the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
An unpredictable body size response to the Permo–Triassic climate crisis
Abstract. A predictive ecological response to both the present and past climate crises is that marine ectotherm species will become smaller before going extinct or fluctuate in abundance and size with environmental conditions. The problem with studying past climate events with high rates and magnitude of warming, which may serve as analogues for projected climate change, is that very few species, or even genera, survived such events. Here, we utilized one of the few records of marine bivalves that spans the Permian–Triassic climate crisis with specimen-level data and at a high resolution. These measurements come from the Bellerophon and Werfen formations of the Dolomites in Italy, representing relatively shallow marine environments. At the species-level, there is almost a complete turnover, and the newly evolved species are typically significantly smaller, but not unusually small, whereas the three surviving species do not show a significant body size change. Our results clarify that the observed temporary size reduction at the genus-level is primarily driven by the preferential evolution of smaller species after the extinction, rather than, as often assumed, by a size decrease within existing species; this challenges the universal validity of the 'Lilliput effect' in the sense of direct intra-species dwarfing, but confirms it as a consequence of faunal turnover. Subsequently, there are two pulses of genus-level body size recovery determined by different mechanisms. The first phase (late Griesbachian) is driven by the size-increase of the existing species, whereas the second phase (early Spathian) is also due to the evolution of larger species. The effects of abiotic and biotic factors in controlling these body size dynamics are superimposed during the Early Triassic. These results suggest a mechanism to explain size reductions during climate crises, but does not find a species-level body size reduction to be a forecastable response to extreme climate warming.
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Status: open (until 09 Oct 2025)
- CC1: 'Comment on egusphere-2025-4038', Kenneth De Baets, 30 Aug 2025 reply
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CC2: 'RC Comment on egusphere-2025-4038', Posenato Renato, 09 Sep 2025
reply
Foster and co-authors investigate the size changes of bivalves across the end-Permian mass extinction by analyzing a large amount of specimens mostly from the Dolomites. The novelty of this study is that the analysis is performed between bivalve taxa occurring before and after the extinction. The comparison is based on data from the literature. The data repository indicated in the manuscript is empty/missing (!).
The results and discussion of the “Lilliput effect” are, however, biased by merging the data of bivalve taxa occurring in the “Extinction interval” (i.e., lower Tesero Member and Gerennavár Limestone Formation) with those occurring in the Mazzin Member of the Werfen Formation. The bivalve assemblage of the Mazzin Member comprehends the species recording the peak of the extinction after the most severe and devasting effects on the marine biota, whereas those bivalve species from the “Extinction interval” belong to the last Permian-type assemblages with articulate brachiopods and calcareous algae. These brachiopods and algae extinguished close to the base of the Triassic, around the first appearance of H. parvus. I think that the bivalves occurring in the “Extinction Interval” (latest Changhsingian-basal Induan) must be separated from those occurring in the Mazzin Member (lower Induan). Consequently, the exceptions of the Lilliput effect suggested throughout in the manuscript must be reconsidered as well as the number of the Permian survivors in the Triassic.
Stutchburia tschernyschewi is proposed as a Permian survivor which does not show the size reduction with respect to the Permian individuals, and thus it would be another exception to the Lilliput effect. However, this species occurs in the late Induan when the size is increased in all the bivalves. This species, not yet discovered in the Mazzin Member, is so rare (cf. Hofmann et al.) that a statistical comparison has no value.
The final statements of the Introduction declare that the Dolomites are “one of the best-studied regions ... for the Permian-Triassic crisis”. Although dozens of articles on this topic have been indeed published in high-impact journals over the last 40 years, only an extended abstract by the authors (Kustatscher et al.) is cited to support this claim. This abstract is also cited in line 94, even though the eastward deepening of the basin is well known in literature since the 1970s. References are also missing about the well-known Triassic carbonate platforms for which the Dolomites are renowned throughout the world. Only a field guide book is cited (Stefani et al., 2004). The Authors omit previous papers dealing with the topic of their study. These serious oversights of literature should be corrected by the authors.
There is no indication of the referred age of the paleogeographic map of the Dolomites (Fig. 1 has already been published in other papers which must be necessarily referred to). The paleogeography of the Southern Alps remarkably changed during the Late Permian, with repeated transgressive and regressive cycles. Nonetheless, this happened even during the Early Triassic when the sea level rose tens of meters and the sea invaded the Lombardy.
In the abstract, Authors write: “These measurements come from the Bellerophon and Werfen formations of the Dolomites in Italy, representing relatively shallow marine environments”. However, in the paleogeographic map the material was collect in sedimentary successions ranging from shoreface to basin settings. What age (Changhsingian, Induan or Olenekian?) does the “relatively shallow marine environments” refer to? Since this presumed great difference in depth, why is it not considered in the Discussion?
Citation: https://doi.org/10.5194/egusphere-2025-4038-CC2 -
EC1: 'Editorial comment: Code and data availability', Niels de Winter, 22 Sep 2025
reply
Dear William Foster and colleagues,
During the discussion of your manuscript, some of the reviewers highlighted that the link in your Code and Data availability section (https://github.com/wjf433/DBiv) leads to an empty GitHub repository. We at Biogeosciences are very keen on keeping all aspects of the review process open, and this includes making the code and data you use in your study available to the reviewers so they can judge the entire methodology and outcomes of your work. This includes code and data availability, and I wanted to stress that manuscripts without open availability of crucial elements of the methodology (such as code) will not be acceptable for publication. I therefore urge you to make your code repository available for the reviewers and indeed the rest of the community, preferably with a DOI.
The latter means that, if you prefer to keep using GitHub to share your code, you will have to link your GitHub repository to an online storage medium such as Zenodo which offers stable DOI's for GitHub releases. For more information on how to do this, please refer to the following guide on Zenodo: https://help.zenodo.org/docs/github/.
Needless to say, you are free to use any other repository as long as you can guarantee that the version of your code used to produce the outcomes exposed in your manuscript is accessible through a DOI to the readers and reviewers.
Kind regards,
Niels de Winter
Citation: https://doi.org/10.5194/egusphere-2025-4038-EC1 -
RC1: 'Comment on egusphere-2025-4038', Kenneth De Baets, 23 Sep 2025
reply
First of all, I want to congratulate you on amassing this unprecedented data and analyses to studying these crucial aspects in Permian-Triassic bivalves from the dolomites. Given the scope and great interdisciplinary relevance of this analysis, I would love to see this published. However, I feel there are some crucial aspects which need to be addressed before publication (part of these can also be found in my online comment):
1) Size changes across mass extinctions and/or extreme environmental perturbations: It is refreshing to see you tackling size changes in bivalves in higher resolution across a mass extinction as well as the associated issues such almost complete turnover, genus versus species. It may be worth pointing out (e.g., around lines 50-52) that similar difficulties may arise also during smaller crises, particularly when marked environmental perturbations occur (e.g., secondary extinction events such as Pliensbachian-Toarcian crisis). For example, it was challenging to study the TOAE as belemnite become rarer at particularly localities (e.g., Peniche) and a complete turnover is visible linked with a belemnite size increase (Rita et al. 2019). However, more comprehensive data obtained from a latitudinal gradient shows that there is consistent evidence for a size increase driven by appearance of larger species although the mechanisms behind it may be multifold warranting the need for additional studies (De Baets et al. 2021).
2) Mechanisms of the Lilliput effect sensu stricto: I feel it would be helpful to even more explicitly discuss about a Lilliput effect sensu stricto (e.g., original discussion by Urbanek 1993) versus lato when other factors are involved. In this respect, it is worth highlighting that the mentioned ammonoid body size pre-extinction decrease by Kiessling et al. (2018) occurs above species-level and not at the species level (line 273). The Lilliput effect sensu stricto was attributed to smaller adult size at the species level. However, in the modern and fossil assemblages, both smaller adult size and higher proportion of early (and therefore smaller) ontogenetic stages (e.g., juveniles) may contribute to smaller body sizes (Daufresne 2009; Ortega et al. 2016; Rita et al. 2019). In the fossil record, smaller specimens may be rarer or less preserved than larger specimens under particular circumstances which could also cause the opposite effect (e.g., we suggested it as a possible explanation for increase in belemnite size distribution during TOAE: De Baets et al. 2021). I would like to see a discussion on these factors in the discussion.
3) Impact of changes of facies and sea-level changes: Mass extinctions are often associated with marked stratigraphic changes associated with sea-level changes which may not only impact diversity but also preservation and organismal traits such as size (Holland 2000, 2020; Holland and Patzkowsky 2015). De Baets et al. 2022 for example found a relationship between changes in facies/lithology and body size distribution of Devonian ammonoids during background conditions with smaller sizes in black shales as opposed to carbonates or marls cautioning to interpret body size changes during marked changes in facies/lithology. Correcting for it, interestingly we found specimens at lower latitudes to be bigger rather than smaller which was the opposite effect as expected. Rita et al. 2019 in belemnites or Nätscher et al. 2023 in ostracods found no strong effect of lithology although these authors focused on individual sections which may not represent the full spectrum of (background) environmental/depositional conditions (compare De Baets et al. 2021). You seem to have a unique opportunity here to see the effect across multiple localities with the same region/basin and I feel this could be exploited more or at least discussed in greater detail (compare also online comment by Renato Posenato). I would at least like to see a small discussion in the discussion on the potential effect of these factors on your dataset. In the aftermath of crises, sometimes unlikely groups may benefit (e.g., deepwater brachiopods with low metabolism: Uhlmann et al. 2023).
4) Sample sizes and pooling of samples: from our own analyses, I am quite understanding of difficulties of obtaining sufficiently large sample sizes across extinct events as well as the impact on statistical power when sample size is lower. 3983 body sizes are unprecedented and impressive for this time interval and region. However, when we subdivide it by the number of studied species and time bins, there seem to be species/genera which are only represented by a single data point while other will be presented by tens to hundreds of data points. When looking at size distributions – 20-30 data points per species per bin would be minimum (likely more when large ontogenetic changes in size are expected: compare Nätscher et al. 2021) to draw meaningful conclusions. In this context, I would be crucial to explicitly provide sample sizes (per species or genus) and designate significant changes in Figure 2. I also feel violin plots may be more appropriate to show the actual distribution of data (is their evidence multimodal distributions in case of multiple species). When dealing with changes within genera, it would be particularly interesting to see if there a change from one species to next species in the next bin (e.g., anagenetic lineages with different species assigned to different genera) or rather from multiple species from one bin to the next time bin. I also feel it is equally crucial for other figures (4-6) to add information on significance (e.g., by connected changes bracketing boundaries and adding as asterisk/different symbol for it) as well as sample sizes in the graphs. Also, consideration of violin plots more generally in these graphs may also be helpful if not in main text, at minimum in the supplementary material. In addition, choosing time bins and pooling specimens at such levels may also affect interpretations (see also online comment by Renato Posenato).
5) Rego et al. approach: I completely agree that changes in components may be sensitive to changes in relative abundance within the time interval using the Rego approach (line 155; see also De Baets et al. 2021). However, the question remains if focusing on dominant taxa where more (or at least sufficient) data is available is not more reliable or at least more significant particularly when attempts were made to sample and include all available specimens (compare Rita et al. 2019). In this respect, I would still like to see additional discussion in the main manuscript on the differences when correcting or not correcting for abundance.
6) Impact of taxonomic practices and preservation: It is great to hear that you standardized taxonomy which is crucial for such studies, and I have little doubt with bivalve experts involved that you thought long and hard about it. For the reader, it would be helpful to see some additional explanation on how this standardization was achieved. More generally, I also wonder if stronger size changes at genus level versus weaker changes in species may not be a partial artefact of stratigraphic gaps, preservation and taxonomic practices at such critical intervals. In an ideal world, we would have large samples of well-preserved specimens at all ontogenetic stages without (major) stratigraphic gaps allowing to make meaningful subdivision based on known phenotypic plasticity, ontogenetic variation and fluctuations over time between species based on morphology. Unfortunately, this is rarely the case across extinction events associated with major environmental perturbations such End-Permian Mass extinction (or even secondary extinction like the TOAE - sometimes even growth may be affected and in different ways in different species: compare Nätscher et al. 2021). In this context, it may be tempting (or collide with conservative taxonomic principles) to assign specimens (particularly those showing marked differences in size and morphology at individual ontogenetic stages or high phenotypic plasticitiy) separated by large stratigraphic gaps to different species versus lumping them within genera. It would be crucial to see a larger discussion on how taxonomic challenges may contribute to the patterns your others observed. You already hint at some of these aspects in text.
Data availability: I greatly appreciate that it is planned to make the script and data available through Github. From the available figures and discussion, you did thorough analyses. Unfortunately, I could not access script/data at the link provided (e.g., Github folder seems to be empty: see also comment by editor). I feel providing your data through a repository with a digital object identifier such as Zenodo would be crucial (it is quite easy to connect and publish Github dataset with Zenodo). Providing additional figures and used data tables also as supplementary materials would also benefit reproducibility. I feel it is crucial such data such be shared at latest upon publication but ideally and as best practice already during reviewing phase (possibly in another way if you have concerns code and data to be re-used before publication).
Additional suggestions:
Line 50-52: I would argue that in some (particularly less extreme) crises - more detailed studies at bed-level are possible without having to go to coarse level and may be worth pointing this out (for example: belemnite - Rita et al. 2019; De Baets et al. 2021; Nätscher et al. 2021; or bivalves - Piazza et al. 2019, 2020; Ullmann et al. 2020 during the TOAE: Rita et al. 2019; Piazza et al. 2019, 2020; Nätscher et al. 2021; De Baets et al. 2021; Ullmann et al. 2020). Nätscher et al. 2025 (which you already cite) also found no consistent association changes in taxonomic level or stratigraphic grain in available data.
Line 105: On which reference(s) is this reconstruction and inferred paleoenvironments in Figure 1 based (see also online comment by Renato Posenato)? Did these locations markedly change their environments across the studied interval?
Line 130-132: You allude to biases related taxonomic practices. Could you explain in greater detail how you tried to resolve these and how they may influence your results and interpretations.
Line 175: Could you explain in greater detail how Schizodus and Neoschizodus are closely related? Are they part of an anagenetic lineage or is it more complicated and difficult to resolve at the moment?
Line 240: can it be falsified fully? Could taxonomic practices also play a role in this?
Line 271-273: “Pre-extinction body size reductions have often been considered a precursor signal of a mass extinction event, and one expectation is that species would have reduced their size prior to their extinction. This has been observed for ammonoids and podocopid ostracods from Iran (Kiessling et al., 2018; Nätscher et al., 2024) and brachiopods from South China (He et al., 2010; Zhang et al., 2016).” I suggest rephrasing as within species changes were not observed in Permian ammonoids (e.g. it rather takes place at genus or higher level: compare data in Kiessling et al. 2018). I also suggest to add these cited changes take place during the Permian to avoid confusion and potentially also cited work of similar observations during other crises (e.g., Piazza et al. 2019)
Line 279: you allude to difficulties related with stratigraphic gaps in studying pre-extinction size reductions. Would such gaps or stratigraphic changes no also not cause wider difficulties in interpreting the lilliput effect or even partially cause it around mass extinction events?
Line 280: you mention “our data reject the “Lilliput effect” in the sense of a temporal within-species size reduction during an extinction/hyperthermal event”. I feel it would be more appropriate to state it more specific and less firm (given the constraints you discussed earlier) as: “our data seem to reject the “Lilliput effect” in the sense of a temporal within species-reduction during the Permian-Triassic extinction/hyperthermal event in bivalves”
Line 284: Can you sure it is at least not partially an artefact of taxonomic level?
Line 286: I would argue taxonomic practice, degree of ontogenetic allometry and representation of juvenile versus adults (and changes therein) may potentially also play into it. I would like to see this discussed in greater detail.
Line 287: I feel influence of changes in depositional environment, facies and/or sea-level changes also need to be discussed under abiotic changes.
Line 338-340: Can you be sure these small forms are adults or rather may reflect an increase of the proportion of juveniles versus adults? It would be crucial to discuss this aspect.
Line 344-346: This discussion is highly interested and potential contribution to such issues on size patterns more generally could be discussed in this context.
Line 350: Could lack of ribs or ornamentation also related to differences in preservation?
Line 388: I would stress Lilliput effect sensu stricto (or how it was traditional seen) here for clarity.
Please also see the annotated pdf to see those comments into their respective context.
I look forward to seeing the revised version of this manuscript published.
Kenneth De Baets
Suggested references (above also references are discussed which are already cited and not repeated here):
Daufresne, M., Lengfellner, K., & Sommer, U. (2009). Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences, 106(31), 12788-12793.
De Baets, K., Nätscher, P. S., Rita, P., Fara, E., Neige, P., Bardin, J., ... & Weis, R. (2021). The impact of the Pliensbachian–Toarcian crisis on belemnite assemblages and size distribution. Swiss Journal of Palaeontology, 140(1), 25.
De Baets, K., Jarochowska, E., Buchwald, S. Z., Klug, C., & Korn, D. (2022). Lithology controls ammonoid size distributions. Palaios, 37(12), 744-754.
Holland, S. M. (2000). The quality of the fossil record: a sequence stratigraphic perspective. Paleobiology, 26(S4), 148-168.
Holland, S. M. (2020). The stratigraphy of mass extinctions and recoveries. Annual Review of Earth and Planetary Sciences, 48(1), 75-97.
Holland, S. M., & Patzkowsky, M. E. (2015). The stratigraphy of mass extinction. Palaeontology, 58(5), 903-924.
Nätscher, P. S., Dera, G., Reddin, C. J., Rita, P., & De Baets, K. (2021). Morphological response accompanying size reduction of belemnites during an Early Jurassic hyperthermal event modulated by life history. Scientific Reports, 11(1), 14480.
Ortega, L., Celentano, E., Delgado, E., & Defeo, O. (2016). Climate change influences on abundance, individual size and body abnormalities in a sandy beach clam. Marine Ecology Progress Series, 545, 203-213.
Piazza, V., Duarte, L. V., Renaudie, J., & Aberhan, M. (2019). Reductions in body size of benthic macroinvertebrates as a precursor of the early Toarcian (Early Jurassic) extinction event in the Lusitanian Basin, Portugal. Paleobiology, 45(2), 296-316.
Piazza, V., Ullmann, C. V., & Aberhan, M. (2020). Temperature-related body size change of marine benthic macroinvertebrates across the Early Toarcian Anoxic Event. Scientific reports, 10(1), 4675.
Ullmann, C. V., Boyle, R., Duarte, L. V., Hesselbo, S. P., Kasemann, S. A., Klein, T., ... & Aberhan, M. (2020). Warm afterglow from the Toarcian Oceanic Anoxic Event drives the success of deep-adapted brachiopods. Scientific Reports, 10(1), 6549.
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Dear colleagues,
I greatly appreciate the detailed and high-resolution analyses of bivalve size responses observed within the dolomites of Italy across the Permian-Triassic extinction and its aftermath. I can only imagine how much effort and work it took also judging from preparation for our own studies. In our meta-analysis, we observed greater size responses related to hyperthermal crises - at least with the currently available published data . As you rightly point out, there is need for more data to better understand the phenomenon. I agree that various factors may contribute to these patterns and as you rightly point out (changes in species versus genus level) and the difficulty of finding locations where species and genera can be studied across such crises particularly during mass extinction events like the Permian-Triassic erasing a large part of diversity as well as associated changes in sedimentation, sea level and environmental factors complete this. I however feel 3 additional factors can be important to understand mechanisms of size changes and their discrepancies between localities/regions, groups and time intervals. In this aspect i remain cautious in generalising the efforts from a single region or study but find all new data to these questions meaningful and important to publish and study. Unfortunately, not a lot of studies are available offering the kind of resolution like yours to allow for it (only a small fraction in literature allow for investigating these mechanisms).
It may however be interesting to these others potential aspects discussed in the discussion. In this respect, to what degree we can generalise mechanisms across groups or studies beyond species/genus. Before me proceeding, i want to say i greatly appreciate the collection and study effort, rigorous analyses and do not want to criticise it in any way as you did the greatest effort ever done on this topic in this group and region. I also acknowledge that this points may not always be easy to study from own experiences related to availability and preservation of specimens. We have been trying to test this in some groups but requires considerable effort and data and not all aspects are possible within the same datasets. I therefore greatly appreciate you tackling at least some of them here. I will draw here from own experiences/studies as i know them best but does not mean other studies do not exist or less interesting or appropriate in any way.
Points i would like a brief discussion on (at least as far as your data allows for it):
1) The use of species versus genus: i agree fully that there is a need to understand and compare patterns at the species level versus genus or higher. However, i am unsure how well resolved this can be across an extinction event or any intervals for that matter (particularly when including gaps in record or different to poor preservational issues) as it would require a precise taxonomy and understanding of intraspecific and intrageneric including understanding of ontogenetic changes and phenotypic plasticity across different environments to fully understand these differences. How can we for example be sure our assignments to particular fossil species or genera is correct if taxa show marked changes through ontogeny and in addition marked different distribution in size and phenotypic variation across time? Can we be sure authors would not assign them to new species or inverse to similar genera if they have marked different or similar morphologies (in relationship to size). We tried to more fully understand this for example in our studies of belemnites (Rita et al. 2019: https://doi.org/10.1098/rsos.190494; Nätscher et al. 2021: https://doi.org/10.1038/s41598-021-93850-0; De Baets et al. 2021: https://doi.org/10.1186/s13358-021-00242-y) or ostracods (Nätscher et al. 2023: https://doi.org/10.1111/pala.12667). How can we be sure that smaller or larger specimens at particular times (particularly when looking differently) are new species without large understanding about ontogeny, growth rates and intraspecific variation which are challenging to obtain? This may the most difficult to tackle as i am not sure how well this is/can be understood in taxa and with data/preservation you have available but if not in the dolomites i would not know where else.
2) Mechanisms within species versus mechanisms at higher levels: it remains the question what are the main drivers of changes in size we observe across time and even we can even capture them particularly in species differing in reproductive strategies (if we have no knowledge on all ontogenetic stages). A single locality/region may not necessarily be sufficient to fully grasp variation in species size and ontogenetic representation (if different ontogenies live in different places). In the case of belemnites across the TOAE (where we also have gaps but have material across a latitudinal gradient), it seems response can differ at different localities (Rita et al. 2019: https://doi.org/10.1098/rsos.190494; Nätscher et al. 2021: https://doi.org/10.1038/s41598-021-93850-0; De Baets et al. 2021: https://doi.org/10.1186/s13358-021-00242-y). For example in Peniche we could document a clear decrease in size across the Pliensbachian-Toarcian boundary when all ontogenetic stages are represented and adults changes consistently but differed between localities) while we consistently see an increase in (adult) size in the TOAE driving by new species arriving (similar to your study). The issue across the TOAE in part seems to be that the new species seems mostly represented by later (ontogenetic) stages (do no live their entire life in same localities). These factors therefore may complicate the interpretations - particularly to understand if patterns with species or even at higher level are driven by shifts in ontogenetic representation (e.g., higher degree of juveniles) or adult size? Given at least some of your are experts on Triassic bivalves i feel you may be best able to tackle this question.
3) The last factor is changes in environmental and depositional conditions across time or space. Ideally we would have representation of species across all habitats to fully control for this but this may not be always possible (e.g., sometimes there are no full representation or comparable environments/conditions before or after an event = from my understanding a large event like Permian-Triassic extinction could qualify as such an event). Sometimes we may only have high resolution data available for a single section which does not make it less interesting to publish and discuss. We tried to understand this be looking at a dataset on size distributions of ammonoid species belonging to a single family across space not time (De Baets et al. 2022: https://doi.org/10.2110/palo.2021.063). Our working hypothesis was initially that specimens / size distribution getter bigger on average at higher latitudes. Interestingly, we found that lithology (before genus assignment or collection effort) has the largest effect on our dataset. If we correct for it, we even see that specimens/ size distributions get larger towards lower latitudes (exactly the opposite from our hypothesis). How could changes in environment or depositional conditions have potentially have affected changes size distribution/representation? You at least seem to correct for abundance and environmental factors and multiple localities so i assume potential depositional environments/facies changes could also be tackled or ruled out.
Unfortunately, datasets able to study such aspects like yours are still to far and few between (i learned this the hard way).
I therefore look forward to see your interesting work published and i hope i convinced you that at least some discussion of these factors may be meaningful as far as possible or at least considering them as aspects worth studying in the future.