Peer review of: Juvenile cleaner fish can socially learn the consequences of cheating (2020)

Reviewers' Comments: 
 
Reviewer #1: 
Remarks to the Author: 
This paper shows that juvenile cleaner fish can learn about the consequences of interacting with 
particular clients by moderating their own behaviour to prolong a cooperative interactions. 
Interestingly, the young fish did not pay any attention to arbitrary client preferences (here based on 
colour). 
 
The fact that fish can learn socially has been known for a very long time (see reviews by Brown and 
Laland), but here the experiments provide some rather interesting information on what the observer 
fish are learning having observed adults interact with clients that respond in various ways. The 
cooperation context is certainly novel. 
 
It may well be the case that social learning is particularly important in these complex social 
interactions, wherein relying solely on individual learning may significantly reduce the probability on 
discovering the optimal social strategy. Perhaps more could be said about this in the discussion. 
 
Given the widespread use of social learning in anti-predator contexts, where individuals rapidly learn 
the negative consequences of predation (punishment), the results of this experiment are perhaps less 
surprising, if not somewhat expected. Again this may be worth mentioning in the discussion. 
 
Overall the paper is very well presented, the stats are appropriate and the results reasonably easy to 
follow. 
 
Specific comments: 
L48: delete “as” 
L90: briefly say that younger observers were more inclined to adjust their preference. 
L150: missing a full-stop at the end of the sentence 
L213: insert a space before the reference 
L346: replace “are” with “were” 
 
 
 
Reviewer #2: 
Remarks to the Author: 
 
This paper reports a series of interesting findings on how cleaner fish can learn by observational 
conditioning what type of response to expect from aribtrarily marked plates, intended to represent 
simulated cleaner clients. I find the results overall convincing although I have a number of substantive 
questions about the statistical analysis, which seems oddly convoluted given that with a designed 
experiment like this it should have been possible (and desirable) to specify and use a single model 
incorporating the logic of the experimental design to specify the effects of interest and any additional 
confounds resulting from the design. I also think that the authors have been somewhat uncritical in 
directly comparing their results using simulated plates with results from humans in actually-interacting 
experimental settings. I can buy that cleaners can learn by observational conditioning the properties 
and behaviour of specific objects in their environment, but I am not so convinced this can be directly 
translated into the natural setting - to illustrate this, imagine the counter-factual experiment on 
humans where instead of other humans the subjects observed interactions with objects - would we 
really be happy describing this as learning about 'reputation' as opposed to learning about the 
properties of objects in the environment? 

 
Specific comments: 
 
L22-24 'They further show that negative responses to cheating can shape the reputation of cheated 
individuals' - the 'show' in the abstract here is not consistent with the 'plausible' when this is 
addressed in the discussion L165: 'It is hence plausible that real clients, as at least equally salient 
interaction partners, gain reputation' - this is unfortunate, and the abstract should be revised. 
 
There are a number of grammatical errors that should be corrected e.g. L47 (and elsewhere) 'which 
constitutes as cheating' L194 'clients where represented by' L345 tense agreement L359 redundant 
comma 
 
L86 It would be preferably to present the complete model summary in a table I feel so that the reader 
can see all parameters estimated and not jsut the reported ones - ideally this should also include the 
full (global) model (see below). 
 
L105 'he effect of observation was significant, although diminishing' - I don't understand the 
'diminishing' part here? 
 
L191-193 direct repeat 
 
L195-196 - 'flakes' contain prawn also? 
 
I got confused over '% flake concentration' vs number of flake patches presented perhaps this can be 
clarified 
 
L272 "Plates' reaction rules in these tests matched the rules they followed during training, and in each 
test trial..." - can the authors be confident, and thus assert, that in assigning plate patterns to specific 
behaviour patterns they were not inadvertently matching reaction styles to patterns and/or colours 
that might be expected to have specific ecological relevance and therefore provoke innate responses 
(e.g. for example the colour red can do this in some species?) 
 
L293 in the control condition what was the cue from the demonstrator that initiated plate 'behaviour', 
and how could the chasing punishment be demonstrated when there was a transparent barrier 
between the plate and fish? 
 
L344 'The significance of dropped predictors was obtained by adding them to this minimal model.' - I 
am confused about why this was done? The authors should note that inferential tests following data 
dependent model selection are unlikely to be valid (see e.g. Heinze et al 2018 doi: 
10.1002/bimj.201700067). It's unclear to me why any model selection was needed at all, given that 
the experiment design was known a priori it should be possible to specify a model in advance and the 
most appropriate one would appear prima facie to be the full (global) one.. In any case, it would be 
good practise for the authors to report these global models, at least in the SI. Finally, it is important if 
AICc is being used that the deltaAICcs are reported between the 'best' and other models - if there is 
model selection uncertainty (i.e. delta < 2), then the authors need to report this and account for it... 
 
L350-351 - " we centred the cleaners' initial preference for prawn according to the cohort in which 
they participated" - this is not well justified for me - I can understand centering on each individuals 
initial preference so that preference at test is presented relative to preference pre-demonstration,but 
it is unclear why the behaviour of different fish that have never interacted with the focal should have 
any impact on the representation of the focal fish's behaviour - if the authors suspect cohort specific 

effects then isn't it most appropriate to model these explicitly using a multi-level approach (as for 
example in experiment 2)? 
 
L351 - averaged across what? Why should this be an average, and not an explicit model of the 
individual responses? 
 
L355 - "The non-linearity" - what non-linearity? I can't find any other mention of this? 
 
L360 'we fitted a linear model between' - please specify which are the dependent and independent 
variables here. Also justify why this needs to be a seperate model rather than including the 
demonstrator consumption in the global model? 
 
L376 'The statistical significance of cleaners' preferences was obtained from simpler versions of these 
models, taking only the treatment groups into account' - I cannot understand how this can be correct 
- such models will ignore any confounding effects of the various other predictors used in the global 
model - surely the appropriate statistical test is from the full (global) model? 
 
L381 justify choice of quasibinomial model here. 
 
L386-388 - there is an inconsistency here with the model selection approach outlined earlier - why is it 
relevant that nothing was significant in the full model? 
 
Fig 2/3 it would be very helpful for rapid comprehension to have a visual legend on these figure. I 
would also like to see the individual data points added to these figures to understand just how much 
the outlier in the cohort 1 observer treatment is driving the 'average' response. 
 
Fig 3 does the different shading indicate anything additional over what is already indicated by the 
group labels - if not, it is redundant and potentially confusing. 
 
Fig 4 caption not always grammatical 
 
SI "However, as it seemed to us that for some of the cleaners, this concentration was very strong..." 
 
The following is unclear to me: "To make sure that our treatment groups would not differ in their 
initial preference, within each cohort, we ranked the 
cleaners' preferences, split them into pairs based on these ranks, and randomly allocated the two 
cleaners in each pair to the two different treatments" 
 
What were the demonstrator training performance criteria? " Demonstrators that showed weak 
preferences at the end of training (non-significant according to a two-tailed Wilcoxon test), would 
receive additional training trials. " 
 
 
 
Reviewer #3: 
Remarks to the Author: 
This is a very interesting paper building on a sound body of prior work with cooperation in cleaner fish. 
The investigation of social learning’s role in cooperative interactions is long over due in animals and 
the paper will be of interest to many researchers. Detailed comments below, but my main comments 
are that: 
(1) In places, the literature referred to in the Introduction and used in the Discussion needs 

broadening. 
(2) The Results section is often not sufficiently explanatory of the methods for the reader to 
understand and interpret the validity of the results reported. 
(3) There is no consideration that repeated test trials allowed individual learning (that coincided with 
the social information) for some of the observer fish. Statistics reporting the results of the first test 
trials (after observation/non-observation phase) are required. 
(4) The findings may be a little underplayed 
a) it is unusual in the social learning literature to find an example of social learning NOT to perform a 
behaviour pattern. 
b) more could be made of the finding that the fish only socially learned behaviours that had tangible 
outcomes (although this statement would need validation with other basic arbitrary preference tests) 
(5) The Discussion does not really discuss any finer nuances of the study. For example, what is the 
ecological validity of the various experiments and do the experiments leave any unanswered questions 
or require replication? etc. 
Rachel Kendal & PhD student 
 
Detailed comments 
Abstract 
Line 15 – if you just mean ‘unlearned’ use that instead of ‘instinct’ as the latter has many 
interpretations. 
Line 19: socially learning not to perform a behaviour is something not reported often, more could be 
made of this 
Introduction 
Line 33 – Also see Richerson et, al., (2016) “Cultural group selection plays an essential role in 
explaining human cooperation: A sketch of the evidence” for a further review into this topic. 
Line 35 – Consider rephrasing this statement as it is not fully clear at first glance which “phenomena” 
are being referred to. 
Line 40 – May be worth briefly mentioning social learning strategies and the individual differences / 
cultural variation present in social learning (specifically for social dilemmas). For example: 
Molleman, L., Van den Berg, P., & Weissing, F. J. (2014). Consistent individual differences in human 
social learning strategies. Nature Communications, 5, 3570. 
Molleman, L., & Gächter, S. (2018). Societal background influences social learning in cooperative 
decision making. Evolution and Human Behavior, 39(5), 547-555. 
Lamba, S. (2014). Social learning in cooperative dilemmas. Proceedings of the Royal Society B: 
Biological Sciences, 281(1787), 20140417. 
Replace the term ‘conveyed’ with ‘used’. 
Line 42 – For clarity, perhaps explain how social learning to adjust cooperation could be beneficial first 
before moving on to relate it to cleaner fish. 
Line 50 – Do cleaner fish then respond to this by increasing their cooperation with that individual? Or 
do they permanently terminate their interaction? 
Line 55 – you can refer to the social learning strategies/transmission bias literature to validate the 
assumptions of social learning in juvenile fish (ie) copy when ignorant, copy when asocial learning is 
costly etc. see Kendal RL, Boogert NJ, Rendell L, Laland KN, Webster M & Jones PL. (2018). Social 
Learning Strategies: Bridge-building between fields. Trends in Cognitive Sciences 22(7): 651-665. 
Line 72 – it would be useful here to explain briefly what the ‘evasive response’ actually was (ie) how 
did the plate move (where to?), did it ‘chase’ the cleaner fish? 
It would be useful to give the rationale for the three different experiments before moving onto the 
results. 
Results 
Line 80 – As described here the control does not sound like a true control? Everything was not held 
constant except the adult interaction with the plate (ie) the plate/client seems not to move in the 

control. However, on line 234-6 we discover that the control was very good. Please give this 
information here. 
Line 87-91 – The explanation of the results here is not clear. How were their preferences influenced? 
What is flake concentration? What is ‘feeding adjustment’? 
Line 98 – not clear how this makes 4 treatments, rather than 6? 
Line 99 – how could observer fish distinguish between tolerant and responsive plates? Were they 
different colours/sizes/shapes? Was the order in which fish experienced treatments counterbalanced? 
If not does this invalidate the results? 
Line 103 – was there not also a control where the plate did not move (ie) control for ‘tolerant’ plate. 
Line 107 – confusingly written “only cleaners of the observer treatments…” Do you mean only 
following ‘observer trials’ as each fish received each of the 4 treatments (according to line 98)? 
Line 115 – state what you actually mean by ‘blindly’? Do you just mean copying of an arbitrary 
preference? 
Line 116 – was this a between subjects design? 
Line 119 – was the preferred plate counterbalanced across observers? 
Line 124 – Consider rephrasing for clarity. Perhaps just “We would expect these preferences to be 
copied”. 
Line 135 – The way this sentence is framed slightly implies that the fish learned about outcomes 
instead of copying behaviour patterns. This and the proceeding discussion could be rephrased to more 
clearly emphasise that cleaner fish seemed selective in which behaviours they copied. They only 
copied behaviour patterns that resulted in tangible outcomes, which is interesting but underplayed. 
Discussion 
Line 145 – but were they actually given a choice of plates at test? This needs clarifying in the results 
section. 
Line 149 – the authors should consider and compare with other literature that has considered payoff 
based social learning in animals eg. 
Vale, G, Flynn, EG., Kendal, JR., Rawlings, B, Hopper LM., Schapiro SJ., Lambeth SP. & Kendal RL. 
(2017). Testing differential use of payoff-biased social learning strategies in children and 
chimpanzees. Proceedings of the Royal Society B 
Bono AEJ, Whiten A., van Schaik C., Krützen M., Eichenberger F., Schnider A., van de Waal E., 2018. 
Payoff- and Sex-Biased Social Learning Interact in a Wild Primate Population. Current Biology, 28 (17) 
pp. 2800-2805.e4. Peer-reviewed. 
 
Line 155 – It would be helpful to consider specific examples. The major alternative which comes to 
mind is the Snowdrift game. 
Doebeli, M., & Hauert, C. (2005). Models of cooperation based on the Prisoner's Dilemma and the 
Snowdrift game. Ecology letters, 8(7), 748-766. 
Line 159 – Consider using a simpler word rather than “hitherto”. Perhaps just “currently”. 
Line 165 – “have an equivalent effect AS CHASERS on juveniles”? 
Line 174-5 - This could be clearer. Do you mean punishment increases cooperation in eavesdroppers 
but reduces the chance that they choose to interact with the punisher they observed? Please clarify 
In general there is no discussion of ecological validity of the studies. For example, could an 
explanation for the lack of social learning of an apparent arbitrary preference for one coloured plate 
over another (experiment 3) be explained by it not representing the differences between clients 
effectively? What cues do cleaner fish use to distinguish clients, perhaps size or pattern is important 
and this did not vary between the two plates. 
Materials and Methods 
Line 191-194 – unnecessary repetition 
Line 213 – Typo, missing space (or missing reference) in brackets. 
Line 214 – who/what “didn’t respond to prawn consumption”? 
Line 238 – the repeated 15 trials at test (with the plates responding as during observation phase) 

indicate that individual learning could easily have taken place. What were the results of the very first 
trial? This is the one for which no individual learning could have yet obscured results? Is there the 
same problem with experiment 2 (Line 298)? 
Line 241: what qualified as a ‘flake item’ being consumed? Did the fish have to nibble at it or consume 
it entirely for it to be counted as eaten? 
Line 245: experiment 2 is described as having 4 treatments in the Results (this needs clarifying). 
Line 322 – Why is it beneficial for the prawns to be on the back of the plates? 
Statistical Analysis 
Line 344 – For those unfamiliar, it would be useful to briefly explain AIC and how it is used to evaluate 
models. 
Line 381 – May be useful to explain the quasibinomial distribution and how it is different to a regular 
binomial distribution.