Ostracodal evolution during the Permian–Triassic transition at the Youping section of the Nanpanjiang Basin

The Permian–Triassic mass extinction has been considered the largest bio-crisis of the Phanerozoic, with more than 90% of marine species extinct. Previous studies showed that ostracods suffered various extinction patterns in different localities and were relatively enriched in the lowermost Triassic shallow marine microbialites. Multiple hypotheses have been put forward to explore the reasons for this phenomenon. Abundant ostracod fossils were collected from the microbialite-bearing Youping section in the Nanpanjiang Basin. 45 species in 22 genera from Wujiaping Formation increased dramatically to 104 species in 33 genera from the microbialites of basal Luolou Formation. However, Ostracods from the Youping section suffered severe extinction during the second phase of the Permian–Triassic crisis, i.e., the earliest Triassic mass extinction (ETME), rather than the first phase, i.e., the latest Permian mass extinction (LPEM). In addition, the Sørenson coefficient has been used to examine the similarity of faunal associations among different sections of the Permian–Triassic transitional beds. There was no significant differences for ostracods between microbialites and non-microbialites sections based on similarity analysis. Thus, we proposed that “Shallow marine refuge” hypothesis could explain the high diversity and high abundance of ostracods of the Permian–Triassic transitional beds. Besides, ostracods showed remarkable geographical differentiation at both regional and global scales during the Permian–Triassic transitional beds and were presumably controlled by geographical isolation.

In comparison with fossil records in various facies, ostracods enriched considerably in the Permian-Triassic boundary microbialites (PTBMs; Crasquin et al., 2008Crasquin et al., , 2010Liu et al., 2010;Forel et al., 2013aForel et al., , 2015. A few hypotheses were proposed to explain the high abundance and diversity of ostracods after the latest Permian mass extinction, i.e., the "microbialites refuge" hypothesis and the "shallow-water refuge" hypothesis (Forel et al., 2013a;Qiu et al., 2019). The "microbialites refuge" hypothesis considered Permian-Triassic microbialites as a refuge for ostracods (Forel et al., 2013a), however, the higher diversity and abundances of molluscan fossils in non-microbialites facies than in microbialites facies indicated the preferential preservation effect of transported fossils in microbialites (Foster et al., 2019). The abundant ostracods from non-microbialites sections Yangou and Aras Valley also challenge the "microbialites refuge" hypothesis but support the "shallow-water refuge" hypothesis (Qiu et al., 2019), which still needs more evidence.
In order to explore the extinction and survival patterns of the ostracod fauna during the Permian-Triassic transition, we investigated the ostracods distribution of the Youping section, i.e., a PTBMs bearing shallow marine carbonates continuous section, in the Nanpanjiang Basin of South China Block. Meanwhile, quantified faunal similarity calculation is employed to test the existing hypotheses on the blooming dynamics of ostracods in the PTBMs.

Geological setting
The South China Block, located at the eastern margin of the Paleo-Tethys Ocean during the Permian and Triassic periods, consisting of the Yangtze Platform, Zhejiang-Fujian-Guangdong clastic region and Nanpanjiang Basin (Figure 1; Tong and Yin, 2002;Yin et al., 2014). The Nanpanjiang Basin, which featured relatively deep water sediments, is mainly distributed in Guangxi Province and southern Guizhou Province (Enos et al., 2006). Several isolated carbonate platforms, including the Great Bank of Guizhou, Chongzuo, Pingguo, Debao, Jinxi and Luolou platforms, had developed in the Nanpanjiang Basin during the Late Permian to earliest Triassic (Figure 1; Lehrmann et al., 1998;Enos et al., 2006).
The Youping section is about 10 km north of Youping Town, Leye County, Guangxi Province, China. The succession, which has a thickness of 16.2 m, comprises the Upper Permian Wujiaping Formation and Lower Triassic Luolou Formation. The Wujiaping Formation was dominated by dark-grey thick-bedded bioclastic limestones, indicating a shallow platform environment ( Figure 2). The basal Luolou Formation is composed of thick-bedded microbialites, overlied by thin-bedded to medium-bedded limestones and intercalated mudstones (Figure 2). The microbialites is about 8.2 m in thickness. The base of the microbialites of the Youping section was assigned to be Triassic in age, as for the presence of Triassic foraminifers and the carbon isotope excursion (Bagherpour et al., 2017).

Materials and methods
A total of 24 samples were collected from the Youping section, including five samples from the Wujiaping Formation, and 16 samples from the PTBMs of basal Luolou Formation, with three additional samples overlying the PTBMs (Figure 2). Three sample (YP-6, YP-11 and YP-14) from PTBMs yielded ostracods but were not analyzed to the species level. Bulk samples were finely crushed into tiny pieces of 1 cm 3 in the laboratory and then dissolved by acetic acid in a heated sand bath at a temperature of 70-80°C for an interval ranging from two days to three weeks. The undissolved sample remains were washed through 200 meshed sieves and dried. In total, 3,717 ostracod specimens have been obtained. Almost all specimens were The individual numbers, species and genera richness, and relative abundances at the genus and family levels were used to reflect the ostracodal diversity changes in this study ( Figure 6). Cluster analysis was carried out to recognize different ostracod communities through the Paleontological Statistics Software Package (PAST version 4.03) (Hammer et al., 2001). The Bray-Curtis parameter was selected to compare the similarities between ostracod fossils from different samples. Four communities were recognized ( Figure 7). Besides, Shannon index, Evenness index and Dominance index were taken as diversity indexes (Figure 7). In addition, rarefaction analysis was taken out to test the sampling efficiency of various communities (Figure 7). When the rarefaction curve becomes flat and shows a typical banana shape, the sample could be considered sufficient (Hammer et al., 2001). The rarefaction curves for Community 2 and 3 indicate sufficient sampling, while the steep rarefaction curves for Community 1 and 4 indicate insufficient sampling (Figure 8).
The fauna similarity between different sections is expressed by the Sørenson coefficient (also known as the Dice coefficient). Sørenson coefficient could be calculated by the following formula: Where QS is the Sørenson coefficient, a and b are the numbers of the genera at each section, and c means the number of shared genera between different sections (Sørenson, 1948;Jost et al., 2011). The Sørenson coefficient is positively correlated with the numbers of shared genera ( Table 2). The QS value has been widely applied to analyze fauna similarities between different sites or communities, such as radiolarians, ammonites, and bivalves (e.g., Zacaï et al., 2016;Suárez-Mozo et al., 2021;Xiao et al., in press). The similarity of ostracod faunas at the genus level between different sections has been recovered (Table 2; Figure 9). The values of similarity are divided into three levels: low similarity (QS < 0.3), moderate similarity (QS between 0.3 and 0.5), and high similarity (QS > 0.5).

Results
The individual numbers of ostracods from each sample within the microbialites are usually over 130, significantly higher than those of the Wujiaping Formation ( Figure 6). The specimen abundance increased abruptly from 48 to 322, followed by a peak of 763 in the Distribution of ostracods fossils at the Youping section.
Frontiers in Ecology and Evolution 04 frontiersin.org upper PTBMs (sample YP-18) ( Figure 6). A distinct decrease, from 587 to 17, of specimen richness occurred at the top of PTBMs. No ostracods were found in sediments overlying the microbialites ( Figure 6). Both species and genus richness showed a fluctuated increasing trend from the Wujiaping Formation to the basal Luolou Formation ( Figure 6). Only four species went extinct at the formation boundary, whilst all genera survived into the PTBMs (Figure 2). There was no obvious diversity change in samples before and above the PTB boundary. Significant diversity reduction, from 55 species of 22 genera to 12 species of eight genera, was not occurring until the upper PTBMs (sample YP-20; Figure 6).
Genus Bairdia was one of the most abundant genera, with the individual proportion ranging from 3.33% (sample YP-17) to 66.67% (sample YP-4), however, the individual proportion of genus Bairdia decreased gradually at the PTBMs of the Youping section ( Figure 6). Genus Paracypris and Liuzhinia increased in abundance significantly at the formational contact, with Paracypris increased from 4.17% at YP-3 to 13.95% at YP-13 and Liuzhinia from 4.17% at YP-3 to 16.67% at YP-20, whilst the individual proportion of genus Bairdiacypris remaining stable ( Figure 6). Genus Cavellina showed up with the development of PTBMs, occupying a certain proportion ranging from 2.7% at YP-10 to a high of 25% at YP-20 ( Figure 6). At the family level, Bairdiidae dominated all samples, with proportions commonly higher than 50% ( Figure 6). Family Cavellinidae and Bythocyprididae were new in the PTBMs, with the lowest value of 2.78% (sample YP-8) and the highest value of 25% (sample YP-20), while the relative abundances of Family Paraparchitidae and Acratiidae decreased sharply in the upper part of PTBMs ( Figure 6). Four communities have been recognized through cluster analysis (Figure 7). Community 1 consist of samples YP-1 to YP-5, corresponding to the limestone of the Wujiaping Formation, and is characterized by abundant Bairdia (38.89%) and Reviya (22.22%). Community 2 contains samples from YP-7 to YP-17 in the PTBMs and was dominated by the genus Bairdia (23.10%), Liuzhinia (22.12%) and Praezabythocypris (19.49%). Samples YP-18 and YP-19 in the PTBMs are clustered as Community 3, which was dominated by the genus Liuzhinia (37.04%) and Praezabythocypris (17.04%). Sample YP-20 from the uppermost part of PTBMs is assigned to Community 4, which was featured by the genus Bairdia (23.53%), Cavellina (17.65%) and Praezabythocypris (17.65%). Diversity indexes of four communities showed significant variations. The Shannon index decreased gradually, but the Dominance index increased gradually from Community 1 to Community 4, while the Evenness index declined from communities 1 to 3, followed by a rebound in community 4 (Figure 7).

Extinction pattern of ostracods during the Permian-Triassic
The diversity of the ostracods at the Youping section increased from the uppermost Permian Wujiaping Formation to the Lower  Table 1). At the Bulla section of Italy (Table 1), ostracodal diversity reduced from 54 species in 25 genera to nine species in eight genera from the conodont Hindeodus praeparvus zone (Crasquin et al., 2008). A similar rapid decrease of ostracods from the uppermost Permian to the Permain-Triassic transitional beds (PTTB) ( Table 1) was also reported at the Dajiang section of South China (Forel, 2012), Elikah River section of north Iran (Forel et al., 2015), Bálvány North section of Hungary (Forel et al., 2013a), and Çürük Dağ section of Turkey (Crasquin et al., 2004a,b). However, at the Youping section of this study, 45 species in 22 genera of ostracod fauna occurred in the uppermost Permian limestone and increased to 104 species in 33 genera from the PTBMs (Figure 2; Table 1). Similarly, ostracodal diversity increases from Permian bioclastic limestone to the PTTB also have been observed at several sections of shallow carbonate facies, e.g., the Aras Valley (Gliwa et al., 2021), Zuodeng (Wan et al., 2019), and Panjiazhang sections (Wan, 2021; Table 1). Ostracod disappeared at the top of the PTBMs at the Youping section, potentially corresponding to the ETME, i.e., the second extinction phase of the Permian-Triassic crisis in Song et al. (2013). The ostracodal taxonomic diversity of many microbialite-bearing shallow carbonate sections, e.g., Youping, Panjiazhuang, and Zuodeng, suffered a critical drop along with the demises of microbialites (Table 1). No ostracod taxa was observed in samples YP-21 to YP-24 at the Youping section, and only two species in sample Zd-44 survived in the thin-bedded limestone overlying PTBMs at the Zuodeng Frontiers in Ecology and Evolution 07 frontiersin.org section (Wan et al., 2019). The Panjiazhuang section also shows a decreasing trend from 68 species in 17 genera in beds two and three to 27 species in seven genera in bed 4 (Wan, 2021). Similarly, ostracod diversity of the Aras Valley section reduced sharply from 51 species in 19 genera during the conodont Hindeodus praeparvus zone to five species in three genera from the conodont Isarcicella staeschei zone (Gliwa et al., 2021). A set of microbialites usually formed on the carbonate platforms in the aftermath of the EPME (e.g., Lehrmann et al., 1998;Wang et al., 2005;Kershaw et al., 2007Kershaw et al., , 2012Tian et al., 2019;Foster et al., 2020). Studies on several microbialite-bearing sections, including Dajiang, Taiping and Pojue sections, suggest that the PTB is at the base of microbialites, for the first occurrence of Hindeodus parvus Wang et al., 2016;Xiao et al., 2018;Chen et al., 2019). Although the precise age of the terminal PTBMs is unsure, the high-resolution conodont biostratigraphic zonation studies of Dajiang and Cili sections show the first occurrence of Isarcicella isarcica from the thinbedded limestone overlying the PTBMs Wang et al., 2016), correlating to the second phase of the Permian-Triassic crisis, i.e., Earliest Triassic mass extinction (ETME; Song et al., 2013). Thus, the base and top of the Youping PTBMs are equivalent to the LPME and ETME horizons, respectively. Song et al. (2013) constrained the earliest Triassic mass extinction (ETME) to the Isarcicella staeschei zone. However, the Youping section shows that the ETME occurred at the top of the microbialites, which corresponds to the upper part of the Hindeodus parvus zone (Bagherpour et al., 2017), implying a potential earlier ETME at Youping.

Biogeographic controls on the ostracods during the Permian-Triassic transition
The "microbial-related refuge" hypothesis was proposed to explain the extremely high abundance and diversity of PTBMs (Forel et al., 2013b). Indeed, extremely high ostracodal diversity occurred at the Temporal variations of the ostracodal diversity, abundances and compositions throughout the Youping section.

FIGURE 8
Rarefaction curves for four ostracod communities of the Youping section. Comm: Community.
Frontiers in Ecology and Evolution 09 frontiersin.org (Forel, 2012), and Çürük Dağ sections (Crasquin et al., 2004a,b), less diverse than the non-PTBMs bearing Yangou and Aras valley sections (Qiu et al., 2019;Gliwa et al., 2021), mismatching the "microbial related refuge" hypothesis. Furthermore, the "microbial related refuge" hypothesis is also denied by the ostracodal faunal similarity analyses. Ostracodal fauna of PTBMs bearing sections show varied similarities, from low to high (Figure 9). Only moderate similarities were recorded among the sections of isolated platforms, i.e., Dajiang (Forel, 2012), Zuodeng (Wan et al., 2019), Pojue (Wan, 2021) and Youping sections, with Laolongdong (Crasquin and Kershaw, 2005), Chongyang (Liu et al., 2010) and Zhaixia (Wan, 2021) sections of the Yangtze Platform, albeit PTBMs occurred at all of them, implying no significant microbial related facies control. The highest similarities occurred at the Yangtze Platform sections, including the PTBMs bearing Laolongdong (Crasquin and Kershaw, 2005), Chongyang (Liu et al.,   Frontiers in Ecology and Evolution 10 frontiersin.org 2010), Zhaixia (Wan, 2021), Panjiazhuang (Wan, 2021) and the non-PTBMs bearing Yangou section, somewhat supporting the "shallow marine refuge" hypothesis (Qiu et al., 2019). In addition, moderate to high fauna similarities were shown between Bulla (Crasquin et al., 2008) and Bálvány-North (Forel et al., 2013a) in western Paleotethys with Aras valley (Gliwa et al., 2021) and Elikah River (Forel et al., 2015) in Cimmerian terranes (Table 2), indicating weak geographic isolation. Increases of the cosmopolitan taxa in the post mass extinction, both in the marine invertebrates and terrestrial tetrapods, were documented (Button et al., 2017;Dai and Song, 2020;Zhang et al., 2022), so as the ostracods. Dai and Song (2020) proposed three models, i.e., (a) selective extinction among endemic taxa, (b) endemics becoming cosmopolitans and (c) newly originated cosmopolitans, for the elevated cosmopolitanism across the Permian-Triassic extinction event. In total, 50 ostracod genera had been discovered from the Permian-Triassic transitional beds mentioned above, at least nine of them were cosmopolitan. At the Youping section, the cosmopolitans contain Callicythere, Hollinella, Fabalicypris, Langdaia, Acratia, Paracypris, Liuzhinia, Bairdia and Bairdiacypris, among which Acratia, Bairdia, Bairdiacypris, Langdaia, Paracypris belong to Model b and Callicythere, Fabalicypris, Hollinella belong to Model c. Besides, the significant ostracod community transition from Community 1 to Community 2 around the Permian-Triassic boundary implies the dominance of several above-mentioned cosmopolitan genera, e.g., Bairdia and Liuzhinia. Although we do not have a specific biogeographic connectedness index of ostracods calculated as other studied groups, we hypotheses that the cosmopolitans elevation of ostracods might be less significant than ammonoids, anthozoan and bryozoan (Dai and Song, 2020;Zhang et al., 2022) during the Permian-Triassic mass extinction event, since ostracods are much more hightemperature and low oxygen tolerances than most other marine invertebrates (Song et al., 2014). Further biogeographic studies are needed to test our scenario to shed new light on deciphering the environmental dynamics of the extinction and survival of ostracods during the Permian-Triassic mass extinction.

Conclusion
This study presented the taxonomic distribution of ostracod fossils from the microbialite-bearing Youping section in the Nanpanjiang Basin: 45 species in 22 genera were found from the Wujiaping Formation while 104 species in 33 genera were identified from the microbialites of basal Luolou Formation. Ostracods disappeared at the top of microbialites, implying a potential earlier ETME at the Youping section. The similarity analysis did not show Frontiers in Ecology and Evolution 11 frontiersin.org significant differences between microbialites and non-microbialites sections, and does not support the "microbial related refuge" hypothesis, but supports the "shallow marine refuge" hypothesis. The biogeographic distribution of ostracods during the Permian-Triassic extinction requires further research to clarify the role of temperature and oxygen levels in the extinction event.

Data availability statement
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.