Journal

Behaviour

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Behaviour is interested in all aspects of animal (including human) behaviour, from ecology and physiology to learning, cognition, and neuroscience. Evolutionary approaches, which concern themselves with the advantages of behaviour or capacities for the organism and its reproduction, receive much attention both at a theoretical level and as it relates to specific behavior.

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Behavioral Neuroscience
Animal Science and Zoology
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  • Dear Claudia, You present an excellent example of how one can combine the often plethora of existing social behavior data with cognitive performance on an array of tests in a way that can shed light on current theory in need of such connections. The social intelligence hypothesis is desperately in need of such connections and your study provides a good step toward understanding its significance. It is extremely rare, yet very important, that all of the data (in this paper and the others for tasks A-D) are collected from the same individuals, therefore the small sample size is justified. Your conclusion that, while you do not provide causal evidence, but rather correlational evidence that cognitive performance relates to an increased involvement in social behaviors is a good distinction to make and will aid future work in developing experiments to test such causal relationships.

    I have only minor comments: Line 56 - give an example of “striking cognitive features” so we have some context.

    Line 62 - might want to also cite Jolly 1966 since she came up with the general idea of social intelligence first (http://www.sciencemag.org/content/153/3735/501.short)

    Lines 80-81 - have a look at Healy & Rowe 2007 (http://rspb.royalsocietypublishing.org/content/274/1609/453.short) and Holekamp 2007 (http://www.sciencedirect.com/science/article/pii/S1364661306003263) to see if you want to cite these here as well. Particularly check the future directions at the end of the Holekamp paper.

    Lines 81-83 - check out Thornton et al 2014 (http://beheco.oxfordjournals.org/content/early/2014/06/02/beheco.aru095.short) as I think you may want to cite it here.

    Lines 83-84 - give an example.

    Line 91 - there is no evidence yet that post-conflict affiliation is cognitively complex because alternative hypotheses have not been ruled out (i.e., bystanders initiating affiliation with victims occurs in species with large and small brain sizes and there is no direct evidence that it involves empathy). A stronger example here would be of the Eurasian jay males attending to their mate’s food preferences, recently published by Ostojic et al. 2013 (http://www.pnas.org/content/110/10/4123.short) and 2014 (http://rsbl.royalsocietypublishing.org/content/10/3/20140042.short).

    Lines 92 and 93 - it is a bit confusing to say “recent” studies and in the next sentence “previously”. Clarification is needed.

    Paragraph starting on line 116 - excellent interpretation. I would add more of this kind of language when explaining your results in the abstract because it will make more sense to the reader that hasn’t read your paper yet.

    Line 136 - hatched, not born.

    I’m a bit confused: do lines 137-140 refer to the time when the social behavior data were collected for this study and lines 140-143 refer to the time when the data were collected for the previously published papers on tasks A-D? If so, clarify.

    Lines 148-149 - how does access to food depend on the number of cache sites? Clarify.

    Lines 155-158 - move this part to earlier in this paragraph because it is distracting when placed after describing individuals going into testing rooms.

    Line 175 - by separated, do you mean isolated?

    Lines 178-184 - I’m not clear about which hand is which and which reward the term “reward” refers to. Distinguish between the exchange item and final reward by giving them different names that go with the different hands.

    Line 201 - by “current study” do you mean Wascher et al (2012a) or the one in review? Clarify.

    Line 228 - explain “pseudo-randomized order”.

    Place the “Data and statistical analysis” section either before Tasks A-D or place “Behavioral protocol data” and “General testing procedure” after Tasks A-D to separate what you did in this study vs previously published research, otherwise I have a hard time keeping track of what goes with what.

    Line 244 - explain what “this pattern” means.

    Line 260 - how are you interpreting what approach means in the context of this study? One can approach another to engage in aggression or affiliation, but in and of itself, what is the significance of the approach? Explain this a bit more earlier.

    Results: I have a hard time keeping track of what task goes with which task letter (A-D) so it would be good to mark which letter the task is in each sentence where you refer to a particular task. What does “respond stronger” mean in the inequity condition and heterospecific recognition experiments? Explain this with more description in the sentences in the results and discussion where you mention it. Also, remind the reader throughout the ms that tail and wing quivering are stress behaviors - I don’t think you directly make this link.

    Line 357 - what are “association values”?

    Line 360 - maybe add the Ostojic et al citations.

    Lines 372-376 - does higher involvement in aggressive interactions also explain the “less impulsive” individuals’ increase in stress behaviors? If so, make the link between these two sentences clearer and explain what less impulsive means and that tail quivering is a stress behavior. Also define which exchange experiment you are referring to on line 375.

    Lines 385-394 - are you saying that to measure optimality, one would need to do this study on relationships that are just forming rather than already established? If so, it isn’t entirely clear so make this part stronger.

    Paragraph starting on line 401 - needs a topic sentence introducing the broader nature of this paragraph. Otherwise it is not clear how it relates to the rest of the discussion.

    Figures: why did you choose to present just those two figures rather than all of the figures for initiating/receiving for each Task (A-D) with affiliative/aggressive/approach? I think all of the figures would be too much, but it isn’t clear why just these were chosen. You could make box plots with the initiated and received frequencies on the same graph but in different colors for comparison. Also, the figure legends say “y-axis”, but I think you mean “x-axis”.

    In Figure 1, do the numbers on the x-axis go with each bird? If so, then I would make that clear. Also, “number of trials choosing the larger quantity” out of how many total trials?

    One last note, the English needs to be cleaned up so if the copy editor doesn’t do this, have a native English speaker go through it for you.

    All my best, Corina Logan

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  • The authors present a thorough descriptive study of personality and contextual plasticity in Nazca boobies for two personality traits measured with three different types of tests. The MS is well-structured and is thus easy to follow; it is well-written; it uses sophisticated statistics to answer a series of basic questions about the structure of behavioural traits; it provides clear rationales for the procedures/methods/approaches used; and the samples sizes, number of repeats and contexts are impressive for a study of a large, wild vertebrate. I have a couple (or so) of questions about the data analysis and some minor comments for clarification/conciseness below that.

    First, LL 397-402: I don't understand the motivation for discarding individuals that occasionally did not perform a particular behaviour. Surely this results in a completely biased sample for which the intercept-slope correlations are based on? What happens if those low-performing individuals are kept in the analyses? Second, was the baseline behaviour analysed (mentioned at LL 166, 176, 189, 196); it seems that it was disregarded in the analyses yet it could be quite important to analyse in terms of 'controls' etc. Third, there are no clear predictions, though they can be guessed from other text in the Introduction. This is really a matter of opinion, but I find it easier to come to grips with the purpose of a study when predictions/aims/hypotheses are clearly stated at some point (though I would like to point out that I found the numbered structure for Qs nice and easy to follow).

    Minor comments: Overall: 'personality syndrome' doesn't seem to be used consistently throughout the MS (e.g. L 16 cf 102) and it is a rather strange 'mix' of two terms ("personality" and "behavioural syndrome" are rather more frequently used). L 9: "temporal consistency repeatability" seems tautological i.e. temporal consistency is repeatability (again, a strange mix of two terms)? LL 10 - 14: This sentence is too long and difficult to follow. I would also avoid introducing the theory of 'individual quality' after saying there is support for it. LL 17-18: This sentence largely repeats/negates the previous one. Simplify and clarify. L 50: The sentence ending here requires a reference. LL 67 & 82: I'm fairly certain the Gosling hyena study was on captive hyenas, not wild ones as indicated by the citation here. LL 92-96: This sentence lists a number of traits about seabirds without explaining why they are actually good for personality studies. Please elaborate. L 101: Introduce the notation for Qs 1 a and 1 b here (not just in the Methods). LL 165, 178… etc. throughout: there should be a space between numbers and units, I think. LL 169-173: This section is probably not necessary. L 293: I don't think this is uninformative, just difficult to analyse. LL 248-252, 257-263: I feel a lot of this information is not necessary. Just define what is meant by 'gardening behaviour' and 'shaking behaviour' and move on. Similarly for the multiple explanations of why gardening and shaking should be considered anxiety-related displacement behaviours. There is no real need to go into this twice in two different paragraphs; it just adds to the length of the MS without adding too much to what the reader needs. I would suggest making this section more concise and focussing on why the authors think these behaviours are representative of anxiety in the tested contexts than on what else the behaviours could mean in other (unrecorded) contexts. LL 333-351: Be more concise. I just wanted to know what SEM does in one-two sentences with a reference (Dingemanse's, perhaps). I'm certainly not bothered that you did not use factor analysis; I think this is more common in psychology than behavioural ecology and I felt the justification was lengthy and confusing. L 589: Why do the authors propose this hypothesis? Please provide a reference. Also, shouldn't the baseline behavioural recordings provide some idea of birds' activity levels that can be controlled for in the analyses? LL 643-645: But the low-responding individuals were removed from these analyses, were they not? This seems rather spurious as the authors are non-randomly disregarding a large proportion of the population and then suggesting that the results apply to the whole population. Please consider reanalysing these data. I don't think it's a problem is there's no elevation-slope correlation after reanalysis. I have found similar results in my own studies of wild animals and I think it's just as interesting to know when these correlations do not occur (also see Nussey et al.'s JEB review on random regressions for alternative interpretations of these intercept-slope relationships).

    Thank you for asking me to review this MS. I hope the authors find the comments helpful. Alecia Carter (Please note I sign all my reviews.)

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  • General comments:

    Many paired Mann-Whitney and Wilcoxon tests were conducted, but no alpha correction, such as the Bonferroni correction, was applied to account for the higher likelihood of obtaining a false positive result with so many tests. Applying an alpha correction to this many pair-wise tests would likely greatly reduce the p value at which results would be significant. Alternatively, a General Linear Model (GLM) could be applied to the whole dataset to determine which factors were similar/different and in which direction. A GLM would eliminate the need to apply an alpha correction. Likely, 2 GLMs would need to be used: one with duration as the response variable (against the explanatory variables) and another with frequency as the response variable (against the same explanatory variables).

    Detailed comments: line 58 - explain more what you mean about how “incorrect decision making” is a cost

    line 62 - explain what the “focal” and “model” individuals are

    line 64 - what do you mean by “an individual’s quality”? Be a bit more specific

    line 67 - when you say “partner” do you mean mate or any kind of relationship? Would be good to clarify.

    line 72 - explain more why social organization can influence attention patterns and how, especially since this is the topic of the next sentence, which is the focus of your study.

    line 75 - “highly complex social system with a flexible social organization” social system and social organization are the same thing so condense the sentence to “highly complex and flexible social system”

    line 90 - define “corvid” on first use

    lines 92-93 - note that rooks and ravens only form non-mate alliances when they are juveniles (rooks) or subadults (ravens). As adults, both species only ally with their mate.

    line 107 - wouldn’t you predict that the crows would pay more attention to models with which they share a valuable relationship rather than models they don’t have a valuable relationship with?

    line 113-114 - why would crows value social info from unknown individuals over familiar individuals? Need to back up a step and fill us in on the logic that brought you here. Familiar individuals likely provide more reliable info while unfamiliar individuals provide information of uncertain reliability, therefore there could be the opposite prediction that crows will pay more attention to social information from familiar individuals.

    line 117 - so you are saying that kin relationships are more strongly bonded than non-kin familiar relationships? I would make this clear, that way your prediction is more apparent.

    lines 118-125 - individuals can use social information to learn about social information or non-social information (i.e., where food is located, what food is good to eat, what food should be avoided, etc.). In the case of gathering non-social information, I could see a further prediction about females: that they will attend more to male models in a foraging context. Foraging information is information females might eventually use. As well, females might need information about social relationships so they know who to avoid (though I guess this is less important if all males are dominant to them because then they know to just avoid males).

    line 123-124 - “male model stimuli should be of larger interest for the crows than females”, shouldn’t this be “male model stimuli should be of larger interest for the MALES than females”?

    line 125 - “with crows paying more attention to individuals they are affiliated with.” When you refer to “crows”, do you mean males or males and females? I would be explicit about this since you are discussing sex differences in this paragraph.

    line 126-128 - do you expect social facilitation regarding the model (model is performing a behavior, which draws the attention of the subject. More models performing the behavior at one time will increase the chance of the subject engaging in that behavior later) or the observers (the more observers watching a model increases the chance that non-observers will become observers)?

    Ethics statement - grammar needs to be cleaned up. Is there a permit number that should go here?

    Study subjects - make it clear which were the birds that were captured in the wild and returned to the wild. I assume the flock and the cooperatively breeding families were all captive birds and the wild birds are the birds you talk about in the next section. I would put the wild birds in the Study Subjects section so this is clear. Was the flock hand raised?

    lines 185-187 - why did unfamiliar birds have twice the amount of sessions as familiar birds? Also, why were the unfamiliar bird sessions treated differently from the familiar bird sessions in terms of the amount of time between presentation (3 days between)

    line 188 - recorded using what kind of camera?

    lines 190-198 - I am confused about the experimental cage and the test compartment set up. I’m not clear about when you are talking about the experimental cage inside the test compartment or the test compartment itself because you also talk about an experimental compartment and an experimental room - be consistent with your terminology. I also don’t understand where the holes are and which birds can see what when looking through them. I guess the birds in the test compartment can see stimulus bird (and vice versa) through the holes in the experimental cage? Could you provide a figure or a picture of the set up and label it? Is the stimulus bird and the model bird the same thing? If so, just use the term model bird. Also, who was in the test compartment observing the stimulus bird: just one bird at a time or multiple individuals? If multiple individuals, were groups delineated by the flock and the two families? If a flock was used as an observer group, who was their familiar model? An individual from within the flock? Same questions for the family groups.

    lines 235-239 - you did this analysis only when the model bird was familiar and not when the model bird was unfamiliar? Why not treat familiar and unfamiliar analyses the same and see if there are differences in the results? Also, if the model bird could only interact with the observer birds by means of two 2cm holes in the wall, how much behavior could occur between them? Was the nearest neighbor measure just applied to observer birds or could the nearest neighbor be the model bird? And was the nearest neighbor calculated for the model bird as well?

    line 241 - how many hours we recorded in total (so we know what percent 5h20m is of the total)?

    lines 248-249 - were the non-breeders the young flocks? If so, then they could be searching for mates and preparing to pair, in which case the model bird could be a potential mate, which would warrant the difference found in the results.

    line 256 - I assume the unit of measurement for the numbers after the sessions are seconds under the duration category and in the frequency category are looks per session? It would be good to clarify this.

    line 280 - watching duration is not significant (p=0.078), therefore do not include it in the sentence that describes significant differences between kin and non-kin.

    lines 282-283 - does the median+/-SE frequency and duration data refer to the non-kin or kin data? Both sets should be shown.

    lines 285-286 - how can you be sure the increase in watching duration and frequency is not just due to the fact that more individuals are watching in a session, therefore increasing the total duration and frequency?

    lines 291-292 - show the statistics

    lines 298-301 - my question about why you chose this prediction still applies (see my comment above for lines 113-114)

    lines 301-303 - Given that there were no significant differences between familiar and unfamiliar individuals, it is unknown what information is gained by observer birds in this situation and whether it is important or not.

    line 315 - you are referring to the unfamiliar birds here, not just the non-kin, correct? Also, they observed more frequently, but not longer since your duration result was not significant.

    line 318 - again, not just non-kin, but unfamiliar individuals

    Sincerely, Corina Logan

    RE-REVIEW Dear editor and authors, The authors carried out excellent revisions: the paper is now clear and adds to the literature on corvids, social interactions, and attention. I only have a few minor comments, listed below.

    All my best, Corina Logan

    line 58 “constraints” line 61 “to whom and what they attend to” line 71 extra parentheses line 72 “decisions”

    lines 75-77 make it clear whether carrion crows are more egalitarian or despotic in the next section so it ties back to this addition in the introduction

    line 95 “but especially juveniles form short- to long-term” line 110 “minute” line 122 “or b)” line 136 “than female models, due to males exploratory” line 139 “sessions when more individuals in the group are watching the model” line 151 “remained in captivity before and” line 232 “individuals”

    lines 239-242 you used these interactions in what way? To calculate dominance hierarchies or quantify affiliative partners? If so, say how.

    line 252 “factors”

    lines 259-272 you could do separate GLMMs just on the subset of your data including the familiar birds to eliminate the Spearman’s tests.

    line 283 MW means Mann Whitney? Spell it out the first time for clarity. lines 300-301 flock individuals? I think this sentence is missing some words. line 306 GLMM

    lines 380-381 describe the social organization and foraging ecology in the next sentences for each species you discuss to show how these factors may play a role in attention patterns.

    line 389 delete “consisting” line 391 “where” line 426 “where”

    lines 634-635 x- and y-axis descriptions are reversed Figure 2: are these averages per bird? It looks like they are because the x-axis refers to the session number and each bird would have experienced multiple models. Were sessions 1 and 2 always with familiar individuals and 3 and 4 always with unfamiliar? It would be good to note this on the x-axis if it is true.

    Figure 3: watching frequency per minute of observation per bird?

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