Response time of an avian prey to a simulated hawk attack is slower in darker conditions, but is independent of hawk colour morph

To avoid predation, many species rely on vision to detect predators and initiate an escape response. The ability to detect predators may be lower in darker light conditions or with darker backgrounds. For birds, however, this has never been experimentally tested. We test the hypothesis that the response time of avian prey (feral pigeon Columbia livia f. domestica) to a simulated hawk attack (taxidermy mounted colour-polymorphic black sparrowhawk Accipiter melanoleucus) will differ depending on light levels or background colour. We predict that response will be slower under darker conditions, which would translate into higher predation risk. The speed of response of prey in relation to light level or background colour may also interact with the colour of the predator, and this idea underpins a key hypothesis proposed for the maintenance of different colour morphs in polymorphic raptors. We therefore test whether the speed of reaction is influenced by the morph of the hawk (dark/light) in combination with light conditions (dull/bright), or background colours (black/white). We predict slowest responses to morphs under conditions that less contrast with the plumage of the hawk (e.g. light morph under bright light or white background). In support of our first hypothesis, pigeons reacted slower under duller light and with a black background. However, we found no support for the second hypothesis, with response times observed between the hawk-morphs being irrespective of light levels or background colour. Our findings experimentally confirm that birds detect avian predators less efficiently under darker conditions. These conditions, for example, might occur during early mornings or in dense forests, which could lead to changes in anti-predator behaviours. However, our results provide no support that different morphs may be maintained in a population due to differential selective advantages linked to improved hunting efficiencies in different conditions due to crypsis.

1. My main problem relates to terminology and measurements of light condition. No reader can have any idea what a "dull light condition" could mean. So here the reader needs to know the light intensity: The easiest way is to say whether this means light conditions on a cloudy day (5 to 100 times dimmer than a sunny day), in a light (10 x dimmer) or thick (upo to 1000 times dimmer) forest, or maybe early or late dusk (which includes a huge range of light intensities). In addition, light measurements are useful, either in human-defined IS units (lux or Candela), but possibly even in spectral data, specifically when working indoors, where light spectra often are completely different to natural spectra. For instance, does the light have a UV component or not? Chickens have different flicker fusion frequency with and without UV, and it is not known whether the same applies to pigeons.
2. The second part of this problem relates to the description of the background and predator dummy intensities. These are not given anywhere. The most relevant information would be a measurement (if these are reasonably close to the black-grey-white colour range this could be done with a candelameter that measures the light reflected from a defined area into a defined angle (Cd/m2) of the predator dummy and the background, from the direction of the pigeon. The contrast between these two measurements is telling you whether indeed the dark morph had lower contrast against the black background and the bright morph, against the white background. From the very nice sketch of the set-up, I am not sure this really is the case. It all depends on the illumination conditions, so it needs to be measured. It is important because it allows you to answer the question whether the the behavior of the pigeons did not differ, simply because contrasts were not different, or whether the contrasts really differed but the pigeons did not care.
Handheld instruments that can measure this are not very expensive and they are quite common. Terms like dark and bright are far too unspecific to be used in the context of such studies, unless they come with a measurement.
3. I am a bit disappointed that the authors missed a very similar case of colour dimorphism, in barn owls, which have a white and a dark morph as well. A lot of work has been done on that system, mostly by the group of Alexandre Roulin. A short discussion on this very similar case would bring a more general perspective to the problem and thus make this paper more interesting to general readers.
Other than these easily fixed points, I think the study is very solid.

25-Jun-2019
Dear Ms Nebel On behalf of the Editors, I am pleased to inform you that your Manuscript RSOS-190677 entitled "Response time of an avian prey to a simulated hawk attack is slower in darker conditions, but is independent of hawk colour morph" 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.
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Once again, thank you for submitting your manuscript to Royal Society Open Science and I look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch. Comments to the Author(s) The authors tested whether pigeons react differently when attacked by dark vs. light sparrowhawk (a colour polymorphic species) under different light conditions. They found that pigeons indeed react different if light conditions are dark or light but not in intereaction with sparrowhawk plumage coloration. This is contrary to their prediction. I quite liked the study and recommend publication. I just wonder whether pigeons are really attacked by these sparrowhawks? And if yes, how frequently are pigeons captured by sparrowhawks? Maybe it could worth using other prey species. And I wonder whether the experimental design is appropriate given that detection time could be measured in only 9.5% of the times?
Even if the authors did not find an effect as expected, I believe that this paper is a useful contribution.

Reviewer: 2
Comments to the Author(s) This interesting study investigates whether feral pigeons detect the dark or bright morph of the black sparrow hawk faster, under different conditions, and thus, whether earlier observed differences in hunting behavior and success of the two morphs may result from prey behavior. The study is mostly well-done and has clearly described results.
1. My main problem relates to terminology and measurements of light condition. No reader can have any idea what a "dull light condition" could mean. So here the reader needs to know the light intensity: The easiest way is to say whether this means light conditions on a cloudy day (5 to 100 times dimmer than a sunny day), in a light (10 x dimmer) or thick (upo to 1000 times dimmer) forest, or maybe early or late dusk (which includes a huge range of light intensities). In addition, light measurements are useful, either in human-defined IS units (lux or Candela), but possibly even in spectral data, specifically when working indoors, where light spectra often are completely different to natural spectra. For instance, does the light have a UV component or not? Chickens have different flicker fusion frequency with and without UV, and it is not known whether the same applies to pigeons.
2. The second part of this problem relates to the description of the background and predator dummy intensities. These are not given anywhere. The most relevant information would be a measurement (if these are reasonably close to the black-grey-white colour range this could be done with a candelameter that measures the light reflected from a defined area into a defined angle (Cd/m2) of the predator dummy and the background, from the direction of the pigeon. The contrast between these two measurements is telling you whether indeed the dark morph had lower contrast against the black background and the bright morph, against the white background. From the very nice sketch of the set-up, I am not sure this really is the case. It all depends on the illumination conditions, so it needs to be measured. It is important because it allows you to answer the question whether the the behavior of the pigeons did not differ, simply because contrasts were not different, or whether the contrasts really differed but the pigeons did not care.
Handheld instruments that can measure this are not very expensive and they are quite common. Terms like dark and bright are far too unspecific to be used in the context of such studies, unless they come with a measurement.
3. I am a bit disappointed that the authors missed a very similar case of colour dimorphism, in barn owls, which have a white and a dark morph as well. A lot of work has been done on that system, mostly by the group of Alexandre Roulin. A short discussion on this very similar case would bring a more general perspective to the problem and thus make this paper more interesting to general readers.
Other than these easily fixed points, I think the study is very solid.

08-Jul-2019
Dear Ms Nebel, I am pleased to inform you that your manuscript entitled "Response time of an avian prey to a simulated hawk attack is slower in darker conditions, but is independent of hawk colour morph" 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 (openscience_proofs@royalsociety.org and openscience@royalsociety.org) to let us know if you are likely to be away from e-mail contact. Due to rapid publication and an extremely tight schedule, if comments are not received, your paper may experience a delay in publication.
Royal Society Open Science operates under a continuous publication model (http://bit.ly/cpFAQ). Your article will be published straight into the next open issue and this will be the final version of the paper. As such, it can be cited immediately by other researchers. As the issue version of your paper will be the only version to be published I would advise you to check your proofs thoroughly as changes cannot be made once the paper is published. Comments to the Author(s) This interesting study investigates whether feral pigeons detect the dark or bright morph of the black sparrow hawk faster, under different conditions, and thus, whether earlier observed differences in hunting behavior and success of the two morphs may result from prey behavior. The study is mostly well-done and has clearly described results.
1.My main problem relates to terminology and measurements of light condition. No reader can have any idea what a "dull light condition" could mean. So here the reader needs to know the light intensity: The easiest way is to say whether this means light conditions on a cloudy day (5 to 100 times dimmer than a sunny day), in a light (10 x dimmer) or thick (upo to 1000 times dimmer) forest, or maybe early or late dusk (which includes a huge range of light intensities).
Thank you for raising this useful point. We have added the following sentence to make a comparison with everyday situation. This will hopefully make it easier for the reader to grasp and understand under which light conditions our experiment was carried out.

. In comparison to a real life situation, 112 lux would be comparable to the light during a very dark overcast day, i.e. as it is encountered in a thick forest or during the early or late hours of the day. The bright light situation, whilst considerably brighter, is comparable to an overcast day during noon. This maximum light intensity was limited by the luminance output of our lamps and the heat production. Our dullest light intensity was limited by the capabilities of our camera to record interpretable images (see Supplementary Material
In addition, light measurements are useful, either in human-defined IS units (lux or Candela), but possibly even in spectral data, specifically when working indoors, where light spectra often are completely different to natural spectra. For instance, does the light have a UV component or not? Chickens have different flicker fusion frequency with and without UV, and it is not known whether the same applies to pigeons.

Thank you for raising this interesting pointwe have now included this following text
The bulbs used were tungsten halogen incandescent lamps that produce a continuous spectrum of light, including near UV light (zeiss-campus.magnet.fsu.edu).
We also do provide information on the light intensities as SI unit (lux) for the dull and bright light level in the material and method part, see here: "We created two light treatments: "bright light", using four lamps on highest intensity (2182 ± 65 lux); and "dull light" with two dimmed lamps (112 ± 12 lux, Figure 1)." 2. The second part of this problem relates to the description of the background and predator dummy intensities. These are not given anywhere. The most relevant information would be a measurement (if these are reasonably close to the black-grey-white colour range this could be done with a candelameter that measures the light reflected from a defined area into a defined angle (Cd/m2) of the predator dummy and the background, from the direction of the pigeon. The contrast between these two measurements is telling you whether indeed the dark morph had lower contrast against the black background and the bright morph, against the white background. From the very nice sketch of the set-up, I am not sure this really is the case. It all depends on the illumination conditions, so it needs to be measured. It is important because it allows you to answer the question whether the the behavior of the pigeons did not differ, simply because contrasts were not different, or whether the contrasts really differed but the pigeons did not care.
Again, thank you for raising this interesting point.

To tackle this issue, we have measured the contrast between the hawk and the background on photos obtained directly from our video footage. The contrast ratio (relative luminance, L), based on the RGB colour space, shows that a light morph has less contrast in front of a white background and a dark morph in front of a black background. Contrary, light morphs show a higher contrast in front of a black background and dark morphs in front of a white background.
We have now added the following text to the main paper "We confirmed that the different hawk morphs were contrasting with the background colour by calculating the contrast ratio (relative luminance). For full details see Table S2 & Figure S3-S4." And we provide more information (see below) to the reader on the methods and results, in the supplementary. We hope this is to the satisfaction of the reviewer.

Contrast ratio between hawk morphs and backgrounds
We used the online tool based on the Web Content Accessibility Guidelines 2.0 (see contrastratio and WCAG10) to calculate the contrast ratio between the background and hawk colour in the RGB colour space, defined as the relative luminance (L). The highest ratio is obtained by plain black and plain white (L = 22) whereas a minimum score is reached by the same colours (L = 1). A high ratio therefore implies high colour contrast (and good visibility) whereas a low ratio indicates low colour contrast (better crypsis).
In our background experiment, we encounter two different light-background conditions: (1) low lightwhite background and (2) low lightblack background. In the light-change experiment, we encounter two different light-background conditions; we used (1) bright lightwhite background (2) low lightwhite background First, we evaluated the consistency in space and time of the background colouration. It showed a high consistency where the hawk first came into view, therefore we chose one pixel of the background colouration at the beginning of every trial video as the background colour.
Second, the contrast of the hawk against the background was measured at four fixed points: first, the breast (one pixel at the front, one in the back) and, second, the underwing coverts (left and right side). These four points are representing areas of high plumage colouration differences between the morphs. Here we expect to see the differences of the contrast ratio between morphs to show a difference with light and dark morphs having a high contrast ratio against a black or white background, respectively, and low contrast values where the colour of the hawk matches the colour of the background.  Figure S3).
No such effect was found for the light-change experimentwhere the background colour stayed the same and only the light condition was altered. The contrast ratio measurements show that the contrast is very high for the dark morph under bright light levels but evens out and becomes more similar to the contrast ratios of the light morph when the light level is decreased. No large drop of the contrast ratio is observed for the light morph, likely because the background colour and the colour of the hawk mount were similarly affected by a change of light conditions (Table  S2, Figure S4)." 3. I am a bit disappointed that the authors missed a very similar case of colour dimorphism, in barn owls, which have a white and a dark morph as well. A lot of work has been done on that system, mostly by the group of Alexandre Roulin. A short discussion on this very similar case would bring a more general perspective to the problem and thus make this paper more interesting to general readers.
We have now added text to the Introduction to introduce two study systems on colourpolymorphic owls (including the barn owl system studied by A. Roulin) to the reader and added this paragraph to the introduction: "Barn owl females (Tyto alba) show different habitat use, with reddish females occupying territories with less wooded areas compared to white females. In the tawny owl (Strix aluco) rufous birds occupied more wooded territories than grey birds, a pattern thought to be driven by crypsis advantages for the different morphs [22]." and to the discussion: "Despite finding for the black sparrowhawk that crypsis was neither morph-nor environmentallydependent, we still recommend similar experiments to be carried out in other study systems of colour-polymorphic raptors to identify the drivers of adaptive colour-polymorphism. For both barn and tawny owls, a difference in crypsis under varying environmental conditions is suspected [22,52,53], but has not been experimentally tested yet." Other than these easily fixed points, I think the study is very solid.
Thank you for your useful comments.