Little evidence that Eurasian jays protect their caches by responding to cues about a conspecific’s desire and visual perspective
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Evaluation Summary:
This paper will be of interest across psychology and ecology. It attempts to replicate influential findings that imply Theory of Mind in food-caching decisions of Eurasian Jays. The authors' approach to both attempting to expand on and replicate earlier findings is both rigorous and thoroughly contextualized. The failure to reproduce earlier findings raises important questions for the field.
(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
Eurasian jays have been reported to protect their caches by responding to cues about either the visual perspective or current desire of an observing conspecific, similarly to other corvids. Here, we used established paradigms to test whether these birds can – like humans – integrate multiple cues about different mental states and perform an optimal response accordingly. Across five experiments, which also include replications of previous work, we found little evidence that our jays adjusted their caching behaviour in line with the visual perspective and current desire of another agent, neither by integrating these social cues nor by responding to only one type of cue independently. These results raise questions about the reliability of the previously reported effects and highlight several key issues affecting reliability in comparative cognition research.
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Author Response:
Reviewer #1:
This study set out to test whether Eurasian jays take into account the perspective and desire on an observing bird during food caching. The inclusion of multiple cues associated with different mental states is a novel and valuable approach to the field of comparative Theory of Mind and social cognition. The rigorous, elegant design over five experiments aims to pinpoint what mechanisms and cues the jays use when choosing where to cache what food and how much depending on the observer's perspective (caching location out of view or not) and current desire (being pre-fed on a single food type). The reader is guided through complex experimental procedures with clear descriptions of predictions and helpful figures. The manuscript is well written and stays on topic, while also expressing important concerns …
Author Response:
Reviewer #1:
This study set out to test whether Eurasian jays take into account the perspective and desire on an observing bird during food caching. The inclusion of multiple cues associated with different mental states is a novel and valuable approach to the field of comparative Theory of Mind and social cognition. The rigorous, elegant design over five experiments aims to pinpoint what mechanisms and cues the jays use when choosing where to cache what food and how much depending on the observer's perspective (caching location out of view or not) and current desire (being pre-fed on a single food type). The reader is guided through complex experimental procedures with clear descriptions of predictions and helpful figures. The manuscript is well written and stays on topic, while also expressing important concerns about the replicability and validity of studies in comparative cognition in general. The results go against many earlier papers by some of the authors, and it is commendable that they set out to replicate their own studies in the first place. This kind of critical assessment of earlier research and presentation of negative results (especially in a replication study of positive results) is certainly welcome after the concerns commonly expressed that this is not done sufficiently often. The results support the conclusion and no inflated interpretations are presented. Other caching corvids can be tested with this method after suitable adjustments, and the general design that includes both perspective and desire of observer has wider uses also in other taxa. The explanation that results did not replicate due to age or experience of the birds is compelling (as is the effect size argument) and would be an interesting avenue for future research if possible. Although it remains an open question why the results differ from those of earlier studies, and what mechanisms the jays employ when caching in the presence of a conspecific, this excellent study will hopefully set the example for many future studies that cover multiple lines of evidence across several experiments to critically examine the validity and replicability of the science of comparative cognition.
We are grateful to the reviewer for their feedback and share the hope that the present study might foster future research examining the robustness of published findings in the field of comparative cognition.
Reviewer #2:
In the present manuscript, Amodio and colleagues investigate whether or not Eurasian jays use cues correlated with the perspective and desires of a potential competitor to shape their caching behavior. The first two studies build on past research to test whether Eurasian jays can integrate cues regarding both the competitor's perspective and desires. The authors fail to find evidence that Eurasian jays integrate these cues to cache undesired food in unobservable locations. Thus, the authors attempt to replicate their own earlier findings showing that Eurasian jays' caching behavior is impacted by these cues when the competitor's perspective and satiety are manipulated in separate tasks. The authors fail to replicate these effects and conclude with a discussion of possible reasons for these failed replications and suggestions for increasing replicability in comparative psychology.
Strengths:
The logic of the experiments is very clear. Beginning with the two novel studies, the authors provide convincing justification for why cue integration is an interesting question to investigate in this species. Additionally, the initial null results for Studies 1 and 2 led logically to the replication attempts for the individual effects of competitor perceptual access and desire on caching behavior.
Notably, several of the authors on this manuscript are also authors on the studies that failed to replicate here. These authors were thus able to discuss the nuances of the past and present experiments in great detail and offer a well-reasoned perspective on why these replication attempts may have failed. This combined with their broader discussion of the importance of replication in comparative psychology make the manuscript even more impactful contribution to the literature.
We appreciate the accurate summary and the positive evaluation of our study.
Weaknesses:
The authors find null results across the board on all five studies, yet they do not have a section of the discussion that explores the implications of what it would mean for Eurasian jay cognition. Do the current findings mean that jays cannot, in fact, track the perspectives and desires of conspecifics? Should the current findings prompt a replication attempt of the desire tracking of mates from Ostojic et al., 2014? What other cues might affect this behavior? Etc.). Obviously, the absence of evidence does not mean evidence of absence but the authors should provide a thorough discussion of the possibility that these replication attempts may not simply be "local failures." Given the preponderance of null results (and the fact that these result could be the first null results on this topic published in a high-impact journal), the authors should at least briefly discuss what it would mean for the avian cognition if these replication failures are not just isolated cases but instead indicative of a broader pattern in bird perspective taking capacities.
We appreciate the concern of the reviewer and have edited and extended the discussion accordingly. In particular, we now clearly specify what we believe our findings mean (and what they do not mean) with regard to the capability of Eurasian jays to respond to the perspective and desires of conspecifics in the caching context (see lines 676-693 of the revised manuscript). Furthermore, we briefly discuss the reliability of the evidence about desire attribution in the food- sharing context in Eurasian jays (see lines 693-702 of the revised manuscript). Finally, we also explore the scenario in which our negative findings would turn out to be indicative of a broader pattern in the field of corvid social cognition (see lines 669-676 and 733-742 of the revised manuscript). In regard to this last point, we are cautious when it comes to generalising from our local failures to more general claims about corvids’ social cognitive abilities, and we explain and discuss the reasons for this caution in the text.
In the authors' discussion of why these replications may be inconsistent with the rest of the literature on this topic, they cite the subjects' age and life experience as reasons why they may have failed on these replication attempts. However, these suggestions feel under-explored and therefore tenuous. The authors should provide more context for this claim. For example, are there any empirical or anecdotal data supporting the proposal that older Eurasian jays are less motivated to guard their caches (or are there any related social changes experienced by older Eurasian jays)? Similarly, to what extent does the experience of living in the aviary reflect or diverge from the caching and pilfering experiences of wild Eurasian jays? For example, do birds in the aviary frequently cache and pilfer even though they receive a maintenance diet? (Given the role of experience in scrub jay caching behavior suggested by Emery & Clayton, 2001 additional context here would be informative).
We thank the reviewer for encouragement to further address these points. We have expanded our discussion about the possibility that the inconsistencies between our findings and those reported by Legg and Clayton (2014) and Ostojic et al. (2017), might have resulted from age- related processes or prior experience and learning (see lines 605-641 of the revised manuscript). We bolstered this discussion by referencing relevant data in corvids (where available) and in other taxa, to provide more context and support for both potential explanations. In addition, we included further details about the caching behaviour exhibited by the Eurasian jays in our lab (see lines 632-638 of the revised manuscript). We believe these additions have strengthened this component of our discussion.
Impact:
This work is a well-thought-out series of studies that performs the valuable function of attempting to replicate previously well-cited findings within the field of comparative cognition. Unfortunately, these findings are null results, but given the uniqueness of this captive population of Eurasian jays, the publication of these findings is of critical importance to our understanding of this phenomenon. Additionally, the format of the paper (two new studies, followed by replications) serves as a nice example for how replication attempts can be integrated into novel investigations of comparative cognition.
We are grateful to the reviewer for their positive assessment of the impact of our study.
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Evaluation Summary:
This paper will be of interest across psychology and ecology. It attempts to replicate influential findings that imply Theory of Mind in food-caching decisions of Eurasian Jays. The authors' approach to both attempting to expand on and replicate earlier findings is both rigorous and thoroughly contextualized. The failure to reproduce earlier findings raises important questions for the field.
(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 study set out to test whether Eurasian jays take into account the perspective and desire on an observing bird during food caching. The inclusion of multiple cues associated with different mental states is a novel and valuable approach to the field of comparative Theory of Mind and social cognition. The rigorous, elegant design over five experiments aims to pinpoint what mechanisms and cues the jays use when choosing where to cache what food and how much depending on the observer's perspective (caching location out of view or not) and current desire (being pre-fed on a single food type). The reader is guided through complex experimental procedures with clear descriptions of predictions and helpful figures. The manuscript is well written and stays on topic, while also expressing important concerns about …
Reviewer #1 (Public Review):
This study set out to test whether Eurasian jays take into account the perspective and desire on an observing bird during food caching. The inclusion of multiple cues associated with different mental states is a novel and valuable approach to the field of comparative Theory of Mind and social cognition. The rigorous, elegant design over five experiments aims to pinpoint what mechanisms and cues the jays use when choosing where to cache what food and how much depending on the observer's perspective (caching location out of view or not) and current desire (being pre-fed on a single food type). The reader is guided through complex experimental procedures with clear descriptions of predictions and helpful figures. The manuscript is well written and stays on topic, while also expressing important concerns about the replicability and validity of studies in comparative cognition in general. The results go against many earlier papers by some of the authors, and it is commendable that they set out to replicate their own studies in the first place. This kind of critical assessment of earlier research and presentation of negative results (especially in a replication study of positive results) is certainly welcome after the concerns commonly expressed that this is not done sufficiently often. The results support the conclusion and no inflated interpretations are presented. Other caching corvids can be tested with this method after suitable adjustments, and the general design that includes both perspective and desire of observer has wider uses also in other taxa. The explanation that results did not replicate due to age or experience of the birds is compelling (as is the effect size argument) and would be an interesting avenue for future research if possible. Although it remains an open question why the results differ from those of earlier studies, and what mechanisms the jays employ when caching in the presence of a conspecific, this excellent study will hopefully set the example for many future studies that cover multiple lines of evidence across several experiments to critically examine the validity and replicability of the science of comparative cognition.
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Reviewer #2 (Public Review):
In the present manuscript, Amodio and colleagues investigate whether or not Eurasian jays use cues correlated with the perspective and desires of a potential competitor to shape their caching behavior. The first two studies build on past research to test whether Eurasian jays can integrate cues regarding both the competitor's perspective and desires. The authors fail to find evidence that Eurasian jays integrate these cues to cache undesired food in unobservable locations. Thus, the authors attempt to replicate their own earlier findings showing that Eurasian jays' caching behavior is impacted by these cues when the competitor's perspective and satiety are manipulated in separate tasks. The authors fail to replicate these effects and conclude with a discussion of possible reasons for these failed …
Reviewer #2 (Public Review):
In the present manuscript, Amodio and colleagues investigate whether or not Eurasian jays use cues correlated with the perspective and desires of a potential competitor to shape their caching behavior. The first two studies build on past research to test whether Eurasian jays can integrate cues regarding both the competitor's perspective and desires. The authors fail to find evidence that Eurasian jays integrate these cues to cache undesired food in unobservable locations. Thus, the authors attempt to replicate their own earlier findings showing that Eurasian jays' caching behavior is impacted by these cues when the competitor's perspective and satiety are manipulated in separate tasks. The authors fail to replicate these effects and conclude with a discussion of possible reasons for these failed replications and suggestions for increasing replicability in comparative psychology.
Strengths:
The logic of the experiments is very clear. Beginning with the two novel studies, the authors provide convincing justification for why cue integration is an interesting question to investigate in this species. Additionally, the initial null results for Studies 1 and 2 led logically to the replication attempts for the individual effects of competitor perceptual access and desire on caching behavior.
Notably, several of the authors on this manuscript are also authors on the studies that failed to replicate here. These authors were thus able to discuss the nuances of the past and present experiments in great detail and offer a well-reasoned perspective on why these replication attempts may have failed. This combined with their broader discussion of the importance of replication in comparative psychology make the manuscript even more impactful contribution to the literature.
Weaknesses:
The authors find null results across the board on all five studies, yet they do not have a section of the discussion that explores the implications of what it would mean for Eurasian jay cognition. Do the current findings mean that jays cannot, in fact, track the perspectives and desires of conspecifics? Should the current findings prompt a replication attempt of the desire tracking of mates from Ostojic et al., 2014? What other cues might affect this behavior? Etc.). Obviously, the absence of evidence does not mean evidence of absence but the authors should provide a thorough discussion of the possibility that these replication attempts may not simply be "local failures." Given the preponderance of null results (and the fact that these result could be the first null results on this topic published in a high-impact journal), the authors should at least briefly discuss what it would mean for the avian cognition if these replication failures are not just isolated cases but instead indicative of a broader pattern in bird perspective taking capacities.
In the authors' discussion of why these replications may be inconsistent with the rest of the literature on this topic, they cite the subjects' age and life experience as reasons why they may have failed on these replication attempts. However, these suggestions feel under-explored and therefore tenuous. The authors should provide more context for this claim. For example, are there any empirical or anecdotal data supporting the proposal that older Eurasian jays are less motivated to guard their caches (or are there any related social changes experienced by older Eurasian jays)? Similarly, to what extent does the experience of living in the aviary reflect or diverge from the caching and pilfering experiences of wild Eurasian jays? For example, do birds in the aviary frequently cache and pilfer even though they receive a maintenance diet? (Given the role of experience in scrub jay caching behavior suggested by Emery & Clayton, 2001 additional context here would be informative).
Impact:
This work is a well-thought-out series of studies that performs the valuable function of attempting to replicate previously well-cited findings within the field of comparative cognition. Unfortunately, these findings are null results, but given the uniqueness of this captive population of Eurasian jays, the publication of these findings is of critical importance to our understanding of this phenomenon. Additionally, the format of the paper (two new studies, followed by replications) serves as a nice example for how replication attempts can be integrated into novel investigations of comparative cognition.
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