Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
Response threshold variance as a basis of collective
rationality
Tatsuhiro Yamamoto and Eisuke Hasegawa
Article citation details
R. Soc. open sci. 4: 170097.
http://dx.doi.org/10.1098/rsos.170097
Review timeline
Original submission:
1st revised submission:
2nd revised submission:
Final acceptance:
6 June 2016
6 February 2017
13 March 2017
14 March 2017
Note: Reports are unedited and appear as
submitted by the referee. The review history
appears in chronological order.
Review History
RSOS-160400.R0 (Original submission)
Review form: Reviewer 1
Is the manuscript scientifically sound in its present form?
Yes
Are the interpretations and conclusions justified by the results?
Yes
Is the language acceptable?
Yes
Is it clear how to access all supporting data?
Yes, it is clear.
Do you have any ethical concerns with this paper?
No
Have you any concerns about statistical analyses in this paper?
No
© 2017 The Authors. Published by the Royal Society under the terms of the Creative Commons
Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use,
provided the original author and source are credited
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
2
Recommendation?
Accept with minor revision (please list in comments)
Comments to the Author(s)
The authors present a new idea about collective rationality that the variation in thresholds plays
the important role in making a collective decision making with yes/no decision units, and
showed that the colony decision in ants agrees with the proposed idea. The idea is very
interesting because each ant is treated as a simple yes/no decision unit. The results clearly
support the predictions of the proposed idea, where ants belonging to the intermediate threshold
class exhibit both yes and no decisions, while most ants in lower (higher) classes choose yes (no)
to the provided sugar water. The experiment is simple and elegant. However, I find the difficulty
in understanding the expressions of some phrases. Probably because of this problem, I have some
difficulty in understanding some sentences. The authors should definitely consult with a native
English speaker specializing in social insects. I believe that the revising English should not be so
difficult.
Major comments:
1. The phrases, such as “quality-dependent responses (behavior)” are highly confusing, since
yes/no responses are also quality-dependent, since a good option get yes, while a bad one, no.
The authors probably mean “qualitative responses (evaluation)” or something like that. Then
yes/no decisions (or responses) is contrasted with qualitative decisions (or responses). This
problem is found in the entire text including the abstract.
2. Is qualitative (quality-dependent in the authors’ term) responses of each ant assumed in the
three previous hypotheses? It is important to explain if they need or not in Introduction section,
instead of Discussion section (Page 2, Lines 47-49 (lines 61-62) and discussion). If all the three
hypotheses assume the qualitative responses of an individual ant, the current results is a clear
experimental demonstration of collective decision by yes/no ants. Therefore, the current
hypothesis stands out from the other three hypotheses in this respect (only need yes/no
decision).
3. Page 7, Lines 36-38 (lines 223-224): As authors explained, dance language in honey bees
suggests the qualitative responses. This is an interesting point. The existence of returning honey
bees with no dance implies that the yes/no system (the proposed mechanism) is also used jointly
with the qualitative dance language. Here they should clearly state that the two hypotheses
(qualitative responses of individual ants and yes/no decisions) are not exclusive. From this point,
the yes/no mechanism may be at work in any collective decisions with qualitative responses.
Note that qualitative responses does not exclude the yes/no decisions at the base. Is there any
case, where only qualitative decisions are responsible for collective decisions?
Minor comments:
1. Page 5, Lines 21-22 (lines 148): “the later is always…” should be “the latter is always…” Here,
the latter and the former can be stated explicitly option B and option A, respectively.
2. Page 5, Lines 33-36 (lines 154-155): I suspect that “influence to make a majority decision
because, in theoretically, all of….” Should be “influence on a majority decision because,
theoretically, all of….”
3. Page 6, Lines 34-35 (line 188): delete “the” in front of each.
4. Page 6, Lines 43-44 (line 193): “but do not so to the worse one” could be “but “no” to the worse
one.”
5. Page 8, Lines 35-36 (line 255): “the later option”: “t” missing (should be latter).
6. Page 8, Lines 40-41 (line 258): “achieve” should be “achieves.”
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
3
7. Page 8, Lines 42-44 (lines 259-260): In such cases, ….” I do not understand its meaning. Please
rewrite it so that I (the reader) can understand immediately.
8. Page 8, Line 44 (line 260): “Therefore” can be deleted.
9. Page 8, Lines 47-55 (lines 249-266): The logic is somewhat wrong. Even if it is not conformed,
we could not reject it. It may be confirmed later. If we did not find the active workers doing this,
then we can reject the hypothesis supported by this behavior. What are the rejected previously
provided mechanisms? Are they different from the next rejected “pre-deposited pheromone
trail?” Please explain them carefully, so that the general readers can understand without
difficulty.
10. Page 9, Line 9 (lines 273): Please add “s” to “increase.”
There may be many more typos!
Review form: Reviewer 2 (Stephen Pratt)
Is the manuscript scientifically sound in its present form?
Yes
Are the interpretations and conclusions justified by the results?
No
Is the language acceptable?
No
Is it clear how to access all supporting data?
Yes
Do you have any ethical concerns with this paper?
No
Have you any concerns about statistical analyses in this paper?
No
Recommendation?
Major revision is needed (please make suggestions in comments)
Comments to the Author(s)
This study presents a well-designed experiment that convincingly shows threshold responses to
sucrose concentration by foragers of Myrmica kotokui. It further shows that these thresholds vary
and that this variance leads to a predicted difference in the number of ants exploiting feeders
containing higher and lower sucrose concentrations. The ants were able to distinguish a
remarkably small difference in sucrose concentration (3.5% vs. 4.0%).
The authors relate these findings to the study of collective decision-making, to which it is highly
relevant. However, I found their arguments and the way they evaluated earlier work sometimes
confusing and occasionally misleading. A key problem is the distinction that they make between
threshold responses and quality-dependent responses. A threshold response is, in fact, a qualitydependent response. It is simply a response that takes a step-like form rather than a linear
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
4
increase, or some other form. A more appropriate term than "quality-dependent" would be
"graded." Thus, honeybee waggle dance duration shows a graded response to quality, whereas
the ants in this study show a step-like response. This difference in response functions is
important, but they are both quality-dependent. It is confusing to say otherwise.
Related to this issue, the paper presents threshold-response functions as alternatives to earlier
mechanisms, when in fact it fits quite nicely with most of them. In fact, I don't see how the
difference in number of responders noted in this paper could be turned into a true decision
without one of these mechanisms. For example, the authors stress that they observe a majority
decision in favor of the better feeder, but this is not really the case. They simply observe more
ants exploiting one feeder than the other. Turning this into a "vote" that would select the better
feeder requires some further step to exaggerate the difference (say, a quorum rule or positive
feedback via recruitment). The phenomenon that is described here is more like allocation of
resource exploitation according to quality than the kind of consensus decision-making studied in
the earlier work referenced here, in which one option is clearly rejected in favor of the other.
The earlier work itself is sometimes characterized in ways that are not really accurate. At line 62,
for example, positive feedback is described as a distinct hypothesis to recruitment latency, with
references to work on Temnothorax house-hunting. In fact, recruitment latency goes hand-inhand with positive feedback to produce decisions in that case.
All in all, I find the results presented here very interesting and highly relevant to collective
decision-making. However, I think the authors should re-frame how they relate their findings to
earlier work.
Other comments:
The writing is generally clear and the paper is well organized. However, it could use revision
throughout to improve English style and grammar.
Line 91: What does it mean that the ants behaved naturally?
Section 3.1 of the results seems better suited to the introduction.
Line 198-203: It may be worth noting here that the range of sucrose concentrations that the colony
can distinguish will depend on the range of thresholds present in the worker population.
Line 208: "Optimal" seems too strong here. It is reasonable to assume that the colony benefits by
exploiting the better food more, but there are many ways of doing this, and it is not obvious that
the outcome seen here is the best one. For example, would it be better to exploit only the stronger
feeder and ignore the weaker one, or to exploit both but at a different ratio than seen here? If so,
the observed behavior is not optimal.
Lines 239-244: The results referred to here seem consistent with a graded response of recruitment
probability to site quality. I agree that a threshold response is also possible, but decisive data
have not been gathered, as far as I know. The authors should either strengthen their argument or
acknowledge this ambiguity.
271: I am not a neuroscientist, but I am skeptical that nervous systems lack graded responses
("quality-dependent responses") to inputs.
Stephen Pratt
Arizona State University
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
5
Decision letter (RSOS-160400)
16-Sep-2016
Dear Dr Hasegawa:
Manuscript ID RSOS-160400 entitled "The response threshold variance as the basis of the
collective rationality." which you submitted to Royal Society Open Science, has been reviewed.
The comments from reviewers are included at the bottom of this letter.
In view of the criticisms of the reviewers, the manuscript has been rejected in its current form.
However, a new manuscript may be submitted which takes into consideration these comments.
Please note that resubmitting your manuscript does not guarantee eventual acceptance, and that
your resubmission will be subject to peer review before a decision is made.
You will be unable to make your revisions on the originally submitted version of your
manuscript. Instead, revise your manuscript and upload the files via your author centre.
Once you have revised your manuscript, go to https://mc.manuscriptcentral.com/rsos and login
to your Author Center. Click on "Manuscripts with Decisions," and then click on "Create a
Resubmission" located next to the manuscript number. Then, follow the steps for resubmitting
your manuscript.
Your resubmitted manuscript should be submitted by 16-Mar-2017. If you are unable to submit
by this date please contact the Editorial Office.
We look forward to receiving your resubmission.
Sincerely,
Alice Power
Editorial Coordinator, Royal Society Open Science
on behalf of
Kevin Padian, Royal Society Open Science
[email protected]
Reviewers' Comments to Author:
Reviewer: 1
Comments to the Author(s)
The authors present a new idea about collective rationality that the variation in thresholds plays
the important role in making a collective decision making with yes/no decision units, and
showed that the colony decision in ants agrees with the proposed idea. The idea is very
interesting because each ant is treated as a simple yes/no decision unit. The results clearly
support the predictions of the proposed idea, where ants belonging to the intermediate threshold
class exhibit both yes and no decisions, while most ants in lower (higher) classes choose yes (no)
to the provided sugar water. The experiment is simple and elegant. However, I find the difficulty
in understanding the expressions of some phrases. Probably because of this problem, I have some
difficulty in understanding some sentences. The authors should definitely consult with a native
English speaker specializing in social insects. I believe that the revising English should not be so
difficult.
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
6
Major comments:
1. The phrases, such as “quality-dependent responses (behavior)” are highly confusing, since
yes/no responses are also quality-dependent, since a good option get yes, while a bad one, no.
The authors probably mean “qualitative responses (evaluation)” or something like that. Then
yes/no decisions (or responses) is contrasted with qualitative decisions (or responses). This
problem is found in the entire text including the abstract.
2. Is qualitative (quality-dependent in the authors’ term) responses of each ant assumed in the
three previous hypotheses? It is important to explain if they need or not in Introduction section,
instead of Discussion section (Page 2, Lines 47-49 (lines 61-62) and discussion). If all the three
hypotheses assume the qualitative responses of an individual ant, the current results is a clear
experimental demonstration of collective decision by yes/no ants. Therefore, the current
hypothesis stands out from the other three hypotheses in this respect (only need yes/no
decision).
3. Page 7, Lines 36-38 (lines 223-224): As authors explained, dance language in honey bees
suggests the qualitative responses. This is an interesting point. The existence of returning honey
bees with no dance implies that the yes/no system (the proposed mechanism) is also used jointly
with the qualitative dance language. Here they should clearly state that the two hypotheses
(qualitative responses of individual ants and yes/no decisions) are not exclusive. From this point,
the yes/no mechanism may be at work in any collective decisions with qualitative responses.
Note that qualitative responses does not exclude the yes/no decisions at the base. Is there any
case, where only qualitative decisions are responsible for collective decisions?
Minor comments:
1. Page 5, Lines 21-22 (lines 148): “the later is always…” should be “the latter is always…” Here,
the latter and the former can be stated explicitly option B and option A, respectively.
2. Page 5, Lines 33-36 (lines 154-155): I suspect that “influence to make a majority decision
because, in theoretically, all of….” Should be “influence on a majority decision because,
theoretically, all of….”
3. Page 6, Lines 34-35 (line 188): delete “the” in front of each.
4. Page 6, Lines 43-44 (line 193): “but do not so to the worse one” could be “but “no” to the worse
one.”
5. Page 8, Lines 35-36 (line 255): “the later option”: “t” missing (should be latter).
6. Page 8, Lines 40-41 (line 258): “achieve” should be “achieves.”
7. Page 8, Lines 42-44 (lines 259-260): In such cases, ….” I do not understand its meaning. Please
rewrite it so that I (the reader) can understand immediately.
8. Page 8, Line 44 (line 260): “Therefore” can be deleted.
9. Page 8, Lines 47-55 (lines 249-266): The logic is somewhat wrong. Even if it is not conformed,
we could not reject it. It may be confirmed later. If we did not find the active workers doing this,
then we can reject the hypothesis supported by this behavior. What are the rejected previously
provided mechanisms? Are they different from the next rejected “pre-deposited pheromone
trail?” Please explain them carefully, so that the general readers can understand without
difficulty.
10. Page 9, Line 9 (lines 273): Please add “s” to “increase.”
There may be many more typos!
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
7
Reviewer: 2
Comments to the Author(s)
This study presents a well-designed experiment that convincingly shows threshold responses to
sucrose concentration by foragers of Myrmica kotokui. It further shows that these thresholds vary
and that this variance leads to a predicted difference in the number of ants exploiting feeders
containing higher and lower sucrose concentrations. The ants were able to distinguish a
remarkably small difference in sucrose concentration (3.5% vs. 4.0%).
The authors relate these findings to the study of collective decision-making, to which it is highly
relevant. However, I found their arguments and the way they evaluated earlier work sometimes
confusing and occasionally misleading. A key problem is the distinction that they make between
threshold responses and quality-dependent responses. A threshold response is, in fact, a qualitydependent response. It is simply a response that takes a step-like form rather than a linear
increase, or some other form. A more appropriate term than "quality-dependent" would be
"graded." Thus, honeybee waggle dance duration shows a graded response to quality, whereas
the ants in this study show a step-like response. This difference in response functions is
important, but they are both quality-dependent. It is confusing to say otherwise.
Related to this issue, the paper presents threshold-response functions as alternatives to earlier
mechanisms, when in fact it fits quite nicely with most of them. In fact, I don't see how the
difference in number of responders noted in this paper could be turned into a true decision
without one of these mechanisms. For example, the authors stress that they observe a majority
decision in favor of the better feeder, but this is not really the case. They simply observe more
ants exploiting one feeder than the other. Turning this into a "vote" that would select the better
feeder requires some further step to exaggerate the difference (say, a quorum rule or positive
feedback via recruitment). The phenomenon that is described here is more like allocation of
resource exploitation according to quality than the kind of consensus decision-making studied in
the earlier work referenced here, in which one option is clearly rejected in favor of the other.
The earlier work itself is sometimes characterized in ways that are not really accurate. At line 62,
for example, positive feedback is described as a distinct hypothesis to recruitment latency, with
references to work on Temnothorax house-hunting. In fact, recruitment latency goes hand-inhand with positive feedback to produce decisions in that case.
All in all, I find the results presented here very interesting and highly relevant to collective
decision-making. However, I think the authors should re-frame how they relate their findings to
earlier work.
Other comments:
The writing is generally clear and the paper is well organized. However, it could use revision
throughout to improve English style and grammar.
Line 91: What does it mean that the ants behaved naturally?
Section 3.1 of the results seems better suited to the introduction.
Line 198-203: It may be worth noting here that the range of sucrose concentrations that the colony
can distinguish will depend on the range of thresholds present in the worker population.
Line 208: "Optimal" seems too strong here. It is reasonable to assume that the colony benefits by
exploiting the better food more, but there are many ways of doing this, and it is not obvious that
the outcome seen here is the best one. For example, would it be better to exploit only the stronger
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
8
feeder and ignore the weaker one, or to exploit both but at a different ratio than seen here? If so,
the observed behavior is not optimal.
Lines 239-244: The results referred to here seem consistent with a graded response of recruitment
probability to site quality. I agree that a threshold response is also possible, but decisive data
have not been gathered, as far as I know. The authors should either strengthen their argument or
acknowledge this ambiguity.
271: I am not a neuroscientist, but I am skeptical that nervous systems lack graded responses
("quality-dependent responses") to inputs.
Stephen Pratt
Arizona State University
Author's Response to Decision Letter for (RSOS-160400)
See Appendix A.
RSOS-170097.R0 (Revision)
Review form: Reviewer 1 (Stephen Pratt)
Is the manuscript scientifically sound in its present form?
Yes
Are the interpretations and conclusions justified by the results?
Yes
Is the language acceptable?
Yes
Is it clear how to access all supporting data?
Yes
Do you have any ethical concerns with this paper?
No
Have you any concerns about statistical analyses in this paper?
No
Recommendation?
Accept with minor revision (please list in comments)
Comments to the Author(s)
This revision substantially corrects the issues with the earlier version. The findings are better
related to earlier work, making it easier to assess the value of the authors’ findings. They present
a strong and convincing demonstration of threshold responses to sucrose solution strength in
ants, and they show how a diversity of thresholds in the worker population can account for a
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
9
colony’s allocation of more workers to better food sources. This work provides a valuable insight
into the emergence of functional group behavior from individual diversity.
There are several minor language issues and small errors that should be corrected:
Title: This would be better without the opening “The”.
Lines 61-62: better as “…explain collective rationality.”
Lines 63-65: This sentence is hard to follow. I suggest the following: “In social insects, more
effective recruitment to the better option results in an increasing return in the number of visited
workers to the best option over time (i.e., positive feedback).”
Line 91: better as “Variance in response thresholds…”
Lines 97-99: This sentence is hard to interpret. I think that the following words should be cut:
“and the number of “yes responses.” Alternatively, the sentence should be re-written.
Lines 200-204: I suggest re-phrasing for clarity as follows: “It is important to note that because, in
theory, our mechanism works regardless of the options' qualities and the threshold distribution, a
single experiment was sufficient to prove the hypothesis. If we set another pair of options, each
with a different quality, ant colonies are predicted to always prefer the better option, as long as
their threshold distribution covers the range of the options’ qualities.”
Lines 245-246: I think that the references here should be numbered 28 and 29.
Table S2: There seems to be a typographical error in the 1st check LOW column for Colony 2.
Rather than 55, this figure should be 5 (I think).
Decision letter (RSOS-170097)
01-Mar-2017
Dear Dr Hasegawa
On behalf of the Editor, I am pleased to inform you that your Manuscript RSOS-170097 entitled
"The response threshold variance as a basis of the collective rationality." has been accepted for
publication in Royal Society Open Science subject to minor revision in accordance with the
referee suggestions. Please find the referees' comments at the end of this email.
The reviewers and Subject Editor have recommended publication, but also suggest some minor
revisions to your manuscript. Therefore, I invite you to respond to the comments and revise your
manuscript.
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10
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Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
11
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Kind regards,
Alice Power
Editorial Coordinator
Royal Society Open Science
on behalf of Kevin Padian
Subject Editor, Royal Society Open Science
[email protected]
Associate Editor Comments to Author:
Comments to the Author:
The manuscript has been significantly improved, but some problematic expressions remain (some
of which are pointed out by the Reviewer). Further attention should be paid to language
(especially grammar) to aid clarity.
I would recommend the title be changed to "Response threshold variance as a basis of collective
rationality" (i.e. dropping both instances of the definite article).
Comments to Author:
Reviewer: 2
Comments to the Author(s)
This revision substantially corrects the issues with the earlier version. The findings are better
related to earlier work, making it easier to assess the value of the authors’ findings. They present
a strong and convincing demonstration of threshold responses to sucrose solution strength in
ants, and they show how a diversity of thresholds in the worker population can account for a
Downloaded from http://rsos.royalsocietypublishing.org/ on June 18, 2017
12
colony’s allocation of more workers to better food sources. This work provides a valuable insight
into the emergence of functional group behavior from individual diversity.
There are several minor language issues and small errors that should be corrected:
Title: This would be better without the opening “The”.
Lines 61-62: better as “…explain collective rationality.”
Lines 63-65: This sentence is hard to follow. I suggest the following: “In social insects, more
effective recruitment to the better option results in an increasing return in the number of visited
workers to the best option over time (i.e., positive feedback).”
Line 91: better as “Variance in response thresholds…”
Lines 97-99: This sentence is hard to interpret. I think that the following words should be cut:
“and the number of “yes responses.” Alternatively, the sentence should be re-written.
Lines 200-204: I suggest re-phrasing for clarity as follows: “It is important to note that because, in
theory, our mechanism works regardless of the options' qualities and the threshold distribution, a
single experiment was sufficient to prove the hypothesis. If we set another pair of options, each
with a different quality, ant colonies are predicted to always prefer the better option, as long as
their threshold distribution covers the range of the options’ qualities.”
Lines 245-246: I think that the references here should be numbered 28 and 29.
Table S2: There seems to be a typographical error in the 1st check LOW column for Colony 2.
Rather than 55, this figure should be 5 (I think).
Author's Response to Decision Letter for (RSOS-170097)
See Appendix B.
Decision letter (RSOS-170097.R1)
14-Mar-2017
Dear Dr Hasegawa,
I am pleased to inform you that your manuscript entitled "Response threshold variance as a basis
of collective rationality." is now accepted for publication in Royal Society Open Science.
You can expect to receive a proof of your article in the near future. Please contact the editorial
office ([email protected] and [email protected]) to let us know if
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Appendix A
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Response to reviewers
to Reviewer: 1
Comments to the Author(s)
The authors present a new idea about collective rationality that the variation in
thresholds plays the important role in making a collective decision making with yes/no
decision units, and showed that the colony decision in ants agrees with the proposed
idea. The idea is very interesting because each ant is treated as a simple yes/no decision
unit. The results clearly support the predictions of the proposed idea, where ants
belonging to the intermediate threshold class exhibit both yes and no decisions, while
most ants in lower (higher) classes choose yes (no) to the provided sugar water. The
experiment is simple and elegant. However, I find the difficulty in understanding the
expressions of some phrases. Probably because of this problem, I have some difficulty
in understanding some sentences. The authors should definitely consult with a native
English speaker specializing in social insects. I believe that the revising English should
not be so difficult.
We are sorry for our poor English usages. We rewrote the MS and, send the MS to
Nature Publishing Group Language Editing (NPGJE) for corrections for English usages.
We hope this treatment satisfy the Rev. 1.
Major comments:
1. The phrases, such as “quality-dependent responses (behavior)” are highly confusing,
since yes/no responses are also quality-dependent, since a good option get yes, while a
bad one, no. The authors probably mean “qualitative responses (evaluation)” or
something like that. Then yes/no decisions (or responses) is contrasted with qualitative
decisions (or responses). This problem is found in the entire text including the abstract.
Thank you very much your indication of our ambiguous word usages. In the revised
version, we used the words, "step-like response"/"yes/no response" and "quality-graded
response" to indicate the threshold response (yes/no) and the response that becomes
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gradually large with the strength of a stimulus (like ants' recruitment or honeybee's
dance), respectively. These treatments will prevent readers from needless confusions.
2. Is qualitative (quality-dependent in the authors’ term) responses of each ant assumed
in the three previous hypotheses? It is important to explain if they need or not in
Introduction section, instead of Discussion section (Page 2, Lines 47-49 (lines 61-62)
and discussion). If all the three hypotheses assume the qualitative responses of an
individual ant, the current results is a clear experimental demonstration of collective
decision by yes/no ants. Therefore, the current hypothesis stands out from the other
three hypotheses in this respect (only need yes/no decision).
We appreciate to your important suggestions. In fact, all the previous three hypotheses
(positive feedback, recruitment latency and best-of-n) require "quality-graded response"
to achieve a collective decision rationally. We clearly explained this point in
Introduction section (L61-71), and this revision will make it easy to understand the
novelty of our finding to readers.
3. Page 7, Lines 36-38 (lines 223-224): As authors explained, dance language in honey
bees suggests the qualitative responses. This is an interesting point. The existence of
returning honey bees with no dance implies that the yes/no system (the proposed
mechanism) is also used jointly with the qualitative dance language. Here they should
clearly state that the two hypotheses (qualitative responses of individual ants and yes/no
decisions) are not exclusive. From this point, the yes/no mechanism may be at work in
any collective decisions with qualitative responses. Note that qualitative responses does
not exclude the yes/no decisions at the base. Is there any case, where only qualitative
decisions are responsible for collective decisions?
Thank you for your correct understanding for our findings. Surely, the yes/no decision
mechanism is not mutually exclusive with the previous mechanisms that need "the
quality-graded response". Rather, we think that the yes/no mechanism is under the
previous mechanisms as a basis of the collective rationality because honeybees and ants
have shown different acceptance (dance or not (recruit or not) for an option) rates for
options with different qualities (as cited in the text; L236-247). The initial differences
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that made by "step-like responses" leads following amplifications of the initial
difference in the number of scouts using "quality-graded responses" in social insects,
presumably to make sure correct decisions since wrong decisions may result in low
(even no) fitness.
Now, we testing a hypothesis that if a colony cannot make a rational decision using only
"step-like responses" (by using only LOW class in a collective decision), whether they
can make a rational decision or not. If they can, social insects can show the collective
rationality without an effective threshold variance. However, such a result does not
mean that they do not use the threshold variance in their collective decision-makings.
We proposed a new mechanism for the collective rationality in this study, and
interactions between our findings and the previous "quality-graded responses" based
mechanisms are waiting for further studies. We made such discussions in the revised
version (L269-276).
Minor comments:
1. Page 5, Lines 21-22 (lines 148): “the later is always…” should be “the latter is
always…” Here, the latter and the former can be stated explicitly option B and option A,
respectively.
Thank you for pointing out our mistake. We corrected this mistake (L00).
2. Page 5, Lines 33-36 (lines 154-155): I suspect that “influence to make a majority
decision because, in theoretically, all of….” Should be “influence on a majority
decision because, theoretically, all of….”
Thank you. We rewrote the MS followed by the reviewer's suggestion.
3. Page 6, Lines 34-35 (line 188): delete “the” in front of each.
We did so (L190).
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4. Page 6, Lines 43-44 (line 193): “but do not so to the worse one” could be “but “no”
to the worse one.”
Thank you. We revised there as your comment (L195).
5. Page 8, Lines 35-36 (line 255): “the later option”: “t” missing (should be latter).
Sorry for our mistake. We corrected there (L62).
6. Page 8, Lines 40-41 (line 258): “achieve” should be “achieves.”
We corrected this mistake.
7. Page 8, Lines 42-44 (lines 259-260): In such cases, ….” I do not understand its
meaning. Please rewrite it so that I (the reader) can understand immediately.
We more clarified our intention at this part (L266-268).
8. Page 8, Line 44 (line 260): “Therefore” can be deleted.
We deleted it.
9. Page 8, Lines 47-55 (lines 249-266): The logic is somewhat wrong. Even if it is not
conformed, we could not reject it. It may be confirmed later. If we did not find the
active workers doing this, then we can reject the hypothesis supported by this behavior.
What are the rejected previously provided mechanisms? Are they different from the
next rejected “pre-deposited pheromone trail?” Please explain them carefully, so that
the general readers can understand without difficulty.
We are sorry for inviting your confusion. We did not intend to say that our experiment
rejects the previous mechanisms. We want to say that the previous mechanisms cannot
explain the current results at 15 min after the start of the experiment as there is no
recruitment behavior. Sure, this is not the evidence that the previously proposed
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mechanisms are not in collective decision-makings in M. kotokui. We rewrote this part
to more understandable contents (L247-352).
10. Page 9, Line 9 (lines 273): Please add “s” to “increase.”
We did so (L288).
There may be many more typos!
We checked for typos throughout the MS.
to Reviewer: 2
Comments to the Author(s)
This study presents a well-designed experiment that convincingly shows threshold
responses to sucrose concentration by foragers of Myrmica kotokui. It further shows
that these thresholds vary and that this variance leads to a predicted difference in the
number of ants exploiting feeders containing higher and lower sucrose concentrations.
The ants were able to distinguish a remarkably small difference in sucrose concentration
(3.5% vs. 4.0%).
The authors relate these findings to the study of collective decision-making, to which it
is highly relevant. However, I found their arguments and the way they evaluated earlier
work sometimes confusing and occasionally misleading. A key problem is the
distinction that they make between threshold responses and quality-dependent responses.
A threshold response is, in fact, a quality-dependent response. It is simply a response
that takes a step-like form rather than a linear increase, or some other form. A more
appropriate term than "quality-dependent" would be "graded." Thus, honeybee waggle
dance duration shows a graded response to quality, whereas the ants in this study show
a step-like response. This difference in response functions is important, but they are
both quality-dependent. It is confusing to say otherwise.
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Thank you very much for an indication to our ambiguous word usages. We replaced the
words "a quality-dependent response " to "a quality-graded response" in the revised
version. We also used the word "a step-like response" to represent the response
occurring by a response threshold. These changes will prevent readers from needless
confusions and miss-readings.
Related to this issue, the paper presents threshold-response functions as alternatives to
earlier mechanisms, when in fact it fits quite nicely with most of them. In fact, I don't
see how the difference in number of responders noted in this paper could be turned into
a true decision without one of these mechanisms. For example, the authors stress that
they observe a majority decision in favor of the better feeder, but this is not really the
case. They simply observe more ants exploiting one feeder than the other. Turning this
into a "vote" that would select the better feeder requires some further step to exaggerate
the difference (say, a quorum rule or positive feedback via recruitment). The
phenomenon that is described here is more like allocation of resource exploitation
according to quality than the kind of consensus decision-making studied in the earlier
work referenced here, in which one option is clearly rejected in favor of the other.
We appreciate to your adequate criticisms. Although the majority-decision for the better
(or the best in the case in which more than two options exist) option is possible by using
only a variable response thresholds within members in a collective decision maker, real
social insects use other mechanisms you pointed out the above. However, even in the
previous studies, honeybees and ants have shown the different acceptance (dance or not,
recruit or not for an option) rates to options with different qualities as cited in the text
(L236-247). These data suggest that the variable thresholds to option's quality may play
a role in collective decision-makings. Presumably, the following quality-graded
responses amplify (or correct) the initial judgment made by the step-like responses, and
need to guarantee a rational decision. In addition, we agree with that a quorum should
be required to determine when they make a decision.
If you understood our results as the rejection of these mechanisms, we apologize for
inviting a misreading. The step-like response mechanism is not mutually exclusive with
the quality-graded mechanisms. Rather, the former is under the latter as a basis of the
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collective rationality, and both the mechanisms is complementary each other to
guarantee the making of a rapid rational collective-decision in group-living animals.
Here, we reported a new possible mechanism for the collective rationality. Threshold
variances exist among workers of many social insects. How do the two mechanisms (the
step-like and the quality-graded responses) interact to make a rapid rational collective
decision would be an important issue to be answered by future studies.
We used the word "prefer" instead of "decision" in this MS at the adequate positions.
And we rewrote the MS as to be understandable the above contents (L253-276). We
hope this treatment satisfy the Rev.2.
The earlier work itself is sometimes characterized in ways that are not really accurate.
At line 62, for example, positive feedback is described as a distinct hypothesis to
recruitment latency, with references to work on Temnothorax house-hunting. In fact,
recruitment latency goes hand-in-hand with positive feedback to produce decisions in
that case.
We are sorry for our incorrect explanations. Your indication is correct. We carefully
rewrote the MS to avoid such ambiguities (L63-69).
All in all, I find the results presented here very interesting and highly relevant to
collective decision-making. However, I think the authors should re-frame how they
relate their findings to earlier work.
Thank you for your relevant advice. We reframed the composition of article to follow
your suggestions.
Other comments:
The writing is generally clear and the paper is well organized. However, it could use
revision throughout to improve English style and grammar.
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The revised manuscript has been checked for English usages by a native scientist who
studying ant behaviors.
Line 91: What does it mean that the ants behaved naturally?
The meaning is that the ants allowed to behave freely. We clarified the meaning (L125)
Section 3.1 of the results seems better suited to the introduction.
We moved this section to Introduction part (L81-106).
Line 198-203: It may be worth noting here that the range of sucrose concentrations that
the colony can distinguish will depend on the range of thresholds present in the worker
population.
Thank you for a useful advice. We added a sentence explaining the above contents
(L200-202).
Line 208: "Optimal" seems too strong here. It is reasonable to assume that the colony
benefits by exploiting the better food more, but there are many ways of doing this, and
it is not obvious that the outcome seen here is the best one. For example, would it be
better to exploit only the stronger feeder and ignore the weaker one, or to exploit both
but at a different ratio than seen here? If so, the observed behavior is not optimal.
We appreciate for your adequate criticisms. Certainly, this study did not show the
observed phenomenon is the best way to exploit food-resources given. So, we weakened
the expressions at this part (L209-210). However, we think that the our system may
enable to realize the best allocation of workers to more than one food resources each of
which has a different qualities, as observed in a slime mold (ex. Nakagaki (2001) Res.
Microbiol. 152:767). This viewpoint is a noteworthy issue to be challenged in future
studies. For this purpose, the description of the existence of the finding system is
required to deepen our understanding for optimization of collective behaviors in
group-living organisms.
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Lines 239-244: The results referred to here seem consistent with a graded response of
recruitment probability to site quality. I agree that a threshold response is also possible,
but decisive data have not been gathered, as far as I know. The authors should either
strengthen their argument or acknowledge this ambiguity.
Thank your for your adequate comments. As you say, decisive data have not been
gathered and should be studied in near future. At present, we weakened this part as "
Therefore, there is a possibility that the "yes/no" mechanism underlays the collective
decision-making even in social insects. Of course, the quality-graded responses could
explain the above differences, and thus, is which (or both) mechanism(s) realizes these
differences should be tested in future studies. Note that both the mechanisms may work
simultaneously to cause the observed differences in number of responded workers to
options each of which has a different quality." See L246-251.
271: I am not a neuroscientist, but I am skeptical that nervous systems lack graded
responses ("quality-dependent responses") to inputs.
Thank you very much for presenting an interesting and debatable issue. We have
searched articles for the decision-making process in vertebrate's brains and found
several interesting papers. These have demonstrated that a region of monkey's brain that
makes the value-coding (the assessment of the quality) for options with different
qualities. In this process, firing rates of the value-coding region to an option increased
with the qualities of the option (e.g. the volume of given juice), and, importantly, the
increasing rate to an option (meaning that the regression slope of the firing rates on the
qualities of options is positive; this suggests that a group of neurons (is this your
nervous systems?) would be used for the value-coding way as Hecht (1924) and
Hogland (1930) have shown; see References in the MS)) is independent (has not been
influenced) from the existence of another option (e.g., the value-coding pattern for the
orange juice has not been influenced by the simultaneous existence of a grape juice).
These findings can be interpreted as that A GROUP OF NEURONS with variable
thresholds for a step-like response exist to assess the quality of an option, which uses
only the step-like responses of a single neuron, and suggest that a brain has numerous
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such units (many groups consisting of multiple "step-like" neurons) for each option, i.e.,
the value of an orange juice and that of a grape juice were assessed by each a different
value-coding unit (a group of neurons). Our mechanism can explain these phenomena
without any "quality-graded response" of a single neuron. However, the previous
mechanisms found in social insets (the positive feedback, the recruitment latency, the
best-of-n) require "quality-graded response" by a single neuron. Whether a single
neuron (is this your nervous systems?) can make a "quality-graded response" or not is
unclear. Of course, a quorum-like response is used in decision-makings in the brain
(when the firing rate reached to a threshold, a neuro-transmittable signal is out to the
next nervous system to make a decision). Anyway, our mechanism can explain the
value-coding and decision-makings in the brain without any "quality-graded responses"
by a single neuron. Thus, if you want to say that there is a "quality-graded response" by
a single neuron, and that a brain use similar mechanisms found in ants and honeybees,
which based on "quality-graded responses ", it must be shown that a single neuron can
respond to a stimulus in the "quality-graded manner". However, that is the works of
neuroscientists, may not be our works. We made such discussion in the revised MS (see
L285-290).
At all, your comments are very useful to improve our MS and we deeply appreciate to
you. In fact, we have once considered to investigate the role of threshold variances in
the house-hunting in M. kotokui because, as you say, such a selection resulted in a clear
decision for the acceptance of an option and the rejections for the other options.
However, measuring the threshold of a worker to the quality of a candidate nest is
difficult because M. kotokui seldom show the tandem-running recruitments. Thus, we
conducted the experiments using sucrose solutions in this study.
We hope our revisions satisfy you.
Stephen Pratt
Arizona State University
Dear Prof. Pratt,
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We feel honored to reviewing our MS by you. We respect your many interesting works
on collective decision-makings in ants (and of course, those have conducted by Prof. T.
Seeley on honeybees). We never intended to reject your findings, because, as you (and
the Rev. 1) know, our findings are compatible with the previous knowledge and
probably bring new insights into scientific understandings of the collective rationality
("hand-in-hand" in your words). As mentioned above, your Temnothorax ants would be
suitable for studies for the role of threshold variances using a clear decision criterion.
We believe that the science will progress with new relevant findings, and that you can
understand the scientific value of our findings because we know that you are a major
and clever scientist in our field.
Sincerely yours,
3 February 2017
Eisuke Hasegawa
Appendix B
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Associate Editor Comments to Author:
Comments to the Author:
The manuscript has been significantly improved, but some problematic expressions remain (some of
which are pointed out by the Reviewer). Further attention should be paid to language (especially
grammar) to aid clarity.
We are not native speakers. Thus, we send the MS to Nature Publishing Group Language Editing
(NPGLE) for corrections of English usage after followed to the suggestions by Rev.2. There is no other
way to improve the MS at this point.
I would recommend the title be changed to "Response threshold variance as a basis of collective
rationality" (i.e. dropping both instances of the definite article).
We followed your suggestion.
We hope these treatments improved the MS to the level of acceptance at Royal Society Open Science.
Responses to the reviewer: 2
Comments to the Author(s)
This revision substantially corrects the issues with the earlier version. The findings are better related to
earlier work, making it easier to assess the value of the authors’ findings. They present a strong and
convincing demonstration of threshold responses to sucrose solution strength in ants, and they show how
a diversity of thresholds in the worker population can account for a colony’s allocation of more workers
to better food sources. This work provides a valuable insight into the emergence of functional group
behavior from individual diversity.
There are several minor language issues and small errors that should be corrected:
Title: This would be better without the opening “The”.
Lines 61-62: better as “…explain collective rationality.”
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Lines 63-65: This sentence is hard to follow. I suggest the following: “In social insects, more effective
recruitment to the better option results in an increasing return in the number of visited workers to the best
option over time (i.e., positive feedback).”
Line 91: better as “Variance in response thresholds…”
Lines 97-99: This sentence is hard to interpret. I think that the following words should be cut: “and the
number of “yes responses.” Alternatively, the sentence should be re-written.
Lines 200-204: I suggest re-phrasing for clarity as follows: “It is important to note that because, in theory,
our mechanism works regardless of the options' qualities and the threshold distribution, a single
experiment was sufficient to prove the hypothesis. If we set another pair of options, each with a different
quality, ant colonies are predicted to always prefer the better option, as long as their threshold distribution
covers the range of the options’ qualities.”
Lines 245-246: I think that the references here should be numbered 28 and 29.
Table S2: There seems to be a typographical error in the 1st check LOW column for Colony 2. Rather
than 55, this figure should be 5 (I think).
Thank your very much for corrections of our poor English expressions. We followed all the your
suggestions. The corrected parts are higlighted in pink in the highlighted version. In addition, the final
MS has been checked for English usages by the Nature Publishing Group Language Editing (NPGLE).
As we are not native English users, there is no other way to improve the MS at this point. Again, we are
much grateful to your efforts to improve our MS. We hope these treatments will satisfy Rev.2.