PONE-D-19-15791

Breeding range shift of the red-crowned crane (Grus japonensis) under climate change

PLOS ONE

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Bi-Song Yue, Ph.D

Academic Editor

PLOS ONE

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Partly

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Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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Reviewer #2: Yes

Reviewer #3: No

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Liu, Liao, Wu, and Zhang present an interesting and important study on how the breeding range of the red-crowned crane could shift under scenarios of future climate. I find that the manuscript is good overall and should be suitable for publication pending minor revision. The main points that I would like to see addressed follow:

1) Provide a clearer statement on which statistical downscale method is applied to future climate fields (I assume the delta method), and that the downscale is a derived product from the CCAFS GCM Data Portal (unless you ran the statistical downscaling?).

2) Provide some justification for choosing HadGEM2-ES instead of a multi-model ensemble mean, or some other individual model (e.g., CCSM4, CESM1). One or two sentences should suffice, ideally with a citation for a study that finds strong realism HadGEM2-ES.

3) Point 2 alludes to the caveat that different models produce different results. That said, it would be helpful to show the reader additional supplementary figures -- temperature and precipitation difference maps for HadGEM2-ES minus baseline modern climate for each of the RCPs (2.6, 4.5, 6.0, 8.5) at year 2100 CE. Annual anomalies will suffice (4 temperature anomaly and 4 precipitation anomaly maps). This will at least give the reader a visual depiction of how HadGEM2-ES projects future climate. I suspect the anomaly patterns will reinforce the importance of precipitation as mentioned in the results.

4) Please also see minor edits in the attached PDF.

Reviewer #2: The topic of how climate change may affect future potential distributions of species is a very important one, and the authors do well to explore this question for one of the 11 endangered species of cranes. Such an analyses has great value especially given the relatively large distribution of this particular species.

The questions I have relate entire to the modeling technique, and authors require to respond to all of these, and perhaps re-run some analyses to validate some of the responses.

While MAXENT is a great tool for this kind of work, there is a lot of emerging work that shows the default setting of the software to not be optimal. Since the settings and software as not fully explanatory, using MAXENT is in a sense using a blackbox with limited insight into how the final results are achieved. A vast majority of the evaluations make the point that independent models that were more parsimonious usually work much better than the more complex models that are run in MAXENT using a large number of variables.

Also, not being able to use spatially filtered records in this particular case has the potential of violating the model assumptions of representative sampling. Can the authors provide a sound explanation and reasoning for their methodology?

One final, and relatively minor comment is the use of variables many of which are known to be auto-correlated spatially. How do the authors think variable redundancy is affecting their outputs, and why should the final models presented in this manuscript be thought to be robust to variable redundancy?

Reviewer #3: This is an interesting and important study on a timely subject but the manuscript suffers from multiple factual errors, sub-standard writing, and a lack of sufficient, up-to-date citations. The authors’ bioclimatic niche models predict a northward shift of the breeding range of the red-crowned crane under climate change, from China into Russia. They point out that national conservation policies in China and Russia as well as Mongolia differ and currently do not consider the effects of climate change, and that the effects of climate change on the red-crowned crane, therefore, should be taken into consideration in conservation planning and international cooperation.

The range shift modeling appears sound to me, but should be validated by an expert in the modeling methods they used. Once these issues have been addressed, I would recommend publication in PLOS ONE because and the results are important and deserving of a wide audience. However, in order to be eligible for publication in PLOS ONE, the factual errors throughout must be corrected, new or updated citations should be added, and the body text thoroughly revised. In its current form, the manuscript is difficult to read and suffers from outdated or erroneous statements throughout that undermine its credibility.

Below I provide a partial list of some of the factual errors and discrepancies and suggested changes and updated citations. Currently the authors list 26 citations for the paper; this list should be augmented through a thorough, up-to-date use of authoritative scientific literature. Furthermore, I strongly recommend the manuscript be rewritten from beginning to end, ideally with assistance from a native or fluent English speaker, to correct many issues with incorrect grammar and unclear or confusing wording.

If the problems with errors, citations, and language are addressed I believe their findings should be considered for the PLOS ONE homepage because they represent significant impacts to biodiversity from human activity that should be highlighted. Specifically, range shifts under changing climate will necessitate changes to conservation planning and increased international collaboration for this and other endangered species threatened by climate change. As mentioned above, selected specific problems and suggestions appear below. Thank you for the opportunity to review this paper. I would be happy to review a revised draft.

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In line 51, the authors write “The red-crowned crane (Grus japonensis) is the largest and rarest crane in the world.” However, the authors do not provide a citation and according to the Handbook of Birds of the World, this species does not appear to be the tallest crane; both the Sarus Crane and Whooping Crane reach taller maximum heights (176 cm and 160 cm compared to Red-crowned Crane’s 152 cm).

This species is also not currently the rarest crane; the Whooping Crane is rarer with population of fewer than 600 individuals compared to Red-crowned Crane’s estimated 3000 individuals.

Archibald, G.W., Meine, C.D. & Garcia, E.F.J. (2019). Red-crowned Crane (Grus japonensis). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona: https://www.hbw.com/node/53564

Archibald, G.W., Meine, C.D. & Garcia, E.F.J. (2019). Sarus Crane (Antigone antigone). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona: https://www.hbw.com/node/53557

Archibald, G.W., Meine, C.D. & Garcia, E.F.J. (2019). Whooping Crane (Grus americana). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona: https://www.hbw.com/node/53562

Authors should consult HBW or other up-to-date, authoritative sources to back up their claims. They might rephrase their opening sentence as follows: “The red-crowned crane (Grus japonensis) is among the largest and rarest cranes in the world.”

In lines 54-55, the authors state “the range of this species contracted and its population declined greatly over last centuries, especially in recent years.” However, according to Archibald et al. (2019; cited in full above) their numbers were lower in the middle of the last century than in recent years, reaching lowest point in the 1950’s.

In line 57, the authors state the species is critical[ly] endangered as listed by the IUCN, citing the Russian Red Book; the authors should instead cite the IUCN authority directly, which is BirdLife International, where the latest listing shows this species as Endangered, not Critically Endangered: BirdLife International 2016. Grus japonensis. The IUCN Red List of Threatened Species 2016: e.T22692167A93339099. http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22692167A93339099.en

In lines 72-74, the authors write: “The anthropogenic habitat change, such as development of agriculture, urbanization, and conversion of wetland to human-built area, had caused great decline of the population and loss of habitats of the red-crowned crane in recent years.” The citation they provide, while authoritative, is from 1983; the authors should add to this citation with a more recent authoritative one. For example, Archibald et al. (2019), who write, “Loss and degradation of wetlands due to agricultural and industrial development constitute main threat to the species’ breeding areas… in the Sanjiang Plain in NE China, and Amur Basin in... SE Russia.”

Archibald et al. (2019) also cite Zhou et al. (2016), who suggest that wild cranes are harvested to supplement the captive-bred population in China, and that this activity is driving population declines:

Zhou, D. et al. (2016). A growing captive population erodes the wild Red-crowned Cranes (Grus japonensis) in China. Avian Research 7: 22

In line 76, the authors state "This species prefers to nesting in wetlands and rivers.”According to Archibald et al. (2019), however, this species nests in wetlands (including “reed, sedge and cat-tail marshes, and extensive bogs and wet meadows”) but not rivers, with nests built in relatively deep standing water. The authors should provide a citation for their statements on crane nesting ecology and I suggest removing the reference to nesting in rivers unless the authors can show clear documentation of this.

Likewise, in lines 78-79 the authors write “In the wintering range, the red-crowned crane prefers to inhabit in paddy fields, grassy tidal flats, and mudflats…” but do not mention that this species is known to winter at rivers, as described by Archibald et al. (2019). Again, I suggest checking their habitat statements against updated authoritative sources.

In lines 170-171, the authors state, “We used Maximum Entropy (MaxEnt) [10], which is the most popular and powerful modeling technique for predicting distribution of species [19].”Because there is no universal measure of “the most population and powerful modeling technique…”authors would better revise this to state to “a powerful, novel modeling technique…”

Later, in lines 420-421, the authors state “The population has been severely declined because of habitat modification, pollution and poaching.” The authors should provide citations for this statement. Habitat modification as a threat is supported by Archibald et al. (2019) but other references could be named; the authors should cite evidence of pollution as a threat to red-crowned cranes as well. Zhou et al. (2016), mentioned above, might be used to support the poaching statement; are there other publications that suggest or demonstrate poaching of red-crowned cranes? Archibald et al. (2019) mention other threats to this species include "overharvesting of wetland resources, human disturbance, intentional setting of fires in breeding areas, and poisoning."

In lines 422-424, the authors state, “Although the population was slightly increased after implementing the conservation policy made for this critical endangered species, and building protected area for it… such as Zhalong National Natural Reserve and Yancheng Biosphere Reserve…” Again, the authors need to back up such statements with evidence as provided in citations, and again, this species is not considered critically endangered but endangered by the IUCN. What conservation policies resulted in increases of this species and how was this measured? Where the protected areas mentioned created specifically for red-crowned cranes or were they one of several or many reasons for their creation?

In lines 451-454, the authors state, “The international collaboration among the three countries would increase the conservation effectiveness of this species, for instance, assisted movement of the red-crowned crane from China to Mongolia and Russia…”What do the authors mean by “assisted movement”? Translocation? I recommend taking such suggestions out of this paper unless there is well-documented support for them.

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

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Breeding range shift of the red-crowned crane (Grus japonensis) under climate change

PONE-D-19-15791R1

Dear Dr. Zhang,

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Bi-Song Yue, Ph.D

Academic Editor

PLOS ONE