Temperature-size rule (TSR) is a phenomenon of plastic changes in body size in response to temperature, originally observed in more than 80% of ectothermic organisms representing various groups (Atkinson 1994). In particular, ectotherms were observed to grow faster and reach smaller size at higher temperature and grow slower and achieve larger size at lower temperature. This response has fired the imagination of researchers since its invention, due to its counterintuitive pattern from an evolutionary perspective (Berrigan and Charnov 1994). The main question to be resolved is: why do organisms grow fast and achieve smaller sizes under more favourable conditions (= relatively higher temperature), while they grow longer and achieve larger sizes under less favourable conditions (relatively lower temperature), if larger size means higher fitness, while longer development may be risky?
This evolutionary conundrum still awaits an ultimate explanation (Angilletta Jr et al. 2004; Angilletta and Dunham 2003; Verberk et al. 2021). Although theoretical modelling has shown that such a growth pattern can be achieved as a response to temperature alone, with a specific combination of energetic parameters and external mortality (Kozłowski et al. 2004), it has been suggested that other temperature-dependent environmental variables may be the actual drivers of this pattern. One of the most frequently invoked variable is the relative oxygen availability in the environment (e.g., Atkinson et al. 2006; Audzijonyte et al. 2019; Verberk et al. 2021; Woods 1999), which decreases with temperature increase. Importantly, this effect is more pronounced in aquatic systems (Forster et al. 2012). However, other temperature-dependent parameters are also being examined in the context of their possible effect on TSR induction and strength.
Food availability is among the interfering factors in this regard. In aquatic systems, nutritional conditions are generally better at higher temperature, while a range of relatively mild thermal conditions is considered. However, there are no conclusive results so far on how nutritional conditions affect the plastic body size response to acute temperature changes. A study by Bazin et al. (2023) examined this particular issue, the effects of food and temperature on TSR, in medaka fish. An important value of the study was to relate the patterns found to fitness. This is a rare and highly desirable approach since evolutionary significance of any results cannot be reliably interpreted unless shown as expressed in light of fitness.
The authors compared the body size of fish kept at 20°C and 30°C under conditions of food abundance or food restriction. The results showed that the TSR (smaller body size at 30°C compared to 20°C) was observed in both food treatments, but the effect was delayed during fish development under food restriction. Regarding the relevance to fitness, increased temperature resulted in more eggs laid but higher mortality, while food restriction increased survival but decreased the number of eggs laid in both thermal treatments. Overall, food restriction seemed to have a more severe effect on development at 20°C than at 30°C, contrary to the authors’ expectations.
I found this result particularly interesting. One possible interpretation, also suggested by the authors, is that the relative oxygen availability, which was not controlled for in this study, could have affected this pattern. According to theoretical predictions confirmed in quite many empirical studies so far, oxygen restriction is more severe at higher temperatures. Perhaps for these particular two thermal treatments and in the case of the particular species studied, this restriction was more severe for organismal performance than the food restriction. This result is an example that all three variables, temperature, food and oxygen, should be taken into account in future studies if the interrelationship between them is to be understood in the context of TSR. It also shows that the reasons for growing smaller in warm may be different from those for growing larger in cold, as suggested, directly or indirectly, in some previous studies (Hessen et al. 2010; Leiva et al. 2019).
Since medaka fish represent predatory vertebrates, the results of the study contribute to the issue of global warming effect on food webs, as the authors rightly point out. This is an important issue because the general decrease in the size or organisms in the aquatic environment with global warming is a fact (e.g., Daufresne et al. 2009), while the question of how this might affect entire communities is not trivial to resolve (Ohlberger 2013).
Angilletta Jr, M. J., T. D. Steury & M. W. Sears, 2004. Temperature, growth rate, and body size in ectotherms: fitting pieces of a life–history puzzle. Integrative and Comparative Biology 44:498-509. https://doi.org/10.1093/icb/44.6.498
Angilletta, M. J. & A. E. Dunham, 2003. The temperature-size rule in ectotherms: Simple evolutionary explanations may not be general. American Naturalist 162(3):332-342. https://doi.org/10.1086/377187
Atkinson, D., 1994. Temperature and organism size – a biological law for ectotherms. Advances in Ecological Research 25:1-58. https://doi.org/10.1016/S0065-2504(08)60212-3
Atkinson, D., S. A. Morley & R. N. Hughes, 2006. From cells to colonies: at what levels of body organization does the 'temperature-size rule' apply? Evolution & Development 8(2):202-214 https://doi.org/10.1111/j.1525-142X.2006.00090.x
Audzijonyte, A., D. R. Barneche, A. R. Baudron, J. Belmaker, T. D. Clark, C. T. Marshall, J. R. Morrongiello & I. van Rijn, 2019. Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? Global Ecology and Biogeography 28(2):64-77 https://doi.org/10.1111/geb.12847
Bazin, S., Hemmer-Brepson, C., Logez, M., Sentis, A. & Daufresne, M. 2023. Distinct impacts of food restriction and warming on life history traits affect population fitness in vertebrate ectotherms. HAL, ver.3 peer-reviewed and recommended by PCI Ecology. https://hal.inrae.fr/hal-03738584v3
Berrigan, D. & E. L. Charnov, 1994. Reaction norms for age and size at maturity in response to temperature – a puzzle for life historians. Oikos 70:474-478. https://doi.org/10.2307/3545787
Daufresne, M., K. Lengfellner & U. Sommer, 2009. Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences USA 106(31):12788-93 https://doi.org/10.1073/pnas.0902080106
Forster, J., A. G. Hirst & D. Atkinson, 2012. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proceedings of the National Academy of Sciences of the United States of America 109(47):19310-19314. https://doi.org/10.1073/pnas.1210460109
Hessen, D. O., P. D. Jeyasingh, M. Neiman & L. J. Weider, 2010. Genome streamlining and the elemental costs of growth. Trends in Ecology & Evolution 25(2):75-80. https://doi.org/10.1016/j.tree.2009.08.004
Kozłowski, J., M. Czarnoleski & M. Dańko, 2004. Can optimal resource allocation models explain why ectotherms grow larger in cold? Integrative and Comparative Biology 44(6):480-493. https://doi.org/10.1093/icb/44.6.480
Leiva, F. P., P. Calosi & W. C. E. P. Verberk, 2019. Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers. Philosophical Transactions of the Royal Society B 374:20190035. https://doi.org/10.1098/rstb.2019.0035
Ohlberger, J., 2013. Climate warming and ectotherm body szie - from individual physiology to community ecology. Functional Ecology 27:991-1001. https://doi.org/10.1111/1365-2435.12098
Verberk, W. C. E. P., D. Atkinson, K. N. Hoefnagel, A. G. Hirst, C. R. Horne & H. Siepel, 2021. Shrinking body sizes in response to warming: explanations for the temperature-size rule with special emphasis on the role of oxygen. Biological Reviews 96:247-268. https://doi.org/10.1111/brv.12653
Woods, H. A., 1999. Egg-mass size and cell size: effects of temperature on oxygen distribution. American Zoologist 39:244-252. https://doi.org/10.1093/icb/39.2.244
DOI or URL of the preprint: https://hal.inrae.fr/hal-03738584v2
Version of the preprint: 2
Below I provide, first, the summary of referees’ comments to the previous version of the text, and the overview of authors’ responses. Later, I present my own comments to the current version of the text, which justify my decision on the manuscript, which is, to revise.
The comments of Referee 1 can be summarized in the way that the reviewer lacks, firstly, a presentation of the research in a broader context and, secondly, a clear emphasis on what new the research brings to the subject. I appreciate the improvement made by the authors in the first of the indicated contexts. The authors have referred more extensively to the literature related to the subject. However, there is some insufficiency regarding the second point, namely the importance of the results presented in light of the research topic. The authors argue that the most important novelty resulting from the work is that the study was performed on a species that is large and is a predatory vertebrate. I am not convinced that this is a sufficient argument, because in that case one could perform similar studies for each species separately and use the same argument accordingly. Then, all knowledge would be limited to "case studies". What I miss is putting the results interpretation in the right context. I have a suggestion, which the authors could use at their discretion. The presented results could be interpreted in the context of the complexity of body size control in different organisms. To date, similar studies have been done on rotifers, copepods, insects and others. By comparing the results based on organism-specific body size control system during the lifecycle, one can make attempts to summarize the similarities and differences found so far. This topic is actually a very clear and important gap in research on the TSR, raised in discussion in many papers while it is just touched in the presented manuscript (actually, in the last sentence of Abstract). Some other ways of interpretation are of course possible.
Summarizing the comments of Referee 2, the major points referred to discussing the results in the wider evolutionary perspective, e.g., proximate vs. ultimate mechanisms, other limiting factors, size at maturity vs. asymptotic size. The authors made attempts to address these points, but I found them insufficient. The least satisfactory seems to be a reference to size at maturity vs. asymptotic size. I suggest to refer to existing literature in this regard (it is indeed limited, but some information is available). In the detailed comments below I aimed to clarify some issues to facilitate the interpretation of data in the more evolutionary context. Referee 2 made also some comments regarding statistical issues and those I found sufficiently addressed.
Below are my detailed comments to the current version of the text:
L. 30-31 - “food restriction appears to amplify TSR by decreasing initial growth rate in the cold treatment” – as invoked by Referee 2, the strength of TSR generally refers to changes in body size and not in growth rate.
L. 34 – though I strongly applaud referring the results to fitness measures, I am not convinced that the reference to “live fast die young” is appropriate/necessary in the case of this study. In the context of response to higher temperature it is quite trivial, because temperature accelerates the biochemical reactions in living organisms and such a result is the only expected.
L. 56-57 – there are also some, though indeed limited, studies on ultimate mechanisms, like the one by Walczynska et al. 2015 (the one suggested by Referee 2; 10.1016/j.jtherbio.2014.11.002).
L. 63-65 – the TSR is weaker in terrestrial systems but it does not implicate that oxygen is not limiting there, but rather that there is quite many other interfering factors, among which the most important seems to be seasonality (e.g., Verberk et al. 2021).
L – 65-66 – “At the individual level, body size shift can be explained by the impact of temperature on the growth of ectotherms” – I do not understand this sentence. It is either trivial, or an unwanted shortcut.
L. 68 – as invoked by Referee 2, originally TSR was referred to size at maturity and not to asymptotic size.
L. 70-72 – to put it simple, ultimate factors refer to fitness, namely, to evolutionary meaning of the studied phenomenon. The current sentence is too complicated and not exactly to the point.
L. 74-76 – again, TSR refers to body size response, which is of course accompanied by the whole growth and development pattern, but body size remains in the centre of interest.
L. 80-83 – I do not understand the reasoning presented in this sentence.
L. 108-122 – This paragraph should be removed from Introduction, because the consequences of the examined effect for the food web interactions were not the aim of the study. Definitely, it is still an important point for Discussion section.
L. 124-129 – Such effects were also studied in rotifers (Kielbasa et al. 2014; 10.1002/ece3.1292) and in diatoms (Walczyńska and Sobczyk 2017; 10.1002/ece3.3263).
L. 142-146 – In this sentence there is a mixture of what was actually addressed in this study and what could be interpreted out of the results.
L. 150-155 – these lengthy sentences should be shortened to one precise message.
L. 147-160 – again, a mixture of goals and interpretations, while in this section the sound, reliable hypotheses are expected.
L. 171-174 – Referee 1 raised an important point about the thermal range investigated. I found the authors’ response to that comment insufficient. First of all, if the optimal temperature for the species is 25 °C, then 30 °C in a thermal treatment is above the optimum and should rather be considered a suboptimal temperature. I totally understand the logistical limitations which sometimes dictate the choice of treatments in the planned study, but the most important then is to correctly interpret the data. In this particular case, the difference between the two thermal regimes is that at 20 °C the response is assumed to be fully plastic, because it is within the ‘optimal thermal range’ for the TSR (Walczyńska et al. 2016; 10.1016/j.jtherbio.2016.06.006, the work suggested by Referee 1), while at 30 °C, being above this range, some compensatory/alternative physiological mechanisms are expected to be launched. Actually, such a distinction makes the interpretation of the patterns found at each temperature much easier.
L. 192-193 – Does it mean the highest pre-maturity mortality in this regime?
L. 273-279 – I find this interpretation of Fig. 2 quite misleading. In reference to the theory presented in Fig. 1, the comparison of crossed vs. nested patterns should be made for the pairs ad_20 vs. ad_30 and res_20 vs. res_30, because this distinction is expected for comparison across temperature. Then, the effect of food should be compared for the patterns found for both ads vs. both reses.
Figure 2 – age at maturity could be additionally displayed in the figure for comparison.
L. 302-306 – If I am correct, survival was estimated starting from the age at maturity. In that case, it should be stated clearly, here and throughout the manuscript, and I suggest considering the change of the name of this trait to ‘life expectancy since maturity’. Otherwise it is misleading, especially that, referring to my comment above, the highest pre-maturity mortality was found in the res_20 regime.
L. 324-331 – this paragraph resembles very much the one presented in Introduction. Please, choose one part of the text, the one in which it will be more suitable. Also, the reference to stronger TSR response with larger size according to Forster et al. 2012 is generally correct, but it is not an argument in this case. Forster et al. 2012 compared species which are close on a phylogenetic tree. For an obvious reason, it would not be correct to expect that fish species have stronger TSR pattern than, e.g., rotifer species, just because they are larger.
Discussion in general – perhaps there are different “schools” in this regard, but I was trained that discussion should start from presentation of the most important findings from the study in the wider perspective. The speculative part should be following this introductory one.
L. 339-354 – This section should be much more concise, as it is speculative and does not refer directly to the main aim of the study. I appreciate the discussion on the consequences of thermally-induced body size changes in a predatory species for the whole community or a trophic web, but this should be much shorter.
L. 364-368 – Which curves did the authors mean to be nested in this sentence? Please, see my comment above about comparing the crossed vs. nested curves. It is not clear what the authors found surprising.
L. 383-400 – This part is far too long. Information is just repeated using slightly different words. Referring to the oxygen as a limiting factor, one of the most important differences between oxygen and food availabilities is that the former generally decreases with increasing temperature (at least relatively to demands), while the latter generally increases with increasing temperature (in ecologically relevant conditions). Walczyńska and Sobczyk (2017; 10.1002/ece3.3263) discuss the differences in thermally driven nutrition vs. thermally driven oxygen effects on plastic body size response.
L. 420-429 – This paragraph is highly speculative and not really understandable. Instead, one would expect a joint discussion of the experimental effects on different life history traits, namely size at maturity, age at maturity, fecundity, clutch size and survival (life expectancy since maturity?). What about the trade-offs, which are mentioned in Introduction?
L. 431-432 – Again, TSR refers to body size and not to growth rate.
L. 447-449 – This assumption should be definitely more elaborated. My feeling while reading this manuscript was that the food-restriction applied in the study was not a real restriction. The authors should provide some references in which such a way of feeding was proven to be a restriction (through, for example, slower growth rate or smaller final size). Shortly, why this particular way of food regimes distinction was chosen?
L. 472-490 – This paragraph is again too speculative and too wordy. Perhaps it should be matched with the very similar paragraph which was presented at the beginning of Discussion to provide a short, reliable and concise information on where and how these results could be implemented.
DOI or URL of the preprint: https://hal.archives-ouvertes.fr/hal-03738584v1
The two Reviewers point out that the study is potentially interesting and relatively well prepared. However, they also point some important shortcomings regarding either the results interpretation and discussion, or the methodology description. The solutions for text improvement provided by the Reviewers are clear and sound, therefore I suggest you to revise the text accordingly.
With kind regards,