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Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids

  1. Lisa Horn  Is a corresponding author
  2. Thomas Bugnyar
  3. Michael Griesser
  4. Marietta Hengl
  5. Ei-Ichi Izawa
  6. Tim Oortwijn
  7. Christiane Rössler
  8. Clara Scheer
  9. Martina Schiestl
  10. Masaki Suyama
  11. Alex H Taylor
  12. Lisa-Claire Vanhooland
  13. Auguste MP von Bayern
  14. Yvonne Zürcher
  15. Jorg JM Massen
  1. Department of Behavioral and Cognitive Biology, University of Vienna, Austria
  2. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Switzerland
  3. Department of Biology, University of Konstanz, Germany
  4. Center for the Advanced Study of Collective Behaviour, University of Konstanz, Germany
  5. Eulen- und Greifvogelstation Haringsee, Austria
  6. Department of Psychology, Keio University, Japan
  7. Faculty of Psychology, Education and Sports, University of Regensburg, Germany
  8. Department of Linguistic and Cultural Evolution, Max Planck Institute for the Science of Human History, Germany
  9. Department of Behavioral Sciences, Hokkaido University, Japan
  10. School of Psychology, University of Auckland, New Zealand
  11. Max-Planck-Institute for Ornithology, Germany
  12. Department of Anthropology, University of Zurich, Switzerland
  13. Animal Ecology Group, Department of Biology, Utrecht University, Netherlands
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Cite this article as: eLife 2020;9:e58139 doi: 10.7554/eLife.58139

Abstract

The investigation of prosocial behavior is of particular interest from an evolutionary perspective. Comparisons of prosociality across non-human animal species have, however, so far largely focused on primates, and their interpretation is hampered by the diversity of paradigms and procedures used. Here, we present the first systematic comparison of prosocial behavior across multiple species in a taxonomic group outside the primate order, namely the bird family Corvidae. We measured prosociality in eight corvid species, which vary in the expression of cooperative breeding and colonial nesting. We show that cooperative breeding is positively associated with prosocial behavior across species. Also, colonial nesting is associated with a stronger propensity for prosocial behavior, but only in males. The combined results of our study strongly suggest that both cooperative breeding and colonial nesting, which may both rely on heightened social tolerance at the nest, are likely evolutionary pathways to prosocial behavior in corvids.

Introduction

The investigation of prosocial behavior (i.e. voluntary actions that benefit another individual at no or low costs to the actor; Marshall-Pescini et al., 2016), is of particular interest from an evolutionary point of view, because the act of benefitting another individual without receiving a direct gain to oneself represents an evolutionary puzzle (Clutton-Brock, 2009; Riehl, 2013). Humans show high levels of prosocial behaviors from an early age on (Silk and House, 2011), although their expression and developmental trajectories are subject to cross-cultural and societal variation (House et al., 2020). The importance of prosociality for human interactions has inspired comparative studies on the evolutionary origin of this trait. The majority of experimental studies in non-human animals have focused on primates (for a review, see Marshall-Pescini et al., 2016), but recent research revealed prosocial tendencies also in other mammals (e.g. domestic dogs [Quervel-Chaumette et al., 2016]; wolves [Dale et al., 2019]; rats [Ben-Ami Bartal et al., 2011; Schweinfurth and Taborsky, 2018a]) and several bird species (e.g. azure-winged magpies [Horn et al., 2016; Massen et al., 2020]; pinyon jays [Duque et al., 2018]; African grey parrots [Brucks and von Bayern, 2020]). Nevertheless, not all tested species have shown prosocial tendencies (e.g. chimpanzees [Silk et al., 2005]; cottontop tamarins [Cronin et al., 2009]; meerkats [Amici et al., 2017]; common ravens [Di Lascio et al., 2013; Lambert et al., 2017; Massen et al., 2015a]). Following these variable initial results, the importance of understanding which social factors and which characteristics of a species’ social system may underlie the expression of prosociality across non-human animal species became particularly evident. Unfortunately, however, comparisons of prosociality across species have been hampered by the diversity of paradigms and procedures used (Marshall-Pescini et al., 2016).

The most comprehensive experimental investigation of prosocial behavior in primates tested 15 species (including human children) in the same experimental set up, that is the group service paradigm (hereafter GSP; Burkart et al., 2014). In the GSP, individuals are tested in their regular social group and can make food available to other group members by operating a simple mechanism, without obtaining any food themselves. Burkart et al., 2014 showed that species-specific prosocial tendencies in the GSP were best explained by the degree of allomaternal care (i.e. offspring care by individuals other than the mother) across the tested species. These results were in line with the cooperative breeding hypothesis, which states that ‘cooperative breeding is accompanied by psychological changes leading to greater prosociality’ (Burkart et al., 2009). Additional factors positively influencing the amount of prosocial behavior – albeit to a lesser degree than allomaternal care – were the presence of monogamous pair bonds and high social tolerance (i.e. equal access to food for all group members) measured during the GSP (Burkart et al., 2014). The latter result fits the self-domestication hypothesis (Hare et al., 2012; Hare, 2017), according to which prosociality arises as a by-product of selection against reactive aggression – particularly in males (Wrangham, 2019) – and selection for increased tolerance (see Sánchez‐Villagra and van Schaik, 2019 for a critical appraisal of historical and current theories on self-domestication). While both the cooperative breeding hypothesis and the self-domestication hypothesis acknowledge an underlying link between increased social tolerance and prosociality, the cooperative breeding hypothesis puts emphasis on allomaternal offspring care, whereas the self-domestication hypothesis suggests the decrease of reactive aggression as the crucial factor for the emergence of human-like prosociality. The comparative approach is particularly promising for distinguishing between these hypotheses (Burkart et al., 2014). However, concentrating solely on the primate order offers only one perspective on the evolution of prosocial behavior, which has also been criticized because of possible effects of common ancestry (e.g. cooperative breeding in primates occurs only in two taxonomic groups – humans and callitrichid monkeys; Thornton and McAuliffe, 2015). Hence, applying a standardized comparative approach to other taxonomic groups would be paramount for drawing more general conclusions (Beran et al., 2014).

From a comparative perspective, the corvid family, which is a cosmopolitan bird taxon that includes crows, ravens, jays, and magpies, is of particular interest for the investigation of prosociality. Corvids have similar neuron counts compared to many primate species (Olkowicz et al., 2016) and show similarly complex cognitive traits (Taylor, 2014; Güntürkün and Bugnyar, 2016; Boucherie et al., 2019). Most corvid species are long-lived, highly social (Emery et al., 2007) and pair bonds are extremely strong, even lifelong in some species (Henderson et al., 2000). About 40% of all extant corvid species from several separate genera are cooperative breeders (defined in birds as more than the two parents caring for the brood; for example azure-winged magpies, carrion crows; see Cockburn, 2006; Griesser et al., 2017). Since related as well as unrelated helpers have been documented to contribute to offspring care, both kin selection (Green et al., 2016) and pay-to-stay strategies (Kingma, 2017) seem important to explain cooperative breeding in birds. Additionally, a number of corvids breed colonially, where several pairs nest in physical proximity, including rooks, Eurasian jackdaws, and azure-winged magpies (see Madge and Burn, 1999). It has been argued that relaxed territorial defense, reduced reactive aggression, and increased tolerance toward conspecifics may lead to the emergence of colonial nesting in birds (Brown, 1974). Consequently, corvids’ variation in cooperative breeding and colonial nesting make them the optimal candidates for testing both the cooperative breeding hypothesis and the self-domestication hypothesis in a lineage other than primates.

Previous experiments in corvids have demonstrated prosocial behavior in azure-winged magpies (using the GSP Horn et al., 2016 as well as an active food-sharing paradigm Massen et al., 2020) and pinyon jays (using a prosocial choice task Duque et al., 2018). Both species breed cooperatively (Cockburn, 2006) and nest in colonies, with several breeding pairs nesting in close proximity (Madge and Burn, 1999). Additionally, there has been tentative evidence for prosocial tendencies in a prosocial choice task in Eurasian jackdaws (Schwab et al., 2012), which also nest in colonies, but do not breed cooperatively (Cockburn, 2006). In contrast, subadult ravens for example, which are able to cooperate with a conspecific partner to receive mutual rewards (Massen et al., 2015b; Asakawa-Haas et al., 2016), have so far not shown any evidence of prosociality, despite having been tested with multiple experimental paradigms (e.g. different prosocial choice tasks [Di Lascio et al., 2013; Lambert et al., 2017]; token exchange task [Massen et al., 2015a]). While ravens tend to form groups for foraging and roosting as non-breeders (Heinrich, 1989; Loretto et al., 2016), they are highly territorial during breeding (Boucherie et al., 2019) and it is not clear whether the characteristics of their social system contribute to their apparent lack of prosocial tendencies. To disentangle the influence of cooperative breeding and colonial/territorial nesting, respectively, on prosociality, it is necessary to test a sample of different species that vary along these factors, and to avoid differences that result from methodological heterogeneity by using the same standardized procedure.

Here, we present the first systematic comparison of prosocial behavior across multiple species in a taxonomic group outside the primate order. We measured prosociality in 11 social groups of eight corvid species (total N = 72 individuals), which were all highly social (i.e. living and foraging in social groups during at least some stages of their life history; Komeda et al., 1987; Uhl et al., 2019; Kubitza et al., 2015; Clayton and Emery, 2007; Braun et al., 2012; Miyazawa et al., 2020; Holzhaider et al., 2011; Ekman and Griesser, 2016), but varied in the expression of cooperative breeding and colonial nesting (Figure 1d). We used a standardized experimental paradigm developed in primates (i.e. the GSP; Burkart et al., 2014), which has recently been adapted and successfully applied in birds (Horn et al., 2016). To keep the results comparable, we kept the procedures as similar as possible to the original study with primates (Burkart et al., 2014). In the prosocial test of the GSP, individuals can land on the provisioning perch of the apparatus, and consequently make food available to their group members via a seesaw mechanism (Figure 1a). Crucially, the bird on the provisioning perch cannot obtain any food itself and it has to remain on the provisioning perch until another individual arrives on the other side of the apparatus (position 1; see Figure 1b) to take the food (see Video 1; see Materials and methods section for details). Habituation, training and two control conditions (i.e. empty control: no food available; blocked control: access to food blocked; see Video 2 and Video 3) ascertain that the individuals understand the experimental task and that landing on the provisioning perch in the prosocial test does not reflect the absence of sufficient inhibitory control (Figure 1c). In addition to prosocial tendencies, the GSP also measures how even the access to sequentially provided food is across the individuals of a given social group (i.e. whether one or few individuals monopolize the food source and obtain most of the food or whether similar numbers of food pieces are obtained by all group members; Figure 1c). In primates, this evenness score has been used as a proxy for social tolerance (Burkart et al., 2014).

Figure 1 with 1 supplement see all
Overview of the study design and set-up.

(a) Experimental set-up as seen from the inside of the aviary with a bird sitting on the provisioning perch, thereby making food available to the group. (b) Schematic of the apparatus with location of positions 0 and 1 in relation to the provisioning perch. (c) Experimental procedure; habituation and training phases are given in blue, test phases are given in yellow; subjects needed to reach a given criterion to be included in the analysis of phases II and IV-VI; see supplementary information for details. (d) Overview of the tested species and their key social system differences; orange boxes represent the presence of obligate or facultative cooperative breeding for the respective species, green boxes represent the presence of colonial nesting.

Video 1
Prosocial test.

Example videos of prosocial test trials taken from three species (i.e. azure-winged magpies, carrion crows, common ravens). Food is placed on the recipient side (position 1). Food can be provided to a group member, if an individual lands on the provisioning perch.

Video 2
Empty control.

Example videos of empty control trials taken from three species (i.e. azure-winged magpies, carrion crows, common ravens). No food is placed on the recipient side (position 1). Therefore, no food can be provided to group members.

Video 3
Blocked control.

Example videos of blocked control trials taken from three species (i.e. azure-winged magpies, carrion crows, common ravens). Food is placed on the recipient side (position 1), but access to the food is blocked with a fine net. Therefore, although food is visible, no food can be provided to the group members.

To assess the explanatory value of cooperative breeding and colonial nesting for prosocial behavior in corvids, we used linear regression models and an information-theoretic approach to model selection and model averaging. Additionally, since sex differences have been observed in prosocial food sharing in natural observations (von Bayern et al., 2007; Scheid et al., 2008; Chiarati et al., 2011) and experiments (Schwab et al., 2012), we also included the individuals’ sex into the model. Further, to test the extent to which common ancestry affected the birds’ prosocial tendencies, we calculated a phylogenetically controlled mixed-effects model (for phylogenetic relationships between the tested species, see Figure 1—figure supplement 1). Finally, because within a species prosocial behavior might be expressed differently between the sexes (Massen et al., 2020; Schwab et al., 2012; von Bayern et al., 2007) and between age classes (Chiarati et al., 2011), we also examined intraspecific provisioning patterns.

Our results demonstrate that cooperative breeding is positively associated with the expression of prosocial behavior in corvids, although this effect is qualified by interactions between sex and both the factors cooperative breeding and colonial nesting, which were also important for explaining the occurrence of prosocial behavior in the birds. Additional separate analyses for the two sexes showed that both cooperative breeding and colonial nesting positively affected prosociality, albeit differently for the two sexes. While the effect of cooperative breeding seemed to be driven by females’ prosociality, colonial nesting only predicted males’ prosocial actions. The phylogenetically controlled model confirmed the importance of both cooperative breeding and colonial nesting and showed that the phylogenetic signal was weak in terms of prosocial behaviors in corvids. Same-sex provisioning dyads were equally common as opposite-sex dyads and we observed both provisioning from adults to juveniles and vice versa. Our results highlight that both alloparental care and increased social tolerance are important evolutionary trajectories for the emergence of prosocial behavior in birds.

Results

Between-species variation in prosocial provisioning and evenness of access to food

Across all species and groups, the amount of food provided by those birds that discriminated between the prosocial test and both control conditions (i.e. landed significantly more often on the provisioning perch when they could provide food to their group members than when there was no food or when access to the food was blocked for the recipient; N = 12; four azure-winged magpies, two carrion crows, two Eurasian jackdaws, one rook, one New-Caledonian crow, one common raven, one large-billed crow; see Appendix 1—table 1), showed high variability and ranged from 0% to 98% (Table 1). The evenness of the birds’ access to food within the group, which was measured in a different phase of the experiment (see Appendix 2) and which has been proposed as a proxy for social tolerance in primates in the original study (Burkart et al., 2014), was medium to high in all tested species (cf. 20; Table 1) and was not correlated with provided food values across groups (Spearman’s rho = −0.326, p=0.327, N = 11).

Table 1
Prosocial food provisioning and evenness of access to food across all tested species and groups.

Given are the classifications of cooperative breeding and nesting type for the tested species, as well as the percentage of food provided in the prosocial test and Pielou’s J’ as a measure for evenness of access to food for each of the groups.

SpeciesCooperative breeding*Nesting typeGroup (N)Phase IV
provided food
Phase II Pielou’s J’
 Azure-winged magpieYesColonial1 (5)98%0.72
2 (4)64%0.83
 Carrion crowyesTerritorial1 (6)57%0.46
 Eurasian jackdawnoColonial1 (14)33%0.73
 RooknoColonial1 (12)2%0.86
 New-Caledonian crowno§Territorial1 (3)70%0.52
2 (2)0%0.36
 Common ravennoTerritorial1 (9)21%0.73
 Large-billed crownoTerritorial1 (9)16%0.97
 Siberian jaynoTerritorial1 (5)0%0.82
2 (3)0%0.91
  1. *Classifications after (Cockburn, 2006).

    Classifications after (Madge and Burn, 1999).

  2. In line with the original publication (Burkart et al., 2014), provided food was calculated as the corrected percentage of food provisioning per group in the last two test sessions of the prosocial test, only by those individuals that passed the criterion of landing significantly more often in the test compared to both control conditions. Note that raw and corrected measures of food provisioning are highly correlated (Spearman’s rho = 0.892, p≤0.001, N = 11).

    §Occurrence of cooperative breeding is classified as unknown, but assumed as absent according to Cockburn, 2006.

Linking cooperative breeding and colonial nesting with prosocial behavior

The averaged model identified the main factors sex and cooperative breeding as having a high explanatory degree for the number of landings on the provisioning perch in the prosocial test (i.e. making food available for conspecifics; see Figure 1a and Video 1; model results in Figure 2—source data 1). Overall, individuals from cooperatively breeding species landed more often on the provisioning perch than individuals from non-cooperatively breeding species (Figure 2a), and males landed more often than females (Figure 2b). These main effects were qualified by the high explanatory degree of the interaction terms of both cooperative breeding and nesting type with sex (Figure 2—source data 1), meaning that the main effects were conditional upon one another.

Number of landings in the prosocial test as a function of the factors with a high explanatory degree.

The box plots represent medians (horizontal lines), inter-quartile ranges (boxes), as well as minima and maxima (whiskers). All data are represented with dots. Dots not encompassed by the whiskers are outliers. Dot colors in all panels indicate the species according to the legend in the top right panel.

In order to ascertain the robustness of our model, we re-did the analysis, always excluding one species at a time. Four out of eight models had the same results as before (removed species: Siberian jays, N = 48; rooks, N = 48; common ravens, N = 44; carrion crows, N = 45), while nesting type had an added high explanatory degree in two models (removed species: New-Caledonian crows, N = 46; azure-winged magpies, N = 43). In one model nesting type, sex, and the interaction between these two factors had a high explanatory degree, while cooperative breeding and the interaction between cooperative breeding and sex were only marginally important (i.e. SWAICc = 0.44; removed species: large-billed crows, N = 42). Finally, in one model the intercept-only model was included in the selection of best-fitting models (removed species: Eurasian jackdaws, N = 41), implying that the averaged model was not robust. Overall, these results are consistent and corroborate the robustness of our original results. We specifically note that the Siberian jays were the only species tested in the wild and that they did not successfully provide food to their group members, which could have been an artifact of them being tested in the wild rather than their social system. The fact that the results remained practically identical after excluding the Siberian jays (see Appendix 1—table 4) suggests that the results obtained with the complete dataset were not driven by the Siberian jays per se.

When splitting the data by sex due to the high explanatory degree of the interaction terms, our analyses showed that for males (N = 25) the factor colonial nesting had a high explanatory degree (Estimate = −15.066, SE = 4.528, z = 3.154, SWAICc = 1.00, NModels = 2): males from colonial species landed more often than males from territorial species (Figure 2d). Cooperative breeding had only a very low explanatory degree in males (Figure 2c; see Figure 2—source data 2 for full model results). In contrast, for the females (N = 26) the factor cooperative breeding had a high explanatory degree (Estimate = 9.686, SE = 4.427, z = 2.076, SWAICc = 1.00, NModels = 2): females from cooperatively breeding species landed more often than females from non-cooperatively breeding (Figure 2c). Nesting type had only a very low explanatory degree in females (Figure 2d; see Figure 2—source data 2 for full model results). Using the same procedure of excluding one species at a time as above, we could ascertain the robustness of the model including only the males: all eight models had the same results as before (see Appendix 1 for details). Additionally, the male birds from colonial species landed significantly more often on the provisioning perch than the male birds from territorial species, when only testing for the factor nesting type (Welch t-test: t = 3.01, df = 13.66, p-value=0.005). The model including only the females, however, was less robust: only two out of eight models had the same results as before, while in five models the intercept-only model was included in the selection of best-fitting models (see Appendix 1 for details). Also when testing only whether the females from cooperatively breeding species landed more often on the provisioning perch than the females from species that do not breed cooperatively, the results were only marginally significant (Welch t-test: t = −1.64, df = 8.30, p-value=0.069).

When looking only at the landings of the birds that discriminated between the prosocial test and both control conditions (N = 12), we found that there was a non-significant trend for the birds from colonial species to land more often on the provisioning perch (N = 7, median = 30, IQR = 29–34) than the birds from territorial species (N = 5, median = 23, IQR = 22–24; Mann-Whitney: W = 30, p=0.0505). The birds from cooperatively breeding species (N = 6, median = 29.5, IQR = 24–35) did not differ significantly in the number of their landings from the individuals from species that do not breed cooperatively (N = 6, median = 26.5, IQR = 22.5–29; Mann-Whitney: W = 13, p=0.470).

Testing the effect of phylogeny on prosocial behavior

As in the original model, also a phylogenetically controlled model showed that the main factors cooperative breeding and sex significantly predicted the number of landings on the provisioning perch in the prosocial test (cooperative breeding: estimate = 10.001, 95% HPD interval [0.082, 19.886], Pmcmc = 0.048; sex: estimate = 19.660, 95% HPD interval [8.899, 30.292], Pmcmc = 0.0002), and that these main effects were again qualified by significant interactions between both cooperative breeding and sex (Estimate = −16.394, 95% HPD interval [−30.183,–2.329], Pmcmc = 0.020) and nesting type and sex (Estimate = −20.576, 95% HPD interval [−33.588,–8.551], Pmcmc = 0.002; see Appendix 1—table 5 for full model results). The phylogenetic signal was weak (mean λ = 0.035; posterior mode = 0.001; 95% HPD interval [0.000, 0.185]).

Dyad-level variation in prosocial provisioning

Opposite-sex provisioning did not occur more often than same-sex provisioning in the tested species, both when considering all individuals in each group (Wilcoxon: N = 7, T+=7, p=0.271) and when only considering provisioning by these individuals that discriminated between the test and the control conditions in each group (N = 7, T+=10, p=0.553). There were species differences in the distribution of sex dyad types, which could, however, not be linked back to either cooperative breeding or nesting type (see Figure 3 and Figure 3—source data 1 for details). With regard to age-dependent provisioning, we had very little data, as only five groups from three species contained juvenile individuals (i.e. azure-winged magpie group 2; New Caledonian crow groups 1 and 2; Siberian jay groups 1 and 2). While there was no uniform pattern among those four groups, we did witness a juvenile providing food to adults in the azure-winged magpie group (33% of total provided food) and the one New Caledonian crow group where provisioning occurred (95% of total provided food).

Distribution of food provisioning per dyad sex composition.

The bars represent the percentage of food provided in the last two test sessions of the prosocial test in those seven groups where provisioning occurred and for which we had data on the individuals’ sex and the dyad identities. Full bars comprise the individuals that passed the criterion of landing significantly more in the test versus both control conditions. Striped bars comprise all individuals. Dyad types: male donor – male recipient (MM), female donor – female recipient (FF), male donor – female recipient (MF), female donor – male recipient (FM). All possible dyads: azure-winged magpies, group 1, 3 MM, 1FF, 6MF/FM; azure-winged magpies, group 2, 0 MM, 3FF, 3MF/FM; carrion crows, 1 MM, 6FF, 8MF/FM; Eurasian jackdaws, 21 MM, 21FF, 49MF/FM; rooks 15 MM, 15FF, 36MF/FM; common ravens, 6 MM, 10FF, 20MF/FM; New Caledonian crows, group 1, 1 MM, 0FF, 2MF/FM.

Discussion

Our results reveal that cooperative breeding is positively associated with the propensity for prosocial behaviors in corvids, but that this main effect is qualified by an interaction with sex. Additional separate analyses for the two sexes showed that both cooperative breeding and colonial nesting positively affected prosociality, albeit differently for the two sexes. Consequently, our results support both the cooperative breeding hypothesis (Burkart et al., 2014; Burkart et al., 2009), which emphasizes the role of allomaternal care, and the self-domestication hypothesis (Hare et al., 2012; Hare, 2017; Wrangham, 2019), which stresses the importance of low levels of reactive aggression and high levels of social tolerance, as explanatory approaches for the evolution of prosocial behavior in the corvid family. An additional model that controlled for common ancestry confirmed the importance of both cooperative breeding and colonial nesting and showed that the phylogenetic signal was weak in terms of prosocial behaviors in corvids.

The conclusion that both cooperative breeding and colonial nesting positively affect prosocial behavior in corvids is corroborated by the species-specific provisioning rates in our study: provisioning was particularly high in the cooperatively breeding, colonially nesting azure-winged magpies (64–98%), high in the facultative cooperatively breeding, territorially nesting carrion crows (57%), and intermediate in the non-cooperatively breeding, colonially nesting jackdaws (33%). In the third colonial species, the rooks, very little food was provided during the prosocial test (2%). However, in this group only three out of 12 individuals could be habituated to the apparatus despite extensive training (see Appendix 1—table 1). Therefore, it is possible that the limited number of possible donors and recipients prevented higher provisioning rates. The provisioning results obtained in jackdaws parallel previous findings with this species when tested in a dyadic prosocial choice paradigm: in that study the jackdaws also provided food for their conspecifics in certain contexts (e.g. more provisioning for opposite-sex recipients; Schwab et al., 2012). Carrion crows, however, were previously not found to exhibit prosocial tendencies in a token exchange paradigm where they had the opportunity to transfer tokens to a conspecific partner, which could in turn be exchanged for food (Wascher et al., 2020). The authors of that study argued that the exchange paradigm might have been too complicated for the birds, as it required understanding the value of the tokens (Wascher et al., 2020). It is therefore possible that the GSP used in the current study, which simply required the birds to land on the provisioning perch in order to make food available for the group members, made it easier for the carrion crows to express their prosocial behavior.

An interesting exception to the predicted pattern is the remarkably high provisioning rate in one group of New Caledonian crows (70%). According to Cockburn, 2006, however, it remains unknown whether this species might engage in cooperative breeding. New Caledonian crows allow their offspring to stay in the parental territory for up to two consecutive breeding seasons (Holzhaider et al., 2011) and feed the juveniles for up to ten months post-fledging (Hunt et al., 2012). Helping by offspring at the nest has never been documented (Holzhaider et al., 2011), but it has proven difficult to observe interactions at the nest in most habitats. Family living, where offspring delay dispersal from the parental territory beyond nutritional independence, has been suggested as one of the evolutionary routes to cooperative breeding (Griesser et al., 2017; Brown, 1974). Nevertheless, Siberian jays, which also live in family groups (Griesser et al., 2017), showed no prosocial behavior in our study. However, one has to consider, that the Siberian jays were the only species not tested in captivity but in the wild. Although the study population is well habituated to the presence of humans and to field experiments (Griesser, 2013), it is possible that they were not as focused on the experiment as the captive species. Additionally, Siberian jays fully rely on scatter hoarding to survive the winters at the study site. Since this behavior has been shown to be predominantly selfish (Ekman et al., 1996), it is possible that Siberian jays’ particular feeding strategy explains their lack of prosocial tendencies. Therefore, to advance understanding of the role of family living in regard to prosociality, it would be important to further investigate prosocial tendencies in other family-living corvid species (Uomini et al., 2020).

In line with the original comparative study using the GSP in primates (Burkart et al., 2014), we corrected the percentage of provided food by including only provisioning by individuals that passed the criterion of landing significantly more often in the test compared to both control conditions, thereby giving the most conservative measure of prosocial provisioning. The rate of individuals that passed this criterion ranged from 0% to 50% across species (see Appendix 1—table 1 for details). Due to the experimental paradigm (i.e. the group setting) it is difficult to unequivocally conclude that the individuals that did not pass this criterion did not understand the task. These individuals might have been willing to land on the apparatus in the prosocial test, but might have simply been slower than other group members. Alternatively, they might have understood the difference between the prosocial test and the two control tasks, but they might just not have had prosocial tendencies. Given that explanation, it is interesting to note that the percentage of birds that passed the criterion was relatively high in the cooperatively breeding and/or colonial species (azure-winged magpies: 4 out of 8 birds (50%); carrion crows: 2 out of 6 (33%); Eurasian jackdaws: 2 out of 10 (20%); rooks: 1 out of 3 (33%)) and relatively lower in most territorial species (New Caledonian crows: 1 out of 5 (20%); common ravens: 1 out of 7 (14%); large-billed crows: 1 out of 9 (11%); Siberian jays: 0 out of 7 (0%)), especially as there is no reason to assume that the latter are cognitively less developed than the former (see e.g., Güntürkün and Bugnyar, 2016). When looking at the number of landings on the provisioning perch (i.e. with and without actual provisioning) of these 12 birds that passed the criterion, we only found a non-significant trend of more landings from the birds from colonial species than from the birds from territorial species and no effect of whether the birds came from a cooperatively breeding species or not. However, an individual would only pass this criterion if it landed relatively often on the provisioning perch in the prosocial test, thereby inherently also demonstrating a prosocial tendency (Burkart et al., 2014). Therefore, it is not surprising that among this group of birds, no strong differences according to cooperative breeding and colonial nesting became apparent with regard to prosocial tendencies. Additionally, the small sample size did not allow us to include further factors in the analysis (e.g. sex) and might have hampered the detection of potential differences.

Across all individuals we found that sex modulated the effects of both cooperative breeding and colonial nesting on how often the birds landed on the provisioning perch. The positive effect of cooperative breeding on the number of landings in the prosocial test was mainly driven by the females, although the results of the female-only model were not very robust. Nevertheless, the fact that the females from cooperatively breeding species were particularly prosocial is surprising, because observations in wild populations showed that in many cooperatively breeding corvids only a minority of the helpers were females (e.g. azure-winged magpies [Ren et al., 2016], their closely related sister species the Iberian magpies [Valencia et al., 2003], carrion crows [Baglione et al., 2002]) and that male helpers provided more care during breeding than females (e.g. carrion crows [Canestrari et al., 2005]). However, due to the high energetic demand of incubation that usually only the females incur, cooperatively breeding females might depend more on helpers’ contributions than males and they might use acts of prosocial behavior throughout the year (note that our studies were all conducted outside the breeding season) to incentivize group members to remain in the group. This argument is in line with the interdependence hypothesis, which states that cooperative acts are expected most when individuals strongly rely on each other (Roberts, 2005). In contrast, among colonially nesting birds, male individuals, but not females, were particularly prosocial, together with an overall main effect of stronger prosocial tendencies in males than in females across all tested groups. According to costly signaling theory (Zahavi, 1997), prosocial acts can be regarded as honest signals that advertise the donor’s underlying qualities (e.g. health, strength, ability to control resources; cf. competitive altruism hypothesis; Hardy and Van Vugt, 2006). Based on these premises, dominant individuals would be expected to show more prosocial behavior than subordinates. This prediction has been supported by experimental evidence from birds (Duque and Stevens, 2016) and several primate species (e.g. long-tailed macaques; Massen et al., 2010; for a review, see Marshall-Pescini et al., 2016). In most corvids, males are dominant over females (Scheid et al., 2008; Massen et al., 2014; Wechsler, 1988; Ode et al., 2015; Chiarati et al., 2010; Sklepkovych, 1997) and would therefore be expected to face greater pressure to advertise their dominance rank than females. This might be most evident in colonial males, which nest in close proximity with many conspecifics and consequently engaging in dominance challenges might be particularly costly for them (Verhulst and Salomons, 2004). The self-domestication hypothesis also emphasizes the importance of reduced reactive aggression and violent conflict between male individuals, not females, as an important factor for the evolution of human-like prosociality (Wrangham, 2019). Beyond that, prosocial actions might represent an attempt of males to trade food for extra-pair copulations (Tryjanowski and Hromada, 2005) or to maintain relationships with affiliative partners other than the mated partner (Miyazawa et al., 2020; von Bayern et al., 2007; Boucherie et al., 2016). In general, the results from the single sex models – especially the female-only model – have to be considered preliminary due to the low sample size. Future studies with larger sample sizes and experiments that specifically address these sex differences are needed to reveal which of these hypotheses explain the sex-specific effects of both cooperative and colonial breeding in birds.

One additional limitation of this study was that, despite the considerable research effort of this multi-lab study, we only managed to test few replicates per species. Finding test populations is a common problem for large-scale comparative studies (e.g. the original GSP study in primates [Burkart et al., 2014]; see also Morales Picard et al., 2020; O'Hara et al., 2017; MacLean et al., 2014; Many Primates et al., 2019). While the provisioning rates were similar in the two groups of azure-winged magpies (i.e. the two highest provisioning rates at 98% and 64%, respectively) and the two groups of Siberian jays (i.e. both 0%), there was a substantial difference between the two groups of New-Caledonian crows: in one group, 70% of the available food was provided to the group members, whereas in the other group there was no successful provisioning at all. One has to consider, though, that the latter group consisted only of two individuals at the time of testing. Therefore, similarly as in the rooks, the limited number of potential donors and recipients might have prevented successful provisioning. Also, within the groups, there was obvious inter-individual variation, with some individuals providing the majority of the food to their group members while other individuals rarely landed on the provisioning perch at all. Due to the unrestricted group setting of the GSP, it is not possible to discern whether the individuals that did not land on the provisioning perch were not motivated to provide food for their group members, or whether they were merely too slow to do so compared to other individuals that for example were bolder or faster. To be able to more confidently demonstrate true species generalizations and rule out a strong effect of individual characteristics, future studies should attempt to increase the number of replicates per species and should bolster the results of the GSP with individual testing paradigms (e.g. prosocial choice experiments).

Within the groups, we would have expected more opposite-sex provisioning than same-sex provisioning, especially from males to females. Observations of naturally occurring food sharing suggest that food provisioning in corvids might serve the function of forming pair bonds and social bonds in general (Massen et al., 2015a; Miyazawa et al., 2020; von Bayern et al., 2007). Also in the context of a prosocial choice experiment with jackdaws, opposite-sex recipients were more likely to elicit prosocial behavior from the donors than same-sex recipients (Schwab et al., 2012). Similarly, in an active food-sharing paradigm, azure-winged magpies shared high-value food items preferably with, although not restricted to, members of the opposite sex (Massen et al., 2020). However, both opposite-sex and same-sex provisioning occurred equally often in our study. This might have been because of the constraints of the GSP, where food is made available to the whole group and the donor has limited possibilities to influence the specific recipient of its prosocial action. There were some differences in the distribution of donor-recipient sex-constellations, which could, however, not be linked back to either cooperative breeding or nesting type, but were more likely a result of the specific group compositions. Interestingly, although the majority of the tested birds were adults, many instances of juveniles providing food to adults were observed in both the azure-winged magpies and the New Caledonian crows, which accounted for almost all the provided food in the latter species. Prosocial acts from juveniles are expected in cooperatively breeding species based on observations in the wild (e.g. Iberian magpies [Valencia et al., 2003]; carrion crows [Baglione et al., 2002]). In contrast, New Caledonian crow parents feed their juvenile offspring for extended periods (Hunt et al., 2012), while food provisioning by juveniles has never been documented (Holzhaider et al., 2011). Our finding of prosocial behavior in a juvenile New Caledonian crow underlines the importance of considering the role of family living in the absence of cooperative breeding for the evolution of prosociality in birds (Uomini et al., 2020). Future studies, where samples show larger age variation within the groups or where the same groups can be tested at different time points with differing age ratios, would also be very informative regarding the question of the influence of age on prosocial behavior (Kaplan, 2020). An additional factor that has been argued to play an important role for prosocial acts between individuals is their relatedness (e.g. Bourke, 2014; but see Schweinfurth and Taborsky, 2018b). However, since kinship relations between individuals were unknown for about half of the groups tested in the current study, we were not able to include kinship as a factor in the analysis. Future studies that track relatedness between group members could further investigate the relevance of this factor for prosocial behavior in corvids.

In contrast to the comparative study on primate prosociality (Burkart et al., 2014), we did not use the degree of allomaternal care, but rather a nominal classification as either cooperatively breeding species or not as a predictor in our models. The reasoning for that change was two-fold. First, there is less information on the specific number and degree of investment of helpers in cooperatively breeding bird species (Cockburn, 2006) compared to primates (Isler and van Schaik, 2012) and even within the same corvid species, the numbers seem to differ greatly depending on the population (e.g. Komeda et al., 1987; Ren et al., 2016; Valencia et al., 2003; Baglione et al., 2002). Second, since we only had two cooperatively breeding species in our sample, a more detailed representation of the degree of cooperative breeding would have decreased the statistical power of our analysis. Additionally, it is important to note that – differently from the general trend in primates – all the species included in our sample express bi-parental care (i.e. care provided by the father and the mother), meaning that there is a certain degree of allomaternal care even in non-cooperatively breeding, territorial corvid species. Future studies that more elaborately evaluate the degree of allomaternal care in wild corvid populations are thus needed to create a comprehensive comparison between the corvids in this study and the primates (Burkart et al., 2014).

The evenness of access to food was medium to high in all tested species in our study (Burkart et al., 2014). Following the argument of the original study in primates (Burkart et al., 2014), that would indicate medium-to-high levels of social tolerance in all groups, irrespective of the prevalence of cooperative breeding or colonial nesting. However, the relatively even access to food among the group members may reflect that most corvids have a tendency to cache food for later consumption (de Kort and Clayton, 2006). In our study, even the most dominant birds rarely monopolized the apparatus for long durations, as it has been documented in despotic primate species (Schnoell and Kappeler, 2018). The corvids rather periodically left the area to cache their obtained food out of sight of their conspecifics (Bugnyar et al., 2016). Therefore, the evenness of access to food in phase II of the GSP might not be a valid proxy for social tolerance in corvids. Other approaches like co-feeding experiments might provide more suitable measures of social tolerance, because they measure how tolerant the individuals of a given group or species are to foraging in close proximity with other group members (Sima et al., 2016). Nevertheless, the use of the GSP has many advantages when attempting to conduct a comprehensive experimental investigation of prosocial behavior (Burkart et al., 2014): the apparatus and procedure are cognitively not demanding and testing individuals within their social groups and home environment reduces stress and increases animal welfare. Additionally, the paradigm offers several criteria to assess whether an individually was sufficiently habituated/trained and its propensity to land on the apparatus was not caused by a lack of inhibitory control. Overall, the birds tested in this study differentiated between the prosocial test and both control conditions and landed more often on the provisioning perch when they could provide food to their group members than when there was no food or when access to the food was blocked for the recipient (see Appendix 1—figure 1). Therefore, the GSP is a highly useful paradigm for comparative investigations of animal prosociality and can be conceivable applied to a much wider range of species and taxa.

The current study is a first attempt to determine how generalizable the predictions of the cooperative breeding hypothesis and self-domestication hypothesis are, or whether they are actually restricted to the primate order (Thornton and McAuliffe, 2015). In a systematic comparison of prosocial preferences across eight corvid species we find, in fact, evidence for both hypotheses. It is important to note, however, that these two hypotheses are not mutually exclusive and that one common underlying mechanism in both hypotheses is likely a heightened level of social tolerance at the nest. In cooperatively breeding species, helpers have to show increased social tolerance toward offspring that is not their own, while the breeders have to tolerate older offspring and immigrant helpers in their territories and close to their nests. In colonially nesting species, a breeding pair has to tolerate the proximity of other breeding pairs close to their nest. Consequently, the combined results of our study strongly suggest that both cooperative breeding and the heightened social tolerance required by colonial nesting are likely evolutionary pathways to prosocial behavior in corvids.

Materials and methods

Subjects

We tested 11 social groups of 8 corvid species (total N = 72 individuals: azure-winged magpies: group 1 N = 5, group 2 N = 4; carrion crows: N = 6; rooks: N = 12; Eurasian jackdaws: N = 14; New-Caledonian crows: group 1 N = 3, group 2 N = 2; common ravens: N = 9; large-billed crows: N = 9; Siberian jays: group 1 N = 5, group 2 N = 3; see Appendix 2—table 1 for information on study sites, subject and husbandry details, and testing period for all study groups). We recruited and tested as many species and birds per species as possible, which resulted in the sample we describe here. Consequently, we did not perform any a priori sample size calculations. Biological replications could be performed for the three species for which we could test two independent social groups (i.e. azure-winged magpies, New-Caledonian crows, Siberian jays).

Besides Siberian jays, all species were tested in captivity, in their home aviary and social group prior to their first feeding of the day. High-quality food reward was used to encourage participation in the experiment. The two Siberian jay groups were tested in the wild near the center of their territory. Here, less preferred food was provided near the apparatus to keep the group near the apparatus. The birds from all species were well habituated to participating in behavioral experiments (see Appendix 2 for habituation procedures and criteria).

Ethical note

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The study followed the Guidelines for the Use of Animals (Vitale et al., 2018), in accordance with national legislations. All animal care and data collection protocols were reviewed and approved by the ethical boards of the respective research institutions (see Appendix 2—table 1).

Apparatus and procedure

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We used the same apparatus with a seesaw mechanism as a previous study (Horn et al., 2016Figure 1a), adjusted in size and weight to the different species. The apparatus consisted of a board outside the aviary, on which the food item was placed, and two sticks reaching through the wire mesh into the aviary on one side of the board with a provisioning perch fixed at their end. For the Siberian jays, the board was placed inside a wire mesh container, preventing individuals to access the board, but allowing them to freely access the provisioning perch on the outside. The apparatus’ mechanism was balanced so that in the starting position the perch pointed up and the board pointed down. When a bird landed on the provisioning perch, its weight moved the seesaw down (Figure 1a). As soon as the bird left the perch, the apparatus automatically moved back to its original position. Near the other side of the board, inside the aviary, were perches that were not connected to the apparatus’ seesaw mechanism. Food could be put on the board in two positions: one in front of the provisioning perch (Position 0) and one on the other side of the board (Position 1) out of reach from the perch. If food was placed in position 0, a subject could deliver food to itself by landing on the provisioning perch, after which the food slid toward the wire mesh and in reach. If food was placed in position 1 and a bird landed on the provisioning perch, it could not obtain the food itself. If it stayed on the perch long enough for another group member to arrive in position 1, it made food available to this group member (Figure 1b, Video 1). However, if the bird left the provisioning perch before another group member arrived, the apparatus moved back in the starting position and the food became unavailable. Therefore, multiple landings on the provisioning perch were possible within one trial.

We replicated the procedures of a previous study (Horn et al., 2016). The experiment consisted of six consecutive phases in a fixed sequence (three habituation/training phases and three test phases) and an additional retest phase for seven of the groups (Figure 1c; see Appendix 2 for detailed procedures).

In the access to food assessment (phase II) the apparatus’ seesaw mechanism was fixed so that any bird landing in position one could obtain food. In two sessions, we placed food pieces sequentially in position one and recorded how many food pieces each group member obtained. In the group service test (phase IV), the seesaw mechanism was fully released and food was placed in position 1, so that a bird landing on the provisioning perch could only make food available to the group, not to itself (Video 1). On alternating days, we conducted empty control sessions, which were identical to test sessions except that no food was placed on the apparatus and therefore no food was available to be provided for the group members (Video 2). In the blocked control (phase V), access to food in position one was blocked with a fine net. Therefore, although food was visible, no food could be provided for the group members (Video 3). This was done to test whether landing was simply elicited by the presence of food. To ensure that the birds had comparable motivation levels (e.g. hunger) in all conditions, we conducted all sessions at the same testing times per day for each respective species. For the analysis of phases IV and V, we used only the summed data from the last two sessions (sessions 4 and 5) of each condition, because by then each bird had had the opportunity to learn about the consequences of operating the apparatus. The group service retest (phase VI) represents a technical replication and was identical to phase IV and consisted of two prosocial test and two empty control sessions. In all sessions of phases IV to VI, we interspersed motivation trials after every five regular trials where food was placed in position 0 to ensure that the birds were still motivated to participate in the experiment (see Appendix 1—table 6). We recorded how often each individual landed on the provisioning perch during the regular trials. Additionally, we recorded which animal obtained the food and which animal provided the food in phases IV and VI.

Data analysis

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Providing/receiving of food and landings on the apparatus were scored live by the experimenter and confirmed via later video scoring. A second rater, who was not the experimenter for the respective group, scored the behavioral variables for 24% of all 270 test sessions, which included 50% of all sessions on which the main analyses were based. Inter-rater reliabilities were excellent across all groups (mean ICCGroup ± SD = 0.975±0.041, minimum ICCGroup = 0.878, maximum ICCGroup = 0.998). All analyses were based on the data from the first rater. Results from the two groups of azure-winged magpies were previously reported in Horn et al., 2016.

For each group, we calculated the evenness of access to food in both sessions of phase II for those individuals that passed the habituation criterion in the preceding phase (total N = 63; see Appendix 1—table 1 for details on each group). To calculate the evenness of access to food for each group (N = 11), we used Pielou's J′ (Pielou, 1977) (i.e. an index ranging from 0, indicating maximal inequality to 1, indicating a completely equal distribution; see Horn et al., 2016) and calculated an averaged Pielou’s J’ across both test sessions (see Source code 1, part one for details). Further, we calculated the percentage of provided food in the last two sessions of phase IV. The percentage of provided food was corrected by including only provisioning by individuals that passed the criterion of landing significantly more often in the test compared to both control conditions (see Burkart et al., 2014), thereby giving the most conservative measure of prosocial provisioning. The rate of individuals that passed this criterion ranged from 0% to 50% across species (see Appendix 1—table 1 for details). Note, however, that raw measures (including all birds) and corrected measures (including only birds that met the criterion) of food provisioning were highly correlated (Spearman’s rho = 0.892, p≤0.001, N = 11 groups).

Since successful food provisioning in the GSP depended not only on a subject’s landing on the apparatus, but also on the temporal and spatial coordination between donor and recipient, we could not exclude that a lack of coordination prevented food provisioning in some cases. Therefore, to further investigate the influence of cooperative breeding and colonial nesting on prosocial tendencies, we used the sum of the number of landings in the last two sessions of the prosocial test (phase IV) of all birds that passed the training criterion in the preceding phase (see Appendix 1—table 1). We had to additionally exclude four birds with unknown sex from this analysis, resulting in a total sample size of 51 birds. Only one data point per individual was used in all statistical analyses.

In a first step, we calculated a linear mixed-effects model (maximum likelihood method; package lme4; Bates et al., 2015) with ‘number of landings in the prosocial test’ as response variable, ‘cooperative breeding’, ‘nesting type’, ‘sex’, and all possible interactions as factors, ‘group size’ as additional factor without interactions, and ‘group ID’ nested within ‘species’ as random factors (see Source code 1, part 2). The variance of the random factors ‘group ID’ and ‘species’ was zero, resulting in a singular fit of the model. Therefore, we decided to calculate a general linear model with the same response variable and factors, but excluding ‘group ID’ and ‘species’ as random factors (see Source code 1, part 3). Note, however, that the results of both models are equivalent (see Appendix 1—table 2). We then obtained the candidate set of models by using the function dredge of the package MuMIn (Bartoń, 2009) to derive all possible sub-models with all possible combinations from the set of factors (including the intercept‐only model) ranked by AICc (Hurvich and Tsai, 1989). Next, we selected the top 2AICc models (i.e. all models with a delta AICc ≤2 compared to the best-fitting model [Burnham et al., 2002]; 2 out of 256 models) and averaged them using the function model.avg in the package MuMIn (see Source code 1, part 3 for complete R script of this procedure). The intercept-only model did not fall within the range of top 2AICc models (delta AICc = 5.80). The factor ‘group size’ was not present in the final selection of best-fitting models (Figure 2—source data 1). Figure 2—source data 2 shows the estimates and their standard errors (SE), z-values, sum of AICc weights, and number of models containing the specific factor of the averaged model. Factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0 were considered to have a high explanatory degree. The quality of all models was confirmed by investigating Q-Q plots and testing the normal distribution of the residuals. To ensure that choosing a threshold of delta AICc ≤2 did not lead to the exclusion of any potentially important factors (e.g. group size) we re-did the model selection and averaging procedure with a threshold of delta AICc ≤7 (see Source code 1, part 3). This model included three additional factors, but all three had only minimal explanatory degree (i.e. the interaction between cooperative breeding and nesting type, the factor group size, the three-way interaction), thereby supporting original threshold of delta AICc ≤2 (see Appendix 1—table 3 for detailed results with top AICc7 models). We used the same procedure as described above when analyzing the data separately for the females and for the males (see Source code 1, part 4). We decided not to include ‘group size’ into these models because of the small sample size and because ‘group size’ did not emerge as an important predictor for the complete dataset. Again, the variance of the random factors ‘group ID’ and ‘species’ was zero and we decided to calculate linear models, with the same response variable and predictors, excluding ‘group ID’ and ‘species’ as random factors (see Source code 1, part 4). We then derived all possible submodels from this set of predictors. For the female birds, there were two top 2AICc models and for the male birds, there were also two top 2AICc models (out of 8 models each). Full results of the two averaged models can be seen in Figure 2—source data 2. For testing the robustness of our model with the complete dataset, as well as the single sex models, we used the same procedure as described for the full dataset, while always excluding one species at a time (see Source code 1, part 5; see Appendix 1 for results on the single sex models; see Appendix 1—table 4 for the detailed results excluding the Siberian jays). Additionally, we used one-sided Welch t-tests to test whether we could find the predicted significant difference when only testing for the effect of nesting type in the males and for the effect of cooperative breeding in the females, respectively. For testing whether there was a difference in the number of landings on the provisioning perch among only these individuals that passed the criterion of landing significantly more often in the test compared to both control conditions, due to the small sample size (N = 12) we used non-parametric Mann-Whitney U tests separately for the factors ‘cooperative breeding’ and ‘nesting type’.

To test the extent to which common ancestry affected the birds’ prosocial tendencies, we used the packages geiger (Harmon et al., 2008) and MCMCglmm (Hadfield, 2010) to calculate a phylogenetically controlled mixed-effects model with ‘number of landings in the prosocial test’ as response variable, and those parameters that were present in the top 2AICc models of the original analysis (i.e. ‘cooperative breeding’, ‘nesting type’, ‘sex’, and the interactions between ‘cooperative breeding’ and ‘sex’ and ‘nesting type’ and ‘sex’). Additionally, we added ‘phylogenetic effect’ and ‘species’ as random effects. We further calculated the posterior mean (mean of the posterior distribution), the posterior mode (most likely value regarding the posterior distribution) and the 95% credible interval of the phylogenetic signal λ (see Source code 1, part 6 for complete R script).

Finally, to investigate whether opposite-sex provisioning occurred more often than same-sex provisioning, we calculated a non-parametric Wilcoxon signed-rank test (two-tailed). For each of the phases, we included only those individuals that had reached the respective habituation/training criterion (see Appendix 2 for details on the criteria). All statistical tests were carried out in R version 3.6.0 (2019-04-26). Figure 2 and Appendix 1—figure 1 were created with the package ggplot2 (Wickham, 2016).

Appendix 1

Supplementary results

Number of individuals reaching the habituation/training criteria

For each group, Appendix 1—table 1 shows the number of individuals that reached the criterion for being included in the analysis of the access to food assessment (phase II), the criterion for being included in the analysis of the prosocial test (phase IV), and the criterion for being included in the provisioning data.

Appendix 1—table 1
Group size and number of individuals passing the selection criteria across all tested groups.

Given are – for each group – the group size and the number of birds passing the criteria for phases II and IV (i.e. taking at least 10 pieces of food in a minimum of five sessions in the previous phase) and the criterion of landing in significantly more trials in the prosocial test than in both the empty and the blocked control (Fisher’s exact test).

SpeciesGroupGroup sizeCriterion Phase IICriterion Phase IVCriterion test vs. controls
NSessions, median (min, max)NSessions, median (min, max)
 Azure-winged magpies1559 (6, 11)523 (22, 30)3
 2447.5 (5, 12)333 (33, 49)1
 Carrion crows1669 (5, 13)611 (9, 17)2
 Rooks112510 (5, 17)365 (65, 65)1
 Eurasian jackdaws1141226 (5, 51)1059 (58, 65)2
 New-Caledonian crows1338 (8, 8)317 (16, 18)1
 2225 (5, 5)213 (12, 14)0
 Common ravens1997 (5, 26)730 (27, 37)1
 Large-billed crows1995 (5, 6)910 (10,12)1
 Siberian jays1555 (5, 9)45 (5, 5)0
 2335 (5, 5)310 (10, 10)0

Full model including ‘group ID’ and ‘species’ as random factors

The full linear mixed-effects model (maximum likelihood method) used ‘number of landings in the prosocial test’ as response variable, ‘cooperative breeding’, ‘nesting type’, ‘sex’, and all possible interactions as predictors, ‘group size’ as additional predictor without interactions, and ‘group ID’ nested within ‘species’ as random factors (see Source code 1, part 1). Variance of the random factors ‘group ID’ and ‘species’ was found to be zero, resulting in a singular fit of the model. We then derived all possible submodels from the set of predictors (including the intercept‐only model), selected the top 2AICc of models (2 out of 256 models), and averaged them using the model.avg function in the MuMIn package in R (see Source code 1, part 1). The predictor ‘group size’ was not present in the final selection of best-fitting models. Appendix 1—table 2 shows the estimates, conditional standard errors (SE), confidence intervals, z-values, p-values, and relative importance of the averaged model.

Appendix 1—table 2
Effects of cooperative breeding, nesting type and sex on the number of landings in the prosocial test.

Given are estimates, standard errors (SE), z-values, sum of AICc weights (SWAICc), and number of models containing the specific factor (NModels) after model averaging. Factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0 were considered to have a high explanatory degree and are given in bold. Number of individuals: N = 51.

ParameterEstimateSEZSWAICcNModels
 (Intercept)6.4033.7391.675--
Cooperation (yes)10.0244.2262.3040.611
 Nesting (territorial)4.0924.0730.9771.002
 Sex (male)17.0755.6722.9471.002
 Cooperation (yes) x Sex (male)−16.0576.4452.4200.611
 Nesting (territorial) x Sex (male)−19.6116.0143.1721.002

Full model with the top 7AICc of models

The full linear model used ‘number of landings in the prosocial test’ as response variable, ‘cooperative breeding’, ‘nesting type’, ‘sex’, and all possible interactions as predictors, and ‘group size’ as additional predictor without interactions (see Source code 1, part 1). We then derived all possible submodels from the set of predictors (including the intercept‐only model), selected the top 7AICc of models (14 out of 256 models), and averaged them using the model.avg function in the MuMIn package in R (see Source code 1, part 1). The intercept-only model fell within the range of top 7AICc models (delta AICc = 5.80). Appendix 1—table 3 shows the estimates, conditional standard errors (SE), confidence intervals, z-values, p-values, and relative importance of the averaged model.

Appendix 1—table 3
Threshold for model selection and averaging set to delta AICc ≤ 7.

Given are estimates, standard errors (SE), z-values, sum of AICc weights (SWAICc), and number of models containing the specific factor (NModels) after model averaging. Factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0 were considered to have a high explanatory degree and are given in bold. Number of individuals: N = 51.

ParameterEstimateSEZSWAICcNModels
 (Intercept)6.8365.4001.240--
Cooperation (yes)9.2015.8771.5340.7310
 Nesting (territorial)3.9744.8590.7990.9712
Sex (male)17.1925.9542.8290.9310
 Cooperation (yes) x Sex (male)−16.1997.0352.2400.595
 Nesting (territorial) x Sex (male)−19.6986.4292.9850.9310
 Cooperation (yes) x Nesting (territorial)−3.9847.6760.5050.174
 Group size−0.1540.5940.2530.194
 Cooperation (yes) x Nesting (territorial) x Sex (male)0.90214.1060.0620.021

Evaluating the robustness of the models

For testing the robustness of our model with the complete dataset, as well as the single sex models, we used the same procedure as described for the full dataset (see main document, section ‘Data analysis’) with reduced datasets in which we always excluded one species at a time. The full linear model used ‘number of landings in the prosocial test’ as response variable, ‘cooperative breeding’, ‘nesting type’, ‘sex’, and all possible interactions as predictors, and ‘group size’ as additional predictor without interactions (see Source code 1, part 5). For each reduced dataset, we then proceeded with model selection and averaging in the same way as we did in the original model.

Four out of eight models had the same results as before (i.e. the main factors sex and cooperative breeding, as well as the interactions between both cooperative breeding and nesting type with sex had a high explanatory degree; removed species: Siberian jays, N = 48; rooks, N = 48; common ravens, N = 44; carrion crows, N = 45), while the main factor nesting type had an added high explanatory degree in two models (removed species: New-Caledonian crows, N = 46; azure-winged magpies, N = 43). In one model nesting type, sex, and the interaction between these two factors had a high explanatory degree, while cooperative breeding and the interaction between cooperative breeding and sex were only marginally important (i.e. SWAICc = 0.44; removed species: large-billed crows, N = 42). Finally, in one model the intercept-only model was included in the selection of best-fitting models (removed species: Eurasian jackdaws, N = 41), implying that the averaged model was not robust.

Siberian jays were the only species tested in the wild. In the prosocial test, they did not manage to coordinate to successfully provide food to their group members. However, even when excluding the Siberian jays from the dataset, the results were equivalent to the original model (Appendix 1—table 4). This confirms that our results were not driven by the low number of landings in the wild population per se.

Appendix 1—table 4
Effects of cooperative breeding, nesting type and sex on the number of landings in the prosocial test without the Siberian jays.

Given are estimates, standard errors (SE), z-values, sum of AICc weights (SWAICc), and number of models containing the specific factor (NModels) after model averaging. Factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0 were considered to have a high explanatory degree and are given in bold. Number of individuals: N = 48.

ParameterEstimateSEZSWAICcNModels
 (Intercept)6.1053.9891.495-
Cooperation (yes)10.3174.6372.1610.671
 Nesting (territorial)3.8354.4390.8391.002
Sex (male)17.6406.0592.8481.002
 Cooperation (yes) x Sex (male)−16.7837.0642.3080.671
 Nesting (territorial) x Sex (male)−18.6786.5742.7631.002

When using reduced datasets that included only the male birds, all eight models had the same results as before (i.e. only the main factor nesting type had a high explanatory degree; removed species: Eurasian jackdaws, N = 20; Siberian jays, N = 23; rooks, N = 24; common ravens, N = 23; New-Caledonian crows, N = 21; large-billed crows, N = 20; carrion crows, N = 23; azure-winged magpies, N = 21). Additionally, the male birds from colonial species landed significantly more often on the provisioning perch than the male birds from territorial species, when only testing for the factor nesting type (Welch t-test: t = 3.01, df = 13.66, p-value=0.005).

When using reduced datasets that included only the female birds, only two out of eight models had the same results as before (i.e. only the main factor cooperative breeding had a high explanatory degree; removed species: Siberian jays, N = 25; common ravens, N = 21), while nesting type had an added high explanatory degree in one model (removed species: azure-winged magpies, N = 22). In five models, the intercept-only model was included in the selection of best-fitting models (removed species: Eurasian jackdaws, N = 21; rooks, N = 24; New-Caledonian crows, N = 25; large-billed crows, N = 22; carrion crows, N = 22), implying that the averaged models were not robust. Also when testing only whether the females from cooperatively breeding species landed more often on the provisioning perch than the females from species that do not breed cooperatively, the results were only marginally significant (Welch t-test: t = −1.64, df = 8.30, p-value=0.069).

Phylogenetically controlled model

To test the extent to which common ancestry affected the birds’ prosocial tendencies, we calculated a phylogenetically controlled mixed-effects model with ‘number of landings in the prosocial test’ as response variable, and those parameters that were present in the top 2AICc models of the original analysis (i.e. ‘cooperative breeding’, ‘nesting type’, ‘sex’, and the interactions between ‘cooperative breeding’ and ‘sex’ and ‘nesting type’ and ‘sex’). Additionally, we added ‘phylogenetic effect’ and ‘species’ as random effects (see Source code 1, part 6). The results were equivalent to the original model: the main factors cooperative breeding and sex significantly predicted the number of landings on the provisioning perch in the prosocial test, and these main effects were again qualified by significant interactions between both cooperative breeding and sex and nesting type and sex (Appendix 1—table 5).

Appendix 1—table 5
Effects of cooperative breeding, nesting type, and sex on the number of landings in the prosocial test in a phylogenetically controlled model.

Given are the posterior mean of the estimate (Post. mean), its 95% credible interval (95% HPD interval), its effective sample size (Eff. samp.), and p-value (PMCMC) of each parameter. Number of individuals: N = 51. *p≤0.05, **p≤0.01, ***p≤0.001.

ParameterPost. mean95% HPD intervalEff. samp.PMCMC
 (Intercept)5.012[−3.198, 13.247]101110.210
 Cooperation (yes)10.001[0.082, 19.886]99980.048*
 Nesting (Territorial)4.346[−5.408, 13.376]99980.347
 Sex (male)19.660[8.899, 30.292]99980.0002***
 Cooperation (yes) x Sex (male)−20.576[−33.588,–8.551]99980.002**
 Nesting (territorial) x Sex (male)−16.394[−30.183,–2.329]99980.020*

Comparison of food provisioning in the original prosocial test and re-test of the prosocial test

Food provisioning in the original prosocial test and the re-test of the prosocial test, which was conducted after the main experiment, was correlated both on the group level (Spearman, N = 7, rho = 0.821, p=0.023) and on the individual level (N = 43, rho = 0.385, p=0.011).

Comparison of the number of landings on the provisioning perch in the different test phases

Across all species and groups (N = 55 birds), the birds differentiated between the prosocial test, the empty control, and the blocked control (Kruskal-Wallis chi-squared = 11.6, df = 2, p=0.003). They landed on the provisioning perch more often in the prosocial test (mean = 11.3, median = 6, min = 0, max = 46) than in both the empty control (mean = 5.0, median = 3, min = 0, max = 24; Wilcoxon W = 1010.5, p=0.003) and the blocked control (mean = 5.5, median = 2, min = 0, max = 45; Wilcoxon W = 994.5, p=0.002). There was no difference between the empty and the blocked control (Wilcoxon W = 1453.5, p=0.723).

When considering the groups with which we conducted the re-test (N = 43 birds), we found that these birds landed on the provisioning perch more often in the repeated prosocial test (mean = 10.1, median = 6, min = 0, max = 47) than in the repeated empty control (mean = 2.4, median = 1, min = 0, max = 10; Wilcoxon W = 547.5, p=0.001). There was no difference between the number of landings in the original prosocial test (mean = 12.7, median = 7, min = 0, max = 46) and in the re-test of the prosocial test (Wilcoxon W = 781.5, p=0.216).

Appendix 1—figure 1 shows the number of landings in the prosocial test, the empty control, and the blocked control, split by species. Additionally, for the six species with which we repeated the prosocial test and the empty control, Appendix 1—figure 1 shows the number of landings in the re-test.

Appendix 1—figure 1
Number of landings in all test phases, split by species.

The box plots represent medians (horizontal lines), inter-quartile ranges (boxes), as well as minima, maxima (whiskers). All data are represented with dots. Dots not encompassed by the whiskers are outliers. NA = not available.

Comparison of the percentage of landings in the motivation trials of the different test phases

Across all groups (N = 11) there was no difference between the percentages of motivation trials in which any bird landed on the provisioning perch across conditions (Kruskal-Wallis chi-squared = 1.1, df = 4, p=0.892). Appendix 1—table 6 shows the percentage of motivation trials with landings in the prosocial test, the empty control, and the blocked control, split by species and group. Additionally, for the six species with which we repeated the prosocial test and the empty control, Appendix 1—table 6 shows the percentage of motivation trials with landings in the re-test.

Appendix 1—table 6
Percentage of motivation trials with landings.

Given are – for each group – the number of motivation trials in the last two sessions of each condition and the percentage of motivation trials in which any bird landed on the provisioning perch, as well as the median, minimum and maximum of these percentages. NA = not available, min = minimum, max = maximum.

SpeciesGroupMotivation trials (N)TestEmptyBlockedRe-test
 TestEmpty
Azure-winged magpies112100100100100100
21292100100100100
Carrion crows11410010010093100
Rooks114100100799393
Eurasian jackdaws126100100100100100
Common ravens120100100100100100
Large-billed crows1201001008010055
New-Caledonian crows18100100100NANA
268383100NANA
Siberian jays112758383NANA
28758850NANA
Median (min, max)100 (75, 100) 100 (83, 100)100 (50, 100)100 (93, 100)100 (55, 100)

Appendix 2

Supplementary methods

Supplementary procedure

The experiment consisted of six consecutive phases in a fixed sequence: three habituation/training phases and three test phases (see Figure 1c). With six species (seven groups) we repeated the test and empty control in an additional phase 1–3 months after the original test sessions to exclude that reduced landings in the blocked control were due to order effects (Figure 1c). None of the groups received any training with the apparatus in-between the original test and the re-test.

Due the groups’ greatly different group sizes, we adjusted the number of trials per session in all phases to the number of individuals in the group. Like this, each individual in each group had an equal chance to obtain food rewards.

Phase 0 – Habituation to the apparatus

The apparatus was installed in the home aviary. After two weeks the seesaw mechanism was fixed with the provisioning perch pointing downwards. A food bowl was mounted in front of the perch on the inside of the aviary (Position 0; Figure 1b). In each session, the bowl was filled with highly preferred food (chosen depending on each species’ preferences) and the birds were video-recorded for thirty minutes. A bird reached criterion when it had landed on the perch and fed from the bowl at least five times.

Phase I – Habituation to the procedure

The seesaw mechanism was still fixed with the perch in a downward position, so that a piece of food placed on the board would automatically slide to the wire mesh and into the birds’ reach. On alternating days, pieces of food were provided either in position 0 or 1 (Figure 1b). In each trial, the experimenter called the birds' attention and placed one piece of food on the board. The next trial started after a bird obtained the food or after a maximum of 2 minutes. If a bird took the piece of food, the experimenter placed the next piece of food on the board. If no bird took the food, the experimenter called the birds' attention again, lifted the same piece of food and placed it back on the board. A session ended after number of individuals (N)*5 trials or when none of the birds landed on the perch for three consecutive trials. If a bird (or several birds) started monopolizing the apparatus, this bird (these birds) was (were) distracted or temporarily separated from the group. A bird reached the habituation criterion when it had taken at least 10 pieces of food in a minimum of 5 sessions. Average number of sessions to criterion, split by group can be seen in Appendix 1—table 1.

Phase II – Access to food assessment (test phase)

The seesaw mechanism was still fixed with the perch in a downward position. The experimenter put N*5 pieces of food on the apparatus in position 1, one at a time and called the birds' attention each time. After the food was taken the experimenter placed the next piece of food on the board. Two sessions of the access to food assessment were conducted on 2 consecutive days. We recorded how many pieces of food each bird obtained.

Phase III – Training

In this phase, the birds learnt to move food towards the wire mesh by landing on the perch. Food was always placed in position 0. To facilitate learning, the seesaw mechanism was first partially released – so that the perch moved only slightly – and food was placed close to the wire mesh. When each bird had obtained food from the apparatus at least once, the mechanism was released further. In the final step, the seesaw mechanism was completely released and the food was placed at the other end of the board.

In each trial, the experimenter called the birds' attention and placed one piece of food on the board. The next trial started after a bird obtained the food or after a maximum of 2 minutes. A session ended after N*5 trials or when none of the birds landed on the perch for three consecutive trials. Again, if a bird started monopolizing the apparatus, this bird was distracted or temporarily separated from the group. A bird reached training criterion when it had taken at least 10 pieces of food in a minimum of 5 sessions with the seesaw mechanism completely released. Average number of sessions to criterion, split by group can be seen in Appendix 1—table 1.

Phase IV – Group service (test phase)

In this phase, the apparatus’ seesaw mechanism was completely released. We conducted five test sessions and five empty control sessions on alternating days. To ensure that the birds had comparable motivation levels (e.g. hunger) in all conditions we conducted all sessions at the same testing times per day for each respective species. Unforeseeable surrounding circumstances (e.g. bad weather) happened equally for the different conditions and did not seem to affect the birds’ motivation to participate.

In a regular trial of a test session, a piece of food was placed in position 1 (see Video 1). Additionally, each session comprised motivation trials with food in position 0 in the very beginning of the session and after every fifth regular trial. Each session consisted of N*5 regular and N+1 motivation trials. In each trial the experimenter called the birds' attention and placed one piece of food on the board. The next trial started after a bird obtained the food or after a maximum of 2 minutes.

The empty control sessions were identical to the test sessions, except that in the regular control trials no food was placed on the board. In these trials, the experimenter approached the apparatus and pretended to leave a piece of food in position 1, while calling the birds’ attention (see Video 2). Control sessions also comprised motivation trials with food in position 0. Each session consisted of N*5 regular and N+1 motivation trials.

For each trial, we recorded which animal(s) landed on the perch in position 0 (i.e. moved the seesaw mechanism) and which animal(s) landed in front of position 1. Additionally, we recorded which animal obtained the piece of food and which animal provided the piece of food.

Phase V – Blocked control (test phase)

In this phase, the access to position one was blocked with a fine-meshed net, so that no food could be obtained in this position. Otherwise, the procedure was exactly the same as in group service and we conducted five blocked control sessions (i.e. food is placed in position 1; see Video 3) and five blocked empty control sessions (i.e. no food is placed in position 1) on alternating days. To ensure that the birds had comparable motivation levels (e.g. hunger) compared to the previous conditions we conducted all sessions at the same testing times per day as previously for each respective species. For each trial, we recorded which animal(s) landed on the perch in position 0 and which animal(s) landed in front of position 1.

Phase VI – Group service re-test (test phase)

The procedure was exactly the same as in group service and we conducted two test sessions and two empty control sessions on alternating days. For each trial, we recorded which animal(s) landed on the perch in position 0 (i.e. moved the seesaw mechanism) and which animal(s) landed in front of position 1. Additionally, we recorded which animal obtained the piece of food and which animal provided the piece of food.

Supplementary subject information

Appendix 2—table 1 shows the study sites, subject and husbandry details, testing period, and ethical approval information for all study groups.

Appendix 2—table 1
Study sites, subject and husbandry details, testing period, and ethical approval information.
SpeciesStudy siteSubject and husbandry detailsTesting periodEthical approval
Azure-winged magpies
(Cyanopica cyana)
Group 1
Haidlhof Research Station, University of Vienna and University of Veterinary Medicine Vienna, AustriaSubjects: two females, three males; all birds were adults and parent-raised.
Housing: outdoor aviary (5 × 3×3 m), partially covered with a semi-transparent roof; the aviary used fine-grained sand as substrate and was equipped with fixed and swinging branches, live plants, stones, woodchips and gravel for caching food, a birdbath, and other enrichment objects.
Feeding: the birds were fed daily with different fruits, insects, and seeds; water and pellets (‘Beo komplet’, NutriBird) were provided ad libitum; vitamin supplements and meat or egg were provided every second week.
Apr – Nov 2015; re-test: Apr 2016All animal care and data collection protocols were approved by the Animal Welfare Board of the Faculty of Life Sciences, University of Vienna (permit no. 2016–008).
Azure-winged magpies
(Cyanopica cyana)
Group 2
Animal Care Facility of the Department of Cognitive Biology, University of Vienna, AustriaSubjects: two adult females, one adult male, one juvenile female (<1 year old); all birds were parent-raised. one additional juvenile bird was housed in the same aviary, but never participated in the experiment due to physical impairments.
Housing: outdoor aviary (6 × 3×3 m), fully covered with a semi-transparent roof; for equipment see group 1.
Feeding: see group 1
Nov 2015 –
Apr 2016; re-test: May 2016
All animal care and data collection protocols were approved by the Animal Welfare Board of the Faculty of Life Sciences, University of Vienna (permit no. 2016–008).
Carrion crows
(Corvus corone)
Haidlhof research station, University of Vienna and university of veterinary medicine vienna, AustriaSubjects: four females, two males; all birds were adults and hand-raised.
By appearance, the crows were either carrion crows or hybrids of carrion and hooded crows, reflecting the hybridization belt in Europe. Both species have highly similar life histories and are often considered to belong to one species complex (Vijay et al., 2016).
Housing: the aviary comprised a large outdoor part (12 × 9 × 5 m) and two adjacent roofed experimental compartments (3 × 4 × 5 m each); the aviary used coarse sand as substrate and was equipped with fixed and swinging branches, live plants, stones, woodchips and gravel for caching food, several birdbaths, and other enrichment objects.
Feeding: the birds were fed a diverse diet containing meat, milk products, cereal, vegetables, and fruit twice a day; water was provided ad libitum.
Oct 2015 –
May 2016; re-test: Jul 2016
All animal care and data collection protocols were approved by the Animal welfare board of the faculty of life sciences, University of Vienna (permit no. 2016–017).
Common ravens
(Corvus corax)
Haidlhof Research Station, University of Vienna and University of Veterinary Medicine Vienna, AustriaSubjects: three adult birds (>4 years old; 1F/2M), six subadult birds (2 years old; 4F/2M); all birds were hand-raised.
Housing: large outdoor aviary (15 × 15×5 m) that could be divided into several compartments; equipment see carrion crows.
Feeding: see carrion crows.
May – Oct 2016; re-test: Nov 2016All animal care and data collection protocols were approved by the Animal Welfare Board of the Faculty of Life Sciences, University of Vienna (permit no. 2016–017).
Large-billed crows
(Corvus macrorhynchos)
Tsukuba Field Station, Keio University, JapanSubjects: nine sub-adult birds (all were 3 years old; 4F and 5M); all birds were parent-raised and born in the wild. They were caught as free-floating yearlings in the wild and group-housed thereafter.
Housing: outdoor aviary (10 × 10 × 3 m) that could be divided four experimental compartments (5 × 5×3 m); the aviary used coarse sand as substrate and was equipped with large branches, a water pool for bathing and other enrichment objects.
Feeding: Dairy diet consisted of dog food, meat, eggs, dried fruits. Water was available ad libitum.
May – Jul 2016; re-test: Dec 2016Animal Care and Use Committee of Keio University (no. 16059)
New-Caledonian crows
(Corvus moneduloides)
Group 1
La Foa, Province Sud, New CaledoniaSubjects: two adult birds (>3 years old; 1F and 1M) and one juvenile bird (1 st year; M); family group; all were wild caught, temporarily housed and released in the wild.
Housing: Crows were housed in an outdoors aviary for temporary behavioral research purposes before being released back into the wild.
Feeding: Daily diet consisted of meat, dog food, eggs, and fresh fruit, with water available ad libitum.
Jun – Jul 2017University of Auckland Animal Ethics Committee (reference no. 001823).
New-Caledonian crows
(Corvus moneduloides)
Group 2
La Foa, Province Sud, New CaledoniaSubjects: one adult bird (>3 years old; M) and one juvenile bird (1 st year; M); father and son dyad; both were wild caught, temporarily housed and released in the wild.
Housing: see group 1
Feeding: see group 1
May – Jul 2016University of Auckland Animal Ethics Committee (reference no. 001823).
Rooks
(Corvus frugilegus)
‘Eulen- und Greifvogelstation’, Haringsee, AustriaSubjects: 10 adult birds (5F/5M), two subadult birds (1F/1M); all birds were parent-raised and born in the wild.
Housing: outdoor aviary (3.3 × 7.4 × 3.1 m) with a roofed platform (3.3 × 1.1 m); the aviary used soil and bark chips as substrate and was equipped with large branches, a water pool for bathing and other enrichment objects.
Feeding: the birds were fed on a daily basis with cereals, dried mealworms, minced meat mixed with calcium carbonate and small pieces of scrambled eggs; water was provided ad libitum; nuts and chicks were provided several times a week.
May 2016 –
Mar 2017; re-test: Jun 2017
All animal care and data collection protocols were approved by the Animal Welfare Board of the Faculty of Life Sciences, University of Vienna (permit no. 2016–017).
Siberian jays
(Perisoreus infaustus)
Group 1
Wild population, studied near
Arvidsjaur, Swedish Lapland (65°40 N, 19°0 E)
Subjects: male breeder, two non-breeders born in spring 2017, two juveniles born in spring 2018; one subject did not participate in phase 4; all individuals are members of a wild group of Siberian jays, part of a long-term study on individually color-ringed Siberian jays (see Ekman & Griesser 2016).
Living area: The study was carried out in a natural setting in a wild population, thus the birds required no care. The apparatus was placed within the focal group’s territory. We provided less preferred food (pig fat) on a standardized feeding device on the side of the experimental apparatus to keep the group near the apparatus.
Sept – Oct 2018
(Experiments were carried out when the birds engage in storing food for winter)
Experiments approved by Umea ethics board, A39-15. Ringing under the license of the Swedish Museum of Natural History.
Siberian jays
(Perisoreus infaustus)
Group 2
Wild population, studied near
Arvidsjaur, Swedish Lapland (65°40 N, 19°0 E)
Subjects: male and female breeder, one juvenile born spring 2018.
Living area: See above for details.
Sept – Oct 2018
(Experiments were carried out when the birds engage in storing food for winter)
Experiments approved by Umea ethics board, A39-15. Ringing under the license of the Swedish Museum of Natural History.
Eurasian jackdaws
(Corvus monedula)
Comparative Cognition Research Group of the Max-Plank-Institute for Ornithology in Seewiesen, GermanySubjects: 7 males and seven females adult birds (>4 years old), most of the birds were hand-raised.
one subject (male) participated only in phases 0–2; one subject (female) only participated in phases 0–3.
two subjects (1 male and one female) joined the group in June 2017 and participated in phases 3–6.
Housing: the birds had access to two aviaries (aviary 1: 15m × 9 m × 2.80 m; aviary 2: 12m × 10 m × 2.80 m) with adjacent experimental compartments. All compartments had natural soil and vegetation, including bushes and small trees, and were equipped with breeding boxes, several birdbaths, and other enrichment objects.
Feeding: the birds were fed a diverse diet consisting of meat, insects, curd, rice, cereals and Versele Laga Nutribird Beo pearls, and fruit twice a day; water was provided ad libitum. The food was enriched with mineral and vitamin supplements.
Aug 2016 –
Aug 2017; re-test: Sep 2017
The study followed the protocols of the University of Vienna and followed the guidelines of the Association for the Study of Animal Behaviour and conformed the European and German legalisations and guidelines for the use of animals. All animals were habituated to humans.

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Decision letter

  1. Ammie K Kalan
    Reviewing Editor; Max Planck Institute for Evolutionary Anthropology, Germany
  2. Detlef Weigel
    Senior Editor; Max Planck Institute for Developmental Biology, Germany

In the interests of transparency, eLife publishes the most substantive revision requests and the accompanying author responses.

Acceptance summary:

This study presents an important contribution to comparative animal cognition research. Using an experimental paradigm that was originally used to test prosociality in primates, this study tests prosociality across eight species of corvids. Of particular interest is the finding that the species-specific traits of cooperative breeding and colonial nesting effect prosocial behavioural tendencies but do so to varying degrees for males and females. This work therefore provides valuable insight into the potential evolutionary pathways and drivers of prosociality.

Decision letter after peer review:

Thank you for submitting your article "Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids" for consideration by eLife. Your article has been reviewed by three peer reviewers, one of whom is a member of our Board of Reviewing Editors, and the evaluation has been overseen by a Reviewing Editor and Detlef Weigel as the Senior Editor. The reviewers have opted to remain anonymous.

The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission.

As the editors have judged that your manuscript is of interest, but as described below that additional analyses are required before it is published, we would like to draw your attention to changes in our revision policy that we have made in response to COVID-19 (https://elifesciences.org/articles/57162). First, because many researchers have temporarily lost access to the labs, we will give authors as much time as they need to submit revised manuscripts. We are also offering, if you choose, to post the manuscript to bioRxiv (if it is not already there) along with this decision letter and a formal designation that the manuscript is "in revision at eLife". Please let us know if you would like to pursue this option. (If your work is more suitable for medRxiv, you will need to post the preprint yourself, as the mechanisms for us to do so are still in development.)

Summary:

The authors present an interesting study on the prosocial tendencies of eight bird species within the Corvid family, using species-specific predictors of colonial nesting and cooperative breeding. Importantly, the study replicates an experimental paradigm used to test prosociality in several species of primates. The authors show that cooperative breeding and colonial nesting affect prosocial behaviors, with interesting interactions by sex, apparently driven by female cooperative breeders and male colonial nesters.

Essential revisions:

The reviewers all found the comparative approach to be worthwhile and the paper to be well written and easy to follow for the most part, but all three had major concerns with the analyses. There were also some concerns with the experimental procedure, which might be addressed by simply modifying or adding analyses. The authors should also include a file with all the R code used to run and interpret the models and all other analyses (e.g, Pielou's J), as well as the source files for figures when submitting a revision.

1) It is not clear why the authors chose to apply different criteria for different parts of the analyses. In particular, passing the last criteria (test vs controls) appears to be crucial to establish prosociality in these species (and actually is a test in itself). We agree with the authors that there are reasons why birds might not have passed (e.g. as discussed lacking cooperation by receiving birds), but at the very least, we would like see the results of an analysis for just the birds that passed the criterion and how these results compare to the presented ones (as the authors did for percentage of provided food). Of course, this will drastically reduce sample size but such an analysis would be especially important considering the percentage of birds passing the criteria was high in the cooperatively breeding and/or colonial species.

2) Why were test and control sessions conducted on alternating days (rather than pseudo-randomly distributing them throughout the session, or even better on a trial level)? With the current design we are concerned that the data is not independent within a day. (The same applies, albeit to a lesser degree as it is only the habituation phase to phase I). Given that this can't be changed anymore, can it be accounted for in the models?

3) Many of the effects observed for each species are driven by very few individuals, which casts doubt on how well the results reflect true species generalizations rather than individual personalities. For example, the species where more than one group could be tested showed a lot of variation, presumably due to the presence of particular individuals. Could the authors (1) clarify in the manuscript that for all models/analyses that only one data point per individual was used? (2) Could the authors provide more discussion about possible inter-individual differences and how this could effect their results?

4) Why was a phylogenetic generalized linear mixed model (pglmm) not used, especially considering the variation in relatedness among the 8 species (seen in Figure 2)? Please provide clear justification or else re-run using a pglmm framework.

5) The model selection approach is problematic for a number of reasons. Firstly, the candidate set of models was not clear (this should be included clearly with the code for the paper) and where did the intercept only model fall relative to the others when ranked by AIC? This needs to be explicitly discussed in the Results section. Second, the p values being reported (e.g., Table 2) are not understandable, are they from two different models? An average? Why are you reporting them at all and not instead model-weighted averages (e.g., summed akaike weights) of the different predictors, including group size, considering you are using an information theory-based approach with AIC? With relatively few predictors and strong theoretical support for each, such as in this study, selecting the best models (delta AIC <2) seems arbitrary and leads to removing potentially important variables, like group size, based on this threshold (note Burnham et al., 2010 also note ' Models where Δ is in the 2-7 range have some support and should rarely be dismissed'). A more parsimonious approach is to use a model set and model weighted averages of coefficients and SEs and Akaike weights to assess covariate support (see Mundry, 2011 and Burnham et al., 2011 for best practices associated with multimodel inference and how to report results).

6) Table 2 of the main results is somewhat misleading since reporting coefficients and p values of main effects when their interaction is significant are problematic (see for example Brambor, Clark and Golder, 2006). It is fine to demonstrate via plotting the unconditional effects of the two factors, but Table 2 on its own is confusing since the interaction tells us that the main effects are conditional upon one another.

7) The Introduction suggests sex ratio of groups may be an important predictor of prosocial tendencies in some species. Considering that sex ratio varies among the social groups of birds tested, this should be included as a predictor in the models. Similarly, is there any reason to suspect variation according to age, i.e., juveniles and adults? If so, should this not also be included?

8) The sex-specific models with only 25/26 data points suggests these models may be incredibly unstable, and there is no mention of group ID or species being included. If these terms were dropped from these models this should have been tested as you did with the full data set but we could not find this mentioned anywhere. Moreover, can you provide some measure of how robust and stable the results of the sex-specific models are? For example, check how much variation there is in your coefficients if one species is removed at a time? A similar exercise would also add credibility to your results for the full data set.

[Editors' note: further revisions were suggested prior to acceptance, as described below.]

Thank you for resubmitting your work entitled "Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids" for further consideration by eLife. Your revised article has been evaluated by Detlef Weigel (Senior Editor) and a Reviewing Editor.

The manuscript has been significantly improved but there are some remaining issues that need to be addressed before acceptance, as outlined below:

1) Regarding our previous major concern, point #2, we understand that day is confounded with test condition, but could the authors not simply add day as a random effect (intercept only, no slopes needed to keep the model simple)? We would like the authors to consider this approach if possible, to fit.

2) Regarding the model stability check for the single sex models and for the full model, we suggest the authors add a short description of how they did this to the section titled 'Data analysis' and when reporting the results, especially for the single sex models, explicitly state in the manuscript that the female model is less robust/stable (similar to what you wrote in your response) and that in general the single sex model results are very preliminary due to the low sample size. More data are definitely needed here.

3) We appreciate the authors checking whether they obtained similar results when using a cut off of AIC<7 for 'top models'. We would suggest that for transparency, the authors also add that they did this additional check (subsection “Data Analysis”) and add Table R1 (in the response letter) as a supplementary table. Since the results do differ slightly, we think it is worthwhile to provide the reader with all possible information.

https://doi.org/10.7554/eLife.58139.sa1

Author response

Summary:

The authors present an interesting study on the prosocial tendencies of eight bird species within the Corvid family, using species-specific predictors of colonial nesting and cooperative breeding. Importantly, the study replicates an experimental paradigm used to test prosociality in several species of primates. The authors show that cooperative breeding and colonial nesting affect prosocial behaviors, with interesting interactions by sex, apparently driven by female cooperative breeders and male colonial nesters.

Essential revisions:

The reviewers all found the comparative approach to be worthwhile and the paper to be well written and easy to follow for the most part, but all three had major concerns with the analyses. There were also some concerns with the experimental procedure, which might be addressed by simply modifying or adding analyses. The authors should also include a file with all the R code used to run and interpret the models and all other analyses (e.g,. Pielou's J), as well as the source files for figures when submitting a revision.

We created a source code file that allows readers to reproduce our calculations of Pielou’s J’ and our statistical models in R. The data used to create Figure 2 is taken from the dataset that is available in full on Dryad (Corvid_GSP_Data.csv). The data used to create Figure 3 is now available as Figure 3—source data 1.

1) It is not clear why the authors chose to apply different criteria for different parts of the analyses. In particular, passing the last criteria (test vs controls) appears to be crucial to establish prosociality in these species (and actually is a test in itself). We agree with the authors that there are reasons why birds might not have passed (e.g. as discussed lacking cooperation by receiving birds), but at the very least, we would like see the results of an analysis for just the birds that passed the criterion and how these results compare to the presented ones (as the authors did for percentage of provided food). Of course, this will drastically reduce sample size but such an analysis would be especially important considering the percentage of birds passing the criteria was high in the cooperatively breeding and/or colonial species.

We agree with the reviewers that it is a very interesting aspect to look at the landings of the individuals that reached the criterion of being “prosocial” (i.e., meeting the criterion of landing significantly more often in the test than in both controls) and whether they differ between individuals from species that are cooperative breeders (or not) or that are colonial nesters (or not). Due to the extremely small sample of significantly “prosocial” individuals (N=12), we were not able to calculate models that included both factors “cooperative breeding” and “colonial nesting” simultaneously or to include the important interactions with “sex”. But we used non-parametric tests to assess differences between the two factors “cooperative breeding” and “colonial nesting” separately. Among the “prosocial” individuals we found a non-significant trend that individuals from colonial species landed more often than individuals from territorial species (Mann-Whitney test, N=12, W=30, p=0.0505). Individuals from cooperatively breeding species did not differ in the number of their landings from individuals from species that do not breed cooperatively (Mann-Whitney test, N=12, W=13, p=0.4696). We report and discuss these results in the manuscript (subsection “Linking cooperative breeding and colonial nesting with prosocial behavior”; Discussion section).

2) Why were test and control sessions conducted on alternating days (rather than pseudo-randomly distributing them throughout the session, or even better on a trial level)? With the current design we are concerned that the data is not independent within a day. (The same applies, albeit to a lesser degree as it is only the habituation phase to phase I). Given that this can't be changed anymore, can it be accounted for in the models?

It is an important aspect of the group service paradigm that each session is composed only of trials of one condition, because the aim is for the animals to learn the contingencies of the specific condition. Intermixing trials of different conditions within one session would have placed much more cognitive load on the participating birds (e.g., attention, inhibition) and might have prevented the birds from ever learning the contingencies. Burkart et al., specifically developed this paradigm to be cognitively simple (discussed in Burkart et al., 2013), while allowing to measure the animals’ prosocial tendencies by testing whether they would continue to provide for their group members after they had learned the contingencies of each condition over 5 sessions each (i.e., that the group members, but not the individual itself obtains food in the prosocial test; that nobody can obtain food in the control conditions). Moreover, the blocked control sessions required a modification of the apparatus (i.e. installing a fine-meshed net that prevented birds on the receiving side to obtain a reward). Due to high levels of neophobia in corvids (Greenberg and Mettke-Hofmann, 2001), this modification required a pause of a few days between Phase IV (Prosocial Test and Empty Control) and Phase V (Blocked Control and Blocked Empty Control) and we could therefore not have alternated sessions with and without the fine-meshed net installed.

We mitigated the problem of having sessions of different conditions on different days by conducting them at the same testing times on each day for each respective species, thereby aiming to have comparable motivation levels (e.g., hunger) for all conditions. Our analysis of the motivation trials shows that there was no significant difference in how many food pieces were obtained in the motivation trials of each condition (see Appendix 1—table 5), which suggests that the birds’ motivation to participate in the experiment was comparable in all conditions. Unforeseeable surrounding circumstances (e.g., bad weather) happened equally often for the different conditions and did not seem to affect the birds’ motivation to participate. Below, we include graphs for the birds’ responses in the different conditions over the five sessions, to illustrate how they learned the contingencies over the testing days and how they behaved across days and between conditions.

We used the procedure of conducting test and control sessions on alternating days to keep the procedure as comparable as possible to the one designed by Burkart et al., and in order to avoid potential carry-over effects from two consecutive test or control sessions. But we agree with the reviewers that for future studies, it might be interesting to introduce a pseudo-randomized sequence or even test the birds’ cognitive abilities by intermixing trials of different conditions within one session and seeing how flexibly the birds can switch from one behavioral strategy to another.

We added more information about this issue in the main manuscript (i.e., “To ensure that the birds had comparable motivation levels (e.g., hunger) in all conditions we conducted all sessions at the same testing times per day for each respective species.” subsection “Apparatus and procedure”) and in Appendix 2 (subsection “Phase IV – Group service (Test phase)”). Since the factor “testing day” is confounded with “condition” in the current procedure, we were not sure how to include this in our statistical models.

Author response image 1
Number of landings across the testing days of Phase IV (prosocial test vs empty control) for all groups.

The box plots represent medians (horizontal lines), inter-quartile ranges (boxes), as well as minima, maxima (whiskers). Dots not encompassed by the whiskers are outliers.

Author response image 2
Number of landings across the testing days of Phase V (blocked control vs blocked empty control) for all groups.

The box plots represent medians (horizontal lines), inter-quartile ranges (boxes), as well as minima, maxima (whiskers). Dots not encompassed by the whiskers are outliers.

3) Many of the effects observed for each species are driven by very few individuals, which casts doubt on how well the results reflect true species generalizations rather than individual personalities. For example, the species where more than one group could be tested showed a lot of variation, presumably due to the presence of particular individuals. Could the authors (1) clarify in the manuscript that for all models/analyses that only one data point per individual was used? (2) Could the authors provide more discussion about possible inter-individual differences and how this could effect their results?

1) We confirm that only one data point per individual was used in all statistical information and added this remark in the subsection “Data analysis”.

2) We added a more substantial discussion about the possible inter-group differences and inter-individual differences, the potential sources of these issues, and some ideas about how to ameliorate such effects in future studies (Discussion section).

4) Why was a phylogenetic generalized linear mixed model (pglmm) not used, especially considering the variation in relatedness among the 8 species (seen in Figure 2)? Please provide clear justification or else re-run using a pglmm framework.

To test the extent to which common ancestry affected the birds’ prosocial tendencies, we added a phylogenetically controlled mixed-effects model with “number of landings in the prosocial test” as response variable, and those parameters that were present in the top 2AICc models of the original analysis (i.e., “cooperative breeding”, “nesting type”, “sex”, and the interactions between “cooperative breeding” and “sex” and “nesting type” and “sex”). Additionally, we added “phylogenetic effect” and “species” as random effects. We further calculated the posterior mean (mean of the posterior distribution), the posterior mode (most likely value regarding the posterior distribution) and the 95% credible interval of the phylogenetic signal λ. We found that the results were equivalent to the original model: the main factors cooperative breeding and sex significantly predicted the number of landings on the provisioning perch in the prosocial test, and these main effects were again qualified by significant interactions between both cooperative breeding and sex and nesting type and sex. The phylogenetic signal was weak. We report and discuss these results in the "manuscript (subsection “Testing the effect of phylogeny on prosocial behavior”; Discussion section).

5) The model selection approach is problematic for a number of reasons. Firstly, the candidate set of models was not clear (this should be included clearly with the code for the paper) and where did the intercept only model fall relative to the others when ranked by AIC? This needs to be explicitly discussed in the Results section.

We explained in more detail how we obtained the candidate set of models and that the intercept-only model did not fall within the final selection of best-fitting models (subsection “Data analysis”).

Second, the p values being reported (e.g., Table 2) are not understandable, are they from two different models? An average? Why are you reporting them at all and not instead model-weighted averages (e.g., summed akaike weights) of the different predictors, including group size, considering you are using an information theory-based approach with AIC?

We revised the table and removed the p-values and confidence intervals. We also realized that the values of the sum of AICc weights was mislabeled as “relative importance” and we corrected this error. We further included a column with the number of models in which each given factor was present. We highlighted these factors in bold, which were considered to have a high explanatory degree (i.e., factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0). The table is now presented as Figure 2—figure supplement 1.

With relatively few predictors and strong theoretical support for each, such as in this study, selecting the best models (delta AIC <2) seems arbitrary and leads to removing potentially important variables, like group size, based on this threshold (note Burnham et al., 2010 also note ' Models where Δ is in the 2-7 range have some support and should rarely be dismissed'). A more parsimonious approach is to use a model set and model weighted averages of coefficients and SEs and Akaike weights to assess covariate support (see Mundry, 2011 and Burnham et al., 2011 for best practices associated with multimodel inference and how to report results).

In order to ascertain that our cut-off point of delta AICc≤2 did not lead us to remove potentially important variables, we repeated the model selection and averaging procedure with delta AICc≤7. The results were equivalent to the original analysis: cooperative breeding, sex, the interaction between cooperative breeding and sex, and the interaction between nesting type and sex emerged as factors with a high explanatory degree (given in bold in Table R1). Setting the cut-off point at delta AICc≤7 only led to the inclusion of three additional factors with minimal explanatory degree (i.e., the interaction between cooperative breeding and nesting type, the factor group size, and the three-way interaction; see below). Therefore, we feel that our original approach with a cut-off point of delta AICc≤2 is supported.

Table R1 – cut-off point set to delta AICc≤7. Given are estimates, standard errors (SE), z-values, sum of AICc weights (SWAICc), and number of models containing the specific factor (NModels) after model averaging. Factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0 were considered to have a high explanatory degree and are given in bold.

6) Table 2 of the main results is somewhat misleading since reporting coefficients and p values of main effects when their interaction is significant are problematic (see for example Brambor, Clark and Golder, 2006). It is fine to demonstrate via plotting the unconditional effects of the two factors, but Table 2 on its own is confusing since the interaction tells us that the main effects are conditional upon one another.

Due to the revised depiction of the results we now don’t report p-values anymore. In the Results section we described in more detail that the main effects have to be viewed in the light of the important interaction terms and that they are conditional upon one another (“These main effects were qualified by the high explanatory degree of the interaction terms of both cooperative breeding and nesting type with sex (Figure 2—figure supplement 1), meaning that the main effects were conditional upon one another.”; subsection “Linking cooperative breeding and colonial nesting with prosocial behavior”) and we also refer to this issue in the Discussion section.

7) The Introduction suggests sex ratio of groups may be an important predictor of prosocial tendencies in some species. Considering that sex ratio varies among the social groups of birds tested, this should be included as a predictor in the models. Similarly, is there any reason to suspect variation according to age, i.e., juveniles and adults? If so, should this not also be included?

We are not aware of any studies suggesting that sex ratio of social groups affects prosocial tendencies in corvids or other non-human animal species. We would be happy to include such references, in case the reviewers have specific suggestions.

In order to investigate a potential effect of sex ratio on prosocial behavior, we re-ran our original analysis and added “sex ratio” as an additional predictor without interactions. We had to exclude all the Siberian jays from this analysis, since sex was unknown for a substantial number of individuals and therefore sex ratio could not be calculated. The results were very similar to the original results and the factor “sex ratio” was not present in the final selection of best-fitting models with delta AICc≤2. In order to explore the importance of the factor “sex ratio” further, we repeated the model selection and averaging procedure with delta AICc≤7. The results were equivalent to the original analysis (see Table R2). “Sex ratio” was included in this selection, but had only minimal explanatory degree (SWAICc=0.22; see results below). Additionally, since we had no a priori predictions about the factor “sex ratio” and because we are already suffering from low power due the low sample size, we would opt to not include the sex ratio in our manuscript.

Table R2 – including the factor “sex ratio”, cut-off point set to delta AICc≤7. Given are estimates, standard errors (SE), z-values, sum of AICc weights (SWAICc), and number of models containing the specific factor (NModels) after model averaging of all models with delta AICc≤7. Factors with a sum of AICc weights larger than 0.5 and whose SE of the estimates did not overlap 0 were considered to have a high explanatory degree and are given in bold.

Regarding the question about a possible effect of age-variation in the group: in our sample, only five groups from three species contained juvenile individuals, while six groups consisted only of adults. Therefore, our data is unfortunately not suitable for investigating this factor. However, we fully agree with the reviewers that future studies either with larger sample sizes, or where samples can be selected specifically with regard to age variation within the group, or where the same groups could be tested at different time points with differing age class ratios would be very informative regarding the question of the influence of age on prosocial behavior. We added this information in the Discussion section.

8) The sex-specific models with only 25/26 data points suggests these models may be incredibly unstable, and there is no mention of group ID or species being included. If these terms were dropped from these models this should have been tested as you did with the full data set but we could not find this mentioned anywhere.

For the datasets split by sex we used the same procedure as for the complete dataset. We first calculated linear mixed-effects models with “group ID” nested within “species” as random factors. As for the complete dataset, the variance of the random factors “group ID” and “species” was zero, resulting in a singular fit of the models and we therefore decided to calculate linear models, as we did it for the complete dataset. This information is now provided more clearly in the subsection “Data analysis”.

Moreover, can you provide some measure of how robust and stable the results of the sex-specific models are? For example, check how much variation there is in your coefficients if one species is removed at a time? A similar exercise would also add credibility to your results for the full data set.

We used the suggested procedure of removing one species at a time and ran the linear models for the complete dataset (N=51) and the two models split by sex (males, N=25; females, N=26).

Results for the complete dataset:

With this approach, 4 (out of 8) models had exactly the same results as before (i.e., “cooperation”, “sex”, “cooperation*sex”, “nesting*sex” as important parameters; removed species: Siberian jays, NModel=48; rooks, NModel=48; ravens, NModel; carrion crows, NModel=45), while in 2 models the parameter “nesting” was also revealed to be important, additionally to the originally important parameters (Removed species: New-Caledonian crows, NModel=46; azure-winged magpies, NModel=43).

In 1 model “nesting”, “sex”, “nesting*sex” were important parameters, while “cooperation” and “cooperation*sex” were only marginally important (i.e., SWAICc=0.44; removed species: large-billed crows, NModel=42)

Finally, in 1 model the null model was included in the selection of best-fitting models (Removed species: jackdaws, NModel=41)

Therefore, while not all models give exactly the same results as the original model, we feel that the results are consistent and show the robustness of our original results. The exception is the model without the jackdaws, where the null model was included in the selection of best-fitting models.

Results for the males:

With the exclusion of one species at a time, 7 (out of 8) models had exactly the same results as before (i.e., “nesting” as important parameter; removed species: jackdaws, N=20; Siberian jays, N=23; rooks, N=24; ravens, N=23; NC crows, N=21; LB crows, N=20; AWM, N=21).

However, in 1 model the null model was included in the selection of best-fitting models (Removed species: carrion crows, N=23)

These results are very consistent (apart from the problem with the model without the carrion crows). Also when we tested whether males from colonial species landed significantly more often than males from territorial species with a simple group comparison, there was a significant difference (Welch t-test: t = 3.01, df = 13.66, p-value = 0.005).

These analyses show the robustness of our original results with the males.

Results for the females:

With the exclusion of one species at a time, 2 (out of 8) models had exactly the same results as before (i.e., “cooperative breeding” as important parameter; removed species: Siberian jays, N=25; ravens, N=21), while in 1 model the parameter “nesting” was also revealed to be important, additionally to “cooperative breeding” (Removed species: azure-winged magpies, N=22).

However, in 5 models the null model was included in the selection of best-fitting models (Removed species: jackdaws, N=21; rooks, N=24; NC crows, N=25; LB crows, N=22; carrion crows, N=22).

Also when testing whether females from cooperatively breeding species land significantly more often than females from non-cooperatively breeding species with a simple group comparison, the difference is only marginally significant (Welch t-test: t = -1.64, df = 8.30, p-value = 0.069). Therefore, while our results are consistent with the original analysis after the removal of 3 species, the results for the females are less robust than the results for the males.

The results of this procedure thus reveal moderate to good robustness of our findings. While we acknowledge the merit of such a procedure, we are not sure if or how to report this, and would be interested in the editors’ and reviewers’ view on that.

[Editors' note: further revisions were suggested prior to acceptance, as described below.]

The manuscript has been significantly improved but there are some remaining issues that need to be addressed before acceptance, as outlined below:

1) Regarding our previous major concern, point #2, we understand that day is confounded with test condition, but could the authors not simply add day as a random effect (intercept only, no slopes needed to keep the model simple)? We would like the authors to consider this approach if possible, to fit.

We appreciate the editors’ concerns about this point. However, the dependent variable in our models was the sum of the number of landings in prosocial test sessions 4 and 5. Therefore, the data from two testing days added together was entered in the models and those testing days were the same for all members of each tested group of birds. Data from the empty sessions, which were conducted on different days, were not added in these models at all. Data collection was also conducted at very different times for the different species (between April 2015 and October 2018; see Appendix 2—table 1), making testing days between species hard to compare. Therefore, we feel that it is not practicable to add a random effect “testing day” to our models. But in order to make it clearer to the readers that the summed data from the last two sessions was entered as the dependent variable in our models, we added the following information to the manuscript:

Subsection “Data analysis”: “we used only the summed data from the last two sessions (session 4 and 5) of each condition”.

Subsection “Data analysis”: “to further investigate the influence of cooperative breeding and colonial nesting on prosocial tendencies, we used the sum of the number of landings in the last two sessions of the prosocial test (phase IV) of all birds that passed the training criterion in the preceding phase”.

2) Regarding the model stability check for the single sex models and for the full model, we suggest the authors add a short description of how they did this to the section titled 'Data analysis' and when reporting the results, especially for the single sex models, explicitly state in the manuscript that the female model is less robust/stable (similar to what you wrote in your response) and that in general the single sex model results are very preliminary due to the low sample size. More data are definitely needed here.

We added the details from the model stability check in the Results section, the Discussion section, subsection “Data analysis” and Appendix 1. We specifically state that more data are needed in the Discussion section.

3) We appreciate the authors checking whether they obtained similar results when using a cut off of AIC<7 for 'top models'. We would suggest that for transparency, the authors also add that they did this additional check (subsection “Data Analysis”) and add Table R1 (in the response letter) as a supplementary table. Since the results do differ slightly, we think it is worthwhile to provide the reader with all possible information.

We added the information about the procedure with the threshold set to delta AICc≤7 to subsection “Data analysis” and added the table as Appendix 1—table 3.

https://doi.org/10.7554/eLife.58139.sa2

Article and author information

Author details

  1. Lisa Horn

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Contribution
    Conceptualization, Data curation, Formal analysis, Supervision, Validation, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing
    For correspondence
    lisa.horn@univie.ac.at
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9586-915X
  2. Thomas Bugnyar

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Contribution
    Conceptualization, Supervision, Funding acquisition, Methodology, Writing - review and editing
    Competing interests
    No competing interests declared
  3. Michael Griesser

    1. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
    2. Department of Biology, University of Konstanz, Konstanz, Germany
    3. Center for the Advanced Study of Collective Behaviour, University of Konstanz, Konstanz, Germany
    Contribution
    Formal analysis, Funding acquisition, Writing - review and editing
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2220-2637
  4. Marietta Hengl

    1. Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    2. Eulen- und Greifvogelstation Haringsee, Haringsee, Austria
    Contribution
    Data curation, Funding acquisition, Investigation
    Competing interests
    No competing interests declared
  5. Ei-Ichi Izawa

    Department of Psychology, Keio University, Tokyo, Japan
    Contribution
    Data curation, Funding acquisition, Investigation, Writing - review and editing
    Competing interests
    No competing interests declared
  6. Tim Oortwijn

    Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
    Contribution
    Data curation, Investigation, Writing - review and editing
    Competing interests
    No competing interests declared
  7. Christiane Rössler

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Contribution
    Data curation, Funding acquisition, Investigation, Writing - review and editing
    Competing interests
    No competing interests declared
  8. Clara Scheer

    1. Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    2. Faculty of Psychology, Education and Sports, University of Regensburg, Regensburg, Germany
    Contribution
    Conceptualization, Data curation, Investigation, Methodology
    Competing interests
    No competing interests declared
  9. Martina Schiestl

    Department of Linguistic and Cultural Evolution, Max Planck Institute for the Science of Human History, Jena, Germany
    Contribution
    Data curation, Investigation
    Competing interests
    No competing interests declared
  10. Masaki Suyama

    Department of Behavioral Sciences, Hokkaido University, Sapporo, Japan
    Contribution
    Data curation, Funding acquisition, Investigation
    Competing interests
    No competing interests declared
  11. Alex H Taylor

    School of Psychology, University of Auckland, Auckland, New Zealand
    Contribution
    Funding acquisition, Writing - review and editing
    Competing interests
    No competing interests declared
  12. Lisa-Claire Vanhooland

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Contribution
    Funding acquisition, Validation, Investigation
    Competing interests
    No competing interests declared
  13. Auguste MP von Bayern

    Max-Planck-Institute for Ornithology, Seewiesen, Germany
    Contribution
    Funding acquisition, Writing - review and editing
    Competing interests
    No competing interests declared
  14. Yvonne Zürcher

    Department of Anthropology, University of Zurich, Zurich, Switzerland
    Contribution
    Data curation, Investigation
    Competing interests
    No competing interests declared
  15. Jorg JM Massen

    1. Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    2. Animal Ecology Group, Department of Biology, Utrecht University, Utrecht, Netherlands
    Contribution
    Conceptualization, Supervision, Funding acquisition, Methodology, Writing - review and editing
    Competing interests
    No competing interests declared

Funding

Austrian Science Fund (P26806)

  • Jorg JM Massen

Austrian Science Fund (Y366-B17)

  • Thomas Bugnyar

Vienna Science and Technology Fund (CS11-008)

  • Thomas Bugnyar

ERA-Net BiodivERsA (31BD30_172465)

  • Michael Griesser

University of Vienna (Förderungsstipendium)

  • Marietta Hengl
  • Christiane Rössler

University of Vienna (Uni:Docs doctoral fellowship)

  • Lisa-Claire Vanhooland

JSPS (KAKENHI 17H02653)

  • Ei-Ichi Izawa

JSPS (KAKENHI 16H06324)

  • Ei-Ichi Izawa

JSPS (KAKENHI 15J02148)

  • Masaki Suyama

JST (CREST JPMJCR17A4)

  • Ei-Ichi Izawa

Keio University (ICR Projects MKJ1905)

  • Ei-Ichi Izawa

Royal Society of New Zealand (Rutherford Discovery Fellowship)

  • Alex H Taylor

Prime Minister's McDiarmid Emerging Scientist Prize

  • Alex H Taylor

University of Vienna (Marie Jahoda grant)

  • Lisa Horn

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Acknowledgements

This study was supported by the Austrian Science Fund (FWF; P26806 to JJMM; Y366-B17 to TB), the Vienna Science and Technology Fund (WWTF; CS11-008 to TB), the ERA-Net BiodivERsA (31BD30_172465 to MG), the University of Vienna (Marie Jahoda grant to LH; Förderungsstipendium to MH and CR; Uni:Docs doctoral fellowship to L-CV), the JSPS KAKENHI (17H02653, 16H06324 to E-II; 15J02148 to MSu), the JST CREST (JPMJCR17A4 to E-II), the Keio University ICR Projects (MKJ1905 to E-II), a Royal Society of New Zealand Rutherford Discovery Fellowship (AHT), and a Prime Minister’s McDiarmid Emerging Scientist Prize (AHT).

We thank Nadja Kavcik-Graumann for drawing the illustrations in Figure 1, Sarah Vlasitz for her help with habituating the ravens, and Hans Frey for granting access to the rooks at the Eulen- und Greifvogelstation Haringsee. Further, we thank Province Sud for granting us permission to work in New Caledonia, Dean M and Boris C for allowing us access to their properties for catching and releasing the crows, Russel Gray for granting access to the New Caledonian Crow Lab at the University of Auckland, and Romana Gruber for her help with reliability coding. Finally, we are grateful to András Péter for constructing the apparatuses and the animal care staff at all involved research facilities.

Ethics

Animal experimentation: The study followed the Guidelines for the Use of Animals (Vitale et al., 2018), in accordance with national legislations. All animal care and data collection protocols were reviewed and approved by the ethical boards of the respective research institutions (see Appendix 2-table 1).

Senior Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Reviewing Editor

  1. Ammie K Kalan, Max Planck Institute for Evolutionary Anthropology, Germany

Publication history

  1. Received: April 22, 2020
  2. Accepted: October 18, 2020
  3. Accepted Manuscript published: October 20, 2020 (version 1)
  4. Version of Record published: November 3, 2020 (version 2)

Copyright

© 2020, Horn et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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