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Palaeoworld 16 (2007) 16–30

Research paper The Capitanian () Kamura cooling event: The beginning of the Paleozoic–Mesozoic transition Yukio Isozaki a,∗, Hodaka Kawahata b, Kayo Minoshima c a Department of Earth Science and Astronomy, The University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan b Graduate School of Frontier Sciences and Ocean Research Institute, The University of Tokyo, Minamidai, Nakano, Tokyo 164-8639, Japan c Geological Survey of Japan, AIST, Tsukuba 305-8567, Japan Received 4 January 2007; received in revised form 12 May 2007; accepted 15 May 2007 Available online 25 May 2007

Abstract

13 The Capitanian (late ) high positive plateau interval of carbonate carbon isotope ratio (␦ Ccarb) was recognized lately in a mid-Panthalassan paleo-atoll in Japan as the Kamura event. This unique episode in the late-middle Permian indicates high productivity in the low-latitude superocean likely coupled with resultant global cooling. This event ended shortly before the Guadalupian– (middle-late Permian) boundary (ca. 260 Ma); however, its onset time has not been ascertained previously. Through a further analysis of the (middle Guadalupian) to lower Capitanian interval in the same limestone at 13 Kamura in Kyushu, we have found that the ␦ Ccarb values started to rise over +4.5‰ and reached the maximum of +7.0‰ within the Yabeina (fusuline) Zone of the early-middle Capitanian. Thus the total duration of the Kamura event is estimated over 3–4 million , given the whole Capitanian ranging for 5.4 million years. This 3–4 million years long unique cooling event occurred clearly after the Gondwana glaciation period (late to early Permian) in the middle of the long-term warming trend toward the Mesozoic. This cooling may have been a direct cause of the end-Guadalupian extinction of low-latitude, warm-water adapted fauna including the large fusulines (Verbeekinidae), gigantic bivalves (Alatoconchidae), and rugose corals (Waagenophyllidae). The 13 Kamura event marks the first sharp excursion of ␦ Ccarb values in the volatile fluctuation interval that lasted for nearly 20 million 13 years from the late-Middle Permian until the early-Middle . This interval with high volatility in ␦ Ccarb values represents the transition of major climate mode from the late Paleozoic icehouse to the Mesozoic–Cenozoic greenhouse regime. The end- Paleozoic double-phased extinction occurred within this interval and the Capitanian Kamura event is regarded as the prelude to this transition. © 2007 Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier Ltd. All rights reserved.

Keywords: Guadalupian; C isotope; Panthalassa; Permo-Triassic boundary; Extinction; Productivity

1. Introduction history (e.g., Erwin, 1993, 2006); however, it was not long time ago when its double-phased nature became The terminal Paleozoic mass extinction represents the widely recognized. Jin et al. (1994) and Stanley and greatest in magnitude throughout the Phanerozoic life Yang (1994) first pointed out that the Permian biodi- versity declined in two steps separated clearly from each other; i.e., first at the Middle-Late Permian boundary ∗ (=Guadalupian–Lopingian boundary; G–LB) and sec- Corresponding author. Tel.: +81 3 5454 6608; fax: +81 3 3465 3925. ond at the Permo-Triassic boundary (P–TB) sensu stricto E-mail address: [email protected] (Y. Isozaki). (or –Induan boundary).

1871-174X/$ – see front matter © 2007 Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.palwor.2007.05.011 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 17

In contrast to the P–TB issue, not much attention mental change and relevant extinction event. A particular has been paid to the G–LB event; however, the signif- emphasis is given to the Kamura event in the context icance of the G–LB event was re-emphasized from a of a long-term change in environmental regime during different aspect relevant to the superocean Panthalassa. the nearly 20 million years of the Paleozoic–Mesozoic The timing of the end-Guadalupian extinction apparently transition. coincides with the onset of the superanoxia in Pantha- lassa, i.e., another global scale geologic phenomenon 2. Geologic setting across the P–TB (Isozaki, 1997a, 2007). In addition to the faunal turnover in mid-oceanic plankton (radiolari- The Permian and Triassic limestone at Kamura ans) detected in deep-sea chert, shallow marine sessile (Takachiho town, Miyazaki prefecture; Fig. 2) in Kyushu benthos (fusulines) also sharply declined in diversity forms a part of an ancient mid-oceanic atoll complex across the G–LB in mid-Panthalassan paleo-atoll com- primarily developed on a mid-oceanic paleo-seamount plex (Isozaki and Ota, 2001; Ota and Isozaki, 2006). (Sano and Nakashima, 1997; Isozaki and Ota, 2001; Ota These positively suggest the global nature of the G–LB and Isozaki, 2006). This limestone, like many other Per- extinction and causal environmental change. mian in Japan, occurs as an allochthonous The mid-oceanic paleo-atoll carbonates also recorded block incorporated in the Middle-Upper disor- secular change in stable carbon isotope composition. ganized mudstone/sandstone of the Jurassic accretionary Musashi et al. (2001, 2007) and Isozaki et al. (2007) complex in the Chichibu belt (the tectonic outlier of the first documented the secular change in carbonate carbon Mino-Tanba belt; Isozaki, 1997b). The limestone blocks 13 isotopic ratio (␦ Ccarb) of mid-Panthalassa across the in the Kamura area retain parts of the primary mid- P–TB and the G–LB, respectively. Besides the bound- oceanic stratigraphy that ranges in age from the Wordian ary negative shifts both at P–TB and G–LB properly (middle Guadalupian) to Norian () with sev- predicted from previous studies (e.g., Baud et al., 1989; eral sedimentary breaks in the Triassic part (Kambe, Holser et al., 1989; Wang et al., 2004), a unique high 1963; Kanmera and Nakazawa, 1973; Watanabe et al., productivity interval in the Capitanian (late Guadalu- 1979; Koike, 1996; Ota and Isozaki, 2006). pian) was newly detected on the basis of the appreciable The Permian part consists of bioclastic limestone with 13 length of high positive ␦ Ccarb (between +5 and +6‰) a typical Tethyan shallow marine fauna that includes interval (Isozaki et al., 2007; Fig. 1). As such high posi- various fusulines, smaller foraminifera, large-shelled tive values over +5.0‰ are quite rare in the Phanerozoic bivalves, gastropods, brachiopods, rugose corals, and record except for several unique events in the Paleo- calcareous algae. The Permian rocks are stratigraphi- zoic (e.g., Veizer et al., 1999; Saltzman, 2005), they cally divided into the Guadalupian Iwato Formation (ca. named this Capitanian episode the “Kamura event”, 70 m thick) and the overlying Lopingian Mitai Formation emphasizing its significance of global cooling and rele- (ca. 30 m thick). Fusulines are the most abundant, and vant extinction of large fusulines and gigantic bivalves they provide a basis for subdividing the Iwato Formation in low-latitude Panthalassa (Isozaki et al., 2007). In into four biostratigraphic units; i.e., the Neoschwagerina the fusuline-tuned section, the waning history of the Zone, Yabeina Zone, Lepidolina Zone, and a barren inter- Kamura event was clearly documented in high reso- val, in ascending order (Ota and Isozaki, 2006; Isozaki lution, whereas the earlier history including the onset and Igo, in preparation). The overlying Lopingian Mitai timing was not yet revealed, owing to the absence of con- Formation is subdivided into two fusuline zones, i.e., tinuous exposure in the previously studied section. This the Codonofusiella-Reichelina Zone and Palaeofusulina left a big chasm in our understanding of the major envi- Zone (Kanmera and Nakazawa, 1973; Ota and Isozaki, ronmental change in the late Guadalupian, in particular 2006). All these fusuline assemblages and associated the cause and processes of the Kamura cooling event. fossils (rugose corals and large-shelled bivalves of Fam- This study aimed to clarify the earlier of the ily Alatoconchidae; Isozaki, 2006) indicate that the Kamura event, particularly focusing on the onset tim- seamount was located in a low-latitude warm-water ing, and to bracket the total duration of the event. In domain in the superocean Panthalassa under a tropical the same Kamura area in Kyushu, Japan, we analyzed climate. 13 ␦ Ccarb chemostratigraphy of two other sections that The Neoschwagerina Zone is correlated with the expose much lower parts of the Guadalupian (Wordian Wordian (middle Guadalupian) of and with the to lower Capitanian) mid-oceanic paleo-atoll carbon- Murgabian in Transcaucasia (Leven, 1996; Wilde et al., 13 ates. This article reports the ␦ Ccarb measurements and 1999), while the Yabeina Zone, Lepidolina Zone, and discusses their implications to the Capitanian environ- most of the barren interval are correlated with the Capi- 18 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30

13 Fig. 1. Schematic diagram showing the late Guadalupian Kamura event documented by high positive ␦ Ccarb values at Kamura in Japan (modified 13 from Isozaki et al., 2007) (A), and the composite Permian secular curve of ␦ Ccarb values modified from Korte et al. (2005) (B). Road: , Wor: Wordian. Note that the Guadalupian large fusuline and bivalve fauna became extinct in the middle of the Kamura cooling event, whereas the post-extinction radiation of the Lopingian small fusulines started during the subsequent warming period. In contrast to the waning history of the Kamura event, its onset timing and processes were unknown previously. In (B), two possible paths (broken lines) for the Guadalupian secular 13 change of ␦ Ccarb values were shown by Korte et al. (2005); the lower for the Tethyan domain, the upper for the Delaware basin in Texas. The 13 Capitanian Kamura event recorded much higher positive ␦ Ccarb values between +5.0 and +7.0‰ in Kamura, suggesting the positive excursion of global context in the late Guadalupian. See text and Figs. 4 and 5 for details. Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 19

Fig. 2. Index map and stratigraphic columns of the three studied sections in the Kamura area, Kyushu. Not to scale. The present chemostratigraphic research focused on the Wordian and lower Capitanian parts of the Iwato Formation exposed in Sections 1 and 3. Refer to Ota and Isozaki (2006) and Isozaki et al. (2007) for more details of the area and Section 2. Loping.: Lopingian; Wuch.: ; C-R: Codonofusiella-Reichelina. 20 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 tanian (upper Guadalupian) of Texas and with Midian tory under the microscope. The black limestone of the in Transcaucasia (Ota and Isozaki, 2006). The strati- Iwato Formation has TOC around 0.1 wt% (Isozaki et graphic relationship between the Yabeina Zone and al., 2007). the Lepidolina Zone has long been controversial (e.g., The micritic part of wackestone from each horizon Toriyama, 1967; Ishii, 1990), however, our recent study was milled by microdrill after examining under the clarified that the former stratigraphically underlies the microscope. Approximately 100 ␮m of the aliquot ◦ latter within the Iwato Formation (Isozaki and Igo, in samples were reacted with 100% H3PO4 at 90 C preparation). The Codonofusiella-Reichelina Zone cor- in an automated carbonate device (Multiprep) cou- responds to the Wuchiapingian (Lower Lopingian) in pled with a Micromass Optima mass spectrometer South China. For details of fusuline biostratigraphy and at the Geological Survey of Japan, AIST. Here, 13 13 12 13 12 age assignment, see Ota and Isozaki (2006) and Isozaki ␦ C = [(( C/ Csample)/( C/ Cstandard)) − 1] × 1000, 18 18 16 18 16 (2006). and ␦ O = [(( O/ Osample)/( O/ Ostandard)) − 1] × The Iwato Formation is exposed in three sections in 1000. All isotopic data are reported as per mil (‰) Kamura; i.e., Sections 1–3 from the east to the west relative to Vienna Pee Dee belemnite (V-PDB) standard. ◦   ◦   (Fig. 2). Section 2 (32 44 58 N, 131 20 02 E; Fig. 2) The internal precision was 0.03‰ and 0.04‰ (1␴) at south of Shioinouso displays a continuous outcrop for ␦13C and ␦18O, respectively, based on replicate of the upper Iwato Formation and the lower Mitai For- measurements of 23 consecutive samples of the NBS-19 mation that spans across the G–LB (Ota and Isozaki, calcite standard (Suzuki et al., 2000). 2006). In this section, a unique high positive plateau in the Lepidolina Zone/barren interval and the follow- 4. Results 13 ing sharp negative shift in ␦ Ccarb were documented 13 (Isozaki et al., 2007). Table 1 lists all the measurements of ␦ Ccarb and 18 In the present study, we analyzed two additional sec- ␦ Ocarb of 47 samples from 34 horizons from Sections tions in the Kamura area that expose the lower part of 1 and 3 in Kamura. Figs. 3 and 4 show secular changes 13 the Iwato Formation; i.e., Sections 1 and 3 (Kambe, in ␦ Ccarb values plotted on the stratigraphic columns 13 1963; Murata et al., 2003; Isozaki, 2006; Fig. 2). Sec- of Sections 1 and 3, respectively. All ␦ Ccarb values tion 1 (32◦4512N, 131◦2055E) to the southeast of showed a wide range from +3.55 to +6.97‰, whereas 18 Saraito village is composed of 57 m-thick limestone that ␦ Ocarb values fluctuated between −7.58 to −12.36‰, belongs to the Neoschwagerina Zone and Yabeina Zone, which might be partly due to a slight diagenetic alter- ◦   ◦   13 whereas Section 3 (32 45 05 N, 131 19 52 E) to the ation, however, the correlation between ␦ Ccarb and 18 northeast of Hijirikawa is 8 m thick and entirely belongs ␦ Ocarb indicates that they behaved independently. Thus 13 to the Yabeina Zone (Fig. 2). Detailed biostratigraphy of we consider that the ␦ Ccarb values were not likely these two sections is under scrutiny and results will be affected by secondary alteration but reflect the primary published elsewhere (Isozaki and Igo, in preparation). isotopic composition of the inorganic carbon reser- Among the three sections in Kamura, Section 1 rep- voir in ancient seawater, in which the carbonates were resents the stratigraphical lowest, whereas Section 2 the deposited. 13 highest (Fig. 2). A slight stratigraphic gap may exist At Section 1, the ␦ Ccarb values range between +3.5 between Sections 2 and 3; however, the similarity in and +5.2‰. This section is divided into two parts in terms 13 lithofacies suggests that the possible gaps are consid- of ␦ Ccarb values; i.e., segment Sr-1 (Neoschwagerina erably small, if at all. The same fauna and lithofacies in Zone; 32 m) and the overlying segment Sr-2 (Yabeina 13 Sections 1 and 3 likewise indicate that a possible gap is Zone; 3.5 m) (Fig. 3). In the segment Sr-1, the ␦ Ccarb much smaller or even absent. values gradually and steadily increased from +3.5 to +4.3‰. On the other hand in the segment Sr-2, the 13 3. Samples and analytical methods ␦ Ccarb values fluctuated between +4.4 and +5.2‰. Although the boundary between the segments Sr-1 and 13 We collected dark gray to black limestone specimens Sr-2 is covered, a general trend of increasing ␦ Ccarb of the Guadalupian Iwato Formation for stable carbon values can be recognized in Section 1. The sample SrB35 and oxygen isotope measurements at 34 horizons; i.e., in the segment Sr-2 marked the lowest horizon of high 13 21 from Section 1 and 13 from Section 3. Rocks of the positive ␦ Ccarb values over +5.0‰ in the Iwato For- two sections are unmetamorphosed and mostly fresh, mation. 13 and those with strong weathering and with many calcite At Section 3, the ␦ Ccarb values range between veins were screened out in the field and in the labora- +5.0 and +7.0‰. This section is chemostratigraphi- Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 21

Table 1 cally divided into two parts; i.e., segment Hi-1 (3.5 m+) ␦13 ␦18 Analytical results of Ccarb and Ocarb normalized to the Vienna and the overlying segment Hi-2 (2.2 m+) (Fig. 4). The Pee Dee belemnite of the Guadalupian Iwato Formation in the Kamura segment Hi-1 is characterized by a gradual increase area, Kyushu 13 in ␦ Ccarb values, whereas the Hi-2 by a reversed ␦13 ␦18 Sample Horizon (m) Ccarb (‰) Ocarb (‰) decrease. The sample Hj-2 with +7.0‰ marked the high- 13 Section 3 (Hijirikawa) est ␦ Ccarb value in the Iwato Formation. Yabeina Zone (13 horizons) In summary, the current C isotope analysis clarified Hj-0.5 7.50 5.332 −10.001 the following two facts: (1) the ␦13C values keep − carb Hj0 6.75 5.817 8.480 increasing from the Neoschwagerina Zone (segment Sr- Hj1 6.15 5.425 −8.366 Hj1.5 5.90 5.936 −11.370 1; Wordian) to the Yabeina Zone (segments Sr-2 and Hj2-1 5.45 6.872 −10.052 Hi-1; lower Capitanian) except for the upper part of the − 13 Hj2-2 5.45 6.970 8.559 Yabeina Zone (segment Hi-2); (2) all the ␦ Ccarb values Hj3 5.15 5.791 −7.578 of the Capitanian Iwato Formation range above +4.4‰ − Hj4 4.55 5.681 9.013 up to the highest value of +7.0‰ in the upper Yabeina Hj5 4.15 5.191 −9.941 Hj5.5 3.75 5.502 −8.697 Zone. Hj6.1 3.35 5.005 −8.616 Hj7.1-1 2.40 5.046 −10.414 5. Discussion Hj7.1-2 2.40 5.008 −10.085 − Hj10 0.70 4.776 11.163 This study confirms the development of the Kamura Hj11 0.20 4.857 −10.913 event in the late Guadalupian, and suggests that the Section 1 (Saraito) interval of this unique event has ranged stratigraphically Yabeina Zone (8 horizons) B41 56.8 4.575 −10.049 further downward. We will discuss here the geologi- B40 56.4 4.478 −8.744 cal implications of the new dataset, focusing on the B39-1 56.1 5.051 −10.426 onset timing and total duration of the Kamura event with B39-2 56.1 5.235 −10.824 respect to the end-Guadalupian environmental changes − B38 55.3 5.013 10.893 and mass extinction, and particularly to the transition of B38Y1 55.3 5.056 −10.789 B38Y2 55.3 4.941 −11.677 climatic regime from the late Paleozoic icehouse (Gond- B37 55.0 4.932 −11.356 wana glaciation) to Mesozoic greenhouse. B37Y2 55.0 4.774 −11.978 B37Y3 55.0 4.917 −11.891 5.1. Onset of the Kamura event B36 54.7 4.704 −8.933 B35 54.1 5.050 −9.350 B34 53.8 4.430 −8.081 The present study has clarified that the lower part of the Iwato Formation (Wordian Neoschwagerina Zone Neoschwagerina Zone (13 horizons) and lower Capitanian Yabeina Zone) is thoroughly char- B12-1 33.9 4.213 −10.435 ␦13 B12-2 33.9 4.384 −10.715 acterized by positive values of Ccarb over +3.5‰ 13 B9 31.0 4.314 −11.773 (Figs. 3 and 4). In particular, all the ␦ Ccarb val- B6-1 28.0 4.042 −10.775 ues of the Yabeina Zone both in Sections 1 and 3 B6-2 28.0 4.267 −9.899 exceed +4.4‰, and they range mostly in a high posi- − B5-1 27.7 4.128 11.003 tive domain between +5.0 to +6.0‰. The Yabeina Zone B5-2 27.7 4.173 −11.245 B4-1 27.0 4.123 −11.414 of the Iwato Formation in general has more or less B4-2 27.0 4.177 −12.362 the same isotopic signature as the overlying Lepidolina B3 26.0 4.201 −7.970 Zone and barren interval in which the Kamura event 51 25.5 3.935 −10.139 was originally recognized (Isozaki et al., 2007). Thus − B2 24.0 4.072 8.329 the interval of the Kamura event with ␦13C values B1-1 21.0 3.550 −10.890 carb B1-2 21.0 3.648 −10.570 over +5.0‰ ranges stratigraphically downward to the X-1 15.0 3.714 −10.602 Yabeina Zone. X-2 15.0 3.969 −7.753 On the other hand, the Wordian Neoschwagerina 07-05 4.5 3.959 −9.192 13 Zone recorded relatively lower ␦ Ccarb values between 07-03 3.4 3.546 −8.841 − +3.5 and +4.2‰, thus the Kamura event had not Z4 0.0 3.536 9.747 13 yet started in the Wordian. However, the ␦ Ccarb record of the Neoschwagerina Zone clearly demonstrates a steadily upward-increasing pattern, suggesting that 22 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30

Fig. 3. Chemostratigraphy of stable carbon isotope of carbonates of Section 1 near Saraito in Kamura. Legends for columnar section are the same as those for Fig. 2. This section is divided into two chemostratigraphic segments: Sr-1 and Sr-2. Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 23

Fig. 4. Chemostratigraphy of stable carbon isotope of carbonates of Section 3 near Hijirikawa in Kamura. Legends for columnar section are the same as those for Fig. 2. This section is divided into two chemostratigraphic segments: Hi-1 and Hi-2.

13 the oceanographic condition started to shift gradually general secular trend of the ␦ Ccarb record positively already in the Wordian toward the extreme state of the indicates that the Kamura event has first emerged around Capitanian with unusual enrichment of 13C in seawater. the Wordian/Capitanian boundary (265.8 Ma according The sample SrB35 in the Yabeina Zone in Sec- to the latest geological timescale by Gradstein et al., 13 tion 1 marks the lowest horizon with ␦ Ccarb values 2004; Fig. 5). It is noteworthy that a strange condition over +5.0‰, suggesting the lower limit of the interval has appeared in the middle of the superocean around of the Kamura event. Unfortunately much lower hori- the Wordian/Capitanian boundary because the Kamura zon of the Yabeina Zone is covered and the boundary event may mark the first episode of large isotopic excur- between the Neoschwagerina Zone and Yabeina Zone sion in the Permian (Fig. 1B). Although the trigger for has not been observed in Kamura. Nonetheless, the this oceanographic change is unknown at present, the 24 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30

13 Fig. 5. Schematic summary of the ␦ Ccarb chemostratigraphy of the Guadalupian Iwato Formation and Early Lopingian Mitai Formation in Kamura, showing the total range of the Kamura event. Not to scale. Note the main extinction occurred in the middle of the high positive plateau interval of 13 ␦ Ccarb values. C-R: Codonofusiella-Reichelina.

onset timing of the Kamura event should be checked 5.2. Duration of the Kamura event further carefully in continuous sections elsewhere in order to examine whether or not this event started syn- As discussed above, the Kamura event apparently chronously throughout the world. ranged through three successive fusuline zones of the Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 25

Capitanian; i.e., the Yabeina Zone, Lepidolina Zone, tion, however, the high productivity will not hold for a and barren interval in ascending order (Fig. 5). The long time because of negative feedback mechanism, if basal part of the Yabeina Zone in Kamura is miss- world oceans are nitrogen-limited. In contrast, under a ing, whereas the uppermost part of the barren interval phosphorous-limited condition, high primary productiv- 13 is free from high positive ␦ Ccarb values. Thus the ity coupled with preferential organic carbon burial will Kamura event likely spanned throughout almost the continue to keep seawater ␦13C in high positive val- entire Capitanian, except for the uppermost and pos- ues for certain duration until effective recycling of P sibly the lowest parts. This is supported by the data stops (Saltzman, 2005). Although the (Ireviken) from the GSSP of the G–LB at Penglaitan and Tieqiao, event remains still controversial (Cramer and Saltzman, South China, as there is no high positive plateau recog- 2007), other eight Paleozoic cases with prominent posi- 13 nized in the uppermost Capitanian immediately below tive ␦ Ccarb excursion all suggest the appearance of cool the -defined G–LB (Wang et al., 2004; Jin et climate. al., 2006). Accordingly, the late Guadalupian Kamura event was Although detailed chronology of the three fusuline nominated as the 10th case in the Paleozoic character- 13 zones of the Capitanian has not yet been established, ized by a remarkable positive ␦ Ccarb excursion, and given the whole Capitanian ranging for 5.4 million years the Kamura event likewise represents a transient cool from 265.8 Ma to 260.4 Ma (according to the timescale interval that appeared in the late Guadalupian (Isozaki by Gradstein et al., 2004), the total duration of the et al., 2007). The unique lithofacies of the Iwato For- Kamura event is estimated to be more than a half of the mation dominated by black to dark gray, organic-rich Capitanian, probably 3–4 million years. Such a remark- (TOC ∼0.1 wt%) wackestone probably reflects the high 13 able period characterized by an unusual positive ␦ Ccarb productivity in surface waters, as most of the Permian excursion has never been recognized in the Permian. paleo-atoll limestone in Japan has much lower TOC 13 It is also noteworthy that the highest ␦ Ccarb value less than 0.01 wt%. It is worth noting that this event 7.0‰ was detected in the sample Hj-2 in the upper marks the first cooling episode, after the Gondwana part of the Yabeina Zone, as no-such high positive value glaciation ended in the (late ; Jones has ever been reported from the Permian rocks (e.g., and Fielding, 2004), in the middle of the long-term Grossman, 1994; Scholle, 1995; Korte et al., 2005). Thus warming trend toward the generally warm Mesozoic 13 the maximum ␦ Ccarb value in the Yabeina Zone sug- era. gests that the Kamura event may have culminated in the In good accordance with the above interpretation, early-middle Capitanian, held the similar condition for the lately compiled Permian sea-level fluctuation curve a while, and finally collapsed quickly in the late Capita- demonstrates that the Permian lowest-stand occurred nian. around the G–LB (Hallam and Wignall, 1999; Tong et 13 In general, extremely high positive ␦ Ccarb values al., 1999). A major hiatus on the top of the Guadalu- indicate extraordinarily high productivity in the ocean. pian Maokou Formation has been recognized extensively As oceanic productivity is strongly controlled by nutri- in South China, and the top of the well-known Per- ent availability, constant supply particularly of limiting mian Reef complex in west Texas is unconformably elements such as P and N is necessary to maintain long- covered by the Lopingian evaporites (e.g., Mei and lasting high productivity. Saltzman (2005) compiled all Wardlaw, 1996). The “Permian chert event” in high 13 available ␦ Ccarb measurements from the Paleozoic latitudes (Beauchamp and Baud, 2002) likely supports (middle to Carboniferous) rocks in the Great the appearance of a cool period in the Guadalupian, Basin of western USA, and demonstrated a compos- too. ite Paleozoic secular curve that is punctuated by nine unique events of remarkable positive excursions by over 5.3. Critical cooling +3.0‰ lasted for more than a few million years. He concluded that these nine events, detected also in dif- The end-Guadalupian is regarded as a timing of one of ferent continents, represent intermediate cool climate the two major extinction events of the terminal Paleozoic intervals between typical greenhouse and icehouse peri- era (Jin et al., 1994; Stanley and Yang, 1994). Isozaki ods. By lowering the sea surface temperature, oceanic (1997a, 2007) emphasized the geological significance circulation can be accelerated to bring sufficient nutri- of the G–LB event from a viewpoint of the timing coin- ents from the deep ocean to the surface and this will cidence between two global geological phenomena; i.e., result in high primary productivity by blooming of the biotic extinction and the onset of the P–TB supera- phytoplankton/cyanobacteria. As to the nutrient condi- noxia in the superocean. As to the cause of the G–LB 26 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 27 event, a global environmental change triggered by the In addition, some gastropods and brachiopods large-scale volcanism of the Emeishan Trap in South behaved similarly as the trio. For example, the China is currently favored by many workers (e.g., Chung occurrence of extraordinarily large gastropods, such et al., 1998; Ali et al., 2002; Wignall, 2001); however, as Bellerophon (13 cm in diameter), Pleurotomaria details including possible direct kill mechanisms are not (18 cm × 16 cm), and Murchisonia (40 cm in height), yet fully clarified. were reported from the Capitanian limestone in Akasaka In this regard, the extinction of the Guadalupian (Hayasaka and Hayasaka, 1953), whereas all the gas- fauna in the middle of the Capitanian Kamura event tropods from the overlying Lopingian are no more appears critical. The clear extinction pattern of large than 1 cm in diameter. It is also noteworthy that some fusulines (Verbeekinidae) and bivalves (Alatoconchi- early-middle Permian brachiopods originated in middle- dae) in the Capitanian part of the Iwato Formation high paleolatitude domains (Attenuatella, Waagenites, (Isozaki, 2006; Ota and Isozaki, 2006) suggests that Strophalosiina, Comuqia) migrated to low-latitudes and the claimed cooling of the Kamura event might have made their first appearance in the paleoequatorial zone at played the key role in the kill scenario, in particular for the end of the Capitanian (Shen and Shi, 2002). Although the creatures well adapted to a warm tropical climate the Permian gastropods and brachiopods as a whole did in low-latitude areas (Isozaki et al., 2007). The occur- not experienced a remarkable diversity loss at the G–LB rence/distribution of the middle Permian Verbeekinidae, (e.g., Pan and Erwin, 1994; Shen and Shi, 2002), these Alatoconchidae, and Waagenophyllidae (rugose coral) observations likewise support the appearance of a cool families was restricted in low-latitude shallow seas in interval in the Capitanian Tethys and Panthalassa. Tethys and Panthalassa, and the gigantism in fusu- The G–LB is placed not at the extinction level of lines and Alatoconchidae bivalves was probably due the Guadalupian fauna but at the first appearance datum to the symbiosis with photosynthetic algae/bacteria in (FAD) of the Wuchiapingian index conodont such oligotrophic environment in mid-ocean in general postbitteri postbitteri as defined at the stratotype section (Isozaki, 2006). (GSSP) at Penglaitan in South China (Jin et al., 1998; In the late Capitanian, large fusulines were screened Henderson et al., 2002). Owing to the absence of con- out by size (Wilde, 2002; Yang et al., 2004; Ota odonts, the G–LB in Kamura is set at the horizon ca. and Isozaki, 2006), aberrant Alatoconchidae bivalves 11 m above the main extinction level in the upper part of became totally extinct (Isozaki, 2006), and the diver- the barren interval on the basis of the first appearance of 13 sity of rugose corals declined remarkably (Wang and the Lopingian fusulines and ␦ Ccarb chemostratigraph- Sugiyama, 2000). The possible drop in sea surface ical correlation (Ota and Isozaki, 2006; Isozaki et al., temperature in low latitudes may have caused a total 2007). The main extinction occurred not at the G–LB malfunction of photosymbiosis factory shared by the per se but in a much lower horizon in the midst of the 13 above-mentioned “tropical trio” that were too much positive ␦ Ccarb excursion interval. Thus an appreciable adapted to warm-water environments to survive the time has elapsed between the end-Guadalupian extinc- change. At Tieqiao, the last occurrence of large fusu- tion and the following radiation of the Lopingian fauna line Metadoliolina (Verbeekinidae)was confirmed in the in shallow mid-Panthalassa (Fig. 1A). 13 xuanhanensis Zone with ␦ Ccarb val- The present study demonstrated that the oceanic car- ues of +3 to +4‰ (Jin et al., 2006), suggesting that the bon cycle started to change in mid-Panthalassa around extinction of large fusulines slightly delayed in South 265 Ma, at least by 4–5 million years earlier than the China probably owing to the local variability in water G–LB (ca. 260 Ma). Should the claimed cooling have temperature. been responsible for the extinction of the Guadalupian

13 Fig. 6. Secular change of ␦ Ccarb in the Paleozoic and early Mesozoic, compiled from Saltzman (2005) for the Cambrian to Carboniferous, from Korte et al. (2005) and this study for the Permian, from Payne et al. (2004) and Gradstein et al. (2004) for the Triassic, and from Palfy et al. (2001) 13 and Katz et al. (2005) for the Jurassic. Note the four distinct intervals of volatility with high positive ␦ Ccarb excursion; i.e., Late Cambrian, Late –Silurian, Late –Early Carboniferous, and the Middle Permian– (=Paleozoic–Mesozoic transitional interval; PMT-interval). The PMT-interval from the Capitanian (Late Middle Permian) to Anisian (Early Middle Triassic) ranged for ca. 20–25 million years, representing the transition from the late Paleozoic icehouse, centered by the to Early Permian Gondwana glaciation, to the Mesozoic/Cenozoic greenhouse. The PMT-interval recorded a period of a transient cool climate with a P-limited oceanographic condition between icehouse and greenhouse modes, and the Kamura event marks the beginning of the mode change from the Paleozoic icehouse to the Mesozoic greenhouse. It is noteworthy that the two major mass extinctions (at the G–LB and P–TB) occurred during the PMT-interval, and that the PMT-interval chronologically overlaps the P–TB superanoxic period (Isozaki, 1997a). 28 Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 fauna, the ultimate cause of the environmental change Late Cambrian, Late Ordovician to Silurian, and Late must have appeared by the early Capitanian time. Devonian to Early Carboniferous (Fig. 6). The first The Emeishan Trap volacanism in South China was two intervals was described as a transient cool interval recently dated 256–259 Ma (Zhou et al., 2002). This between two greenhouse periods when the globe was early Lopingian age is obviously too young for the trap almost running into an icehouse but did not. Unlike these, to be responsible for the environmental change in the the rest two correspond to bona fide transient cool periods early Capitanian (ca. 265 Ma). In general, large-scale between an icehouse and a greenhouse period. The late basaltic volcanism likely drives the opposite conse- Paleozoic (Carboniferous to Early Permian) was domi- quence; i.e., global warming, rather than 3–4 million nated by the icehouse climate centered by the Gondwana -long cooling. Thus the superficial correlation glaciation, while the Mesozoic in total was governed by between the end-Guadalupian extinction and the trap warm greenhouse climate (e.g., Frakes et al., 1992). volcanism needs re-consideration. Refer to Isozaki and It is noteworthy that this PMT-interval with high 13 Ota (2007) for more details of relative timing between ␦ Ccarb volatility approximately overlaps the super- the G–LB extinction and the Emeishan Trap volcanism. anoxic period in the superocean (Isozaki, 1997a). Regardless of climatic modes, the deep-sea cherts both 13 5.4. δ Ccarb volatility in the Paleozoic–Mesozoic of the Pennsylvanian–Guadalupian (icehouse interval) transition interval and the Middle Triassic to Jurassic (greenhouse interval) were well oxygenated. This indicates that the growth and The Guadalupian major environmental change of retreat of superanoxia have been controlled not solely global context has appeared around 265 Ma (early by the climate-dependent, global oceanic circulation but Capitanian) several million years earlier than the end- also by other factors. Guadalupian mass extinction at the latest Capitanian. At any rate, a major re-organization of global In a long-term viewpoint, the Capitanian Kamura event oceanography, including the global carbon cycle, is particularly significant because it marks not only the occurred during the PMT-interval, and this clearly sep- 13 onset of wild ␦ Ccarb fluctuations across the P–TB into arated the ancient regime of the Paleozoic and the new the early Anisian, middle Triassic, but also the first one of the Mesozoic. The causes and processes of the 13 remarkable positive ␦ Ccarb excursion after a nearly 85 two major mass extinction events, at the G–LB and at million years of relative quiescence (Fig. 6). In addi- P–TB, should better be explained in the scope of such tion to the well-known sharp negative shift across the long-term geological context. P–TB (Baud et al., 1989; Holser et al., 1989; Musashi After all, the late Guadalupian Kamura event pre- et al., 2001), more positive and negative excursions of ludes all these drastic change in the PMT-interval from greater magnitude occurred particularly in the early Tri- the Paleozoic to post-Paleozoic world, and the ultimate assic (Payne et al., 2004). As to the Lopingian, similar trigger(s) of this major mode change in environment 13 ␦ Ccarb fluctuations are likely expected from the pre- can be found neither in the strict G–LB nor P–TB liminary results (Baud et al., 1996; Shao et al., 2000; intervals but likely in the upper Guadalupian rock Korte et al., 2005); however, the dataset is too immature records. to document detailed secular change particularly for the Wuchiapingian (lower Lopingian). 6. Summary In sharp contrast to the Paleozoic–Mesozoic transi- tion (PMT)-interval, such a wild fluctuation varying from The present study on the mid-Panthalassan paleo-atoll +8 to −3‰ has not been recognized in the Cisuralian to complex clarified the following new aspects of the late early Guadalupian nor in the middle Triassic and later Guadalupian environmental change relevant to the mass 13 part of the Mesozoic (Fig. 6). In fact, ␦ Ccarb value extinction: over +5.0‰ has never been recorded throughout the 13 Mesozoic and Cenozoic (e.g., Veizer et al., 1999; Katz (1) The Kamura event with high positive ␦ Ccarb values et al., 2005). Thus a volatile change in global carbon ranged for nearly 3–4 million years in the Capitanian cycle relevant to oceanography is restricted solely to the (ca. 265–260 Ma), late Guadalupian. ∼20 million year-long PMT-interval from the Capitanian (2) The end-Guadalupian extinction occurred in the (ca. 265 Ma) to early Anisian (ca. 245 Ma). middle of the Kamura cooling event. As pointed out by Saltzman (2005), there are three (3) The Kamura event marks the beginning of the major other intervals in the Paleozoic that are characterized mode change of global climate and oceanography 13 by volatile fluctuations of ␦ Ccarb values; i.e., the from the Paleozoic to post-Paleozoic regime. Y. Isozaki et al. / Palaeoworld 16 (2007) 16–30 29

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