Unexpected spatial population ecology of a widespread terrestrial salamander near its southern range edge

Under the current amphibian biodiversity crisis, common species provide an opportunity to measure population dynamics across a wide range of environmental conditions while examining the processes that determine abundance and structure geographical ranges. Studying species at their range limits also provides a window for understanding the dynamics expected in future environments under increasing climate change and human modification. We quantified patterns of seasonal activity, density and space use in the eastern red-backed salamander (Plethodon cinereus) near its southern range edge and compare the spatial ecology of this population to previous findings from the core of their range. This southern population shows the expected phenology of surface activity based on temperature limitations in warmer climates, yet maintains unexpectedly high densities and large home ranges during the active season. Our study suggests that ecological factors known to strongly affect amphibian populations (e.g. warm temperature and forest fragmentation) do not necessarily constrain this southern population. Our study highlights the utility of studying a common amphibian as a model system for investigating population processes in environments under strong selective pressure.


Review form: Reviewer 2
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

Recommendation?
Accept with minor revision (please list in comments)

Comments to the Author(s)
This paper illustrates a small 2-year study on red-backed salamanders using spatial capturerecapture at a few sites located on the range edge of the species. The survey design and statistical approaches were excellent. The value of long-term and spatially replicated monitoring cannot be emphasized enough, and hopefully SPARCnet enables this work to continue (and expand).
My only criticism is that the narrative in the discussion tends to go a bit beyond the data and analysis provided. The paper is very well written and the material is interesting and relevant. Having season and site specific parameters makes for difficult interpretation when the mechanisms are not known (as the authors state on Line 249), but the general comparisons with other published estimates are compelling. The authors should consider keeping more focus on what was actually observed and estimated, and what it means. For example, the large season/year differences for sigma at site 1 that were not observed for sites 2 and 3. Are there ecological reasons site 1 would differ from sites 2 and 3? Finally, the site-year interactions and differences should not be treated as absolute evidence of ecological variation as there is no influence of sampling error.
Season is a confusing description here, as opposed to "session" or "year". When discussion of season 1 vs season 2 happens, it evokes phenological seasons when in reality the seasons are different years of sampling. Session is a common alternative if concerns about using "year" is that the closed sampling periods spanned multiple calendar years. Figure 4 is portraying site-year combinations as if they are independent sites (with an arbitrary "site" number on the x-axis). Are the NY and PA data also site-year combos? If the true comparison is between regions, maybe a mean (+SE) density per region is necessitated. Having all the estimates together is great but some of that variability is sampling error, not true ecological differences.
Minor comments: L73: It's not clear why anthropogenic disturbances and forest fragmentation would "play a role" in range edge dynamics. They make sense as referenced in L76 ("together with the combined effect of climate change and human modifications") as independent processes that interact with range edge processes. But range edges can occur anywhere, independent of human influences. Just needs some rephrasing here. L158: "captured" L172: Confusing to call an area measurement the buffer size. Better to list the buffer size and the resulting state space area. L177: Subscripted indices (and Greek letters) should be italicized (or not) to be consistent with text. Italics are commonly used for such notation. L178: The "e" here should probably be "exp", unless the function is a superscript: e^dist(x,s). L181: List the terms in the order they appear in the equation. L183: "…sigma is equivalent to space use" is awkward and vague. Sigma is the scale parameter of the half-normal distance function. The "implied model of space usage" is the distance function itself, not a single parameter. L185: Size is vague. "Area" is the intended metric.
L325: Maybe a figure of density vs. sigma would be enlightening? Hard to see how a "significant" relationship could be illustrated with only 2 data points (conceivably site1-year1 vs. site1-year2). I think it would be useful to include reference to Murray Efford's recent Ecography paper (2016) on density-dependence in home-range size, especially given the use of SCR modeling. https://doi.org/10.1111/ecog.01511 L348: "The variation of population parameters among sites and site-season interactions we report demonstrates the dynamic properties of southern populations of red-backed salamanders." Not sure such inferences can be supported from 6 data points.

24-Apr-2019
Dear Dr Hernández-Pacheco, The editors assigned to your paper ("Unexpected spatial population ecology of a widespread terrestrial salamander near its southern range edge") have now received comments from reviewers. We would like you to revise your paper in accordance with the referee and Associate Editor suggestions which can be found below (not including confidential reports to the Editor). Please note this decision does not guarantee eventual acceptance.
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Kind regards, Andrew Dunn Royal Society Open Science openscience@royalsociety.org on behalf of Professor Len Thomas (Associate Editor) and Kevin Padian (Subject Editor) openscience@royalsociety.org Associate Editor's comments (Professor Len Thomas): Associate Editor: 1 Comments to the Author: Both reviewers are pretty positive about your work. One reviewer recommends some largerscale editorial changes, particularly a shortening of the discussion section. Both reviewers note that you stray far from your actual findings and into the realm of speculation. I am therefore recommending major revision -please focus the paper, particularly the discussion, on what your data and analyses actually show. Please provide a point-by-point response showing what changes you have made to reviewers' comments.

Comments to Author:
Reviewers' Comments to Author: Reviewer: 1 Comments to the Author(s) The ecology of southern salamanders differs from northern salamanders. Using state of the art spatial capture-recapture methods, the authors show that densities and home ranges are different. Thus, this study makes an important contribution to the growing body of studies which document intraspecific variation among amphibian populations.
I like the methods and results sections but I don't like the introduction and discussion.

Comments on the introduction:
The hypothesis is that density and home range should vary spatially. I don't think that the reasons given why home ranges should vary spatially are convincing (there is not much on line 103 …). I think that home ranges should depend on resources such as food, refuges and mates. Why should it depend on the position within the species range? Is there a good theoretical justification for this hypothesis? Line 49. I think it would be better to cite some data papers which quantify declines rather than general reviews. For North American amphibians, the paper by Grant et al. 2016 in Scientific Reports would be a good choice. Line 61, 79. A nice example is the paper by Petrovan and Schmidt 2016 in Plos One. Line 66-67. Less favourable habitats regulate amphibian populations. Isn't that circular reasoning? How do you infer habitat suitability? Is habitat less suitable because abundance is lower? Anyway, I think the sentence would be better if you would avoid the term 'regulation'. Regulation has a specific meaning in population ecology (see Sinclair 2. Comments on the discussion: In my opinion, the discussion is too long. I think it should be shortened (50% is possible, I think; for example, I think the discussion of local adaptation is very speculative.) and focused on the key results. The result is that home ranges and densities are different from home ranges and densities elsewhere. That's an interesting result but a long discussion is not worthwhile if you cannot explain the causes. You would need a multi-site SCR study to test which factors affect density and home range size.
3. Other comments I think you should define 'density' precisely. You estimate the density of the salamander population that is present at the surface? You don't estimate 'superpopulation' size which would also include salamanders which are underground? Line 187. Only after initial capture or after every capture? Reference [24] is missing (it's the one on local extinction due to stochastic events). References 5 and 24 are identical.

Reviewer: 2
Comments to the Author(s) This paper illustrates a small 2-year study on red-backed salamanders using spatial capturerecapture at a few sites located on the range edge of the species. The survey design and statistical approaches were excellent. The value of long-term and spatially replicated monitoring cannot be emphasized enough, and hopefully SPARCnet enables this work to continue (and expand).
My only criticism is that the narrative in the discussion tends to go a bit beyond the data and analysis provided. The paper is very well written and the material is interesting and relevant. Having season and site specific parameters makes for difficult interpretation when the mechanisms are not known (as the authors state on Line 249), but the general comparisons with other published estimates are compelling. The authors should consider keeping more focus on what was actually observed and estimated, and what it means. For example, the large season/year differences for sigma at site 1 that were not observed for sites 2 and 3. Are there ecological reasons site 1 would differ from sites 2 and 3? Finally, the site-year interactions and differences should not be treated as absolute evidence of ecological variation as there is no influence of sampling error.
Season is a confusing description here, as opposed to "session" or "year". When discussion of season 1 vs season 2 happens, it evokes phenological seasons when in reality the seasons are different years of sampling. Session is a common alternative if concerns about using "year" is that the closed sampling periods spanned multiple calendar years. Figure 4 is portraying site-year combinations as if they are independent sites (with an arbitrary "site" number on the x-axis). Are the NY and PA data also site-year combos? If the true comparison is between regions, maybe a mean (+SE) density per region is necessitated. Having all the estimates together is great but some of that variability is sampling error, not true ecological differences.
Minor comments: L73: It's not clear why anthropogenic disturbances and forest fragmentation would "play a role" in range edge dynamics. They make sense as referenced in L76 ("together with the combined effect of climate change and human modifications") as independent processes that interact with range edge processes. But range edges can occur anywhere, independent of human influences. Just needs some rephrasing here. L158: "captured" L172: Confusing to call an area measurement the buffer size. Better to list the buffer size and the resulting state space area. L177: Subscripted indices (and Greek letters) should be italicized (or not) to be consistent with text. Italics are commonly used for such notation. L178: The "e" here should probably be "exp", unless the function is a superscript: e^dist(x,s). L181: List the terms in the order they appear in the equation. L183: "…sigma is equivalent to space use" is awkward and vague. Sigma is the scale parameter of the half-normal distance function. The "implied model of space usage" is the distance function itself, not a single parameter. L185: Size is vague. "Area" is the intended metric.
L325: Maybe a figure of density vs. sigma would be enlightening? Hard to see how a "significant" relationship could be illustrated with only 2 data points (conceivably site1-year1 vs. site1-year2). I think it would be useful to include reference to Murray Efford's recent Ecography paper (2016) on density-dependence in home-range size, especially given the use of SCR modeling. https://doi.org/10.1111/ecog.01511 L348: "The variation of population parameters among sites and site-season interactions we report demonstrates the dynamic properties of southern populations of red-backed salamanders." Not sure such inferences can be supported from 6 data points.

21-May-2019
Dear Dr Hernández-Pacheco, I am pleased to inform you that your manuscript entitled "Unexpected spatial population ecology of a widespread terrestrial salamander near its southern range edge" 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. Thank you so much for the positive evaluation and for the invitation to submit a revised version of the attached manuscript entitled "Unexpected spatial population ecology of a widespread terrestrial salamander near its southern range edge". We also like to thank the Associate Editor and the referees that helped improving significantly the manuscript by their excellent comments. We have addressed all the reviewers' comments and suggestions in this revised version and hope that it fulfills the standard for being published in Royal Society Open Science. We have also deposited all of our data and codes under the following temporary Dryad doi; doi.org/10.5061/dryad.4bq41sg.
Please, find our detailed answers to each comment below.

Sincerely, Raisa Hernandez Pacheco
Comments to Author: Reviewers' Comments to Author: Reviewer: 1 Comments to the Author(s) The ecology of southern salamanders differs from northern salamanders. Using state of the art spatial capture-recapture methods, the authors show that densities and home ranges are different. Thus, this study makes an important contribution to the growing body of studies which document intraspecific variation among amphibian populations. I like the methods and results sections but I don't like the introduction and discussion.

Comments on the introduction:
The hypothesis is that density and home range should vary spatially. I don't think that the reasons given why home ranges should vary spatially are convincing (there is not much on line 103 …). I think that home ranges should depend on resources such as food, refuges and mates. Why should it depend on the position within the species range? Is there a good theoretical justification for this hypothesis?
 We have added two citations supporting our hypothesis (Efford et al. 2016 andMuñoz et al. 2016). Given the expected relationship between resource availability and home range size, population density is hypothesized to have an inverse relationship with home range sizea hypothesis that has not been widely addressed in amphibians due to the lack of spatial capture recapture analyses. We now highlight this in Lines 96-98 of the revised version.