Earth-Science Reviews 149 (2015) 1–4
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Global review of the Permian–Triassic mass extinction and subsequent recovery: Part II
1. IGCP Projects 572 and 630 The present volume represents Part II of a thematic issue of EarthScience Reviews titled “Global Review of the Permian-Triassic Mass Extinction and Subsequent Recovery”. Part I of this thematic issue was published in May 2014 as Earth-Science Reviews Volume 137 (see Chen et al., 2014). The nine studies in the present volume rely extensively on research undertaken in the context of IGCP Project 572 (“Restoration of Marine Ecosystems following the Permian-Triassic Mass Extinction: Lessons for the Present”), which brought together a large number of geoscientists from around the world for a series of ﬁeld workshops, meetings, and symposia from 2008 to 2014. IGCP 572 members published an average of ~120 research papers annually, with many studies contributing to a better understanding of the mechanisms and causes of the PTB biocrisis and the protracted recovery that followed it. This project yielded eight journal special issues prior to the two Earth-Science Reviews volumes (Algeo et al., 2011b, 2013a; Chen et al., 2009, 2013; Crasquin, 2013; Heydari et al., 2010; Metcalfe and Isozaki, 2009; Xie and Kershaw, 2012). A successor project, IGCP 630 (“Permian-Triassic Climatic and Environmental Extremes and Biotic Response”) was initiated in 2014 and will run through 2019. Its principal goals are to better understand (1) connections between extreme warming, environmental changes, and contemporaneous biotic decline and recovery, and (2) interactions between terrestrial and marine ecosystems and their interdependent response to large-scale climate and environmental changes. 2. The Permian-Triassic boundary crisis and Early Triassic recovery The ~ 252-Ma Permian–Triassic boundary (PTB) mass extinction represents the largest biocrisis of the Phanerozoic (Alroy et al., 2008; Sepkoski, 1984; see reviews in Algeo et al., 2011b, and Chen et al., 2014). It eliminated ~90% of marine and ~70% of terrestrial species, triggering far-reaching changes in ecosystem structure and dominance among biotic clades (Chen and Benton, 2012; Chen et al., 2010; Foster and Twitchett, 2014). The pattern and signiﬁcance of these changes in the Meishan global stratotype section and point (GSSP) are considered in a paper in the present volume by Chen et al. (2015b). The recovery of marine and terrestrial ecosystems following this biocrisis was a protracted process, lasting (depending on the deﬁnition of “recovery”) on the order of 5 million years or longer (Bottjer et al., 2008). Changes in marine ecosystems occurred at every trophic level, including among primary producers (Luo et al., 2014a,b; Xie et al., 2005). The extent of productivity changes during and following the PTB biocrisis is the
http://dx.doi.org/10.1016/j.earscirev.2015.09.007 0012-8252/© 2015 Published by Elsevier B.V.
focus of a paper in the present volume by Shen et al. (2015). Equally far-reaching changes took place in terrestrial ecosystems (Benton and Newell, 2014; Hochuli et al., 2010), in which previously dominant conifer forests were widely replaced by disaster taxa, as documented by two studies in the present volume (Tewari et al., 2015; Yu et al., 2015). The causes of the PTB mass extinction are better understood today than several decades ago, when proposals linking this biocrisis to the eruption of the Siberian Traps Large Igneous Province were ﬁrst advanced (e.g., Campbell et al., 1992; Renne et al., 1995). Recent work has implicated massive releases of the greenhouse gases CO2 and CH4 to the atmosphere (Black et al., 2012; Svensen et al., 2009), resulting in climatic hyperwarming during at least the ﬁrst ~ 1.5 Myr of the Early Triassic (Joachimski et al., 2012; Romano et al., 2013; Sun et al., 2012; see review by Cui and Kump, 2015, in the present volume). Warming of the ocean surface layer and a ﬂattening of the equator-topole temperature gradient (Galfetti, et al., 2007; Hotinski et al., 2001) were responsible for stagnation of global-ocean overturning circulation, leading to widespread development of ocean anoxia (Grice et al., 2005; Wignall and Twitchett, 1996), especially in the form of expanded oxygen-minimum zones in the oceanic thermocline region (Algeo et al., 2010, 2011a; Winguth and Winguth, 2012). This hyperwarming event was a major factor in contemporaneous global changes, e.g., intensiﬁcation of subaerial weathering (Algeo and Twitchett, 2010; Algeo et al., 2011b), ocean stratiﬁcation (Song et al., 2013), and ocean acidiﬁcation (Hinojosa et al., 2012), as well as changes in ocean chemistry (Li et al., 2015, this volume). These stresses appear to have begun concurrently with the PTB mass extinction and to have continued, with some ﬂuctuations in intensity, at least through the Early Triassic (Brennecka et al., 2011; Retallack et al., 2011). The relationship of environmental (re)stabilization to marine ecosystem recovery is the focus of a study by Wei et al. (2015) and is also considered in the study of the Meishan GSSP by Chen et al. (2015b), both in this volume. Many of the environmental changes that occurred during the PTB mass extinction have analogs in the modern world, including rapid climatic warming (Levitus et al., 2001), enhanced continental erosion (Syvitski et al., 2005), slowing ocean circulation (Rahmstorf et al., 2015), ocean acidiﬁcation (Orr et al., 2005), and marine dead zones (Diaz and Rosenberg, 2008). Although the effects of these changes on the biosphere have been modest to date (e.g., Chen et al., 2011), there is a growing scientiﬁc consensus that the Earth may be on the cusp of another mass extinction (Barnosky et al., 2011). Because biotic systems are not easily modeled on a ﬁrst-principles basis, study of ancient biotic crises such as the PTB mass extinction has the potential to provide insights regarding the extent of biosphere resilience in the face of global
climatic and environmental changes. The studies in the present volume of Earth-Science Reviews are relevant in this regard. The present volume also includes two methods papers. The paper by Schoepfer et al. (2015) examines the relationship between productivity in modern marine environments and its record in the sediment, as proxied by total organic carbon, organic phosphorus, and biogenic barium. This study derived a series of equations based on these geochemical proxies that can provide quantitative estimates of productivity in paleomarine systems, as shown by Shen et al. (2015). The paper by Chen et al. (2015a) examines REE patterns in conodonts from several PTB sections. The signiﬁcance of this paper lies not in any revelations about contemporaneous marine environmental changes but, rather, in its conclusion that the REE signatures of many, and perhaps most, bioapatite fossils are acquired from diagenetic porewaters rather than from seawater and, thus, that the REE composition of such fossils has little if any utility for reconstructing paleoenvironmental conditions.
3. Synopsis of individual papers in this volume The global stratotype section and point (GSSP) for the PermianTriassic boundary at Meishan, Zhejiang Province, China has been the focus of intensive research for several decades, resulting in the publication of some hundreds of technical papers. Chen et al. (2015b) undertake a comprehensive integration and assessment of the extant biostratigraphic, chemostratigraphic, and other types of data from Meishan. They focus on the uppermost Permian-lowermost Triassic interval, comprising Beds 22-24 of the Changxing Formation and Beds 2559 of the Yinkeng Formation, providing a bed-by-bed description of the lithologic, paleobiotic, ichnologic, and geochemical character of the section. Their analysis is undertaken within a revised conodont biozonation framework consisting of eight zones ranging from the Clarkina yini Zone through the C. planata Zone. Both fossil and ichnologic data show that PTB ecologic crisis comprised two discrete stages, coinciding with but lagging slightly behind the 1st and 2nd stages of biodiversity loss during the PTB mass extinction. This study infers that the precipitous decline in biotic diversity and abundance at the end-Permian extinction horizon was more closely associated with a sharp rise in SSTs rather than with deteriorating redox conditions, because the Meishan section records frequent ﬂuctuations between oxic and euxinic conditions throughout the latest Permian-earliest Triassic study interval. The ﬁrst pulse of the biocrisis coincided with a rapid SST increase of ~9 °C and a short anoxic or acidiﬁcation event, whereas the second pulse of the biocrisis coincided with development of more prolonged and intense ocean anoxia. This study examines in detail the irregular surface in the middle of Bed 27 that represents the biostratigraphically deﬁned Permian-Triassic boundary, re-interpreting it as a ﬁrmground of the Glossifungites ichnofacies rather than as a submarine dissolution surface or hardground. The PTB crisis is thought to have been associated with sharp rises in atmospheric greenhouse gas concentrations and in average global temperatures. Cui and Kump (2015) compile, review, and critically assess the geochemical proxy data and climate modeling evidence for global warming during this crisis. They conclude that atmospheric CO2 levels may have been as high as 4000 ppm during the Late Permian and rose by a factor of ca. 3X (i.e., one-and-a-half doublings) during the crisis. They further conclude that tropical sea-surface temperatures (SST) could have been as high as 35 °C during the Late Permian, and that SSTs could have risen another 5 to 9 °C during the crisis. These ﬁndings imply a climate sensitivity of 5 to 6 °C per doubling, which is within the upper range of values produced by models of present-day climate. Cui and Kump also investigated potential sources of 13C-depleted carbon during the Early Triassic, concluding that release of massive amounts of CO2 and CH4 from the Siberian Traps was the most plausible source. They infer strongly enhanced weathering inputs of phosphate from land as the main cause of widespread euxinia in the global ocean.
Primary productivity and export productivity are key parameters of marine systems, but they are notoriously difﬁcult to estimate for paleomarine environments owing to the generally small proportion of organic matter that is preserved in most marine facies. Schoepfer et al. (2015) attempt to establish a more solid quantitative foundation for paleomarine productivity estimates by undertaking a comprehensive evaluation of the relationship of commonly used sedimentary productivity proxies (i.e., total organic carbon (TOC), organic phosphorus (Porg), and biogenic barium (Babio)) for a range of modern marine facies. They found that the single most important control on organic burial ﬂuxes and preservation factors (i.e., the fraction of export productivity ultimately preserved in the sediment) is sediment bulk accumulation rate (BAR), although redox conditions (i.e., oxic versus anoxic) exert a strong secondary inﬂuence. The inﬂuence of BAR on organic matter preservation is substantially larger in oxic facies than in anoxic facies. Schoepfer et al. converted the documented relationships to equations from which primary or export production in paleomarine systems can be estimated as a function of TOC and BAR. They concluded that both organic carbon and phosphorus ﬂuxes have strong potential as paleoproductivity proxies, but that the applicability of biogenic barium ﬂuxes may be limited to certain (mainly deep) oceanic settings. The end-Permian mass extinction coincided with major changes in the composition of marine plankton communities, yet little is known about concurrent changes in primary productivity. Published studies have inferred both decreased and increased productivity in the aftermath of the end-Permian crisis. Shen et al. (2015) undertook a comprehensive assessment of marine productivity changes during the latest Permian and Early Triassic based on 14 stratigraphic sections with a wide global distribution. They speciﬁcally made use of the productivity transform functions developed by Schoepfer et al. (see above) to constrain productivity changes each section. Primary productivity rates appear to have increased from the pre-crisis Late Permian through the Early Triassic in many parts of the world, although the South China Craton is unusual in exhibiting a pronounced decline over the same interval (cf. Algeo et al., 2013b). Most of the 14 study sections examined by Shen et al. show concurrent increases in sediment BAR, suggesting links to subaerial weathering rate changes through (1) intensiﬁed chemical weathering, resulting in an increased riverine ﬂux of nutrients that stimulated marine productivity, and/or (2) intensiﬁed physical weathering, leading to higher ﬂuxes of particulate detrital sediment to continental shelves, thus enhancing the preservation of organic matter in marine sediments. An additional factor, especially in the South China region, may have been the intensiﬁed recycling of bacterioplankton-derived organic matter in the ocean-surface layer, reducing the export ﬂux rather than primary productivity per se (cf. Luo et al., 2014a,b). The ecosystem stresses imposed by elevated ﬂuxes of nutrients and particulate sediment, as well as by locally reduced export ﬂuxes of organic matter, may have been important factors in the ~2- to 5-million-year-long delay in the recovery of Early Triassic marine ecosystems. The relationship of environmental stability, or lack thereof, to the pace of marine ecosystem recoveries following mass extinction events has not received detailed examination to date. Sustained or episodic environmental disturbances may play an important role in the delayed recovery of marine ecosystems, as following the end-Permian mass extinction. The study by Wei et al. (2015) takes a detailed look at marine environmental stability during the Early Triassic in four sections, three from South China (Chaohu, Daxiakou, and Zuodeng) and one from northern India (Mud). They determined that these shelfal marine systems were subject to recurrent environmental perturbations during the Early Triassic, as reﬂected in proxies for marine productivity, redox conditions, and terrigenous detrital ﬂuxes. In general, higher productivity correlated with more reducing conditions and larger terrigenous ﬂuxes, suggesting a causal relationship among these variables—most plausibly, that land-derived nutrients stimulated marine productivity and anoxia. The four sections studied by Wei et al.
span the latest Permian to early Middle Triassic, providing a detailed assessment of secular patterns that revealed disturbances during the early Griesbachian, the late Griesbachian, the mid-Smithian, and (more weakly) the mid-Spathian. These intervals were also associated with a slowing or reversal of ecosystem recovery based on metrics of biodiversity, within-community (alpha) diversity, infaunal burrowing, and ecosystem tiering, suggesting that the pattern and pace of recovery was strongly modulated by environmental conditions. The four sections revealed a water depth-dependency of the response to perturbations—the relatively deeper sections (Chaohu and Daxiakou) exhibited stronger, more persistent environmental changes compared to the shallower sections (Zuodeng and Mud). Finally, Wei et al. undertook a metadata comparison of post-extinction environmental stability and marine ecosystem recovery for the other four “Big Five” Phanerozoic mass extinctions. Major changes in seawater chemistry are inferred to have occurred during the PTB crisis, including rapid ﬂuctuations in carbonate saturation levels. The contribution by Li et al. (2015) examines the global occurrence of ooids during the Permian–Triassic transition. Ooids were widespread in shallow marine carbonate settings at that time, especially in association with microbialites. The greatest frequency of ooids is found around the latest Permian extinction (LPME), but occurrences continue sporadically into the Early Triassic Isarcicella isarcica Zone. Latest Permian ooids were mostly small (0.3-0.7 mm diam.) and aragonitic, whereas Early Triassic ooids tend to be larger (to 5-10 mm diam.) and are sometimes bimineralic. The proliferation of ooids was probably due to the development of warm ocean-surface waters with high levels of carbonate saturation, both factors that favor precipitation of inorganic carbonates. The authors propose that the shift from calcite to aragonite seas around the time of the P-Tr boundary crisis inﬂuenced patterns of extinction, survival, and post-extinction diversiﬁcation, although these ideas will require more testing for validation. The relationship of seawater chemistry to biomineralization patterns has not been resolved to date. The distribution patterns of rare earth elements (REEs) have been used frequently as proxies for ancient seawater chemistry, despite existing evidence of diagenetic remobilization and inter-elemental fractionation. In a two-part study, Chen et al. (2015a) ﬁrst review the existing literature on diagenetic inﬂuences on REEs in marine sediments, and then apply these ﬁndings to an analysis of the primary versus secondary origin of REEs in a Permian-Triassic boundary section. The modern literature review demonstrated that REEs undergo signiﬁcant redistribution among sediment phases during both early and late diagenesis as a consequence of adsorption and desorption processes. Remobilization of REEs, commonly linked to redox changes in sediment porewaters, can result in inter-elemental fractionation that variously enriches or depletes the light, middle, or heavy REE fractions. This study identiﬁed three characteristic REE distribution patterns: (1) a ‘ﬂat distribution’ signifying predominantly terrigenous siliciclastic inﬂuence, (2) a ‘middle-REE bulge’ probably due to adsorption of light and heavy REEs to Mn- and Fe-oxyhydroxides, respectively, and (3) a ‘heavy-REE enrichment' indicative of hydrogenous (seawater) inﬂuence. Analysis of conodonts and whole rocks from West Pingdingshan, a Permian-Triassic boundary section in South China, revealed two REE components in most samples: one representing an early diagenetic signature associated with suboxic conditions, and the second a late diagenetic signature linked to detrital siliciclastics (e.g., clay minerals). Based on their inability to isolate a hydrogenous REE component in the study samples, the authors inferred that many, and perhaps most, ancient bioapatites do not preserve information about seawater REE chemistry. Two papers in the present volume examine terrestrial ﬂoral changes associated with the Permian-Triassic transition. The study by Yu et al. (2015) is based on fossil plant material from eastern Yunnan and western Guizhou provinces in southwestern China, an area located near the paleo-equator and within the Cathaysian ﬂoral province. There, terrestrial and terrestrial-marine transitional facies yielded abundant fossil
plants (105 species in 39 genera) in the Changhsingian (Late Permian) Xuanwei Formation but more limited biodiversity (18 species in 14 genera) in the lowermost Triassic Kayitou Formation. South China may have served as a refuge for some plants during the P-Tr transition. Late Permian plants belong to the Lobatannularia multifolia– Gigantoclea guiyangensis (L–G) assemblage, which declined gradually during the Changhsingian before being decimated at the LPME. Lower Triassic plants belong to the Annalepis–Peltaspermum (A–P) assemblage. Some gigantopterids of the L–G assemblage are found in Lower Triassic strata but only as tiny, possibly reworked fragments. Annalepis acted as a pioneering lycopsid genus initiating the recovery of land plants in the earliest Triassic. Palynoﬂoras are characterized by a dramatic drop in both the abundance and diversity of palynomorphs and show a stepwise extinction pattern during the P-Tr transition. The paleobotanical study by Tewari et al. (2015) is based on fossil plant material from northern India, which was located at temperate mid-latitudes in the Southern Hemisphere during the Permian-Triassic transition and within the Gondwanan ﬂoral province. This report represents the ﬁrst palynological study of the Permian–Triassic succession at Guryul Ravine, Kashmir. The Guryul Ravine section yielded relatively small amounts of mostly poorly preserved spore and pollen, a condition attributed to the offshore marine location of the study site and its thermal alteration during Cenozoic collisional tectonism between India and Asia. The recovered palynomorph assemblages can be broadly correlated to the Densipollenites magnicorpus and Klausipollenites decipiens palynozones of peninsular India and to similar palynoﬂoras spanning the Permian–Triassic boundary elsewhere in Gondwana. In summary, the present thematic issue of Earth-Science Reviews on the largest mass extinction of life on Earth is timely given the growing interest among scientists, policy makers, and the public in present-day global warming, environmental change, elevated extinction rates, and potential ecosystem collapse. The set of papers assembled in this thematic issue provides insight into a spectrum of past climate and environmental events that offer stimulating suggestions for future studies on these topics. Although deep-time hothouse climates are not exact analogs for the climate of the future, past greenhouse regimes and, in particular, rapid warming events could provide important insights into how physical, biogeochemical, and biological processes operate under conditions of extreme warmth. Accordingly, we hope that this special issue of Earth-Science Reviews will prove stimulating. Acknowledgments We are grateful to the reviewers for their constructive reviews of the papers collected in this thematic issue. TJA gratefully acknowledges research support from the U.S. National Science Foundation (Sedimentary Geology and Paleobiology program), the NASA Exobiology program, and the China University of Geosciences-Wuhan (SKL-GPMR program GPMR201301, and SKL-BGEG program BGL21407). ZQC's work is supported by the 973 Program of China (2011CB808800) and the 111 Program of China (B08030). This thematic issue is a contribution to IGCP Projects 572 and 630. References Algeo, T.J., Twitchett, R.J., 2010. Anomalous Early Triassic sediment ﬂuxes due to elevated weathering rates and their biological consequences. Geology 38, 1023–1026. Algeo, T.J., Hinnov, L., Moser, J., Maynard, J.B., Elswick, E., Kuwahara, K., Sano, H., 2010. Changes in productivity and redox conditions in the Panthalassic Ocean during the latest Permian. Geology 38, 187–190. Algeo, T.J., Kuwahara, K., Sano, H., Bates, S., Lyons, T., Elswick, E., Hinnov, L., Ellwood, B.B., Moser, J., Maynard, J.B., 2011a. Spatial variation in sediment ﬂuxes, redox conditions, and productivity in the Permian-Triassic Panthalassic Ocean. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 65–83. Algeo, T.J., Chen, Z.Q., Fraiser, M.L., Twitchett, R.J., 2011b. Terrestrial–marine teleconnections in the collapse and rebuilding of Early Triassic marine ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 1–11. Algeo, T.J., Fraiser, M.L., Wignall, P.B., Winguth, A.M.E., 2013a. Permian–Triassic paleoceanography. Glob. Planet. Chang. 105, 1–6.
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Thomas J. Algeo Department of Geology, University of Cincinnati, Cincinnati, OH 45221, USA Corresponding author. E-mail address: [email protected]
Zhong-Qiang Chen State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan 430074, China E-mail address: [email protected]
David J. Bottjer Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, USA E-mail address: [email protected]