Temperature alters the predator-prey size relationships and size-selectivity of Southern Ocean fish

Domain: earth_science
Published: 2024-05-10
Editorial outcome: minor_revision

Abstract
A primary response of many marine ectotherms to warming is a reduction in body size, to lower the metabolic costs associated with higher temperatures. The impact of such changes on ecosystem dynamics and stability will depend on the resulting changes to community size-structure, but few studies have investigated how temperature affects the relative size of predators and their prey in natural systems. We utilise >3700 prey size measurements from ten Southern Ocean lantern fish species sampled across >10° of latitude to investigate how temperature influences predator-prey size relationships and size-selective feeding. As temperature increased, we show that predators became closer in size to their prey, which was primarily associated with a decline in predator size and an increase in the relative abundance of intermediate-sized prey. The potential implications of these changes include reduced top-down control of prey populations and a reduction in the diversity of predator-prey interactions. Both of these factors could reduce the stability of community dynamics and ecosystem resistance to perturbations under ocean warming.

Introduction
Global warming represents a major threat to the structure and functioning of ecosystems. One possible consequence of rising temperatures is a decrease in body size across many species and communities1. At the individual level, warming alters the physiology of organisms and is likely to reduce body sizes within populations as organisms attempt to maintain metabolic functioning1,2. At the community level, warming may alter assembly processes through environmental filtering, competition, or trophic interactions, which may result in communities dominated by smaller-bodied species1,3. The subsequent impacts on population abundances and species interactions can drive changes to structure and function at the ecosystem scale4. Aquatic ectotherms such as fish are particularly susceptible to temperature-induced reductions in body size, due to the lower rates of oxygen diffusion in water and the energetic costs associated with maintaining water flow over surfaces5. Additionally, gape-limited feeding means that many fish species display ontogenetic changes in prey selection, with larger predators consuming larger, more energetically valuable prey6,7. Declines in prey size with warming may therefore reduce the rates of energy acquisition by larger predators, resulting in reduced fish growth and smaller overall body sizes within populations8. Furthermore, such altered prey size distributions may favour smaller-sized predator species, providing them with a competitive advantage and thereby shifting the fish community composition towards smaller body sizes9. Evidence from the last interglacial period suggests that fish communities experienced declining body size in response to warmer conditions10,11, and the average size of contemporary fish is expected to show a similar pattern under the current rate of global warming12. However, there is currently little understanding of how these changes will impact the structure and stability of marine ecosystems.

Body mass is a key life-history trait that determines factors such as consumption rates, handling times and gape size13,14. As such, body mass provides an important link between individual physiology and food web structure and is therefore often used to parameterise models of population dynamics and energy flow within ecosystems15,16. In the marine environment, predators are generally larger than their prey, and the predator-prey mass ratio (PPMR) is a good predictor of trophic interactions. For example, allometric diet breadth models accurately predict who eats who in aquatic ecosystems13, whilst declines in PPMR typically result in lower per capita interaction strengths as predators are able to gain the same amount of energy by consuming fewer large prey17. At the community level, larger ectotherms may decline in size more rapidly than smaller ectotherms with warming as a result of their reduced surface area to body mass ratio and the associated challenge of maintaining a higher metabolic rate5,18. This is particularly true for the marine environment, where larger fish and invertebrates display the strongest temperature-size responses19. If warming causes a greater decline in the size of ectotherm predators relative to that of their smaller prey (i.e. changes in community size structure), the average PPMR might decrease, with consequences for interaction strengths and thus energy flow through marine ecosystems.

The physiological basis for temperature effects on PPMR at the community level may be complicated by behavioural responses to environmental change. For example, predators may select for more nutritious (larger) prey in an effort to increase per capita energy intake under energetically stressful conditions, thus reducing their PPMR20,21. Alternatively, predators might feed in a more density-dependent manner, consuming a greater proportion of abundant but relatively smaller prey and thereby increasing PPMR. Importantly, behavioural responses are unlikely to be uniform across predator body sizes, given the different dietary niches of small and large organisms and their differential susceptibility to warming. Previous research has identified variable size-dependent relationships between PPMR and temperature, such that both systematic increases22 and decreases23 to per capita interaction strength are possible.

It is clear we still have limited understanding of how temperature-driven changes in body size may alter community-level feeding relationships, and it is vital to address this knowledge gap if we are to predict ecosystem responses to warming. This is particularly true for the Southern Ocean, which is experiencing widespread environmental changes including rapid regional warming in areas such as the western Antarctic Peninsula24 and northern Scotia Sea25. The Southern Ocean supports a diverse array of higher predator populations including seabirds, seals, penguins and whales, with a food web largely centred around krill (particularly Euphausia superba)26. However, it is expected that krill will shift their distribution southward in response to ocean warming27, with potentially drastic consequences for many regional predator populations unless other suitable prey are available28. Previous research has identified mesopelagic lantern fish (Family Myctophidae, hereafter myctophids) as one such potential alternative resource, due to their extremely high biomass and their role in supporting energy flow to higher predators including seals and penguins during periods of low krill availability29. Additionally, myctophids themselves are major generalist consumers of prey including krill, amphipods and copepods, and therefore exert significant influence over food web dynamics30. Myctophids are strongly size distributed in the Southern Ocean, with smaller species and individuals found at lower (warmer) latitudes31, and they display clear size-selectivity in their feeding32,33. Warming may therefore alter the size distribution of myctophids and the size relationships between these predators and their prey, and it is important that we understand what these likely changes will be in order to model ecosystem responses.

In this study, we assessed the relationship between temperature and the relative sizes of myctophids and their prey using a dataset of 1576 stomachs and 3707 prey size measurements from 10 myctophid species sampled across >10° of latitude in the Southern Ocean (Fig. 1). We hypothesised that myctophids would exhibit a decline in PPMR with increasing temperature, due to (1) a greater decrease in the size of these predators versus their prey, and/or (2) predators selecting for larger prey as temperature increases.

Results
PPMR declined by ~11% per °C increase in sea surface temperature (SST), associated with a significant decline in predator body size at a rate of ~6% per °C and no coherent trend in the mean body size of prey in the diet (Fig. 2 and Table 1). Chlorophyll a was initially used as a further explanatory variable but it was not significant in any model and was therefore excluded during model selection (Tables S1–S7). The same general results were found when temperature at ~1000 m (the estimated maximum of myctophid depth distributions) was considered instead of SST (Fig. S1 and Tables S8–S15). A similar decline in predator body size was also found when using a larger dataset of fish body masses (n=6143, the majority without stomach content data; Fig. S2 and Tables S16–S18). In all, 7 of the 10 myctophid species also displayed significant declines in size with increasing temperature (Fig. S3 and Tables S19–21). Together, these results suggest that the decline in PPMR is associated with a greater decrease in the size of these predators relative to their prey as temperature increases.

The effect of declining PPMR on interaction strengths will depend on the interactive effects of temperature and body mass on metabolism and consumption34, making it difficult to predict the consequences for ecosystem stability. It has previously been found that temperature alters the directionality and shape of the relationship between PPMR and predator attack rate and prey handling time, with low PPMR destabilising community dynamics under warming due to elevated predation rates at low prey density34. Additionally, when declines in body mass under warming are restricted to isolated trophic

Methods

Peer review rounds
[{"round": 1, "reviewer_comments": {"reviewer_1": "I very much enjoyed reading this manuscript, and find myself in the rather unusual position of having very few comments. My only substantive concern, detailed below, is that lack of information provided about spatial autocorrelation. Such information should absolutely be included in a revised manuscript, and ideally included in your mixed models.\nL41-67. Although I am personally a little sceptical of the mechanistic explanations proposed to explain observed size reductions, it is nonetheless quite clear that such declines are occurring. And so I very much enjoyed reading this introduction, which nicely links the side-dependence of size declines with the use of predator-prey mass ratios as indicators of trophic interactions, and then to ecosystem function. Nice work.\nFigure 1. My first impression when viewing this figure is that there is likely to be significant spatial autocorrelation in the data, which has the potential to significantly undermine your conclusions. I was therefore very pleased to see that you considered spatial autocorrelation in the data (L322). However, I was then disappointed that I cannot find any information about these analyses in the main text or supplementary information to reassure the reader. I apologise if I have missed this somehow, but I think that it will be important to present this information in a revised manuscript (and ideally you would account for the presence of spatial autocorrelation in your mixed models).", "reviewer_2": "The study is carefully designed and the manuscript well written. I like how authors have combined predator and prey observations with the sampling of potential prey in the field. The subject is timely and impactful and helps to better understand the effects of temperature on community structure and biotic interactions. The outcomes demonstrate the effects of temperature after environmental and biotic filters have shaped the community. This, in my view, makes the work very informative for projecting the long-term effects of warming.\nMy primary concern is the emphasis on temperature effects on physiology and body size that authors have used to contextualize the paper. However, this paper examines the body size effects of temperature on the myctophid community. Hence, declines in body size can both be driven by changes in body sizes due to a physiological temperature effect on species, as well as community assembly processes that select differently sized species along the temperature gradient.\nIn my view, all observed outcomes can also be interpreted through the lens of community assembly, without necessarily considering potential physiological temperature effects on body size. For instance, there is a noticeable absence of zooplankton between -2 and 0 log10 gram in the warmer waters (Fig 3B). This absence forces large fish to feed on relatively small prey (Fig 3A and indicated in lines 201-202). Consequently, the larger fish are outcompeted by smaller ones in warmer waters, which can be expected when both small and large fish target the same small size prey (as shown in the right part of Fig 3A). As a result, assembly processes favor small fish in warm waters and shift the size distribution of the myctophid community towards smaller body sizes (Fig 2B).\nImportantly, this alternative narrative is not intended as a criticism of the current line of thinking but aims to encourage the authors to consider a different, non-physiological, explanation for the observed patterns. The above line of reasoning also introduces some uncertainties to two results of the manuscript:\n• the decline in size preference in large fish (Fig 3A) could be driven by the absence of large prey in the environment, instead of, as stated in the manuscript, large predators preferring smaller prey in warm waters (lines 172-173),\n• the temperature-size response of fish can solely be explained through a zooplankton community shift with temperature that, through assembly processes, selects for smaller sized myctophids. This contradicts the statement that there is a stronger temperature-size response among the myctophid predators than their smaller prey (line 118 and 155-156).\nI would recommend that the authors leverage the community perspective and emphasize the distinction between individual/species and community-level processes in their interpretation of the results. This may only need some re-writing of the manuscript. Possibly, authors may be able to uncover the relative importance of the two processes (selection of different species by community assembly along the temperature gradient versus body size shifts with temperature in species). Authors should have information on the species composition in warm and cold waters. In addition, authors may be able to use the information from two co-authors (Saunders and Tarling, Bergmann’s rule paper) to estimate the expected decline in body size with temperature within each species. However, this analysis is not essential for the paper.\n--- minor comments ---\n1) Initially, I was worried that there was too strong a focus on temperature without testing any other potential factors that may affect predator and prey size. It might be good to mention in the result section that the effects of CHL-A were insignificant (it is now only stated at the end of the paper). It might also be good to mention that fishing intensity is low (is it?) as fishing could have a much stronger effect on body size than temperature.\n2) My suggestion would be to avoid stating that there is a stronger temperature-size response among the myctophid predators than their smaller prey and mainly discuss that this is a likely explanation of the observed patterns.\nAuthors make this statement already in line 118 and 155-156, while the available evidence for such a statement is limited at that stage. The observations of prey only consist of the selected prey that are in the stomach, and these do not reflect the size distribution of the “prey” populations in the field. The prey populations could still have a strong temperature-size response.\nOnly after seeing the dashed lines in Fig 3B (lines 168-176), there is some evidence that the temperature-size response is small on the prey (i.e. average size of prey is unchanged with temperature). Nonetheless, there still seems to be a clear decline in the 5 to 10% largest zooplankton with temperature in Fig 3B.\n3) Lines 261-268: were all stations sampled in all three surveys (and seasons/years)? I expect this is the case but please make it explicit. If all warm water communities were sampled in a specific season/year, this could generate a bias that might not be accounted for with the random effect.\n4) The mean prey size in the stomach is in some sampling stations >0.1 gram (Fig 2C), whereas the body mass distributions of zooplankton in the environment tend to be smaller (Fig 3B). Did authors obtain samples where the prey size in the stomach was not observed in the environment? How did authors estimate size preference in that case?"}, "author_response": "Reviewer # 1:\nI very much enjoyed reading this manuscript, and find myself in the rather unusual\nposition of having very few comments. My only substantive concern, detailed below, is\nthat lack of information provided about spatial autocorrelation. Such information\nshould absolutely be included in a revised manuscript, and ideally included in your\nmixed models.\nResponse #1: Many thanks for your very positive feedback on our manuscript, and for the\nhelpful comment regarding the need to provide more detail on spatial autocorrelation (this is\naddressed in response #3).\nL41-67. Although I am personally a little sceptical of the mechanistic explanations\nproposed to explain observed size reductions, it is nonetheless quite clear that such\ndeclines are occurring. And so I very much enjoyed reading this introduction, which\nnicely links the side-dependence of size declines with the use of predator-prey mass\nratios as indicators of trophic interactions, and then to ecosystem function. Nice work.\nResponse #2: Thank you. In response to Reviewer #2, we have broadened our discussion of\nthe possible mechanisms underlying temperature-driven shifts in myctophid community size\nstructure to include assembly processes in addition to our original focus on physiological\nmechanisms. We hope that this reduces any scepticism you felt regarding the original draft.\nFigure 1. My first impression when viewing this figure is that there is likely to be\nsignificant spatial autocorrelation in the data, which has the potential to significantly\nundermine your conclusions. I was therefore very pleased to see that you considered\nspatial autocorrelation in the data (L322). However, I was then disappointed that I\ncannot find any information about these analyses in the main text or supplementary\ninformation to reassure the reader. I apologise if I have missed this somehow, but I think\nthat it will be important to present this information in a revised manuscript (and ideally\nyou would account for the presence of spatial autocorrelation in your mixed models).\nResponse #3: We have improved the clarity of the statement in the methods regarding the use\nof Moran’s I test to make it clearer that we found no significant evidence of spatial\nautocorrelation in our predator-prey size models (Ln 370-372). We have also added tables to\nthe supplementary information providing an overview of the Moran’s I estimates and p-\nvalues for each of the selected model structures (Tables S7, S15, S17, S20, S23). We only\nfind evidence of significant spatial autocorrelation in new species-level analyses of\nmyctophid body mass which we performed to address a concern by Reviewer #2 (cf.\nResponse #5), but we now provide the spatial autocorrelation structure implemented in all the\nrelevant models (e.g. see Table S20 which we include below as an example of the new clarity\non spatial autocorrelation analyses). Note that we have also updated all the statistical outputs\nin the manuscript with outputs from models fitted with ‘method = REML’ rather than our\noriginal use of ‘method = ML’, to match the recommendations of Zuur et al. (2009). Changes\nto resulting statistical outputs are extremely minor and there is no qualitative change to any of\nthe results in the original manuscript.\nZuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. and Smith, G.M.. Mixed effects models\nand extensions in ecology with R (Vol. 574, p. 574). New York: springer. (2009).\nLn 370-372: The absence of spatial autocorrelation in model residuals was confirmed using\nMoran’s I (Table S7), therefore autocorrelation structures were not included in the models.\nTable S20: Identification of the optimal fixed effects structure for the models involving\npredator mass for each myctophid species. Thetable shows the fixed effects structures for the\nlinear modelsof the relationship between predator size and sea-surface temperature (SST) for\neach species, using a larger dataset of myctophid body sizes (n = 6,143). Each model includes\nthe optimal random effects and variance weighting structure identified in Table S19. The most\nparsimonious model based on Akaike’s Information Criterion (AIC) and retaining only\nsignificant fixed effects is highlighted in bold. The results of a Moran’s I test for spatial\nautocorrelation are provided for the optimal models, along with the optimal correlation\nstructure implemented based on AIC for any models with significant autocorrelation.\nSpecies Fixed effects AIC Moran’s I P-value Autocorrelation\nstructure structure\nSST -1340.507\nE. carlsbergi\nNull -1342.335 <0.001 0.717\nSST 1542.642 0.026 <0.001 Rational\nE. antarctica\nNull 1569.967\nSST 34.019 0.060 0.004 Exponential\nG. fraseri\nNull 68.081\nSST 55.946 0.004 0.689\nG. nicholsi\nNull 71.849\nSST 1356.068 0.009 0.017 Exponential\nG. braueri\nNull 1366.125\nSST 824.964 -0.010 0.034 Spherical\nK. anderssoni\nNull 1001.208\nSST -72.145\nN. achirus\nNull -73.502 -0.104 0.091\nSST -469.989 -0.004 0.950\nP. tenisoni\nNull -442.164\nSST -83.925 -0.013 0.094\nP. bolini\nNull -76.457\nSST -93.411 -0.021 0.925\nP. choriodon\nNull -78.834\nReviewer # 2:\nThe study is carefully designed and the manuscript well written. I like how authors have\ncombined predator and prey observations with the sampling of potential prey in the\nfield. The subject is timely and impactful and helps to better understand the effects of\ntemperature on community structure and biotic interactions. The outcomes\ndemonstrate the effects of temperature after environmental and biotic filters have\nshaped the community. This, in my view, makes the work very informative for\nprojecting the long-term effects of warming.\nResponse #4: Thank you very much for your overall endorsement of our work.\nMy primary concern is the emphasis on temperature effects on physiology and body size\nthat authors have used to contextualize the paper. However, this paper examines the\nbody size effects of temperature on the myctophid community. Hence, declines in body\nsize can both be driven by changes in body sizes due to a physiological temperature\neffect on species, as well as community assembly processes that select differently sized\nspecies along the temperature gradient.\nResponse #5: We agree that it is important to recognize the potential for community-level\nprocesses to influence the observed relationships and to provide a more balanced appraisal of\nthe physiological (population-level) and environmental filtering (community-level)\nmechanisms. To tackle this, we have revised the introduction to include an overview of how\ntemperature-mediated community-assembly processes could result in declines in body size\nwith temperature at the community level (Ln 43-45 & Ln 53-56).\nWe have also conducted new analyses to explore the possibility that community assembly\nprocesses are driving the observed changes in predator size with temperature (i.e. through\nchanges in species composition). This involved the use of a larger dataset of myctophid body\nmasses containing length measurements for 6,143 individuals of the ten species investigated\nhere (only 1,576 of these were originally kept for stomach content analyses and that subset\ntherefore underlies our core analyses for Figure 2 in the main text). This larger dataset\nincludes a local density estimate of each species for every haul and is therefore useful for\ndemonstrating an increase in myctophid community diversity with temperature, as larger\nspecies become less dominant in warmer regions (Figure S4; Tables S22-S24), supporting the\npossibility that community assembly processes are contributing to the results e.g. the higher\ntemperatures and shift in prey size distributions favours smaller predators. We also confirm\nthe previously reported decline in predator body mass at the myctophid community level\n(Figure 2b) with this larger dataset (Ln 128-130; Figure S2; Tables S16-S18), and\ndemonstrate that seven of the ten myctophid species display a decline in size with increasing\ntemperature (Ln 130-131; Figure S3; Tables S19-S21), which supports the possibility that\nphysiological processes (i.e. population-level) are contributing to our results. We provide an\noverview of these new analyses in the methods section (Ln 405-423) and discuss how both\ncommunity assembly processes and individual physiology may play a role in driving the\nobserved trends in PPMR and predator body mass with temperature (Ln 172-186 & Ln 237-\n245).\nLn 43-45: At the community level, warming may alter assembly processes through\nenvironmental filtering, competition, or trophic interactions, which may result in communities\ndominated by smaller-bodied species.\nLn 53-56: Furthermore, such altered prey size distributions may favour smaller-sized\npredator species, providing them with a competitive advantage and thereby shifting the fish\ncommunity composition towards smaller body sizes.\nLn 128-130: A similar decline in predator body size was also found when using a larger\ndataset of fish body masses (n = 6,143, the majority without stomach content data; Figure S2,\nTables S16-S18).\nLn 130-131: Seven of the ten myctophid species also displayed significant declines in size\nwith increasing temperature (Figure S3, Tables S19-21 ).\nLn 172-186: There was a significant increase in Shannon diversity of the myctophid\ncommunity with increasing SST, driven by a shift in species abundances from communities\ndominated by a few large-bodied species (e.g. E. antarctica) at cold high latitudes to a more\neven distribution of abundances in the more northerly warmer regions (Figure S4, Tables\nS22-24), as previously documented40. This indicates that the link between temperature and\nbody size at the community level may be driven in part by community assembly processes\nwhich select for species of different sizes as it becomes warmer, e.g. smaller predators are\nable to outcompete larger ones under the altered prey size distribution and relatively lower\nmetabolic demands. However, our analyses of the relationship between body mass and SST at\nthe population level also revealed significant declines in size with increasing temperature for\nmany of the myctophid species, both for large-bodied taxa such as E. antarctica and for small\nspecies like K. anderssoni (Figure S3, Tables S19-21). The observed trends at the community\nlevel therefore are not explained by community assembly processes alone, but also by\ntemperature effects on populations, likely mediated by physiological responses to warming.\nLn 237-245: These changes in size-selectivity may also explain the increasing prevalence of\nsmaller myctophid species in warmer regions (Figure S4), as they can capitalise on the\navailable prey field and outcompete their larger counterparts. The increasing dominance of\nsmaller myctophids, which feed preferentially on larger prey in warmer regions, is likely to\ndrive the observed decline in overall PPMR across the predator community. Thus, we suggest\nthat the observed patterns in myctophid size and foraging with temperature are likely to be\nthe result of a combination of interacting processes acting at both the population and\ncommunity levels, and we encourage further efforts to disentangle them.\nLn 405-423: To differentiate the potential individual-level and community-level mechanisms\nunderlying trends in body size with temperature, we also conducted analyses of predator body\nsize and community composition using a larger dataset of individual body sizes and species\nabundance estimates (n = 6,143). We fitted a Generalised Least Squares (GLS) regression\nmodel of species diversity (Shannon–Wiener (log e) diversity index) as a function of SST and\nChl-a to investigate whether there was any change in community structure with\nenvironmental conditions. For this analysis, densities of each species caught during each\nhaul were estimated by multiplying counts by the product of the distance towed multiplied by\nthe nominal net mouth area (25 m2), and then standardised to values of individuals per 1,000\nm-3. A square-root transformation was then applied to the density estimates to reduce the\nweighting of dominant species. An LMM was fitted to the relationship between body mass and\nthe interaction between SST and Chl-a at the community level, before linear models of body\nsize and SST were fitted for each predator species individually, to identify whether\ncommunity-level trends in size with temperature were present at the population level. The\noptimal model structure for each species-level analysis varied, and very low but statistically\nsignificant levels of spatial autocorrelation were identified for a small number of species and\ndealt with by incorporating spatial autocorrelation functions. See Tables S16-S24 for model\nselection of the optimal variance weighting, random and fixed effects structures, Moran’s I\ntest results and implemented autocorrelation structures, and model outputs.\nIn my view, all observed outcomes can also be interpreted through the lens of\ncommunity assembly, without necessarily considering potential physiological\ntemperature effects on body size. For instance, there is a noticeable absence of\nzooplankton between -2 and 0 log10 gram in the warmer waters (Fig 3B). This absence\nforces large fish to feed on relatively small prey (Fig 3A and indicated in lines 201-202).\nConsequently, the larger fish are outcompeted by smaller ones in warmer waters, which\ncan be expected when both small and large fish target the same small size prey (as\nshown in the right part of Fig 3A). As a result, assembly processes favor small fish in\nwarm waters and shift the size distribution of the myctophid community towards\nsmaller body sizes (Fig 2B).\nResponse #6: We agree that, as you suggest, the decline in zooplankton size distribution in\nwarmer waters could indeed alter competitive dynamics between large and small predators,\nleading to a greater proportion of small-bodied species (though body sizes between -2 and 0\nlog10 g are still present, if rare, in warmer regions – see Response #13). Our new analysis of\nmyctophid community composition provides some support for this mechanism, though our\nnew species-level analyses suggest that physiological processes are also contributing, and we\nthus discuss both as likely mechanisms driving the observed trends (see Response #5).\nImportantly, this alternative narrative is not intended as a criticism of the current line\nof thinking but aims to encourage the authors to consider a different, non-physiological,\nexplanation for the observed patterns. The above line of reasoning also introduces some\nuncertainties to two results of the manuscript:\n• the decline in size preference in large fish (Fig 3A) could be driven by the absence of\nlarge prey in the environment, instead of, as stated in the manuscript, large predators\npreferring smaller prey in warm waters (lines 172-173)\nResponse #7: We agree that the likely explanation for the decline in size preference for large\npredators is that larger prey become so scarce that the predators are forced to feed on smaller\nprey. This was the intended explanation in the original draft, but we acknowledge that our\nwording did not make this clear. We have adjusted our discussion of the changes in size\nselectivity to emphasise that large predators are forced to feed on smaller prey under warmer\nconditions (Ln 228-232).\nLn 228-232: Under warmer conditions, the shift in the distribution of suitable prey sizes\ntowards intermediate body masses restricts the feeding behaviour of large predators and\nforces them to feed sub-optimally on smaller prey while small predators actively select for\nthese abundant intermediate prey sizes, possibly because they provide greater per capita\nenergy intake.\n• the temperature-size response of fish can solely be explained through a zooplankton\ncommunity shift with temperature that, through assembly processes, selects for smaller\nsized myctophids. This contradicts the statement that there is a stronger temperature-\nsize response among the myctophid predators than their smaller prey (line 118 and 155-\n156).\nResponse #8: Our new analyses (Response #5) provide some support for assembly processes\nselecting for smaller myctophids but also suggest that physiological mechanisms are acting at\nthe population-level to drive a decline in the body size of individuals within most species.\nBased on your minor comment 2, we have adjusted the text to make our statements about\nrelative changes to predator and prey body sizes a description of the likely driver of the\nobserved trends (see Response #11).\nI would recommend that the authors leverage the community perspective and\nemphasize the distinction between individual/species and community-level processes in\ntheir interpretation of the results. This may only need some re-writing of the\nmanuscript. Possibly, authors may be able to uncover the relative importance of the two\nprocesses (selection of different species by community assembly along the temperature\ngradient versus body size shifts with temperature in species). Authors should have\ninformation on the species composition in warm and cold waters. In addition, authors\nmay be able to use the information from two co-authors (Saunders and Tarling,\nBergmann’s rule paper) to estimate the expected decline in body size with temperature\nwithin each species. However, this analysis is not essential for the paper.\nResponse #9: Thanks for this suggestion, which guided the new analyses (see Response #5)\nand helped to strengthen the manuscript.\nMinor comments\n1). Initially, I was worried that there was too strong a focus on temperature without\ntesting any other potential factors that may affect predator and prey size. It might be\ngood to mention in the result section that the effects of CHL-A were insignificant (it is\nnow only stated at the end of the paper). It might also be good to mention that fishing\nintensity is low (is it?) as fishing could have a much stronger effect on body size than\ntemperature.\nResponse #10: We have added a statement to the results to clarify that Chl-a was not a\nsignificant predictor in our models (Ln 124-126). We have also provided an explanation in\nthe methods section for the omission of fishing effort as a predictor in our models (Ln 349-\n356).\nLn 124-126: Chlorophyll a was initially used as a further explanatory variable but it was not\nsignificant in any model and was therefore excluded during model selection (Tables S1-S7).\nLn 349-356: We did not consider the effects of spatial heterogeneity in fishing effort as there is\ncurrently no targeted myctophid fishery in the Southern Ocean. Fish constitute the majority of\nbycatch by the winter krill fishery in the Scotia Sea but appear to consist predominantly of\nmembers of the Channichthyidae and Nototheniidae. Overall annual average bycatch weights\nacross all bycatch taxa (0.1-51.3 tonnes) are low compared to the estimated biomass of\nmesopelagic fish in the Scotia Sea (~4.5 million tonnes) and would therefore be expected to\nhave negligible impact on community structure.\n2). My suggestion would be to avoid stating that there is a stronger temperature-size\nresponse among the myctophid predators than their smaller prey and mainly discuss\nthat this is a likely explanation of the observed patterns.\nResponse #11: We have adjusted statements to put forward the idea of a greater decline in\npredator size relative to prey as a potential explanation for the observed trends in PPMR,\nrather than a statement of fact (Ln 131-133). We have also removed the statement that greater\noxygen limitation in larger than smaller organisms drives a stronger temperature-size\nresponse in the predator community than their prey (Ln 153-156 of the original manuscript),\ngiven your comments and our new discussion.\nLn 131-133: Together, these results suggest that the decline in PPMR is driven by a greater\ndecrease in the size of these predators relative to their prey as temperature increases.\n3) Lines 261-268: were all stations sampled in all three surveys (and seasons/years)? I\nexpect this is the case but please make it explicit. If all warm water communities were\nsampled in a specific season/year, this could generate a bias that might not be accounted\nfor with the random effect.\nResponse #12: The majority of cruise stations were fixed to allow inter-cruise comparisons,\nalthough some were allowed to vary between cruises to allow adequate sampling of dynamic\nenvironmental conditions. Overall, the distribution of sampling locations remained quite\nsimilar and a broad latitudinal range of stations was sampled during each cruise. We have\nadded two new figures to the supplementary material (Figures S5-S6, reproduced below)\nwhich depict the distribution of fish and zooplankton sampling stations during each cruise.\nWe have also added a statement to the methods (Ln 299-301) identifying the variability in\nlocation of some stations.\nLn 299-301: The exact location of these stations varied between cruises but was similar\nacross years, with a broad latitudinal range sampled during each cruise (Figures S5-S6).\nFigure S5: Distribution of myctophid sampling stations from each cruise.\nFigure S6: Distribution of zooplankton sampling stations from each cruise.\n4) The mean prey size in the stomach is in some sampling stations >0.1 gram (Fig 2C),\nwhereas the body mass distributions of zooplankton in the environment tend to be smaller\n(Fig 3B). Did authors obtain samples where the prey size in the stomach was not observed\nin the environment? How did authors estimate size preference in that case?\nResponse #13: These larger prey body sizes are in fact present at all temperatures, however the\nextremely high relative abundance of smaller organisms prevents these larger prey from being\nvisible in the fitted probability density functions of Figure 3b. We have added a statement to\nthe figure legend noting this issue (Ln 217-219). The maximum prey size in the environment\nranged from -0.07 to -0.11 (log10 g) in the coldest and warmest stations, respectively, which\nmatches the maximum prey sizes in Figure 2c. Below, we provide a version of Figure 3b with\ntick marks added along the upper portion of each plot, representing the presence of a given\nprey body size. We are reluctant to use this in the final manuscript as we feel it is cluttered and\noverly complex, but we hope this provides reassurance regarding the existence of larger prey\nsizes in the environment.\nLn 217-219: Note that in panel b, the large prey sizes (above approx. -2 log10 g) are present\nat all temperatures, but their extremely low abundance relative to smaller organisms prevents\nthem from being visible in the figure."}, {"round": 2, "reviewer_comments": {"reviewer_1": "I am entirely satisfied by the authors' responses to my comments, and am happy to say that I have no further suggestions for revision. Congratulations on a fine paper!", "reviewer_2": "Thank you for addressing my comments and those of the other reviewer. The new analyses on species and community responses to temperature are nicely integrated in the manuscript. The present version of the manuscript is enjoyable to read, clear and timely."}, "author_response": ""}]

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