Habitat fragmentation mediates the mechanisms underlying long-term climate-driven thermophilization in birds

Reviewer #1 (Public Review):

Summary:

This study reports on the thermophilization of bird communities in a network of islands with varying areas and isolation in China. Using data from 10 years of transect surveys, the authors show that warm-adapted species tend to gradually replace cold-adapted species, both in terms of abundance and occurrence. The observed trends in colonisations and extinctions are related to the respective area and isolation of islands, showing an effect of fragmentation on the process of thermophilization.

Strengths:

Although thermophilization of bird communities has been already reported in different contexts, it is rare that this process can be related to habitat fragmentation, despite the fact that it has been hypothesized for a long time that it could play an important role. This is made possible thanks to a really nice study system in which the construction of a dam has created this incredible Thousand Islands lake. Here, authors do not simply take observed presence-absence as granted and instead develop an ambitious hierarchical dynamic multi-species occupancy model. Moreover, they carefully interpret their results in light of their knowledge of the ecology of the species involved.

Weaknesses:

Despite the clarity of this paper on many aspects, I see a strong weakness in the authors' hypotheses, which obscures the interpretation of their results. Looking at Figure 1, and in many sentences of the text, a strong baseline hypothesis is that thermophilization occurs because of an increasing colonisation rate of warm-adapted species and extinction rate of cold-adapted species. However, there does not need to be a temporal trend! Any warm-adapted species that colonizes a site has a positive net effect on CTI; similarly, any cold-adapted species that goes extinct contributes to thermophilization.

Another potential weakness is that fragmentation is not clearly defined. Generally, fragmentation sensu lato involves both loss of habitat area and changes in the spatial structure of habitats (i.e. fragmentation per se). Here, both area and isolation are considered, which may be slightly confusing for the readers if not properly defined.

Reviewer #2 (Public Review):

Summary:

This study addresses whether bird community reassembly in time is related to climate change by modelling a widely used metric, the community temperature index (CTI). The authors first computed the temperature index of 60 breeding bird species thanks to distribution atlases and climatic maps, thus obtaining a measure of the species realized thermal niche.

These indices were aggregated at the community level, using 53 survey transects of 36 islands (repeated for 10 years) of the Thousand Islands Lake, eastern China. Any increment of this CTI (i.e. thermophilization) can thus be interpreted as a community reassembly caused by a change in climate conditions (given no confounding correlations).

The authors show thanks to a mix of Bayesian and frequentist mixed effect models to study an increment of CTI at the island level, driven by both extinction (or emigration) of cold-adapted species and colonization of newly adapted warm-adapted species. Less isolated islands displayed higher colonization and extinction rates, confirming that dispersal constraints (created by habitat fragmentation per se) on colonization and emigration are the main determinants of thermophilization. The authors also had the opportunity to test for habitat amount (here island size). They show that the lack of microclimatic buffering resulting from less forest amount (a claim backed by understory temperature data) exacerbated the rates of cold-adapted species extinction while fostering the establishment of warm-adapted species.

Overall these findings are important to range studies as they reveal the local change in affinity to the climate of species comprising communities while showing that the habitat fragmentation VS amount distinction is relevant when studying thermophilization. As is, the manuscript lacks a wider perspective about how these results can be fed into conservation biology, but would greatly benefit from it. Indeed, this study shows that in a fragmented reserve context, habitat amount is very important in explaining trends of loss of cold-adapted species, hinting that it may be strategic to prioritize large habitats to conserve such species. Areas of diverse size may act as stepping stones for species shifting range due to climate change, with small islands fostering the establishment of newly adapted warm-adapted species while large islands act as refugia for cold-adapted species. This study also shows that the removal of dispersal constraints with low isolation may help species relocate to the best suitable microclimate in a heterogenous reserve context.

Strength:

The strength of the study lies in its impressive dataset of bird resurveys, that cover 10 years of continued warming (as evidenced by weather data), 60 species in 36 islands of varying size and isolation, perfect for disentangling habitat fragmentation and habitat amount effects on communities. This distinction allows us to test very different processes mediating thermophilization; island area, linked to microclimatic buffering, explained rates for a variety of species. Dispersal constraints due to fragmentation were harder to detect but confirms that fragmentation does slow down thermophilization processes.

This study is a very good example of how the expected range shift at the biome scale of the species materializes in small fragmented regions. Specifically, the regional dynamics the authors show are analogous to what processes are expected at the trailing and colonizing edge of a shifting range: warmer and more connected places display the fastest turnover rates of community reassembly. The authors also successfully estimated extinction and colonization rates, allowing a more mechanistic understanding of CTI increment, being the product of two processes.

The authors showed that regional diversity and CTI computed only by occurrences do not respond in 10 years of warming, but that finer metrics (abundance-based, or individual islands considered) do respond. This highlights the need to consider a variety of case-specific metrics to address local or regional trends. Figure Appendix 2 is a much-appreciated visualization of the effect of different data sources on Species thermal Index (STI) calculation.

The methods are long and diverse, but they are documented enough so that an experienced user with the use of the provided R script can follow and reproduce them.

Weaknesses:

While the overall message of the paper is supported by data, the claims are not uniformly backed by the analysis. The trends of island-specific thermophilization are very credible (Figure 3), however, the variable nature of bird observations (partly compensated by an impressive number of resurveys) propagate a lot of errors in the estimation of species-specific trends in occupancy, abundance change, and the extinction and colonization rates. This materializes into a weak relationship between STI and their respective occupancy and abundance change trends (Figure 4a, Figure 5, respectively), showing that species do not uniformly contribute to the trend observed in Figure 3. This is further shown by the results presented in Figure 6, which present in my opinion the topical finding of the study. While a lot of species rates response to island areas are significant, the isolation effect on colonization and extinction rates can only be interpreted as a trend as only a few species have a significant effect. The actual effect on the occupancy change rates of species is hard to grasp, and this trend has a potentially low magnitude (see below).

While being well documented, the myriad of statistical methods used by the authors ampere the interpretation of the figure as the posterior mean presented in Figure 4b and Figure 6 needs to be transformed again by a logit-1 and fed into the equation of the respective model to make sense of. I suggest a rewording of the caption to limit its dependence on the method section for interpretation.

By using a broad estimate of the realized thermal niche, a common weakness of thermophilization studies is the inability to capture local adaptation in species' physiological or behavioral response to a rise in temperature. The authors however acknowledge this limitation and provide specific examples of how species ought to evade high temperatures in this study region.

Reviewer #3 (Public Review):

Summary:

Juan Liu et al. investigated the interplay between habitat fragmentation and climate-driven thermophilization in birds in an island system in China. They used extensive bird monitoring data (9 surveys per year per island) across 36 islands of varying size and isolation from the mainland covering 10 years. The authors use extensive modeling frameworks to test a general increase in the occurrence and abundance of warm-dwelling species and vice versa for cold-dwelling species using the widely used Community Temperature Index (CTI), as well as the relationship between island fragmentation in terms of island area and isolation from the mainland on extinction and colonization rates of cold- and warm-adapted species. They found that indeed there was thermophilization happening during the last 10 years, which was more pronounced for the CTI based on abundances and less clearly for the occurrence-based metric. Generally, the authors show that this is driven by an increased colonization rate of warm-dwelling and an increased extinction rate of cold-dwelling species. Interestingly, they unravel some of the mechanisms behind this dynamic by showing that warm-adapted species increased while cold-dwelling decreased more strongly on smaller islands, which is - according to the authors - due to lowered thermal buffering on smaller islands (which was supported by air temperature monitoring done during the study period on small and large islands). They argue, that the increased extinction rate of cold-adapted species could also be due to lowered habitat heterogeneity on smaller islands. With regards to island isolation, they show that also both thermophilization processes (increase of warm and decrease of cold-adapted species) were stronger on islands closer to the mainland, due to closer sources to species populations of either group on the mainland as compared to limited dispersal (i.e. range shift potential) in more isolated islands.

The conclusions drawn in this study are sound, and mostly well supported by the results. Only a few aspects leave open questions and could quite likely be further supported by the authors themselves thanks to their apparent extensive understanding of the study system.

Strengths:

The study questions and hypotheses are very well aligned with the methods used, ranging from field surveys to extensive modeling frameworks, as well as with the conclusions drawn from the results. The study addresses a complex question on the interplay between habitat fragmentation and climate-driven thermophilization which can naturally be affected by a multitude of additional factors than the ones included here. Nevertheless, the authors use a well-balanced method of simplifying this to the most important factors in question (CTI change, extinction, and colonization, together with habitat fragmentation metrics of isolation and island area). The interpretation of the results presents interesting mechanisms without being too bold on their findings and by providing important links to the existing literature as well as to additional data and analyses presented in the appendix.

Weaknesses:

The metric of island isolation based on the distance to the mainland seems a bit too oversimplified as in real life the study system rather represents an island network where the islands of different sizes are in varying distances to each other, such that smaller islands can potentially draw from the species pools from near-by larger islands too - rather than just from the mainland. Thus a more holistic network metric of isolation could have been applied or at least discussed for future research. The fact, that the authors did find a signal of island isolation does support their method, but the variation in responses to this metric could hint at a more complex pattern going on in real-life than was assumed for this study.
Further, the link between larger areas and higher habitat diversity or heterogeneity could be presented by providing evidence for this relationship. The authors do make a reference to a paper done in the same study system, but a more thorough presentation of it would strengthen this assumption further.

Despite the general clear patterns found in the paper, there were some idiosyncratic responses. Those could be due to a multitude of factors which could be discussed a bit better to inform future research using a similar study design.

Author response:

We would like to 1) response one comment from the public review, which is also related to the eLife assessment, and 2) give provisional author responses.

(1) Regarding the definition of the colonization-extinction rate, the first reviewer may misunderstand it: “However, there does not need to be a temporal trend! Any warm-adapted species that colonizes a site has a positive net effect on CTI; similarly, any cold-adapted species that goes extinct contributes to thermophilization.” We here clarify the definition:

In a single iteration of our MSOM (Multi-species occupancy model), the occupancy rate of species[n] in transect[i] from year[t-1] to year[t] is related to the colonization rate and extinction rate, and is defined as:
muz[n,i,t] = z[n,i,t-1]*(1-eps[n,i,t-1]) + (1-z[n,i,t-1])*gam[n,i,t-1], (also shown in Line411 in our MS).

If the colonization rate (gam) and extinction rate (eps) remain constant, the occupancy rate(muz) will be a constant number which is related to the state of real occupancy (0 or 1). The occupancy rate will only increase if colonization rate increases (or the extinction rate decreases). That is why we are considering the temporal trend in colonization/extinction rate.

(2) Provisional author responses:

We will revise and improve the manuscript according to the public reviews and mainly focus on:

(1) clarify the general definition of habitat fragmentation in the Introduction.

(2) provide a wider perspective about how our results can be applied to conservation biology in the Discussion.

(3) discuss the diversity of isolation metrics for future research and provide more evidence about the link between larger areas and higher habitat diversity or heterogeneity.