The importance of active search for effective social learning: an experimental test in young passerines

Animal Behaviour 108 (2015) 165e173

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The importance of active search for effective social learning: an experimental test in young passerines Noa Truskanov*, Arnon Lotem Department of Zoology, Faculty of Life Sciences, Tel-Aviv University, Tel-Aviv, Israel

a r t i c l e i n f o Article history: Received 17 May 2015 Initial acceptance 5 June 2015 Final acceptance 8 July 2015 Available online MS. number: 15-00405 Keywords: active search attention learning mechanisms scrounging social foraging social learning

Despite extensive research on social learning in humans and animals, the mechanisms of social learning and the causes of its success or failure are still being debated. In the case of social foraging, there is conflicting evidence as to whether scrounging on conspecifics' food finding facilitates social learning or, rather, inhibits learning of food-related cues. In house sparrows, Passer domesticus, social learning has previously been shown to be inhibited during scrounging. In the present study, we found that handreared fledgling house sparrows that were imprinted on a mother model and scrounged on the food that she found readily learned the colour chosen by the mother as a food-related cue. However, our experiment also demonstrated that this social learning may indeed be less effective when it is not mediated by active search: fledglings following a mother model that pointed at the location of the seeds, forcing them to dig actively in the sand, developed a stronger preference for the target colour than fledglings whose mother had exposed the seeds for them. The latter were much more sensitive to information that they had acquired from independent search, which may explain a wide spectrum of variable results in social learning and highlight the potential importance of mechanistic details in its evolution. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.

One of the potential benefits of sociality is the ability to acquire information about the environment through social learning: learning that is influenced by observation or interaction with another individual or with the products of its behaviour (Heyes, 1994; Shettleworth, 2010). Social learning is widespread throughout the animal kingdom (Heyes & Galef, 1996; Hoppitt & Laland, 2008) and is suggested to be adaptive in a variety of contexts, including predator avoidance, mate choice and foraging behaviour (Arbilly, Motro, Feldman, & Lotem, 2011; Galef, 1995; Galef & Giraldeau, 2001; Reader, Kendal, & Laland, 2003; Rendell et al., 2010; Shettleworth, 2010). The ability to learn socially is also a prerequisite for cultural transmission and for the development of traditions in humans and animals (Boyd & Richerson, 1985; Cavalli-Sforza & Feldman, 1981; Danchin, Giraldeau, Valone, & Wagner, 2004; Galef, 2013). However, despite the wide interest it attracts and the vast amount of empirical and theoretical research it has elicited, even the most basic mechanisms underlying social learning are not entirely clear and the extent to which these mechanisms have evolved specifically for social learning is still

* Correspondence: N. Truskanov, Department of Zoology, Faculty of Life Sciences, Tel-Aviv University, Tel-Aviv, 69978, Israel. E-mail address: [email protected] (N. Truskanov).

being debated (Galef, 2013; Heyes & Pearce, 2015; Leadbeater, 2015). Consequently, when animals fail to learn socially it is not clear whether this is because of mechanistic constraints (e.g. Heyes & Pearce, 2015) or, rather, because it is simply not adaptive to employ social learning in such cases (Laland, 2004). A combination of these two explanations may also be possible: learning mechanisms that support social learning might have been modified by natural selection, making it either more or less likely that animals learn socially under different conditions (Heyes, 2012; Laland, 2004; Leadbeater, 2015; Lotem & Halpern, 2012). Social learning may especially be expected to thrive in the context of social foraging, in which individuals that follow other group members and scrounge on the food that they find (Barnard & Sibly, 1981; Giraldeau & Caraco, 2000; Giraldeau & Dubois, 2008) have the opportunity to learn food-related cues or specific foraging techniques from those they follow (Giraldeau, 1984; Laland, 2004). However, empirical evidence suggests that this may not always be the case. While there are examples in the literature in which scrounging indeed promotes social learning (Aisner & Terkel, 1992; Caldwell & Whiten, 2003; Fritz & Kotrschal, 1999; Midford, Hailman, & Woolfenden, 2000; Thornton & Malapert, 2009), in many other cases social learning appears to be inhibited during scrounging on conspecifics' food finding (Beauchamp & Kacelnik,

http://dx.doi.org/10.1016/j.anbehav.2015.07.031 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.

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1991; Fragaszy & Visalberghi, 1989; Giraldeau & Lefebvre, 1987; Humle & Snowdon, 2008; Ilan, Katsnelson, Motro, Feldman, & Lotem, 2013; Nicol & Pope, 1994). Different mechanisms have been suggested to explain why scrounging inhibits social learning. One possibility is that learning to associate cues or actions with food reward may be blocked or overshadowed by associating the food reward mainly with the presence (or with the behaviour) of the demonstrator (Beauchamp & Kacelnik, 1991; Giraldeau & Lefebvre, 1987). Interestingly, in both pigeons, Columba livia, and zebra finches, Taeniopygia guttata, for which these mechanisms have been suggested, social learning works successfully if followers observe the demonstrator but cannot access the food and scrounge (Giraldeau & Lefebvre, 1987; Riebel, Spierings, Holveck, & Verhulst, 2012). Accordingly, blocking or overshadowing occurs in those cases in which the observer is engaged in scrounging from the demonstrator, but may not occur when it merely observes it. An alternative explanation is that positive experience with scrounging reduces the motivation to learn the searching behaviour or to exhibit behaviours that have in fact been learned (Giraldeau & Templeton, 1991). Finally, it has also been suggested that scrounging on other individuals' food finding distracts the scrounger's attention from relevant cues, especially in a flock and when more than a single scrounger is involved (Lefebvre & Helder, 1997). Given that there are some cases in which scrounging inhibits social learning, how can we explain those cases in which scrounging seems to facilitate it (Aisner & Terkel, 1992; Caldwell & Whiten, 2003; Fritz & Kotrschal, 1999; Midford et al., 2000; Thornton & Malapert, 2009)? One possible explanation is that under circumstances in which social learning is especially important, (Aisner & Terkel, 1992; Caro & Hauser, 1992; Clarke, 2010; Thornton & Clutton-Brock, 2011; Thornton & McAuliffe, 2006), the attentional mechanisms directing the learner to process the relevant data (Heyes, 2012; Lotem & Halpern, 2012) have evolved to minimize the effects of blocking and overshadowing. Another possibility is that the facilitation (as opposed to inhibition) of social learning during scrounging is related not to differences in attentional mechanisms, but to differences in certain important behavioural aspects that facilitate successful learning. One such important aspect may be the extent to which the learning process involves active search and selfexperience. As strongly emphasized in the past (Galef, 1995; Galef & Giraldeau, 2001), social learning may be best perceived as individual learning that is facilitated by social stimuli (Heyes, 2012; Heyes & Pearce, 2015; Leadbeater, 2015). Accordingly, social learning should be as successful as individual learning as long as the conditions for the learning process are the same, that is, when demonstrators merely provide opportunities for individual learning while minimizing their own influence. A previous study on socially foraging house sparrows, Passer domesticus, inspired us to test these ideas experimentally. That study, by Ilan et al. (2013), showed that adult sparrows failed to learn the sand colour that indicated the presence of food when they scrounged from other flock members. The sparrows' colour preference was based only on what they had experienced during independent search. Thus, they had either failed to learn socially or failed to use social information (which was perhaps indeed learned) in order to find food. Moreover, individuals also failed to learn when the seeds were already exposed by other birds (Ilan et al., 2013). It is possible that a lack of active search in the sand prevented the sparrows from learning socially. Therefore, it is predicted that social learning will be more effective when learners are provided with the opportunity to search actively and to practise the same foraging process that they normally experience during individual learning (Laland & Plotkin, 1992; Moscovice & Snowdon, 2006).

To test this hypothesis we studied social learning of food-related cues (sand colour) in hand-reared house sparrow fledglings that were imprinted on a mother model (a stuffed female house sparrow) and scrounged on the food that she found. Our goal was twofold. First, we determined whether young sparrows that follow their parents can learn socially food-related cues under the scrounging conditions that appear to inhibit social learning in adult individuals. Second, we determined whether the success of such social learning is mediated by different degrees of active search performed by the fledgling. To that aim, fledglings were assigned to one of two experimental treatments. In one treatment, the mother model (activated by the experimenter) exposed hidden seeds in one of two types of coloured sand and allowed the fledgling to approach them directly. In the other treatment, the mother merely pointed to the location of the seeds, prompting the fledgling to dig actively in the coloured sand. Following a training period, we tested the fledglings' sand colour preference during independent foraging, and examined to what extent their preference in the test was related to the degree of active search and to the relative success when searching and scrounging in different sand colours during the training period. METHODS Hand Rearing and Pre-experimental Training We hand-reared house sparrow nestlings, using methods developed by Grodzinski and Lotem (2007) and by Katsnelson, Motro, Feldman, and Lotem (2008, 2011). Hand-reared sparrows were imprinted on a stuffed model of a female sparrow (hereafter: the mother model) that had been used to feed the nestlings during the rearing stage, and was consequently followed by them in their search for food after fledging. Two cohorts of 12 nestlings were collected from nests in a captive house sparrow breeding colony at the I. Meier Segal's Garden of Zoological Research, Tel-Aviv University, Israel. In each cohort, no more than three nestlings were taken from the same nest, with two nestlings from each nest being the common procedure. Our final sample size of 16 fledglings (see below) originated from nine different nests and nestmates were assigned to separate experimental treatments where possible (i.e.: [2:1] [1:1] [1:1] [1:1] [1;1] [1:1] [1] [1] [1]). Nestlings were raised in three incubators, containing separate rearing boxes (10
10 cm and 8 cm high) lined with cotton wool and dry straw, weighed every morning before feeding started, and fed from syringes containing a mixture of commercial hand-rearing blend, vitamins, calcium and minced fly larvae (supplemented by mashed boiled eggs from the age of 8 days). Feeding sessions during which nestlings were fed to satiation were carried out at 15e30 min intervals throughout the day (0700e1900 hours). To imprint the nestlings on the mother model, they were fed adjacent to its beak, while the mother model itself was oriented towards the nestling. All individuals were ringed with a numbered aluminium ring to ensure individual recognition at later stages. Towards fledging, at the age of 13e15 days, all individuals were transferred to individual cages. The cages were visually isolated from each other and were located in the outdoor premises of the Zoological Garden. Each cage (75
45 cm and 45 cm high) contained a rearing box (the old ‘nest’ from which the young had fledged), wooden branches and artificial foliage at the rear, and a wooden foraging grid (47
38.5 cm) with 30 wells (2.5 cm diameter, 1.8 cm deep and 8.5 cm distance between well centres) at the front. A water bowl and a food bowl containing an ad libitum supply of commercial seed mixture and grated boiled eggs were placed on top of the grid, so that the fledglings got used to landing and hopping on the grid. Feeding was gradually shifted from hand

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rearing to joint pecking with the mother model, which continued to be introduced to the fledglings throughout this stage. The shift from hand rearing to joint pecking took place over 4 and 5 days (in the second and first cohorts, respectively), and was accomplished by the age of 19e20 days. Upon reaching independence, the fledglings were capable of independent feeding but still attached to the mother model. At this pre-experimental training stage they were first trained to look for exposed millet seeds in the feeding wells of the foraging grid (which they learned to do within 2 days), and then gradually trained to find the seeds when they were covered with natural uncoloured sand (which they learned to do within 1e2 days). This pre-experimental training was conducted in the presence of the foraging mother model, which was connected by wire to a long pole, allowing the experimenter to move it to various locations and to mimic a foraging sparrow (Fig. 1a). Thus, in the final stages of training, the mother model directed the fledglings to wells containing covered seeds by repeatedly pointing towards the well surface as if she was pecking, but without touching the sand. Note that no teaching or intentional pointing is assumed by this activity or by the term pointing; it merely aims to mimic a mother's foraging activity that does not expose seeds to the fledglings (i.e. a mother that eats the seeds she has found but, in so doing, stimulates the fledglings to search in the same spot). Having ensured that all individuals had responded to this pointing and could retrieve the covered seeds, we then randomly assigned the fledglings to one of two experimental conditions (see below), while controlling for body mass on the day of fledging and for nest of origin (randomized block design). Social-learning Experiment The training phase During the training stage the feeding wells were covered with either blue or red sand, assigned randomly (across individuals) to either 15 constant or 15 variable rewarding feeding wells. All the constant wells contained two millet seeds while only three of the variable wells (20%) contained seeds, but in a large quantity of ca. 15 seeds. In each training session (i.e. the presentation of a new foraging grid in the cage), the mother model was made to approach only the variable rewarding wells that contained the 15 or so seeds, guiding the fledgling to find a reward in these wells and thus helping it to learn to prefer their associated colour (hereafter the target colour). Note that for fledglings that followed the mother, the reward probability of the variable wells was no longer variable (they always found seeds when following the mother). However, the overall low probability of finding a reward in the variable wells

(a)

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implies that a fledgling is unlikely to learn to prefer the target colour through independent search (i.e. through individual learning). To further reduce this probability, each of the variable rewarding wells was surrounded by wells of the nontarget colour (see Fig. 1b). Since the nontarget colour (hereafter the alternative colour) always contained a small reward of two seeds, individuals that searched independently near the mother were likely to learn to prefer the alternative colour. Thus, our experimental set-up created a situation in which success in independent search was almost always associated with the alternative colour (see Fig. 1b), while a preference for the target colour could only be explained as a result of social learning (excluding the very few rare cases of finding a rewarding variable well through independent search. These cases could be identified in the videos and controlled for in our analysis). As stated above, beyond the first goal of determining whether young sparrows can learn socially from their parents, our second goal was to determine whether the parent's behaviour (exposing the food or merely pointing at its hidden location) can affect the success of this learning. To that aim, the fledglings were assigned to one of two experimental conditions. In one condition, the mother model pecked at the sand and exposed the seeds, thus allowing the young to scrounge directly on the food that she found (hereafter the ‘exposing mother’ treatment). This treatment may cause the fledgling to focus on the seeds (or on the ‘mothereseed’ complex), which may thus block the learning process (Beauchamp & Kacelnik, 1991; Fragaszy & Visalberghi, 1989; Giraldeau & Lefebvre, 1987; Humle & Snowdon, 2008; Ilan et al., 2013; Nicol & Pope, 1994). In the second experimental condition, instead of pecking at the sand and exposing the seeds, the mother model only pointed towards the well (as described above), moved back, and then pointed again repeatedly (hereafter the ‘pointing mother’ treatment). This behaviour stimulated the fledglings to search actively in the well and presumably also to pay attention to the stimuli preceding the reward (i.e. the coloured sand), as they must have done to achieve successful individual learning of colour in previous studies (Ilan et al., 2013; Katsnelson, Motro, Feldman, & Lotem, 2011). Note that all fledglings had been previously trained to search actively in the sand (see above), and that uncovering hidden seeds required very little effort. It is therefore unlikely that our experiment created treatment group differences in state that affected the value of the reward (Kacelnik & Marsh, 2002). The training procedure of both treatment groups comprised 10 training sessions. Each session (the presentation of a new foraging grid in the cage) lasted 3 min or until the fledgling had consumed the seeds in the variable rewarding wells (if this occurred first). In cases in which fledglings hardly pecked at any of the variable rewarding wells, leaving a large amount of seeds, the mother model

(b) 2

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Figure 1. Experimental set-up: (a) a fledgling imprinted on the mother model following it during an habituation session with natural sand (note the pole and the wire that allow the experimenter to control and activate the mother model); (b) an example of the distribution of coloured sand and reward (number of seeds) used during the training sessions of both treatments. In this example the target colour is blue. To avoid pseudoreplications and specific spatial effects we applied the same principles (including the positioning of a variable rewarding well among constant wells) in creating 36 different grid distributions that were used randomly (18 for each target colour).

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was returned to this well during the training session in order to allow for additional learning opportunities. The 10 training sessions were carried out in pairs of morning (at about 0900 and 1000 hours) and afternoon sessions (at about 1500 and 1600 hours). One hour of food deprivation preceded each pair of training sessions (i.e. before 0900 and 1500 hours). Thus, the 10session training schedule was composed of four training sessions on days 1 and 2, and two additional sessions on the morning of day 3. The test phase At the end of the training phase, the fledglings' sand colour preference was tested in two sessions (of 5 and 3 min, respectively), on a seedless foraging grid and in the absence of the mother model. To allow equal access to both colours from any point on the grid during the test, the red and blue wells were distributed alternately as on a checkerboard (not as in the training session distribution depicted in Fig. 1b). If young sparrows can learn food-finding cues when joining their foraging parents, sparrows of both experimental treatments should exhibit in the test sessions a preference for the target colour. However, a weak or no preference for the target colour by sparrows of the ‘exposing mother’ treatment would be consistent with the view that while direct scrounging can block social learning, scrounging that encourages active search may result in successful social learning. Ethical Note The study was carried out under an animal care permit from the Tel Aviv University Animal Care Committee L-12-028. At the end of the experiment, all 22 fledglings that had participated in the experiment were transferred to a shared aviary in our breeding colony in which they formed a separate flock. Excluding two individuals that did not survive to the next breeding season, which is a normal mortality rate for house sparrows, the rest of the flock became part of the breeding colony and bred successfully in the subsequent year. Behavioural and Data Analyses All training and test sessions were videorecorded to allow a step-by-step analysis of individual experience and behavioural preferences. Every visit to a well that included at least one peck (a foraging step) was classified according to the social context (joining the mother model versus independent search), characteristics of the well (sand colour and expected payoff: constant, variable rewarding or no payoff) and the state of the well (‘intact’ wells versus ‘open’ wells that had already been pecked by the fledgling earlier on in the same training session and thus may or may not contain seeds). The distinction between intact and open wells is important because previous work has suggested that sparrows learn food-related cues only when searching in intact wells (Ilan et al., 2013). Repeated pecks at the same well were distinguished and classified as different foraging steps if between pecks there was a clear shift in body orientation (i.e. the bird's legs were directed away from the well for at least 3 s). Joining was defined as visiting a well in which the mother model was present or was present for up to 1 s before the fledgling's arrival. Of the 24 nestlings collected and hand-reared, 22 developed well and participated in the experiment. Final sample size for the statistical analysis was reduced to 16 (eight for each treatment group, and 11 and five from the first and second cohorts, respectively). This was done in order to include only fledglings that pecked at least six times during the test phase and could thus provide a colour preference score (proportion of choices in the

target colour) that was sufficiently reliable. The six-step criterion was chosen a priori (Ilan et al., 2013) because this is the minimal number of steps that allows a significant preference to be detected using a sign test. The number of pecks carried out during the test phase by the fledglings in our final sample ranged from eight to 24 (mean ¼ 14). Statistical analysis was done in SPSS version 22 (IBM, Armonk, NY, U.S.A.), using generalized linear models (GLM, distribution ¼ normal, link function ¼ identity). The proportion of correct choices in the target colour in the test was taken as the dependent variable and arcsine (square-root) transformed for normality. Treatment group and cohort were tested as factors, and numbers of successful or unsuccessful pecks in the different colours when joining the mother model or when searching independently during the training phase were tested as covariates. To select between candidate models that used different predictors we compared between their goodness of fits using Akaike's information criterion, correcting for small sample size (AICc), and calculated Akaike's weights to compare their relative likelihoods (Burnham & Anderson, 2002). Following a lack of significant effect of cohort in all models we removed this factor from the final analysis. Including it in the models did not change the main results but reduced goodness of fit (statistical output is available upon request). RESULTS Social-learning Ability Of the 16 sparrows whose colour preference could be measured in the test phase and were thus included in the final analysis (see above), almost all individuals (15/16) exhibited a preference for the target colour during the test (Fig. 2a; sign test: P < 0.001). This preference was also statistically significant for 11 of them (i.e. in 11 tests of individual preferences; see Table A1 in the Appendix). Thus, most fledglings were able to learn the target colour, suggesting an ability to learn socially. An alternative explanation for the preference for the target colour could have been that fledglings occasionally discovered one of the three wells of the target colour that contained seeds through independent search (before it was pointed or exposed to them by the mother). However, our experimental design minimized the probability that this would happen (see above); indeed, only two such cases occurred during the entire training phase. Removing the two individuals involved in these two cases from the data does not change the results (a preference by 13 of the remaining 14 individuals remains significant: sign test: P < 0.005). Effect of Treatment and Foraging Experience during Training The simplest statistical model testing the effect of the experimental treatment on the proportion of correct choices in the test shows that fledglings of the ‘pointing mother’ treatment exhibited a stronger preference for the target colour than fledglings of the ‘exposing mother’ treatment (Fig. 2a, and Model A in Table 1). Including the number of searching steps to empty wells of the target colour as a possible covariate in the model (Fig. 2b and Model B in Table 1), shows that the number of such ‘disappointments’ in respect to the target colour did not reduce the preference for it and cannot explain the treatment group effect. If anything, fledglings of the ‘pointing mother’ treatment experienced more such disappointments than those of the ‘exposing mother’ treatment (see Fig. 2b). The difference between treatment groups is also not explained by the very few cases in which fledglings found food in the target colour through independent search (see Models A and B in Table A2 of the Appendix).

Proportion of correct choices in the test

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1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1

(a)

1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1

Exposing mother Pointing mother

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(b) 2 4 6 8 10 12 Search in empty wells of target colour

1 0.9 0.8 0.7 0.6 0.5 0.4 0.3

0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1

(c)

21 23 25 27 29 31 33 35 37 39 Joining steps during training

0.2 0.1

(d) 2 4 6 8 10 Search in intact alternative colour

1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1

(e) 0 0.1 0.2 0.3 Relative success in intact alternative colour

Figure 2. The proportion of ‘correct choices’ (i.e. choosing the target colour) in the test phase of fledglings from the ‘pointing mother’ treatment (C) and the ‘exposing mother’ treatment (B) in relation to: (a) experimental treatment, (b) number of searching steps in empty wells of the target colour during the training phase, (c) number of joining steps during the training phase, (d) number of searching steps in intact wells of the alternative colour during training, (e) relative success in intact wells of the alternative colour during training (see text for how relative success is calculated). Enlarged dots in (bee) represent two data points at exactly the same location. Box plots in (a) show the median, quantiles and 0.95% confidence interval.

The number of joining steps to the mother model (steps that were always rewarded with seeds and could facilitate social learning) was positively related to the proportion of correct choices in the test (Fig. 2c and Model C in Table 1). However, this factor cannot explain treatment group differences, because fledglings of the ‘pointing mother’ treatment did not perform more joining steps than those of the ‘exposing mother’ treatment (Fig. 2c, mean ± SD: 29.88 ± 5.17 versus 32.13 ± 4.19, respectively; t13.427 ¼ 0.957, P ¼ 0.356). On the other hand, the number of searching steps in intact wells of the alternative colour (wells that always contained two seeds), although not differing between treatment groups, had a significant effect on the proportion of correct choices in the test, as well as a significant

interaction with the effect of experimental treatment (Fig. 2d and Model D in Table 1). That is, while in both treatments the proportion of correct choices in the test decreased with the number of searching steps in intact wells of the alternative colour, in the ‘exposing mother’ treatment it decreased much more sharply. Thus, while individuals from both treatments developed a similarly strong preference for the target colour in the absence of such steps (upper left corner of Fig. 2d), the difference between treatment groups emerged mostly from the much stronger impact of such steps (i.e. successful search in the alternative colour) on the ‘exposing mother’ treatment. Considering that the bird might weigh the effect of its searching success in the alternative colour against its joining success in the

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Table 1 Statistical models exploring the effect of experimental treatment and various parameters of individual experience on the proportion of correct choices in the test Model

Effects

Likelihood ratio c2

df

P

AICc

R2

A B

Treatment Treatment Search in empty wells of target colour Interaction Treatment Joining steps during training Interaction Treatment Search in intact alternative colour Interaction Treatment Relative success in intact alternative colour Interaction Treatment Search in intact alternative colour Joining steps during training Interaction (Treatment)Search in intact alternative colour)

4.832 2.87 0.278 0.152 1.111 5.052 0.376 3.031 19.989 7.858 3.768 21.559 8.223 4.919 18.679 4.222 9.796

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

0.028 0.090 0.598 0.697 0.292 0.025 0.540 0.082 <0.0001 0.005 0.052 <0.0001 0.004 0.027 >0.0001 0.040 0.002

9.937 17.659

0.208 0.092

12.876

0.326

2.607

0.744

3.988

0.765

1.496

0.786

C

D

E1

E2

Bold type indicates P < 0.05. Generalized linear models with distribution ¼ normal, link function ¼ identity. All models included intercept (not shown) and were based on N ¼ 16 birds. AICc scores represent goodness of fit (lower scores represent better fit). Adjusted R2 represent the proportion of variance explained by the model. The difference in more than 10 AICc units between models A, B, C and Models D, E1, E2 implies that the former are much less probable then the latter (relative likelihood < 0.007).

target colour, we also tested the effect of a combined variable termed ‘relative success in intact alternative colour’, which was calculated as: (number of searching steps in intact alternative colour)/(number of searching steps in intact alternative colour þ number of joining steps during training). The results of this analysis reveal some improvement in goodness of fit (see Fig. 2e and Model E1 in Table 1; calculated relative likelihood ¼ 0.501, implying that the previous Model ‘D’ is only half as probable as the new Model ‘E1’). While this improvement is not large, the new model may better represent biological reality and is also supported by the fact that when the two covariates are included in a single model, each of them exhibits a significant effect (Model E2 in Table 1; note that the slightly higher AICc score, indicating a lower goodness of fit, is expected in this case due to the larger number of parameters). Overall, for the range of variation experienced by the birds in our study, the number of joining steps appears to have a much weaker effect on social learning than the effect of searching success in the alternative colour (Fig. 2, Table 1). Finally, it is worth noting that the main results depicted in Fig. 2d, e remain significant also when the data point of the individual with the lowest proportion of correct choices (0.25, lower right corner of figure) is removed from the analysis (Appendix Table A2, models C, D and E), and also when all searching steps in wells of the alternative colour are considered, not only steps in intact wells (Appendix Table A2, models F, G and H). This latter analysis added only four searching steps by three individuals that revisited open wells, and resulted in a slightly lower goodness of fit, which was to be expected from previous evidence of poor learning from open wells (Ilan et al., 2013), as well as from the depletion of reward in revisited wells. DISCUSSION He who wishes to teach us a truth should not tell it to us, but simply suggest it with a brief gesture, a gesture which starts an ideal trajectory in the air along which we glide until we find ourselves at the feet of the new truth... He who wants to teach us a truth should place us in a position to discover it ourselves.  Ortega y Gasset (1914). Jose This 100-year-old quote by the Spanish philosopher Ortega (Ortega y Gasset, 1961, p. 67), illustrates nicely the view according

to which social learning may be best promoted by merely initiating the processes of individual learning, as has been recognized by philosophers and educators for quite some time (Bonawitz et al., 2011). Recent approaches to social learning appear to follow this line (Galef, 1995; Galef & Giraldeau, 2001; Heyes, 2012; Heyes & Pearce, 2015) and, as described above, the same intuition guided our present work: we hypothesized that social learning would be better served by a mother that merely points at the location of the seeds, forcing the fledglings to dig actively in the sand, rather than by a mother that exposes the seeds for them. Although our results are basically consistent with this prediction, they are clearly more complex. The better social learning exhibited by the ‘pointing mother’ treatment was mainly due to the strong interaction between treatment group effect and searching success in the alternative colour. Importantly, individuals from the ‘exposing mother’ treatment that did not experience searching success in the alternative colour (N ¼ 3) or experienced it only once (N ¼ 1) learned to prefer the target colour as strongly as the learners of the ‘pointing mother’ treatment (Fig. 2d; correct/total choices in test: 9/9, 16/16, 18/21 and 7/9), giving no indication that scrounging food exposed by the mother model had blocked their social-learning ability. However, for the other fledglings in the ‘exposing mother’ treatment, a few successful searching events in intact wells of the alternative colour (offering two seeds each) were sufficient to compromise the effect of social experience in more than 20 successful joining events in wells offering ca. 15 seeds (compare the number of steps along the horizontal axis of Fig. 2c, d). Thus, the difference between experimental treatments was not a result of a simple blocking process during scrounging but was strongly related to the additional, other, type of information obtained through the fledglings' successful searching events in the alternative colour. Importantly, the effect of searching payoffs was much stronger than the effect of scrounging payoffs, unless scrounging also involved active search, as in the ‘pointing mother’ treatment. While our results clearly suggest that active search helps to facilitate social learning, it is difficult to determine whether this is because it affects the learning process or the decision process. Affecting the learning process implies that, during learning, fledglings somehow pay more attention or assign greater weight to information gained through active search, so that in their memory the sand colour that covered the hidden seeds is associated with a

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food reward more strongly than the sand colour adjacent to the exposed seeds. This explains why the target colour preference of fledglings of the ‘exposing mother’ treatment was easily compromised by the few searching steps in the alternative colour while fledglings of the ‘pointing mother’ treatment, which were engaged in active search during both scrounging from the mother and searching in the alternative colour, were not affected in the same manner. The alternative idea, according to which active search affects the decision process, implies that the fledglings learn and remember both colours equally well, but in the test context, where they encounter two sand colours with no visible seeds, they rely more heavily on their experience with active search, which represents a similar context (of searching for hidden seeds). Note that for social learning to be effective, learners must be able to transfer information learned socially to the context of independent search. Our results suggest that the fledglings are capable of doing so, but it is very possible that socially mediated active search (as in the ‘pointing mother’ treatment) makes it easier for them by providing a context resembling that of independent search. Although it is certainly interesting to understand which of the two processes is taking place in the bird's brain (i.e. assigning more weight during learning or making context-appropriate decisions), from a functional point of view the result is the same: information acquired through active search has a much stronger impact on the outcome of the learning process compared to incidental observations (i.e. picking exposed seeds). The idea that the inhibition of social learning by scrounging is related to the relative payoffs obtained from searching versus scrounging has been suggested by Giraldeau and Templeton (1991) and is clearly supported by our present findings. Similarly to our study, the experiments carried out by Giraldeau and Templeton (1991) showed that scrounging did not really block the ability of pigeons to learn a new task, but only caused them to use what they had learned less frequently than pigeons that did not scrounge. Previous findings on pigeons (Giraldeau & Lefebvre, 1987) may be explained in the same manner, as it seems that individual pigeons can almost always learn during scrounging (Lefebvre & Helder, 1997). Thus, different experimental results in social learning may not necessarily represent real differences in social-learning ability but, rather, may frequently reflect different exposures to searching versus scrounging payoffs, as well as different degrees of active search during scrounging, as illustrated by the range of possible outcomes in our study (see Fig. 2d). Similarly, apparent differences in social-learning abilities across species should be considered with caution. For example, our earlier work suggested that house sparrows fail to learn socially during social foraging (Ilan et al., 2013) while studies on great tits, Parus major, demonstrated impressive social-learning abilities in the wild (Aplin et al., 2015). Although it is possible that great tits have evolved better social-learning abilities than house sparrows, our present study suggests an alternative explanation: the socially foraging sparrows studied by Ilan et al. (2013) received frequent different types of information between active search on the foraging grids and when scrounging only on exposed seeds. Accordingly, they may be analogous to the sparrows represented in the lower right corner of our Fig. 2d (fledglings of the ‘exposing mother’ treatment that experienced repeated successes in the alternative colour). This predicts reliance on private rather than on social information. On the other hand, the experimental set-up used by Aplin et al. (2015) to study social transmission in great tits was based on an observational learning apparatus (puzzle box) that allowed many repeated observations but also required followers to shift a door in order to access the food. This may resemble the situation experienced by

171

our fledglings in the ‘pointing mother’ treatment, whose scrounging involved active search and which, despite acquiring additional, other, type of information from nonsocial exploration, learned to prefer the socially learned cue (upper right corner of our Fig. 2d). It is also interesting to consider here the study by Beauchamp and Kacelnik (1991) in zebra finches, in which the presence of a knowledgeable partner overshadowed the learning of a light signal rather than facilitating social learning. Importantly, the overshadowing in this study did not prevent the learning of the light signal (as a predictor of access to food) but only slowed it down and reduced the frequency of using the signal to about a half (Beauchamp & Kacelnik, 1991). This result is explained by the fact that learners had two competing signals to rely on: the light signal and the behaviour of the partner. Note that this situation does not greatly differ from that in our sparrows. Although the experimental set-up and the learning task differed, the sparrows in our study also had to learn and to rely on two competing signals: the sand colour learned during scrounging and the colour learned during searching. Interestingly, in the zebra finch study, in which none of the competing signals was acquired through active search, their effect was about equal, whereas in our study, when one of the signals was acquired through active search, its effect was much stronger. Why does active search thus affect the learning process so strongly? Is it adaptive to rely more heavily on information gained through active search than on passive observation? In the context of social foraging, Ilan et al. (2013) suggested that active search may provide reliable information on both success and failure for each potential cue, whereas social learning during scrounging may be misleading. This is because the occasional foraging success of a flock member in the vicinity of a certain cue may not reveal how frequently the same cue was also associated with failures (which does not typically elicit scrounging and attention). This idea may not be restricted to social foraging and may be suggested more generally for any type of learning: active search, as opposed to incidental food discoveries, may allow learners to sample potential cues more systematically, which minimizes the risk of sampling biases. If this idea is correct, the tendency to rely more heavily on information acquired through active search may represent a general adaptation for learning that has not evolved specifically for social learning. However, in considering what can evolve in sociallearning evolution, the relative weight assigned to active search versus passive observation of the behaviour of others may certainly be suggested as a possible genetically variable trait on which selection may operate (Heyes, 2012; Leadbeater, 2015; Lotem & Halpern, 2012). Finally, although there is nothing in our study that can hint that social learning in house sparrows involves some form of animal teaching (Thornton & McAuliffe, 2006), it certainly suggests that small modifications in parental behaviour (such as pointing rather than exposing) can enhance the effectiveness of social learning. For example, a parent that forages in a rich food patch but without leaving exposed seeds for its offspring may inadvertently behave like the pointing mother in our experiment. Whether such behavioural modifications may have evolved as a result of their contribution to social learning, and may thus be viewed as teaching, is an open question for future work. Acknowledgments We thank T. Shalev, L. Novak, A. Moran, Y. Melman, I. Brickner, Y. Brenner, Z. Yanai and the helpful staff of I. Meier Segal's Zoological Garden for lab and technical assistance; O. Kolodny, Y. Vortman and E. Katsnelson for valuable comments and suggestions; J. Morand-

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Appendix Table A1 Individual data and statistical tests (binomial one-tailed sign test) for choices in the target and alternative colours during the test phase ID

Experimental treatment

2 3 4 7 8 11 25 27 1 5 9 10 12 15 18 28

A A A A A A A A B B B B B B B B

Number of pecks In target colour

In alternative colour

7 2 8 7 16 14 18 9 7 14 23 9 12 19 17 14

4 6 3 2 0 5 3 0 2 1 1 0 0 0 0 1

Total

P

11 8 11 9 16 19 21 9 9 15 24 9 12 19 17 15

0.27 0.14 0.11 0.09 0.0001 0.03 0.0007 0.002 0.09 0.0005 0.0001 0.002 0.0002 0.0001 0.0001 0.0005

Experimental treatment groups A and B represent the ‘exposing mother’ and the ‘pointing mother’ treatments, respectively.

Table A2 Additional models exploring the effect of experimental treatment and various parameters of individual experience on the proportion of correct choices in the test (generalized linear models, distribution ¼ normal, link function ¼ identity, all models included intercept (not shown) and were based on N ¼ 16 birds, unless otherwise specified) Model

Effects

A

Treatment Search in intact wells of the target colour that contained seeds (two cases) Treatment Search in any wells of the target colour that contained seeds (including repeated visits in open wells, N¼15) Interaction Treatment Search in intact alternative colour Interaction Treatment Relative success in alternative colour Interaction Treatment Search in intact alternative colour Joining steps during training Interaction (Treatment*Search in intact alternative colour) Treatment Search in alternative colour Interaction Treatment Relative success in alternative colour Interaction Treatment Search in alternative colour Joining steps during training Interaction (Treatment)Search in intact alternative colour)

B

Ca

Da

Ea

Fb

Gb

Hb

Likelihood ratio c2

df

P

4.054 0.019 3.197 0.884

1 1 1 1

0.044 0.89 0.074 0.347

0.329 1.839 12.229 5.217 2.23 13.538 5.865 3.318 27.779 7.16 12.844 3.261 19.206 8.056 4.013 20.912 8.132 5.219 17.768 3.885 9.548

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

0.566 0.175 <0.0001 0.022 0.135 <0.0001 0.015 0.069 <0.0001 0.007 <0.0001 0.071 <0.0001 0.005 0.045 <0.0001 0.004 0.022 <0.0001 0.049 0.002

AICc

R2

13.555

0.148

17.003

0.128

0.384

0.574

1.995

0.618

0.404

0.683

1.692

0.729

3.28

0.755

0.243

0.768

Bold type indicates P < 0.05. AICc scores represent goodness of fit (lower is better). a N ¼ 15 after removing the individual with the lowest proportion of correct choices; otherwise these models are the same as models D, E1 and E2 in Table 1. b These models correspond to models D, E1 and E2 in Table 1, but the effect of searching in intact wells of the alternative colour was replaced with the effect of all searching steps in wells of the alternative colour, which adds four steps (by three individuals) to open wells of the alternative colour.