Naïve individuals promote collective exploration in homing pigeons
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Evaluation Summary:
This study in the field of collective behavior addresses how naïve and experienced individuals (i.e., homing pigeons) pool information in order to navigate while flying back home. The authors show that the passage of information is largely democratic, meaning information passes both ways, and that, unexpectedly, exploration of the route is initiated both by naïve and experienced birds. The work provides a new perspective on information sharing during collective learning.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Group-living animals that rely on stable foraging or migratory routes can develop behavioural traditions to pass route information down to inexperienced individuals. Striking a balance between exploitation of social information and exploration for better alternatives is essential to prevent the spread of maladaptive traditions. We investigated this balance during cumulative route development in the homing pigeon Columba livia . We quantified information transfer within pairs of birds in a transmission-chain experiment and determined how birds with different levels of experience contributed to the exploration–exploitation trade-off. Newly introduced naïve individuals were initially more likely to initiate exploration than experienced birds, but the pair soon settled into a pattern of alternating leadership with both birds contributing equally. Experimental pairs showed an oscillating pattern of exploration over generations that might facilitate the discovery of more efficient routes. Our results introduce a new perspective on the roles of leadership and information pooling in the context of collective learning.
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Author Response:
Reviewer #2 (Public Review):
Valentini et al. explore the contribution of inexperienced homing pigeons in a pair, while finding the most efficient route back home. My comments below mostly concern the need of broadening the scope of the introduction and discussion by discussing and citing literature beyond homing pigeons as at the moment the manuscript could be characterized as too specific for the readership.
We thank the reviewer for their suggestions which allowed us to expand the focus of our manuscript. Our answers to the reviewer’s comments are reported below together with modifications done on the revised manuscript.
The authors use and present transfer entropy methods which regard the transmission of information from one individual to the other and effect of this information on behaviour. I haven't used …
Author Response:
Reviewer #2 (Public Review):
Valentini et al. explore the contribution of inexperienced homing pigeons in a pair, while finding the most efficient route back home. My comments below mostly concern the need of broadening the scope of the introduction and discussion by discussing and citing literature beyond homing pigeons as at the moment the manuscript could be characterized as too specific for the readership.
We thank the reviewer for their suggestions which allowed us to expand the focus of our manuscript. Our answers to the reviewer’s comments are reported below together with modifications done on the revised manuscript.
The authors use and present transfer entropy methods which regard the transmission of information from one individual to the other and effect of this information on behaviour. I haven't used such methods myself, but I think the methodology is nicely explained and easy to follow as it's written here. However, I would still encourage the authors to avoid jargon and un-introduced terms while first presenting their methods and results in the introduction and results sections. I also think that the paragraph in the introduction (L92-104) that refers to transfer entropy (TE) has to be extended and also direct readers to reviews such as [1] that attempt to make TE accessible to a broad audience of non-physicists. Behavioural ecologists and primatologists that study leadership and influence in animals, using less data hungry methods than TE, will probably be interested in reading this manuscript. Because eLife is a journal that attracts a very broad audience I would suggest investing more on better introducing TE to biologist and anthropologists.
We thank the reviewer for their suggestions. In the revised version of our manuscript, we clarified the meaning of symbols and unintroduced terms and extended the introduction paragraph about transfer entropy to provide more information. We now discuss data requirements of information-theoretic approaches, point the reader towards recent literature reviews aimed at introducing these (and similar) approaches to the community of behavioural ecology, and better introduce the advantages of transfer entropy with respect to methods based on models of alignment, attraction, and repulsion.
“Leader–follower interactions of this sort can be accurately captured using information-theoretic measures that quantify causal relations in terms of predictive information (Butail, Mwaffo, and Porfiri 2016; Kim et al. 2018; Crosato et al. 2018; Ray et al. 2019; Valentini et al. 2020). This methodological approach, which generally requires large amounts of data (but see (Porfiri and Ruiz Marín 2020)), is gaining popularity among behavioural ecologists (Strandburg-Peshkin et al. 2018; Pilkiewicz et al. 2020) as tools for automatic monitoring and extraction of the necessary volumes of behavioural data become increasingly available (Egnor and Branson 2016). One of these measures, transfer entropy, quantifies information about the future behaviour of a focal individual that can be obtained exclusively from knowledge of the present behaviour of another subject (Schreiber 2000). Transfer entropy measures information transferred from the present of the sender to the future of the receiver (Lizier and Prokopenko 2010). It explicitly accounts for autocorrelations characteristic of individual birds’ trajectories (Mitchell et al. 2019) by discounting predictive information available from the sender’s present that is already included in the receiver’s past (see Figure 1). Furthermore, it does not require a model of how sender and receiver interact, and it is well suited to study social interactions both over space and time (Lizier, Prokopenko, and Zomaya 2008; Strandburg- Peshkin et al. 2018). This aspect of transfer entropy encompasses traditional methods to quantify collective movement that are based on modelling an individual’s behaviour as a combination of three motional tendencies (Couzin et al. 2002) – alignment of direction to nearby group members, attraction towards sufficiently distant members, and repulsion from sufficiently close members – that allow an individual to maintain proximity to the group. In this context, transfer entropy is advantageous as it can capture causal interactions due not only to alignment forces (Nagy et al. 2010) but also to attraction and repulsion forces that result in temporarily unaligned states (Pettit, Perna, et al. 2013).”
A thought I had while reviewing this work regards the theory of the wisdom of the crowd [2]. This indicates that when a group or a collective averages the different estimates of its members, they reach a more accurate collective estimate. Studies have also shown that animals can average their movement directions to resolve conflicts of interest [3,4]. The current manuscript also shows that pooling infomration leads to better movement decisions. Would it thus make sense for this manuscript to discuss how its findings may support the wisdom of the crowd theory?
We thank the reviewer for the suggestion. In the revised version of out manuscript, we included a new paragraph where we discuss a possible connection with the phenomenon of the wisdom of crowds as well as how our results might generalize to flocks of larger size.
“The ability of groups to outperform single individuals by pooling information across their members is an aspect of collective intelligence that has long intrigued researchers. One potential mechanism underlying this phenomenon, popularly known as the wisdom of crowds (Surowiecki 2005), is averaging many individuals’ estimates independent from each other. Averaging individual decisions is expected to provide a more accurate group estimate than any individuals’ guess. Previous studies have also shown that animals can average their movement decisions to reach a compromise (Biro et al. 2006; Strandburg-Peshkin et al. 2015). Although the mechanisms by which experienced and naïve individuals pool information during route development remain unknown, our study points to the importance of naïve group members within the information-pooling process. Moreover, the wisdom of crowds is known to require personal information to be independent among group members (Couzin 2018) otherwise group performance can degrade quickly for increasing group size (Kao and Couzin 2014). Experimental pairs could thus benefit from pooling information with naïve individuals that, at least at the beginning of each generation, likely provide a source of information independent from that of the experienced bird. The potentially deleterious effects of losing independence may provide another pressure to shift over time from innovative exploration to route6 preserving exploitation. It remains to be explored how our results generalize to larger flock sizes. Previous experiments without generational replacement showed that, even in larger flocks, birds flying ahead of the flock had a tendency to assume leadership positions (Nagy et al. 2010). However, the repeated introduction of naïve individuals into larger flocks might complicate the dichotomy between leaders and followers by inducing turnover dynamics between the front and the back of the flock.”
As briefly mentioned earlier, I think that the cited literature in this manuscript (especially in L58-138 and throughout the discussion) includes mostly studies on homing pigeons whereas relevant studies to the current manuscript have been performed on other species and by discussing and citing relevant studies on various species the manuscript would become more attractive to a broader audience and wouldn't read as homing-pigeon specific.
We thank the reviewer for pointing us towards additional literature related to our study. We included the suggestions from the reviewer as well as further references to a broader literature to expand the scope of our manuscript.
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Evaluation Summary:
This study in the field of collective behavior addresses how naïve and experienced individuals (i.e., homing pigeons) pool information in order to navigate while flying back home. The authors show that the passage of information is largely democratic, meaning information passes both ways, and that, unexpectedly, exploration of the route is initiated both by naïve and experienced birds. The work provides a new perspective on information sharing during collective learning.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
This paper tests the hypothesis that the transfer of information within a pair of birds flying to their home loft, where one is experienced and the other naive, occurs unidirectionally. The authors use information theoretic methods to analyze trajectory data from a previous study and find interesting results. First, that the passage of information is largely democratic, meaning information passes both ways, second, unexpectedly, that exploration of the route is initiated both by the naive and the experienced bird, and third, mostly in agreement with previous work, that the leading bird is mostly in front of the pair.
The results presented here contributes to large body of information-theoretic methods being applied toward better understanding of natural processes as well as improves our understanding of …
Reviewer #1 (Public Review):
This paper tests the hypothesis that the transfer of information within a pair of birds flying to their home loft, where one is experienced and the other naive, occurs unidirectionally. The authors use information theoretic methods to analyze trajectory data from a previous study and find interesting results. First, that the passage of information is largely democratic, meaning information passes both ways, second, unexpectedly, that exploration of the route is initiated both by the naive and the experienced bird, and third, mostly in agreement with previous work, that the leading bird is mostly in front of the pair.
The results presented here contributes to large body of information-theoretic methods being applied toward better understanding of natural processes as well as improves our understanding of social learning.
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Reviewer #2 (Public Review):
Valentini et al. explore the contribution of inexperienced homing pigeons in a pair, while finding the most efficient route back home. My comments below mostly concern the need of broadening the scope of the introduction and discussion by discussing and citing literature beyond homing pigeons as at the moment the manuscript could be characterized as too specific for the readership.
The authors use and present transfer entropy methods which regard the transmission of information from one individual to the other and effect of this information on behaviour. I haven't used such methods myself, but I think the methodology is nicely explained and easy to follow as it's written here. However, I would still encourage the authors to avoid jargon and un-introduced terms while first presenting their methods and results …
Reviewer #2 (Public Review):
Valentini et al. explore the contribution of inexperienced homing pigeons in a pair, while finding the most efficient route back home. My comments below mostly concern the need of broadening the scope of the introduction and discussion by discussing and citing literature beyond homing pigeons as at the moment the manuscript could be characterized as too specific for the readership.
The authors use and present transfer entropy methods which regard the transmission of information from one individual to the other and effect of this information on behaviour. I haven't used such methods myself, but I think the methodology is nicely explained and easy to follow as it's written here. However, I would still encourage the authors to avoid jargon and un-introduced terms while first presenting their methods and results in the introduction and results sections. I also think that the paragraph in the introduction (L92-104) that refers to transfer entropy (TE) has to be extended and also direct readers to reviews such as [1] that attempt to make TE accessible to a broad audience of non-physicists. Behavioural ecologists and primatologists that study leadership and influence in animals, using less data hungry methods than TE, will probably be interested in reading this manuscript. Because eLife is a journal that attracts a very broad audience I would suggest investing more on better introducing TE to biologist and anthropologists.
A thought I had while reviewing this work regards the theory of the wisdom of the crowd [2]. This indicates that when a group or a collective averages the different estimates of its members, they reach a more accurate collective estimate. Studies have also shown that animals can average their movement directions to resolve conflicts of interest [3,4]. The current manuscript also shows that pooling infomration leads to better movement decisions. Would it thus make sense for this manuscript to discuss how its findings may support the wisdom of the crowd theory?
As briefly mentioned earlier, I think that the cited literature in this manuscript (especially in L58-138 and throughout the discussion) includes mostly studies on homing pigeons whereas relevant studies to the current manuscript have been performed on other species and by discussing and citing relevant studies on various species the manuscript would become more attractive to a broader audience and wouldn't read as homing-pigeon specific.
References
1. Strandburg-Peshkin A, Papageorgiou D, Crofoot MC, Farine DR. Inferring influence and leadership in moving animal groups. Philos Trans R Soc B Biol Sci [Internet]. 2018;373:20170006. Available from: https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0006
2. Galton F. Vox populi (The wisdom of crowds). Nature. 1907;75:450-451.
3. Strandburg-Peshkin A, Farine DR, Couzin ID, Crofoot MC. Shared decision-making drives collective movement in wild baboons. Science (80- ) [Internet]. 2015;348:1358-61. Available from: https://www.sciencemag.org/lookup/doi/10.1126/science.aaa5099
4. Biro D, Sumpter DJT, Meade J, Guilford T. From Compromise to Leadership in Pigeon Homing. Curr Biol. 2006;16:2123-8.
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