memory for its imprinting object (or The Absolute Discrimination task showed that males prefer set of objects). As a result of filial imprinting, an increase in to associate with the familiar numerosity set, while females fear is observed when exposed to novel stimuli (Bolhuis, 1991). This leads the young animals to avoid proximity with showed no preference. This may indicate that in a novel envi- ronment, as the testing apparatus was, males are motivated to novel objects, which therefore could explain why chicks tend approach the familiar numerosity sets, while females are to associate with the set composed of the largest number of equally motivated to explore the two sets. The Relative familiar objects and the fewest number of unfamiliar objects. Discrimination task revealed a completely different pattern The number of pecks here is not to be interpreted as a of results, but this time more similar to what Rugani et al. feeding behavior. Instead, it likely reflects a social, either (2010b) described initially. Males and females behaved alike affiliative or aggressive, behavior toward familiar or 62 Learn Behav (2021) 49:54–66 unfamiliar objects (Vallortigara, 1992a), providing inter- 1992a, b). Hence, it is possible that chicks used esting cues as to the possible nature of sex differences. numerical/quantitative information available to determine While affiliative pecks are usually equally distributed which object was more likely to be unfamiliar. across time among familiar individuals, aggressive pecks A similar interpretation can be made by looking at the are reiterated toward unfamiliar individuals/objects results obtained in the Relative Discrimination task. Chicks (Schjelderup-Ebbe, 1935). Pecking behavior may, there- repeatedly pecked at the blue object incorporating the larger fore, reveal lack of recognition when intensively exhibited set of familiar objects (three red objects), demonstrating that toward an individual (Guhl & Ortman, 1953; Vallortigara, they recognized the blue object as being unfamiliar within a 1992a, b). In the Absolute Discrimination task, males familiar set. pecked more at the familiar numerosity set. This measure Our results suggest that male and female domestic correlates with the time spent near the familiar numerous- chicks use numerical/quantity information slightly differ- ness and shows a preference of male chicks to interact ently depending on the familiarity of the objects. In a more with the familiar set rather than with the novel familiar context, males tend to use numerical/quantity in- one. A peculiar behavior emerged from the analysis of formation to discriminate between two sets of familiar the distribution of pecks toward the array of three objects: objects, while females focus on each familiar object indi- males seemed to peck more at the left object than at the vidually. Interestingly, in a context composed of unfamil- central or at the right one. This left-sided preference could iar objects, males and females expressed similar behaviors be related to a general bias in the allocation of spatial and chose to associate with the set containing less unfa- attention (Diekamp et al., 2005; Regolin, 2006; Rugani miliar objects. In the previous study (Rugani et al., et al., 2011b). Day-old domestic chicks, in fact, associate 2010b), no difference was found between the Absolute numbers with space in different contexts. Chicks trained and Relative Discrimination tasks. Therefore, the authors to respond to a certain numerical value spontaneously concluded that chicks mainly use the number of familiar associated a smaller number with the left side and a larger objects to discriminate between two sets of stimuli and number with the right side of space (Rugani et al., 2020, that they choose to associate with the larger set of familiar 2015a). Chicks, trained to identify a target element (e.g., objects. Our data instead support the idea that chicks the fourth) in a sagitally oriented series of identical ele- mainly rely on the number of unfamiliar objects instead ments, when required to react to an identical series but of the number of familiar ones. This difference could be rotated by 90°, identified most often the left target than possibly explained by the colors used: yellow and light the right one (Rugani et al., 2010a, 2015a). A lateral bias pink in the study by Rugani et al. (2010b), versus red has also been found in a numerical task which required to and blue in the present study. The relevance of the unfa- discriminate between two groups of artificial social com- miliar object may have been emphasized using novel blue panions. Female chicks were reared with a set of identical objects instead of light pink ones. Even if different strat- objects. At test, the objects disappeared one at a time egies seem to be at the basis of the current study (avoid behind one of two identical screens, one on the left and the larger number of unfamiliar objects) and in the previ- one on the right. On a free-choice test, chicks showed a ous study (approach the larger number of familiar objects), preference for the larger group. Nevertheless, their perfor- nevertheless both studies converge in demonstrating that mance was higher when the larger group was hidden on day-old chicks do discriminate numerousness in the ab- the right side (Rugani, Rosa Salva, & Regolin, 2014). sence of any numerical training. Differences in strains This evidence suggests that also in a spontaneous search should also be considered. for social companions a tendency can emerge to associate To better understand to which degree unfamiliarity influ- numbers and space. The latter evidence is also in line with ences chicks’ behaviors, we conducted a second experiment. our new findings in which male chicks tend to explore the The task in this second experiment shared properties with the smaller numbers of social companions on the left side. Absolute and Relative Discrimination tasks. During testing, Going back to our current study, females, in contrast, chicks were offered a choice between a set of one or three visited and pecked at all objects individually, which can objects (suchasinthe Absolute condition). However, we probably explain why they did not express any preference slightly changed the appearance of the familiar numerosity in the time spent analysis (females were at chance-level). set so that it neither appeared completely familiar nor Curiously, when imprinted with the set composed of three completely unfamiliar, by adding a small yellow dot on one objects, both sexes significantly pecked more at the single of the objects of the familiar numerosity set (for the stimulus as if they were treating it as a less familiar indi- discriminability of imprinting object based on individual vidual. Indeed, pecking can also demonstrate a lack of features depicted on them, see Fontanari et al., 2011). recognition when it is repeatedly directed toward a spe- In the second experiment, chicks tended to explore the cific individual (Guhl & Ortman, 1953; Vallortigara, unfamiliar numerosity set. This demonstrates that even a slight Learn Behav (2021) 49:54–66 63 change in the appearance of one object influences the chick’s a context, using numerical abilities would be an efficient strat- decision to associate with either set. Although no sex differ- egy, as has been shown to occur in several other species ence was observed in terms of time spent close to either set, (Benson-Amram et al., 2011; Bonanni et al., 2011; Cassidy the pecking analysis revealed that males and females behaved et al., 2015; McComb, Packer, & Pusey, 1994;Van Belle & differently. When imprinted with one, females pecked more at Scarry, 2015; Wilson et al., 2012). the single object (with the yellow dot) than at the other objects In conclusion, our results show that young and almost (set of three, where they spent 72% of their time). As in the naïve domestic chicks rely on numerical information to make Absolute Discrimination task, females seem to focus more on social decisions. They first discriminate between familiar ver- individual recognition, which suggests that they do not treat sus unfamiliar objects based on their perceptual features, and the single stimulus (with the yellow dot) as entirely unfamiliar. then they estimate the numerousness of both sets to avoid the In contrast, males completely avoided the single stimulus larger number of unfamiliar objects. Moreover, the degree of (with the yellow dot) and pecked more at the set of three. novelty of the unfamiliar objects seems to correlate with the The results of this second experiment appear to be in agree- avoidance of the unfamiliar set. Numerousness is, therefore, a ment with the study by Rugani, Regolin and Vallortigara relevant information animals can spontaneously use in a social (2010b) and with our first experiment, suggesting that chicks context to optimize their fitness. firstly discriminate between familiar and unfamiliar objects Acknowledgements We are grateful to Elif Karakoç for helping to test before making a decision based on their numerousness. the animals, and to Nicholas Zampiero and Chiara Eccher for assisting in Our study provides additional information concerning the the coding of the chicks’ behaviors. use of numerical or quantitative information by young domes- This project was supported by funding from the European Research tic chicks in the specific context of filial imprinting. Taken Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No. 833504 SPANUMBRA) to together, our results confirm that chicks can use numerousness GV. The project also received funding from the European Union’s to discriminate between different set of objects. It also dem- Horizon 2020 research and innovation program under the Marie onstrates that male and female domestic chicks do not always Sklodowska-Curie (grant agreement No. 795242 SNANeB) to RR; and use available numerical cues similarly, and that, instead, they from a PRIN 2017 ERC-SH4–A (2017PSRHPZ) to LR and GV. might prefer to use different strategies depending on the fa- Funding Open access funding provided by Università degli Studi di miliarity of the objects. Overall, females seem more flexible in Trento within the CRUI-CARE Agreement. the use of numerical/quantitative cues depending on the con- text. In a familiar context, females perform individual recog- Data availability The datasets (.csv) are available on Fig Share (10.6084/ nition rather than using numerical/quantitative information to m9.figshare.12336140). make a decision. In an environment composed of familiar as Open Access This article is licensed under a Creative Commons well as unfamiliar objects, females used numerical informa- Attribution 4.0 International License, which permits use, sharing, tion to discriminate between two sets of objects. In contrast, adaptation, distribution and reproduction in any medium or format, as males tend to rely upon numerical information either by ap- long as you give appropriate credit to the original author(s) and the proaching the familiar numerosity set when exposed to famil- source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article iar objects or the larger set of familiar objects when exposed to are included in the article's Creative Commons licence, unless indicated sets of familiar and unfamiliar objects. otherwise in a credit line to the material. If material is not included in the Likely the sex difference we observed may derive from the article's Creative Commons licence and your intended use is not natural history of feral birds. Adult fowls are organized in permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a groups comprising a dominant rooster and many hens copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. (Queiroz & Cromberg, 2006). Males are more solitary as they spend most of their time maintaining and patrolling their ter- ritory, whereas females tend to live in strict hierarchies that they develop and maintain through time (Gottier, 1968; References McBride & Foenander, 1962; McBride et al., 1969; Schjelderup-Ebbe, 1922). Such organization may favor the Agrillo, C., Dadda, M., & Bisazza, A. (2006). 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