Range geographies, not functional traits, explain convergent range and phenology shifts under climate change
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Curated by eLife
eLife Assessment
This article presents valuable findings on the impact of climate change on odonates, integrating phenological and range shifts to broaden our understanding of biodiversity change. The study leverages extensive natural history data, offering a combined analysis of temporal trends in phenology and distribution and their potential drivers. The support for the findings is solid, though additional clarification regarding the methods and alternative sensitivity analyses could make the conclusions more convincing.
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Abstract
Climate change may introduce conditions beyond species’ tolerances; to survive, species must avoid these extremes. Phenological shifts are one strategy, as species move their activity or life history events in time to avoid extreme conditions. Species may also shift in space, moving their ranges poleward to escape extremes. However, whether species are more likely to exhibit one or both strategies, and whether this can be predicted based on a species’ functional traits, is unknown. Using a powerful macroecological dataset of European and North American odonate observations, we assessed range and phenology shifts between two time periods (1980-2002 and 2008-2018) to measure the strength and direction of the association between responses. Species with the greatest poleward range shifts also showed the largest phenological shifts toward earlier annual activity periods, with half of all species shifting in both space and time. This response was consistent across continents, despite highly divergent land use and biogeographical histories in these regions. Surprisingly, species’ range and phenology shifts were not related to functional traits; rather, southern species shifted their range limits more strongly, while increasing temperature variability hindered range shifts. By reducing risk through phenological shifts, the resulting larger populations may be more likely to disperse and expand species’ ranges. While species shifting in both space and time may be more resilient to extreme conditions, we identified a small number of species (approximately 10%) that failed to shift at all; these species are likely to be particularly vulnerable to climate change, and should be prioritized for conservation intervention.
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Author response:
Public Reviews:
Reviewer #1 (Public review):
Summary:
This study evaluates whether species can shift geographically, temporally, or both ways in response to climate change. It also teases out the relative importance of geographic context, temperature variability, and functional traits in predicting the shifts. The study system is large occurrence datasets for dragonflies and damselflies split between two time periods and two continents. Results indicate that more species exhibited both shifts than one or the other or neither, and that geographic context and temp variability were more influential than traits. The results have implications for future analyses (e.g. incorporating habitat availability) and for choosing winner and loser species under climate change. The methodology would be useful for other taxa and study …
Author response:
Public Reviews:
Reviewer #1 (Public review):
Summary:
This study evaluates whether species can shift geographically, temporally, or both ways in response to climate change. It also teases out the relative importance of geographic context, temperature variability, and functional traits in predicting the shifts. The study system is large occurrence datasets for dragonflies and damselflies split between two time periods and two continents. Results indicate that more species exhibited both shifts than one or the other or neither, and that geographic context and temp variability were more influential than traits. The results have implications for future analyses (e.g. incorporating habitat availability) and for choosing winner and loser species under climate change. The methodology would be useful for other taxa and study regions with strong community/citizen science and extensive occurrence data.
We thank Reviewer 1 for their time and expertise in reviewing our study. The suggestions are very helpful and will improve the quality of our manuscript.
Strengths:
This is an organized and well-written paper that builds on a popular topic and moves it forward. It has the right idea and approach, and the results are useful answers to the predictions and for conservation planning (i.e. identifying climate winners and losers). There is technical proficiency and analytical rigor driven by an understanding of the data and its limitations.
We thank Reviewer 1 for this assessment.
Weaknesses:
(1) The habitat classifications (Table S3) are often wrong. "Both" is overused. In North America, for example, Anax junius, Cordulia shurtleffii, Epitheca cynosura, Erythemis simplicicollis, Libellula pulchella, Pachydiplax longipennis, Pantala flavescens, Perithemis tenera, Ischnura posita, the Lestes species, and several Enallagma species are not lotic breeding. These species rarely occur let alone successfully reproduce at lotic sites. Other species are arguably "both", like Rhionaeschna multicolor which is mostly lentic. Not saying this would have altered the conclusions, but it may have exacerbated the weak trait effects.
We thank the reviewer for their expertise on this topic. We obtained these habitat classifications from field guides and trait databases, and we will review our primary sources to clarify the trait classifications. We will also reclassify the species according to the expertise of this reviewer and perform our analysis again.
(2) The conservative spatial resolution (100 x 100 km) limits the analysis to wide- ranging and generalist species. There's no rationale given, so not sure if this was by design or necessity, but it limits the number of analyzable species and potentially changes the inference.
It is really helpful to have the opportunity to contextualize study design decisions like this one, and we thank the reviewer for the query. Sampling intensity is always a meaningful issue in research conducted at this scale, and we addressed it head-on in this work.
Very small quadrats covering massive geographical areas will be critically and increasingly afflicted by sampling weaknesses, as well as creating a potentially large problem with pseudoreplication. There is no simple solution to this problem. It would be possible to create interpolated predictions of species’ distributions using Species Distribution Models, Joint Species Distribution Models, or various kinds of Occupancy Models. None of these approaches then leads to analyses that rely on directly observed patterns. Instead, they are extrapolations, and those extrapolations typically fail when tested, although they have still been tested (for example, papers by Lee-Yaw demonstrate that it is rare for SDMs to predict things well; occupancy models often perform less well than SDMs and do not capture how things change over time - Briscoe et al. 2021, Global Change Biology). The result of employing such techniques would certainly be to make all conclusions speculative, rather than directly observable.
Rather than employing extrapolative models, we relied on transparent techniques that are used successfully in the core macroecology literature that address spatial variation in sampling explicitly and simply. Moreover, we constructed extensive null models that show that range and phenology changes, respectively, are contrary to expectations that arise from sampling difference. 100km quadrats make for a reasonable “middle-ground” in terms of the effects of sampling, and we will add a reference to the methods section to clarify this.
(3) The objective includes a prediction about generalists vs specialists (L99-103) yet there is no further mention of this dichotomy in the abstract, methods, results, or discussion.
Thank you for pointing this out - it is an editing error that should have been resolved prior to submission. We will replace the terms specialist and generalist with specific predictions based on traits.
(4) Key references were overlooked or dismissed, like in the new edition of Dragonflies & Damselflies model organisms book, especially chapters 24 and 27.
We thank Reviewer 1 for making us aware of this excellent reference. We will review this text and include it as a reference, in addition to other references recommended by Reviewer 1 and other reviewers.
Reviewer #2 (Public review):
Summary:
This paper explores a highly interesting question regarding how species migration success relates to phenology shifts, and it finds a positive relationship. The findings are significant, and the strength of the evidence is solid. However, there are substantial issues with the writing, presentation, and analyses that need to be addressed. First, I disagree with the conclusion that species that don't migrate are "losers" - some species might not migrate simply because they have broad climatic niches and are less sensitive to climate change. Second, the results concerning species' southern range limits could provide valuable insights. These could be used to assess whether sampling bias has influenced the results. If species are truly migrating, we should observe northward shifts in their southern range limits. However, if this is an artifact of increased sampling over time, we would expect broader distributions both north and south. Finally, Figure 1 is missed panel B, which needs to be addressed.
We thank Reviewer 2 for their time and expertise in reviewing our study.
It is possible that some species with broad niches may not need to migrate, although in general failing to move with climate change is considered an indicator of “climate debt”, signaling that a species may be of concern for conservation (ex. Duchenne et al. 2021, Ecology Letters). We will revise the discussion to acknowledge potential differences in outcomes.
We used null models to test whether our results regarding range shifts were robust, and if they varied due to increased sampling over time. We found that observed northern range limit shifts are not consistent with expectations derived from changes in sampling intensity (Figure S1, S2).
We thank Reviewer 2 for pointing out this error in Figure 1. This conceptual figure was a challenge to construct, as it must illustrate how phenology and range shifts can occur simultaneously or uniquely to enable a hypothetic odonate to track its thermal niche over time. In a previous version of the figure, we had a second panel and we failed to remove the reference to that panel when we simplified the figure.
Reviewer #3 (Public review):
Summary:
In their article "Range geographies, not functional traits, explain convergent range and phenology shifts under climate change," the authors rigorously investigate the temporal shifts in odonate species and their potential predictors. Specifically, they examine whether species shift their geographic ranges poleward or alter their phenology to avoid extreme conditions. Leveraging opportunistic observations of European and North American odonates, they find that species showing significant range shifts also exhibited earlier phenological shifts. Considering a broad range of potential predictors, their results reveal that geographical factors, but not functional traits, are associated with these shifts.
We thank Reviewer 3 for their expertise and the time they spent reviewing our study. Their suggestions are very helpful and will improve the quality of our manuscript.
Strengths:
The article addresses an important topic in ecology and conservation that is particularly timely in the face of reports of substantial insect declines in North America and Europe over the past decades. Through data integration the authors leverage the rich natural history record for odonates, broadening the taxonomic scope of analyses of temporal trends in phenology and distribution to this taxon. The combination of phenological and range shifts in one framework presents an elegant way to reconcile previous findings improving our understanding of the drivers of biodiversity loss.
We thank Reviewer 3 for this assessment.
Weaknesses:
The introduction and discussion of the article would benefit from a stronger contextualization of recent studies on biological responses to climate change and the underpinning mechanism.
The presentation of the results (particularly in figures) should be improved to address the integrative character of the work and help readers extract the main results. While the writing of the article is generally good, particularly the captions and results contain many inconsistencies and lack important detail. With the multitude of the relationships that were tested (the influence of traits) the article needs more coherence.
We thank Reviewer 3 for these suggestions. We will revise the introduction and discussion to better contextualize species’ responses to climate change and the mechanisms behind them. We will carefully review all figures and captions, and we will make changes to improve the clarity of the text and the presentation of results.
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eLife Assessment
This article presents valuable findings on the impact of climate change on odonates, integrating phenological and range shifts to broaden our understanding of biodiversity change. The study leverages extensive natural history data, offering a combined analysis of temporal trends in phenology and distribution and their potential drivers. The support for the findings is solid, though additional clarification regarding the methods and alternative sensitivity analyses could make the conclusions more convincing.
-
Reviewer #1 (Public review):
Summary:
This study evaluates whether species can shift geographically, temporally, or both ways in response to climate change. It also teases out the relative importance of geographic context, temperature variability, and functional traits in predicting the shifts. The study system is large occurrence datasets for dragonflies and damselflies split between two time periods and two continents. Results indicate that more species exhibited both shifts than one or the other or neither, and that geographic context and temp variability were more influential than traits. The results have implications for future analyses (e.g. incorporating habitat availability) and for choosing winner and loser species under climate change. The methodology would be useful for other taxa and study regions with strong …
Reviewer #1 (Public review):
Summary:
This study evaluates whether species can shift geographically, temporally, or both ways in response to climate change. It also teases out the relative importance of geographic context, temperature variability, and functional traits in predicting the shifts. The study system is large occurrence datasets for dragonflies and damselflies split between two time periods and two continents. Results indicate that more species exhibited both shifts than one or the other or neither, and that geographic context and temp variability were more influential than traits. The results have implications for future analyses (e.g. incorporating habitat availability) and for choosing winner and loser species under climate change. The methodology would be useful for other taxa and study regions with strong community/citizen science and extensive occurrence data.
Strengths:
This is an organized and well-written paper that builds on a popular topic and moves it forward. It has the right idea and approach, and the results are useful answers to the predictions and for conservation planning (i.e. identifying climate winners and losers). There is technical proficiency and analytical rigor driven by an understanding of the data and its limitations.
Weaknesses:
(1) The habitat classifications (Table S3) are often wrong. "Both" is overused. In North America, for example, Anax junius, Cordulia shurtleffii, Epitheca cynosura, Erythemis simplicicollis, Libellula pulchella, Pachydiplax longipennis, Pantala flavescens, Perithemis tenera, Ischnura posita, the Lestes species, and several Enallagma species are not lotic breeding. These species rarely occur let alone successfully reproduce at lotic sites. Other species are arguably "both", like Rhionaeschna multicolor which is mostly lentic. Not saying this would have altered the conclusions, but it may have exacerbated the weak trait effects.
(2) The conservative spatial resolution (100 x 100 km) limits the analysis to wide-ranging and generalist species. There's no rationale given, so not sure if this was by design or necessity, but it limits the number of analyzable species and potentially changes the inference.
(3) The objective includes a prediction about generalists vs specialists (L99-103) yet there is no further mention of this dichotomy in the abstract, methods, results, or discussion.
(4) Key references were overlooked or dismissed, like in the new edition of Dragonflies & Damselflies model organisms book, especially chapters 24 and 27.
-
Reviewer #2 (Public review):
Summary:
This paper explores a highly interesting question regarding how species migration success relates to phenology shifts, and it finds a positive relationship. The findings are significant, and the strength of the evidence is solid. However, there are substantial issues with the writing, presentation, and analyses that need to be addressed. First, I disagree with the conclusion that species that don't migrate are "losers" - some species might not migrate simply because they have broad climatic niches and are less sensitive to climate change. Second, the results concerning species' southern range limits could provide valuable insights. These could be used to assess whether sampling bias has influenced the results. If species are truly migrating, we should observe northward shifts in their southern range …
Reviewer #2 (Public review):
Summary:
This paper explores a highly interesting question regarding how species migration success relates to phenology shifts, and it finds a positive relationship. The findings are significant, and the strength of the evidence is solid. However, there are substantial issues with the writing, presentation, and analyses that need to be addressed. First, I disagree with the conclusion that species that don't migrate are "losers" - some species might not migrate simply because they have broad climatic niches and are less sensitive to climate change. Second, the results concerning species' southern range limits could provide valuable insights. These could be used to assess whether sampling bias has influenced the results. If species are truly migrating, we should observe northward shifts in their southern range limits. However, if this is an artifact of increased sampling over time, we would expect broader distributions both north and south. Finally, Figure 1 is missed panel B, which needs to be addressed.
-
Reviewer #3 (Public review):
Summary:
In their article "Range geographies, not functional traits, explain convergent range and phenology shifts under climate change," the authors rigorously investigate the temporal shifts in odonate species and their potential predictors. Specifically, they examine whether species shift their geographic ranges poleward or alter their phenology to avoid extreme conditions. Leveraging opportunistic observations of European and North American odonates, they find that species showing significant range shifts also exhibited earlier phenological shifts. Considering a broad range of potential predictors, their results reveal that geographical factors, but not functional traits, are associated with these shifts.
Strengths:
The article addresses an important topic in ecology and conservation that is particularly …
Reviewer #3 (Public review):
Summary:
In their article "Range geographies, not functional traits, explain convergent range and phenology shifts under climate change," the authors rigorously investigate the temporal shifts in odonate species and their potential predictors. Specifically, they examine whether species shift their geographic ranges poleward or alter their phenology to avoid extreme conditions. Leveraging opportunistic observations of European and North American odonates, they find that species showing significant range shifts also exhibited earlier phenological shifts. Considering a broad range of potential predictors, their results reveal that geographical factors, but not functional traits, are associated with these shifts.
Strengths:
The article addresses an important topic in ecology and conservation that is particularly timely in the face of reports of substantial insect declines in North America and Europe over the past decades. Through data integration the authors leverage the rich natural history record for odonates, broadening the taxonomic scope of analyses of temporal trends in phenology and distribution to this taxon. The combination of phenological and range shifts in one framework presents an elegant way to reconcile previous findings improving our understanding of the drivers of biodiversity loss.
Weaknesses:
The introduction and discussion of the article would benefit from a stronger contextualization of recent studies on biological responses to climate change and the underpinning mechanism.
The presentation of the results (particularly in figures) should be improved to address the integrative character of the work and help readers extract the main results. While the writing of the article is generally good, particularly the captions and results contain many inconsistencies and lack important detail. With the multitude of the relationships that were tested (the influence of traits) the article needs more coherence.
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