PCLM-D-25-00174

Predator response diversity to warming enables ecosystem resilience in the Galápagos

PLOS Climate

Dear Dr. Bruno,

Thank you for submitting your manuscript to PLOS Climate. After careful consideration, we feel that it has merit but does not fully meet PLOS Climate’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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PLOS Climate

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Climate’s publication criteria?>

Reviewer #1: Partly

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?-->?>

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English??>

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Review Report for “Predator response diversity to warming enables ecosystem resilience in the Galápagos”, submitted to PLoS Climate

General Comments

This manuscript investigates how thermal response diversity among predatory invertebrates can support the resilience of ecological functions under climate warming. The authors conducted a laboratory experiment with four marine predators from the Galápagos—three whelks and one sea star—and exposed them to a gradient of temperatures to evaluate their predatory performance. They found that two species showed performance declines under warming, while the other two—especially one whelk—maintained or improved their predation rates, even under temperatures expected by 2100. This suggests that variability in species’ thermal responses could help maintain key ecological functions, like predation, under climate change. I appreciate the authors’ effort to conduct this experiment in the Galápagos, especially given the potential logistical constraints. The interpretation of a relatively simple experimental design through the lens of broader ecological theory is commendable. However, the manuscript would benefit from more information on the ecological relevance of the chosen predator species, including their abundance and diet in the field, and how redundant or complementary their roles truly are. It is also unclear how well the experimental temperature ranges reflect natural conditions in the Galápagos. This is essential to establish the ecological validity of the findings. Furthermore, the methods need greater clarity to ensure reproducibility, especially regarding the experimental setup, replication, and temperature control. I also recommend that the authors consider incorporating a phylogenetic perspective into their discussion or analysis, given that species-level differences may partially reflect evolutionary divergence. Overall, I believe the manuscript has potential and offers an interesting perspective on ecosystem resilience but requires revision to clarify methods and strengthen ecological grounding. Please see my specific comments below.

Introduction

• Lines 53-58: “In contrast, even on the world’s most biodiverse coral reefs there is very little variation in thermal tolerance among species within functional groups such as the fast-growing and habitat providing acroporid corals [16]. Anthropogenic heatwaves only one or two degrees C above typical conditions can kill off hundreds of species within this and other functional groups of reef corals [17]. In this case species richness is a poor predictor of ecosystem resistance to warming, because although functional redundancy is very high (i.e., many species can fill the same functional role), response diversity is low.”

This discussion on low variation in thermal tolerance among species within functional groups such as Acroporid corals is appropriate and highlights an important point about the limits of species richness as a predictor of ecosystem resistance. However, this section could be strengthened by incorporating additional nuances. For example:

o Among habitat variation in thermal tolerance has been documented and could moderate the patterns discussed (e.g. https://www.nature.com/articles/srep17639)

o Functional redundancy may not be as high in regions already impacted by coral bleaching, especially where entire functional groups have been eroded: e.g. https://www.pnas.org/doi/abs/10.1073/pnas.1716643115 and https://www.nature.com/articles/s41586-018-0041-2

o Mortality is disproportionately higher in branching than massive corals, , which could skew the functional structure post-disturbance and further reduce resilience: e.g. https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.7808 and https://www.int-res.com/abstracts/meps/v434/meps09203

• The manuscript presents a solid theoretical framework but does not adequately justify the choice of study system or model organisms. The introduction would benefit from clearer arguments about why these species are ecologically relevant, how representative they are of broader functional dynamics, and why they serve as useful proxies for understanding ecosystem responses in other regions or systems.

Methods

• Please provide more detailed information on the experimental setup to ensure reproducibility. This should include the exact number of tanks, number of animals used per treatment, number of replicates for each condition, and how the centralized chiller system functioned across treatments. Clarifying these aspects is essential for readers to fully understand and replicate the experiment.

• If the predators were fed different prey species, it is unclear how their varied functional responses to temperature would collectively contribute to “maintaining a critical function.” For instance, if all predators that feed on barnacles exhibit similar and negative responses to warming, then barnacle predation as a function would likely decline regardless of overall predator response diversity. Please clarify how functional equivalence across prey types was considered.

• Lines 109–110: The manuscript mentions the use of a centralized chiller, which is partially illustrated in the supplementary figure. However, it is unclear whether this system connected all tanks or operated independently for each one. Additionally, it is important to explain what would happen if multiple tanks required simultaneous activation of the chiller. Please elaborate on how temperature control was achieved across treatments.

• Lines 115–118: The rationale behind the selected temperatures (as presented in Table 1) is unclear. Are these values based on field measurements? If so, please specify over what time period the field temperatures were recorded and under what environmental conditions (e.g., season, tidal phase). This information is crucial to assess the ecological relevance of the warming scenarios used in the experiment. Please clarify.

• Lines 125–126: The manuscript states that “one control aquarium was included for each temperature incubation,” but does not mention any control replicates. Please clarify whether control conditions were replicated and, more broadly, how many replicates were used for each treatment. Table 1 lists numbers, but it is not clear whether these refer to the number of tanks or the number of predators per treatment.

• Lines 130–131: The rationale for using 16 temperature levels is not explained. Where did these specific values come from? It would strengthen the manuscript to include a characterization of the natural thermal environment in the field and to justify how the chosen temperature treatments represent ecologically realistic current and future scenarios.

Results and Discussion

• Line 180: “We found a high degree of response diversity to acute warming.” This could be expected, given that the experiment involved species from different genera. Incorporating a phylogenetic perspective into the analysis would help determine whether the observed differences in thermal responses are phylogenetically structured (e.g. https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.2741). This could strengthen the ecological and evolutionary interpretation of the findings. Lines 205 and 206: “dependence of functional performance is related to (possibly mechanistically) species-specific metabolic sensitivity to temperature.” Therefore, accounting for the phylogenetic differences could be informative.

• Lines 208-210: “Our results suggest that, at least for these functions and species, the relative thermal sensitivity of metabolism is predictive of the relative sensitivity of the ecological functions species fulfill in communities (that are typically much more difficult to measure).” The authors claim that the relative thermal sensitivity of metabolism is predictive of the sensitivity of ecological functions, but this conclusion relies on the assumption that the selected species play key roles in their native ecosystems. While this is plausible, the manuscript lacks empirical support for their ecological importance. Please consider including evidence—either from the literature or field observations—that supports the choice of these species as relevant models to generalize about functional response diversity and its implications for ecosystem resilience

• The paragraph between lines 212–219, which discusses seasonal and diel temperature variability in the Galápagos, should be moved to the Methods section. It should also be expanded with quantitative data on natural temperature regimes across seasons, tidal cycles, and during extreme events such as El Niño. Since warming is central to the manuscript’s rationale and experimental design, providing evidence that the tested temperature range reflects ecologically relevant conditions is essential.

• A key result is that Hexaplex and Heliaster are predicted to lose their predatory roles under warming scenarios, while Tribulus and Vasula appear more thermally tolerant and may compensate. However, the manuscript lacks information on what these species feed on in the field and in what proportions. Without understanding their natural diets and functional equivalence, it is difficult to assess whether their differing responses to temperature can indeed buffer predation loss through compensatory dynamics. Please elaborate on this point and clarify to what extent these predators are redundant or complementary in their ecological roles.

Reviewer #2: This manuscript reports on a complementary set of laboratory assays on the (1) feeding rates and (2) respiration rates of 4 different ‘functionally equivalent’ invertebrate predators from a highly variable oceanographic region in the Galapagos Islands. The reported study aimed to test the idea that despite the functional redundancy (i.e., they all consume small crustaceans and molluscs) of the four predators, they may be ‘response diverse’ to ocean warming. This is an interesting and timely question. The Introduction is well-written, well-supported by relevant literature, and provides a broad context for the study. The study is simple and straightforward and is provides useful data from a part of the world that is underrepresented in climate science, despite the disproportionate effects of climate change it is experiencing. I have a couple of larger issues with two related aspects of the manuscript and some other, more minor issues, which I elaborate on below. However, after some revision, I think the study is worthy of publication and would appear to be a good fit for this particular venue.

One issue that should be dealt with is the issue of density of predators and prey in the experimental venues, particularly given that the prey species themselves differ among the focal predators. It’s mentioned that five snails were put in containers, but it is not indicated how many barnacles were present. It’s well known that predator density, prey density, and predator: prey ratio can influence the attack rates of predators and so it would strengthen the manuscript to have some justification for comparing consumption rate performance curves among predators fed different prey types and potentially also different prey densities. Further, were the densities of prey provided to the predator realistic (i.e., within the range of what predators would encounter in the field)? Again, some treatment of this potential issue would help strengthen the manuscript and allay any concerns by a reader.

Another important and related issue to address is how temperature may have affected the prey in the experimental venues, again given that different predators were offered different prey types. It is good that that the study included a treatment without predators to control for prey mortality and it is encouraging that the prey did not die in any temperature treatment. However, that does not mean that the prey weren’t negatively affected by any of the temperature treatments, especially in ways that may have affected their vulnerability to predators. For example, perhaps the barnacles were weaker, could not close their valves as tightly under warmer temps, or perhaps the snails were less mobile and less able to escape certain predators under warmer conditions. In short, under warmer, potentially stressful temperatures, prey may have been generally less well-defended and more susceptible to predators. This may be particularly problematic because some prey were different among predators, but also because the predators themselves were different and even though they are treated as ‘functionally redundant’ because they consume the same prey, they may hunt, attack, and consume prey differently (e.g., stars vs whelks) and so temperature effects on prey susceptibility could alter predator consumption differently among predators. I think this issue needs to be dealt with in a revision.

The respiration assays were done at 11 different temperatures, but the feeding assays were done at fewer temperatures. It’s not clear from the manuscript why the temperature treatments were not equalized across assays. They don’t necessarily need to be, but it would’ve had made for a nice 1:1 comparison between metabolism and functional traits. Perhaps the manuscript could provide some reasoning why fewer temperatures were used for the feeding experiments.

It’s not entirely clear from the manuscript as written, what the sample size for the respiration assays was. Was it n = 9 per temperature? In contrast, the manuscript provides a table with the sample sizes for the feeding assays. Please revise to make the sample size for the temperature treatments in the respiration assays explicit.

The study found a high degree of response diversity among their focal predators, which is an interesting finding, especially relative to the low response diversity one may find in reef building corals, e.g. I wonder if this finding could have been predicted given the highly variable oceanic conditions in Galapagos (in contrast to many tropical reef-building coral habitats). Further, is there anything about the distributions (e.g., vertical, or relative to upwelling regions etc.) of the focal species that could have been used to predict the thermal performance curve differences you observed? Might be worth touching on if there’s something there.

Lines 64-65 the phrase ‘Functional response diversity of complex ecological functions’ is a bit redundant. You can probably drop the first ‘functional’

Line 227 Please italicize genus names

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Reviewer #1: Yes:  Guilherme O. Longo

Reviewer #2: No

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Predator response diversity to warming enables ecosystem resilience in the Galápagos

PCLM-D-25-00174R1

Dear Dr. Bruno,

We are pleased to inform you that your manuscript 'Predator response diversity to warming enables ecosystem resilience in the Galápagos' has been provisionally accepted for publication in PLOS Climate.

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Best regards,

Jennifer Lee Wilkening, Ph.D

Academic Editor

PLOS Climate

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Additional Editor Comments (if provided):

The authors have submitted a substantially improved manuscript. Their responses to the previous comments are clear, thorough, and well substantiated, and the revised text reflects meaningful engagement with the feedback. Overall, the revisions address the earlier concerns and enhance both the scientific contribution and readability of the manuscript.

Reviewer Comments (if any, and for reference):