Rapid riparian ecosystem recovery in low-latitudinal North China following the end-Permian mass extinction

Reviewer #1 (Public review):

Summary:

This is a very well-written paper presenting interesting findings related to the recovery following the end-Permian event in continental settings, from N China. The finding is timely as the topic is actively discussed in the scientific community. The data provides additional insights into the faunal, and partly, floral global recovery following the EPE, adding to the global picture.

Strengths: The conclusions are supported by an impressive amount of sedimentological and paleontological data (mainly trace fossils) and illustrations.

Weaknesses: [eliminated in revision]

Reviewer #2 (Public review):

Summary:

The authors made a thorough revision of the manuscript, strengthening the message. They also considered all the comments made by the reviewers and provided appropriate and convincing arguments.

Strengths:

The revised manuscript clarifies all the major points raised by the reviewers, and the way the information is presented (in the text, figures and tables) is clear.

Weaknesses:

The authors provided an appropriate and convincing rebuttal regarding the potential weakness I pointed out in the first review of the manuscript. Therefore, I do not see any major issue in their work.

Reviewer #3 (Public review):

Summary:

The manuscript by Guo and colleagues features the documentation and interpretation of three successions of continental to marginal marine deposits spanning the P/T transition and their respective ichnofaunas. Based on these new data inferences concerning end-Permian mass extinction and Triassic recovery in the tropical realm are discussed.

Strengths:

The manuscript is well written and organized and includes a large amount of new lithological and ichnological data that illuminate ecosystem evolution in a time of large scale transition. The lithological documentations, facies interpretations and ichnotaxonomic assignments look alright (with few exceptions).

Weaknesses: [all eliminated in revision]

Author response:

The following is the authors’ response to the original reviews

Public Reviews:

Reviewer #1 (Public review):

Summary:

This is a very well-written paper presenting interesting findings related to the recovery following the end-Permian event in continental settings, from N China. The finding is timely as the topic is actively discussed in the scientific community. The data provides additional insights into the faunal, and partly, floral global recovery following the EPE, adding to the global picture.

Strengths:

The conclusions are supported by an impressive amount of sedimentological and paleontological data (mainly trace fossils) and illustrations.

We thank Reviewer #1 for the positive assessments.

Weaknesses:

The occurrence of MISS (Microbially Induced Sedimentary Structures) could be discussed more in detail as these provide interesting information directly linked to the delayed recovery of the biota.

We appreciate the reviewer for highlighting this important point. In the Phanerozoic, increase of microbial abundances generally occurred with rapid warming when documented and those hyperthermal events had causal links to mass extinction in continental realms, including the Permian–Triassic mass extinction (Mays et al., 2021). Accumulations of cyanobacteria and other microbes was favored by low dissolved oxygen concentrations (Pacton et al., 2011) and the produced secondary metabolites may also be toxic to animals (Paerl and Otten, 2013). Therefore, repeated algal and bacterial blooms in the post-extinction interval could disrupt ecological stability and inhibit the restoration of ecosystems.

So, the sentence from Lines 127–130 “The depauperate ichnofauna of the late Smithian were monospecific, representing initial recolonization of empty niches by opportunists, but the coeval thrived microbial mats indicated harsh environments, which might have inhibited the recovery of freshwater ecosystems (Tu et al., 2016; Chu et al., 2017; Mays et al., 2021).” is rephased by:

“The depauperate ichnofauna of the late Smithian were monospecific, representing initial recolonization of empty niches by opportunists. However, recurrent occurrences of microbial induced sedimentary structures (MISS) in the Liujiagou Formation imply that depressed ecosystems persisted until the Smithian (Tu et al., 2016; Chu et al., 2017). Studies revealed that the increase in microbial abundances were generally associated with hyperthermals, which would be the principal causes for mass extinction on land (Mays et al., 2021). Accumulations of microbes were favored by low dissolved oxygen concentration condition and their secondary metabolites could also be toxic to animals (Pacton et al., 2011; Paerl and Otten, 2013). Therefore, repeated thriving of MISS during the Dienerian–Smithian disrupted ecological stability in freshwater ecosystem and delayed biotic recovery in North China.”

References:

Mays, C., et al. 2021. Lethal microbial blooms delayed freshwater ecosystem recovery following the end-Permian extinction. Nat. Commun. 12, 5511. https://doi.org/10.1038/s41467-021-25711-3

Pacton, M., et al. 2011. Amorphous organic matter—Experimental data on formation and the role of microbes. Rev. Palaeobot. Palynol. 166, 253–267. https://doi.org/10.1016/j.revpalbo.2011.05.011

Paerl, H. W. & Otten, T. G. 2013. Harmful cyanobacterial blooms: causes, consequences, and controls. Microb. Ecol. 65, 995–1010. https://doi.org/10.1007/s00248-012-0159-y

Reviewer #2 (Public review):

Summary:

A rapid recovery of the ecosystems during the late Early Triassic, in the aftermath of the end-Permian mass extinction, is discussed based on different types of fossils.

Strengths:

The combined study of invertebrate trace fossils, tetrapod bones, and plant remains together with their stratigraphic distribution in different sections provides a convincing case to support a rapid recovery as the authors hypothesize.

We thank Reviewer #2 for the positive comments on our work.

Weaknesses:

The study is based on three regions with Triassic successions from the North China block. While a first-hand study of other localities of similar age would be ideal, this is of course a difficult task. Instead, the authors provide comparisons with other worldwide regions to build their case and support the initial hypothesis.

Globally, ichnoassemblages reported from the Lower Triassic are relatively impoverished (Guo et al., 2019). We have compiled ichnoassemblages from several continental basins before, including South Africa, Antarctica, North America, European Basin and North China (Fig. 14 in Guo et al., 2019). However, most of the Early Triassic strata lack bioturbation (e.g., Guo et al., 2019, Buatois et al., 2021). On the contrary, the coeval deposits in North China contain diverse trace fossils, making it an ideal place for ichnological investigations. Hence, this study mainly focuses on the ichnological records in North China, but we hope more work will be done in other basins.

References:

Guo, W.W, et al. 2019. Secular variations of ichnofossils from the terrestrial Late Permian–Middle Triassic succession at the Shichuanhe section in Shaanxi Province, North China. Glob. Planet. Change 181, 102978. https://doi.org/10.1016/j.gloplacha.2019.102978

Buatois, L.A., et al. 2021. Impact of Permian mass extinctions on continental invertebrate infauna. Terra Nova 33, 455–464. https://doi.org/10.1111/ter.12530

Reviewer #3 (Public review):

Summary:

This manuscript by Guo and colleagues features the documentation and interpretation of three successions of continental to marginal marine deposits spanning the P/T transition and their respective ichnofaunas. Based on these new data inferences concerning end-Permian mass extinction and Triassic recovery in the tropical realm are discussed.

Strengths:

The manuscript is well-written and organized and includes a large amount of new lithological and ichnological data that illuminate ecosystem evolution in a time of large-scale transition. The lithological documentations, facies interpretations, and ichnotaxonomic assignments look okay (with a few exceptions).

We thank Reviewer #3 for the positive assessments.

Weaknesses:

Some interpretations in Table 1 could be questioned: For facies association FA2 the interpretation as „terrestrial facies with periodical flooding" should be put into the right column and, given the fossil content, other interpretations, such as "marine facies" or "lagoonal environment" with some plant debris and (terrestrial) animal remains washed in, could also be possible. For FA3 the statement "bioturbation is absent" is in conflict with the next statement "strata are moderately reworked". For FA5 the observation of a "monospecific ichnoassemblage" contradicts the listing of several ichnotaxa.

We thank the reviewer for this feedback. The “FA2: terrestrial facies with periodical flooding” has been moved to the right column. As for the interpretation of depositional environment of FA2, this interval was basically terrestrial accordingly to the well-developed paleosols (Yu et al., 2022). Meanwhile, regional geological surveys have shown a faunal transition in this interval among a series of successions, from typical marine fauna containing Lingula, Eumorphotis, etc. in the southwest to a marine bivalve-terrestrial conchostracan mixed fauna in the northeast (Yin and Lin, 1979; Chu et al., 2019). Therefore, occurrence of episodic transgressions is suggested.

The FA3: Costal mudplain facies distributed to both the upper Sunjiagou Formation and Lower Heshang Formation (Fig S1), where the former lack bioturbation and the latter were moderately disturbed. We have stated this clearly in the table S1.

Ichnofauna in FA5 are dominated by Skolithos, Lockeia and Gordia, with only one poorly preserved specimen of Palaeophycus, which are distributed at the Shichuanhe and Liulin sections. However, there ichnotaxa were distributed separately, characterized by low diversity (single ichnogenus) and high density. We have deleted the “monospecific ichnoassemblage” for clarity.

References:

Chu, D., et al. 2019, Mixed continental-marine biotas following the Permian-Triassic mass extinction in South and North China: Palaeogeography, Palaeoclimatology, Palaeoecology, v. 519, p. 95–107, doi:10.1016/j.palaeo.2017.10.028.

Yu, Y., et al. 2021, Latest Permian–Early Triassic paleoclimatic reconstruction by sedimentary and isotopic analyses of paleosols from the Shichuanhe section in central North China Basin: Palaeogeography, Palaeoclimatology, Palaeoecology, v. 585, p. 110726, doi:10.1016/j.palaeo.2021.110726.

Yin, H.F., Lin, H.M., 1979. Marine Triassic faunas and the geologic time from Shihchienfeng Group in the northern Weihe River Basin, Shaanxi Province. Acta Stratigr. Sin. 3, 233–241 (in Chinese).

Concerning the structure of the manuscript, certain hypotheses related to the end-Permian mass extinction and the process of the P/T extinction and recovery, namely the existence of a long-persisting "tropic dead zone" are introduced as a foregone conclusion to which the new data seemingly shall be fit as corroborating evidence. Some of the data - e.g. the presence of a supposedly Smithian-age ichnofauna are interpreted as a fast recovery shortening the duration of the "tropic dead zone" episode - but these interpretations could also be interpreted as contradicting the idea of a "dead zone" sensu stricto in favour of a "normal" post-extinction environment with low diversity and occurrence of typical disaster taxa. Due to their large error bars the early Triassic radiometric ages did not put much of a constraint on the age determination of the earliest post-extinction ichnofaunas discussed here.

In the first ~5 Myr of the Triassic, there is evidence for a broad equatorial belt (30°N-40°S) where marine and terrestrial animals were nearly absent (namely “equatorial tetrapod gap”; Sun et al., 2012). However, the nature, duration and range of the “equatorial tetrapod gap” remain debated. Allen et al. (2020) show poleward migrations of terrestrial tetrapods during the Late Permian to Middle Triassic, with marine reptile diversity peak still restricted to northern low latitudes. Romano et al. (2020) argued that the Early Triassic equatorial terrestrial tetrapod gap would be narrower and restricted the “death belt” between 15° N and about 31° S, while Liu et al. (2022) consider that the exact boundaries of this gap likely varied with climate change (hot phases). Moreover, duration of the gap is also questioned, it’s long-lasting (Late Permian to Middle Triassic), during Induan (Bernardi et al., 2018), or from Induan to the early Spathian (Liu et al., 2022). Regardless of these discrepancies, all the related studies show the existence of the “low latitudinal tetrapod gap”, which is mentioned as background information. On this basis, this study aims to reveal when and how terrestrial ecosystems recovered from the “tropic dead zone” from the ecological point of view, rather than tetrapods only.

The fast recovered terrestrial ecosystems are represented by diverse traces, and concurrent tetrapods and plants found in the Heshanggou Formation. We acknowledge that the chronostratigraphy of the Lower Triassic in North China (and most of continental basins globally) are not controlled by precise ages, this formation, however, could be constrained to Spathian (or even straddle to earliest Middle Triassic), based on integrated magnetostratigraphic correlation, fossil records and geochemical data (Liu, 2018; Guo et al., 2022). The Smithian-age ichnofaunas here are not interpreted as a rapidly recovering biota, but early occurring opportunist-dominated communities that explore the empty ecospace under inhospitable environments. Our study also constrains roughly the “tropical dead zone” from Induan to late Smithian in North China (Fig. 4).

References:

Allen, B.J., et al. 2020. The latitudinal diversity gradient of tetrapods across the Permo-Triassic mass extinction and recovery interval. Proc Biol Sci 287, 20201125. https://doi.org/10.1098/rspb.2020.1125

Bernardi, M., et al. 2018. Tetrapod distribution and temperature rise during the Permian-Triassic mass extinction. Proc Biol Sci 285, 20172331. https://doi.org/10.1098/rspb.2017.2331

Guo, W., et al. 2022. Late Permian–Middle Triassic magnetostratigraphy in North China and its implications for terrestrial-marine correlations. Earth Planet. Sci. Lett. 585, 117519. https://doi.org/10.1016/j.epsl.2022.117519

Liu, J. 2018. New progress on the correlation of Chinese terrestrial Permo-Triassic strata. Vertebrata Palasiatica, 56, 327-342. 10.19615/j.cnki.1000-3118.180709

Liu, J., et al. 2021. Permo-Triassic tetrapods and their climate implications. Glob. Planet. Change 103618. https://doi.org/10.1016/j.gloplacha.2021.103618

Romano, M., et al. 2020. Early Triassic terrestrial tetrapod fauna: a review. Earth-Sci. Rev. 210, 103331. https://doi.org/10.1016/j.earscirev.2020.103331

Sun, Y., er al. 2012. Lethally hot temperatures during the early triassic greenhouse. Science 338, 366–70. https://doi.org/10.1126/science.1224126

Considering the somewhat equivocal evidence and controversial ideas about the P/T transition, the introduction could be improved by describing how the idea of a "tropic dead zone" arose against the background of earlier ideas, alternative views, and conflicting data. In the discussion section, alternative interpretations of the extensive data presented here - e.g. proximal-distal shifts in lithofacies with respect to the sediment source, sea level changes, preservation bias, the local occurrence of hostile environments instead of a regional scale, etc. should be discussed, also to avoid the impression that the author's conclusion was driven by confirmation bias.

As mentioned above, it’s still controversial about the nature, duration and range of the “equatorial tetrapod gap”, which primarily derived from the database (body fossils only vs. both skeletal and footprint data) and analytical methods. However, detailed discussions about these differences are beyond the scope of our study. This paper provides new evidence for the "tropical dead zone" from the ecological perspective (invertebrate ichnology, paleobotany and newly found tetrapods). Our results show that the "tropical dead zone" in North China terminated in the Smithian, followed by the reappearance of many animals in the Spathian, shedding light on the more rapidly recovering terrestrial ecosystems than previously thought.

We have improved the Introduction section by providing a summary of the “equatorial tetrapod gap”. Lines 33-35: “A tropical “tetrapod gap”, spanning between 15°N and ~31°S, prevailed through the Early Triassic, or at least during particular intervals of intense global warming (Bernardi et al., 2018; Allen et al., 2020; Romano et al., 2020; Liu et al., 2022).” is revised to:

“A tropical “tetrapod gap”, spanning between 15°N and ~31°S, prevailed in the Early Triassic, or at particular interval of intense global warming, even though the nature, duration and range remain debated (Bernardi et al., 2018; Allen et al., 2020; Romano et al., 2020; Liu et al., 2022).”

In the Discussion section, Lines 180-181: “Although the specimens are not yet fully prepared for taxonomic description, they clearly show the existence of tetrapod at this level” is revised to:

“Although the specimens are not yet fully prepared for taxonomic description, they clearly show the existence of tetrapods at this level, narrowing the “tetrapod gap” to the Spathian.”

we also add a new paragraph from Line 208:

“Our results also shed light on the timing of the tropical dead zone. The late Smithian-age ichnofauna, although impoverished, represents early opportunist-dominated communities that explored empty ecospace under inhospitable environments, which constrains the equatorial death belt to the late Smithian in North China.”

Contrary to the authors' claim, Figures S7 and S8 suggest that burrow size does not vary much within the studied sections. Size decreases and increases in the Shichuanhe and Liulin sections do not contemporaneously, are usually within the error-bar range, and might be driven by ichnotaxa composition, i.e. the presence or absence of larger ichnotaxa, rather than by size changes in the same ichnotaxon (and producer group). Here the measurement data would be needed as well to check the basis of the authors' interpretations.

We thank the reviewer for highlighting this important point. We have checked the accuracy of our raw data. Both the average size of all ichnogenera and single ichnogenera do not change obviously, but increase slightly upwards in the Spathian (Figures S7c and S8). This tendency is congruent with other coeval studies in North China (e.g., Shu et al., 2018; Xing et al., 2020). The presence of larger ichnotaxa will indeed improve the average sizes of fossil-bearing horizons, however, burrows of single ichnogenera in the Spathian generally show wider size distributions than in the Smithian, which might be associated with enriched producer groups or different growth stages of the same biota.

The asynchronous burrow size changes in the Shichuanhe and Liulin sections could be attributed to sedimentary facies. Late Permian deposits at Shichuanhe are finer than those at Linlin, which is located at the basin margin. As a result, tiny traces, like Helminthoidichnites, which were widely distributed at Shichuanhe, are absent at Linlin section. Those traces significantly reduce the average sizes in this interval, leading to inconsistent size variation patterns.

References:

Shu, W., et al. 2018. Limuloid trackways from Permian-Triassic continental successions of North China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 508, 71–90. https://doi.org/10.1016/j.palaeo.2018.07.022

Xing, Z.F., et al. 2020. Trace fossils from the Lower Triassic of North China—a potential signature of the gradual recovery of a terrestrial ecosystem. Palaeoworld 30, 95–105. https://doi.org/10.1016/j.palwor.2020.06.002

Some arthropod tracks assigned here to Kouphichnium might not represent limulid traces but other (non-marine) arthropod taxa in accordance with their occurrence in terrestrial facies/non-marine units of the succession. More generally, the ichnotaxonomy of arthropod trackways is not yet well reserved - beyond Kouphichnium and Diplichnites various similar-looking types may occur that can have a variety of distinct insect, crustacean, millipede, etc. producers (including larval stages).

Well, individual trace-makers can produce different traces, and different organisms can make morphologically similar traces. In consideration of this, it’s hard to give a one-on-one relationship between trace fossils and their producers in most cases, especially for the invertebrates. So, Kouphichnium could be made by arthropods other than limuloidss.

However, horseshoe crabs, originating in the early Ordovician, invaded freshwater environments twice in the Paleozoic and once in the Mesozoic (Lamsdell, 2016), and their body fossils have been found from the Early Triassic of Germany (e.g., Hauschke and Wilde, 2008) and North China (which occur with their traces; unpublished data). Accordingly, we tentatively speculate Kouphichnium found in this interval could be primarily produced by limuloids.

References:

Hauschke, N., Wilde, V. 2008. Limuliden aus dem Oberen Buntsandstein von Süddeutschland. Hallesches Jahrb. Für Geowiss. 30, 21–26.

Lamsdell, J.C. 2016. Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation. Palaeontology 59, 181–194. https://doi.org/10.1111/pala.12220

Recommendations for the authors:

Reviewer #1 (Recommendations for The Authors):

(1) Line 112 - was identified during..; please change to ...was identified in successions of late Changsian-early Smithian age.

Revised as suggested.

(2) Line 116 - change prolong to prolonged.

Revised as suggested.

(3) Line 121 - change ichnofaunal to ichnofauna (check the entire sentence).

We checked the manuscript thoroughly and revised as suggested.

(4) Figure 1 caption - check sentence starting with - Base map...(delete 'of is')

Revised as suggested.

(5) Line 471 - tiny instead of tinny.

Revised as suggested.

(6) Figure S9 - would it be possible to include this reconstruction in the main manuscript?

We have moved the artistic illustration to the main text as Figure 5.

(7) Add the illustrators name / or indicate if it is produced by AI.

We have added the sentence “The artistic illustration is credited to J. Sun” at the end.

Reviewer #2 (Recommendations for The Authors):

(1) Line 15 – change 252 million years ago to ca. 252 million years ago.

Revised as suggested.

(2) Line 18 – change low-latitude North China to low-latitude present-day North China.

Actually, the paleolatitude of North China during the Early Triassic is about 17-18°N according to paleomagnetic results (Huang et al., 2018; Guo et al., 2022,).

References:

Guo, W., et al. 2022. Late Permian–Middle Triassic magnetostratigraphy in North China and its implications for terrestrial-marine correlations. Earth Planet. Sci. Lett. 585, 117519. https://doi.org/10.1016/j.epsl.2022.117519

Huang, B., et al. 2018. Paleomagnetic constraints on the paleogeography of the east asian blocks during Late Paleozoic and Early Mesozoic times. Earth-Sci. Rev. 186, 8–36. https://doi.org/10.1016/j.earscirev.2018.02.004

(3) Line 25 - "possible" doesn't seem the appropriate term here for the structure of the sentence. Could it be "to make possible" that it meant? Or otherwise you could write "possibly". Please revise this.

Revised “possible” to “possibly”.

(4) Line 33 – change “are” to “were”.

Revised as suggested.

(5) Line 43 – There are other, more appropriate articles that should (also) be cited here, especially because Mujal et al. (2017) doesn't deal with the Central European Basin (so you could even remove this reference). For sure this one should be cited:

Scholze, F., Wang, Z., Kirscher, U., Kraft, J., Schneider, J.W., Götz, A.E., Joachimski, M.M., Bachtadse, V., 2017. A multistratigraphic approach to pinpoint the Permian-Triassic boundary in continental deposits: the Zechstein–Lower Buntsandstein transition in Germany. Glob. Planet. Chang. 152, 129–151. http://dx.doi.org/10.1016/j.gloplacha.2017.03.004.

We have replaced Mujal’s paper with Scholze et al., (2017) in the main text.

(6) Line 46 – change “Roopnarinev et al., 2019” to “Roopnarine et al., 2019”.

Revised as suggested.

(7) Line 53 – Here Mujal et al. (2017) would be more appropriate, since it deals with a basin from the western peri-Tethys, also, this other article by Mujal et al. (2017) discussed the recovery in the western peri-Tethys based on tetrapod footprints:

Mujal, E., Fortuny, J., Bolet, A., Oms, O., López, J.Á., 2017. An archosauromorph dominated ichnoassemblage in fluvial settings from the late Early Triassic of the Catalan Pyrenees (NE Iberian Peninsula). PLoS One 12 (4), e0174693. http://dx.doi.org/10.1371/journal.pone.0174693.

Revised as suggested.

(8) Line 58 – change “relatively diversified trace fossils have been found during the late Early Triassic” to “because relatively diversified trace fossils have been found in upper Lower Triassic deposits”.

Revised as suggested.

(9) Line 58 – change “recovered” to “ecosystems recovered”.

Revised as suggested.

(10) Line 81 – These two paragraphs could be under a section named Geological setting or similar.

Yes, these two paragraphs are brief introductions of the geological background of North China, so we change the section name to “Geological Settings and Methods”.

(11) Line 99 – change “behavioural” to “behavioral”.

Revised as suggested and check spelling throughout.

(12) Line 103 – add “is” before adopted.

The sentence “Tiering, referring to the life position of an animal vertically in the sediment, is divided into surficial, semi-infaunal (0–0.5 cm), shallow (0.5–6 cm), intermediate (6–12 cm) and deep infaunal tiers (> 12 cm), adopted from Minter et al. (2017).” is changed to “…, based on Minter et al. (2017).”

(13) Line 113 –change “mainly” to “were mainly”.

Revised as suggested

(14) Line 116 - change prolong to prolonged.

Revised as suggested.

(15) Line 121 – add “preserved” before in.

Revised as suggested.

(16) Line 123 - change “were” to “are”.

Revised as suggested.

(17) Line 127 – “Kouphichnium” instead of “Kouphichnim”.

Revised as suggested.

(18) Line 135 – change to “Occupied by”.

Revised as suggested.

(19) Line 140 – change “bioturbations” to “bioturbated deposits”.

Revised as suggested.

(20) Line 145 – “Spathian” rather than “Spthian”.

Revised as suggested.

(21) Line 140 – change “displayed” to “displays”.

Revised as suggested.

(22) Line 160 – change “continental” to “terrestrial”.

Revised as suggested.

(23) Line 165 – “Marchetti” rather than “Marchettti”.

Revised as suggested.

(24) Line 168 – change “relationships” to “relation”.

Revised as suggested.

(25) Line 177 – “including” instead of “includes”.

Revised as suggested.

(26) Line 181 and Line 214– change “tetrapod” to “tetrapods”.

Revised as suggested.

(27) Line 195 and Line 218 – change “cooccurred” to “co-occurring”.

Revised as suggested.

(28) Line 540 – delete “herein”.

Revised as suggested.

(28) Line 559 – “Helminthoidichnites tenuis”, it should be in italics.

Revised as suggested.