Size Variation of Conodont Elements of the Hindeodus–Isarcicella Clade During the Permian–Triassic Transition in South China and Its Implication for Mass Extinction

Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Size variation of conodont elements of the Hindeodus–Isarcicella clade during the Permian–Triassic transition in South China and its implication for mass extinction

Genming Luo a, Xulong Lai a,⁎, G.R. Shi b, Haishui Jiang a, Hongfu Yin a, Shucheng Xie c, Jinnan Tong c, Kexin Zhang a, Weihong He c, Paul B. Wignall d a Faculty of Earth Science, China University of Geosciences,Wuhan 430074, PR China b School of Life and Environmental Sciences, Deakin University, 221 Burwood Hwy, Burwood VIC 3125, Australia c Key Laboratory of Geobiology and Environmental Geology, China University of Geosciences, Wuhan 430074, PR China d School of Earth and Environment, University of Leeds, Leeds. LS2 9JT, United Kingdom

ARTICLE INFO ABSTRACT

Article history: Based on the analysis of thousands of conodont specimens from the Permian –Triassic (P–T) transition at Meishan Received 17 August 2007 (the GSSP of P–T Boundary) and Shangsi sections in South China, this study investigates the size variation of Received in revised form 1 April 2008 Hindeodus and Isarcicella P1 elements during the mass extinction interval. The results demonstrate that Hin- Accepted 3 April 2008 deodus–Isarcicella underwent 4 episodes of distinct size reduction during the P–T transition at the Meishan Section and 2 episodes of size reduction in the earliest Triassic at Shangsi. The size reductions at Meishan took Keywords: Multi-episode mass extinction place at the junctions of beds 24d/24e, 25/26, 27b/27c and 28/29, and at the junctions of beds 28/29c and 30d/31a Conodont at Shangsi. The two earliest Triassic size reduction episodes were correlative between the two sections. These Hindeodus-Isarcicella changes coincide with some important geological events such as eustatic sea-level changes, anoxic events, carbon Size reduction isotope oscillations, miniaturization of brachiopods and microbial changes. Through detailed investigation of the Permian–Triassic transition palaeoenvironment and the palaeoecology of Hindeodus–Isarcicella, the authors propose that the main causes of South China the size reduction was a sharp decline of food availability because of the mass extinction and the anoxic event during the P/T transition. The pattern of size reduction supports suggestions that the end-Permian mass extinction was multi-episodal, consisting of 3 extinction events rather than a single catastrophic event. © 2008 Elsevier B.V. All rights reserved.

1. Introduction There are several opinions about the causes and patterns of the P–T mass extinction (Isozaki, 1997; Kozur, 1998; Wang and Cao, 2004; The end-Permian biotic crisis was the largest mass extinction in Fang, 2004a,b; Grice et al., 2005; Racki and Wignall, 2005). Some the fossil record. It eliminated over 90% of species in the oceans authors have proposed a single-episode catastrophic mass extinction (Stanley and Yang, 1994; Bambach et al., 2004) and about 70% of (Jin et al., 2000; Kaiho et al., 2006), while others have argued for a vertebrate families on land (Benton, 1988; King, 1991; Maxwell, 1992). multi-episode mass extinction (Wu and Liu, 1991; Wignall and The cause or causes and duration as well as the nature of the Hallam, 1993; Yin and Tong, 1998; Fang, 2004a,b; Xie et al., 2005; extinction remain uncertain and actively debated (Wu and Liu, 1991; Shen et al., 2006; Yin et al., 2007a). In this paper, we attempt to test Wignall and Hallam, 1993; Isozaki, 1997; Kozur, 1998; Yin and Tong, these various scenarios by using the size variation data of a group of 1998; Jin et al., 2000; Yin et al., 2001; Wang and Cao, 2004; Fang, conodont species from a single clade from several continuous 2004a,b; Grice et al., 2005; Racki and Wignall, 2005; Yin et al., 2007a). Permian–Triassic boundary sections in South China. The fundamental The Global Stratotype Section and Point (GSSP) of the Permian– question addressed in the study is to see if the sizes of conodont Triassic Boundary at Meishan in Zhejiang Province, China has served species varied across the PTB and, if so, whether or not the timing of as a focal point in this global debate, as it has provided much critical the signiﬁcant size changes actually corresponded to any of the stratigraphical and palaeontological data. As a result, the section has proposed PTB extinction intervals. A related question, also investi- received intensive multidisciplinary studies by various research gated as an integral part of this study, is to elucidate the possible cause groups, including lithostratigraphy, biostratigraphy, sedimentology, (s) for the size change of the conodont species across the PTB. sequence stratigraphy, isotope geochemistry, eventostratigraphy, and There is now a considerable literature relating size variation in magnetostratigraphy (Yin et al., 2001 and references therein). lineages through time to biotic crises caused by environmental changes in earth history. Initially, Urbanek (1993) coined the term “Lilliput effect” for an observed size reduction of Silurian graptolites ⁎ Corresponding author. Faculty of Earth Sciences, China University of Geosciences, Wuhan, Hubei 430074, PR China. Tel.: +86 27 67883139; fax: +86 27 87515956. during a biotic crisis. Subsequently, other researchers have reported E-mail address: [email protected] (X. Lai). similar size decreases during times of extinction; for example, the size

Fig. 1. A: Location map of study area in South China; Meishan Section (B) and Shangsi Section (C). (after Wingnall et al., 1995 and Jiang et al., 2007). of late Devonian conodonts (Girard and Renaud, 1996), heart urchins study of large conodont samples. Furthermore, unlike most other across the Cretaceous/Tertiary boundary (Jeffery, 2001), and various organisms, most Late Permian conodont species or their lineages organisms around the Permian/Triassic boundary (Twitchett, 2001; persisted through into the Lower Triassic. Therefore, these conodonts He et al., 2005; Twitchett, 2005a,b; Luo et al., 2006; Twitchett, 2006; can serve as the best material for the study of the size variation during He et al., 2007; Twitchett, 2007). the P–T transitional period. Luo et al. (2006) reported a size reduction It is widely held that there was no obvious change in conodont in P1 elements of the conodont genus Neogondolella at the bed 24d/ fortunes during the end-Permian mass extinction, because many 24e junction (Upper Permian) at Meishan. However, the limited conodont lineages clearly survived through the PTB (e. g. Clark et al., Neogondolella specimens from the Lower Triassic did not allow us to 1986; Jiang et al., 2007). However, the survival of lineages tends to perform a full-scale size variation study throughout the Permian– overlook the potential ecological information that can come from the Triassic transition. To overcome this shortfall, in this paper we have

Table 1 The total number, mean size, standard deviation, percentage of specimens larger than 0.5 mm and 95% conﬁdence interval of the mean for the P1 element of Hindeodus–Isarcicella from the P/T transition at the Meishan Section, Changxing, Zhejiang Province

Bed 24a 24b 24c 24d 24e 25 26 27a 27b 27c 27d 28 29 Number 79 39 5 77 17 2 8 94 133 141 270 171 47 Mean (mm) 0.458 0.459 0.443 0.534 0.436 0.533 0.392 0.455 0.503 0.421 0.467 0.580 0.459 Standard deviation 0.132 0.143 0.079 0.096 0.100 0.006 0.043 0.098 0.108 0.103 0.158 0.150 0.108 Percentage (N0.5mm) 29.11 33.33 20.00 76.62 25.53 100 0 27.66 47.37 18.44 34.44 67.84 38.30 95% conﬁdence interval of the mean 0.4913 0.4989 0.7002 0.5610 0.4951 0.5838 0.4048 0.4725 0.5182 0.4372 0.4871 0.6008 0.4926 0.4244 0.4026 0.1831 0.5144 0.3595 0.4822 0.3619 0.4298 0.4811 0.4017 0.4472 0.5536 0.4264 178 G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187 chosen hindeodid conodonts because as a lineage they survived across only previously been undertaken for the P –T transition (Luo et al., the P–T boundary. The recovery and size measurement of abundant 2006). The present paper examines the size variations, in large conodont specimens is time-consuming, and this kind of study has samples, of conodonts from the Hindeodus–Isarcicella clade during the

Fig. 2. Size distribution histogram of P1 elements of Hindeodus–Isarcicella from each bed in ascending order (24a to 29 except for bed 25) through the P/T transition at the Meishan Section A. The figures above each histogram are the total number of specimens in each size range. G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187 179 end Permian to earliest Triassic interval, with the aim of improving our tions of the evolution of the hindeodid–isarcicellid lineage are understanding of the mass extinction patterns and of biotic recovery. controversial (Kozur, 1996; Ding et al., 1997; Lai, 1997; Wang and Wang, 1997). Ding et al. (1997) thought that Hindeodus latidentatus–H. 2. Material and method parvus–Isarcicella turgida–I. isarcica formed an anagenetic lineage. However, Wang and Wang (1997) replaced I. turgida with I. staeschei Thirteen successive bulk samples ranging from bed 24 to bed 29 in the evolutionary sequence of (Ding et al., 1997). Nevertheless, (the PTB is sited at the bottom of bed 27c) were collected from Section almost all authors have accepted the idea of an evolutionary sequence A at Meishan, Changxing, Zhejiang province (Fig. 1). The sample from from hindeodid to isarcicellid. Nicoll et al. (2002) proposed that the bed 24 was divided into 5 sub-beds (beds 24a–e). Bed 27 was also growth pattern of hindeodids occurred by the addition of denticles at evenly separated into 4 sub-beds (beds 27a–d). Each of these 13 the posterior. The length between the anterior and posterior is samples weighed 20 kg. The clay samples collected from beds 25 and therefore an important size parameter for Hindeodus–Isarcicella. 28 were processed directly by water. The other samples were crushed During the past two decades, the P–T conodonts at the Meishan into 1 cm3 size fragments and treated with dilute acetic acid (10%) to section have received intensive studies (Lai et al., 1995; Zhang et al., dissolve the samples. A 2.80–2.81 g/ml gravity liquid made of 1995; Ding et al., 1997; Wang and Wang, 1997; Mei et al., 1998). Based bromoform (2.89 g/ml) and acetone (0.79 g/ml) was used in the on large conodont samples, our group has established parallel conodont separation for all the samples. The conodonts were picked gondolellid and hindeodid zones at this section (Jiang et al., 2007), one by one under the binocular stereoscope. All the Meishan samples and the hindeodid zones in ascending order are H. latidentatus zone, have been entirely processed over 20 months. The samples from the H. praeparvus zone, H. changxingensis zone, H. parvus zone, Isarcicella Shangsi Section have not been completely processed but in the earliest staeschei zone and I. isarcica zone from beds 24a to 29. According to Triassic there are Hindeodus–Isarcicella elements for this work. the latest radiometric dates, the absolute age of bed 28 at the Meishan Over 20,000 specimens were obtained from this processing. Among Section (GSSP) is 250.7±0.3 Ma, and that of bed 25 (white clay) is these, more than 14,000 were P1 elements of Neogondolella, Hindeodus 251.4 Ma (Bowring et al., 1998). Mundil et al. (2004) rectified their and Isarcicella, which are important elements during the P/T transition. earlier data (Mundil et al., 2001), and suggested that the duration of A binocular stereoscope and micrometer were used to measure the the mass extinction was shorter. In any case, the duration from bed 25 length between the anterior and posterior ends of each well-preserved to 28 is about 0.7 million years. This 0.7 myr interval corresponds to 4 Hindeodus–Isarcicella P1 element. First, the complete elements with hindeodid conodont zones and hence indicates that the evolutionary both anterior and posterior parts were measured under the binocular rates were high for the conodonts. stereoscope with the micrometer in the ocular. Secondly, each measured element was arrayed according to its size recorded in the notebook. 4. Size variation in the Hindeodus–Isarcicella clade Thirdly, the size of some randomly-chosen elements was measured and compared to the measurements obtained from the first step and found 4.1. Data from the Meishan section to be nearly the same. Finally, different personnel were employed to measure some of the randomly chosen elements (about 30–40 elements The number (all the complete elements from each bed), mean size of each bed) and compared their measurements with those of the first and standard deviation of P1 elements of Hindeodus–Isarcicella for person, and again both results were found to be nearly the same. each bed are shown in Table 1, together with the 95% confidence The mean size, distribution histogram, standard deviation and 95% interval of the mean and the percentage of Hindeodus–Isarcicella P1 confidence interval of the mean size were used to analyse the size elements larger than 0.5 mm. The size distribution within each bed is distribution and variation of the conodonts. shown in Fig. 2. The mean size of all the individuals within a The mean size (X), which reflects the condition of a community, is community which can more precisely reflect the living environment based on the following equation: of this community is shown in Fig. 3, of which the shadow interval shows the 95% confidence interval of the mean. XN The dominant peak for bed 24a is 0.4–0.5 mm, with element length X ¼ 1=N 4 li showing a normal distribution (Fig. 2). The dominant peak for bed 24b i¼1 is 0.3–0.4 mm, but with a marked right-skewed distribution where X is the mean size, N is the number measured in each bed and li (skeweness=0.3112). The dominant peak for bed 24c is also 0.4– is the length of each element. The 95% confidence interval, reflecting 0.5 mm, with a normal distribution, although with fewer elements. whether the size reduction is credible on 95% confidence, is based on the following equation:

S Y ¼ ta= pffiffiffiffi 2 N where Y is the fluctuating range, ta=2 is the t-test value of 1−α confidence, S is the standard deviation and N is the number measured from each bed. So, the confidence interval is (X−Y, X+Y), where X is the mean size, X−Y is the lower line, while X+Y is the upper line.

3. Taxonomy and evolution of Hindeodus–Isarcicella

Both hindeodid and isarcicellid P1 elements are scaphate, with a robust cusp at the anterior and numbers of smaller denticles following the cusp. The hindeodid P1 elements are symmetrical or slightly asymmetric, whilst the isarcicellid P1 elements are extremely asymmetric. The cavity of hindeodid shows slight swelling but no Fig. 3. Variation of the mean size of P1 elements of Hindeodus–Isarcicella from the end thickening, whilst that of isarcicellids is both swollen and thickened. Permian (bed 24a) to early Triassic (bed 29) at the Meishan Section. The black area is the Some of the isarcicellid P1 elements have a denticle or series of 95% conﬁdence interval of the mean size, and the central white circle and line show denticles on one side or both sides of the cavity surface. Interpreta- variation of the mean size. 180 G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187

Fig. 4. Variation of the mean size of P1 elements of Hindeodus typicalis from the end Permian Fig. 5. Variation of the mean size of P1 elements of Hindeodus–Isarcicella from the (bed 24a to bed 24e) at the Meishan Section. The black area is the 95% conﬁdence interval of earliest Triassic of the Shangsi Section, Sichuan Province. the mean size, and the central white circle and line show variation of the mean size.

The dominant peak for bed 24d is 0.5–0.6 mm, and it also appears to mean size are 0.4–0.5 mm and 0.503 mm, and the percentage with a have a normal distribution. The dominant peak for bed 24e is 0.4– size larger than 0.5 mm is 47.37%, while in bed 27c, the dominate peak 0.5 mm, with a marked left-skewed trend. Both the two elements of and the mean size are 0.3–0.4 mm and 0.421 mm respectively, and the bed 25 are larger than 0.5 mm, while the elements of bed 26 are 0.3– percentage of size larger than 0.5 mm is 18.44%. The upper line 0.5 mm, with no element larger than 0.5 mm. The dominant peaks for (0.4372) of the 95% confidence interval of the mean at bed 27c is bed 27a and 27b are within 0.4–0.5 mm, and their distribution smaller than that of the lower line (0.4811) at bed 27b. The t-test for approaches a normal distribution. The dominant peaks for bed 27c means (p=0.000) indicated that this reduction of size was undoubted. and 27d are 0.3–0.4 mm, with slight right skew. The dominant peak In bed 27d, the dominant peak is 0.3–0.4 mm, the same as bed 27c, but for bed 28 is 0.5–0.7 mm, while that for bed 29 is 0.4–0.5 mm. the mean size is 0.467 mm, and the percentage with a size larger than Fig. 3 shows the size variation of conodont Hindeodus-Isarcicella 0.5 mm is 34.44%. The mean size in bed 28, where the largest P1 element from the end Permian (bed 24a) to earliest Triassic (bed specimens in these beds are found, is 0.580 mm, the dominant peak is 29). The black area stands for the 95% confidence interval of the mean, 0.5–0.6 mm, and the percentage with a size larger than 0.5 mm is and the central white points and line of the area show the variation of 67.84%. However, in bed 29, the dominant peak and mean size are 0.4– mean size of specimens in each bed. As the graph (Fig. 3) shows, 0.5 mm and 0.459 mm, respectively, and the percentage with a size during the transitions between beds 24e/24d, 26/25, 27c/27b and 29/ larger than 0.5 mm is 38.30%. At the transition between these two 28, the characters (mean size, dominant peak, percentage) of size beds, all the parameters vary distinctly, and the upper line (0.4926) of variation exhibit distinct changes. The dominant peak and the mean the 95% confidence interval for bed 29 is much smaller than the lower size for bed 24d are 0.5–0.6 mm and 0.534 mm respectively, and the line (0.5536) for bed 28. t-test for means shows no reason to believe percentage with a size larger than 0.5 mm is 76.62%, while these that the size reduction was not significant (p=0.000). characters for bed 24e are 0.4–0.5 mm, 0.436 mm and 25.53%, It is interesting to note that the size of P1 elements of Hindeodus– respectively. The 95% confidence interval of the mean size shows that Isarcicella in beds 25 and 28 is comparatively very large, especially in the upper line of bed 24e (0.4951) is smaller than the lower line of bed bed 28 (see above). Both of these are clay beds, and previous workers 24d (0.5144), so the size reduction is credible at a 95% confidence level. have thought that the extinction took place at these levels (Fang, The t-test for means shows that the size reduction was distinct 2004a,b; Xie et al., 2005). (p=0.000). There are only two Hindeodus–Isarcicella P1 elements in In order to determine whether or not the size variation of Hindeo- bed 25, both of which are larger than 0.5 mm, with a mean size of dus–Isarcicella populations was affected by the presence of different 0.533 mm, while in bed 26 all the elements are less than 0.5 mm, and species, we investigated the size variation of a single species, Hindeodus the mean size is only 0.392 mm. The t-test for means (p=0.002) typicalis, from beds 24a to 24e. This reveals fluctuations similar to those indicates the size variation was significant. Also, the size reduction in shown by the overall population of conodonts, with a peak size in Bed bed 26 is credible as shown by the 95% confidence interval of the mean 24d and a marked reduction in Bed 24e (Fig. 4). t-test for means shows shown in Table 1. In beds 27 and 28, Hindeodus–Isarcicella replaced that the size reduction during this transition was significant (p=0.007). Neogondolella as the dominant genera. There are abundant Hindeo- dus–Isarcicella P1 elements in these beds. Jiang et al. (2007) identified 4.2. Data from the Shangsi section three assemblages from the end Permian (bed 24a) to the earliest Triassic (bed 29) by comparing the ratio of Hindeodus–Isarcicella P1 Table 2, Figs. 5 and 6 show the size variation of P1 elements of elements to the Neogondolella P1 elements, and beds 27 and 28 belong Hindeodus–Isarcicella and Hindeodus from the Shangsi Section, to their second assemblage. In bed 27b, the dominant peak and the Sichuan Province. The first change was recognized in the transition

Table 2 The total number, mean size, standard deviation and 95% conﬁdence interval of the mean of specimens of the P1 element of Hindeodus-Isarcicella of earliest Triassic age from the Shangsi Section, Guangyuan, Sichuan Province

Bed 28c 28d 29a 29b 29c 30(b+c) 30d 31a 31b 32 33 Number 11 1 1 24 7 7 32 104 41 19 15 Mean(mm) 0.355 0.431 0.194 0.339 0.313 0.390 0.402 0.348 0.364 0.343 0.455 Standard deviation 0.051 0 0 0.066 0.044 0.105 0.066 0.078 0.114 0.062 0.131 95% Conﬁdence interval of the mean 0.3949 0.3630 0.3538 0.4681 0.4256 0.3631 0.4004 0.3735 0.5277 0.3272 0.3043 0.2731 0.3123 0.3783 0.3329 0.3277 0.3134 0.3829 G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187 181

other important geological events such as an anoxic event, sea-level changes and carbon isotope oscillations (Fig. 7).

5.1. Palaeoecology of conodont Hindeodus–Isarcicella

The palaeoecology of Hindeodus and Isarcicella is still controversial. There are two main views: one viewpoint considered Hindeodus– Isarcicella to be a near-shore, shallow water taxon (Clark, 1974; Wardlaw and Collinson, 1984; Tian, 1993; Hirsch, 1994; Baud, 1996; Krystyn and Orchard, 1996; Orchard, 1996); the other supposed that Hindeodus–Isarcicella had a wide facies range and occurred both in shallow and deeper water environments (Behnkn, 1975; Clark, 1981; Zhang, 1990; Kozur, 1995, 1996; Kozur, 1998). Kozur (1995) also pointed out that Hindeodus shows no provincialism and straddles the P/T boundary and is therefore the most suitable genus for defining the Fig. 6. Variation of the mean size of P1 elements of Hindeodus from the earliest Triassic P/T boundary within a phylomorphogenetic line. fi of the Shangsi Section, Sichuan Province. The black area is the 95% con dence interval of Lai et al. (2001) and Lai and Zhang (1999), based on the evolution of the mean size, and the central white circle and line show variation of the mean size. Hindeodus–Isarcicella and Clarkina (Neogondolella), and on palaeoenvironmental interpretations of the Meishan D Section, concluded that between beds 29c and 28 (combined beds 28c and 28d) in the Hin- Hindeodus was pelagic, found in sediments deposited at different deodus parvus zone (Lai et al., 1996). The upper line (0.3538) of the 95% depths, but living in the top layer of the ocean water. They also confidence interval of the mean size of bed 29c is larger than the lower suggested that the replacement of Clarkina by Hindeodus was caused line (0.3272) of bed 28, while the upper line of the 75% confidence by the development of anoxic bottom waters during the Permian– interval of the mean size of bed 29c (0.3321) is smaller than that of the Triassic transition and into the Early Triassic. If the upper water lower line of bed 28 (0.3381), and the t-test for means (p=0.021) also became anoxic (Grice et al., 2005; Huang et al., 2007), even Hindeo- shows there is no reason to doubt this size reduction.. The second size dus–-Isarcicella would be affected. Nicoll et al. (2002) also noted that change was during the transition between bed 30d and 31a, in the I. Hindeodus was present in a wide range of marine depositional isarcica zone. The upper line (0.3631) of the 95% confidence interval of environments, but they thought the replacement of Neogondolella by the mean size of specimens in bed 31a is smaller than the lower line Hindeodus–Isarcicella was due to an increase of turbidity levels. If the (0.3783) for bed 30d. So, the size reduction of this episode is credible turbidity of the water was one of the main factors affecting the size at a 95% confidence level, and the t-test for means (p=0.001) also reduction of Neogondolella as proposed by Luo et al. (2006), it cannot supports this phenomenon. As in the Meishan section, these data show have been the reason for the size reduction of the conodont Hindeo- that conodont size underwent two-episodes of reduction at the Shangsi dus–Isarcicella. section during the earliest Triassic. A comparison of the mean sizes of On the basis of previous literature regarding the ecology of Hin- elements in these two sections shows that the mean size of hindeodid deodus–Isarcicella and the characters of these conodonts at the conodonts from the Shangsi Section is smaller than that of the Meishan Meishan A section, the authors consider that Hindeodus–Isarcicella Section. There is no reason to doubt that the difference in mean size is were pelagic conodonts, maybe dwelling in the photic-zone or creditable as shown by a t-test of the means (p=0.000). This difference somewhat deeper, thereby appearing as fossils in both shallow and in means size between the two sections will be discussed below. deep water facies. The anoxic event may have impacted on the evolution of Hindeodus–Isarcicella, which suggested that perhaps 5. Discussion implying photic zone anoxia (such as bed 27 at the Meishan Section, Grice et al., 2005). The genera Hindeodus and Isarcicella survived the P–T mass There are also different opinions regarding the feeding mechan- extinction and then flourished in the earliest Triassic. Taxonomically, isms of conodonts. Nicoll (1985, 1987) thought that the conodont both genera present no obvious change after the major extinction apparatus is the filtering array of a microphagous active suspension events during the P–T transition. However, the Hindeodus–Isarcicella feeder, while others have interpreted it to be the grasping and food- populations show several episodes of size reduction of P1 elements in processing structure of a macrophagous predator or scavenger (Briggs this interval. As shown in Fig. 3–6, from the latest Permian to earliest et al., 1983; Aldridge et al., 1987; Purnell, 1993). In either case, the Triassic the mean size of P1 elements of Hindeodus–Isarcicella abrupt decline of food supplies could have driven the size reduction of remained nearly the same except for the several times when they the conodont populations, by creating high juvenile mortality. Based experienced obvious size reductions. If the size changes are evidence on the detailed study of the polygonal microsculpture of Neogondo- of biotic crisis (Girard and Renaud, 1996; Schmidt et al., 2006; lella elements from bed 24e at Meishan (Jiang et al., 2008) indicates an Twitchett, 2007), it would indicate that there were several crises that high juvenile mortality at this bed. affected the growth of the conodonts in the P/T transition period. Normally, it is difficult to distinguish juvenile hindeodids from 5.2. Palaeoenvironmental changes during the P/T transition small adult elements (Dr. Robert Nicoll, personal communication 2006). However, the texture and the thickness of the cavity are 5.2.1. Sea-level changes different in the juvenile and adults. The cavity of the juvenile is thin Zhang et al. (1996) studied the sequence stratigraphy of the and translucent, whilst that of the adult is thick and non-translucent. Meishan D section in detail and proposed that the top contact of bed Using this criterion, we interpret the size reductions of Hindeodus– 24d is a type II sequence boundary, that bed 24e was an upward Isarcicella elements in our study to be indicative of populations with shallowing parasequence, and that bed 27b to 29 belongs to a a higher proportion of juveniles. The evolutionary rate of the transgressive systems tract. Lai et al. (2001) and Lai and Zhang (1999) hindeodid–isarcicellid clade through the PTB interval is very high, analyzed the sea-level change bed by bed from bed 24d to 29 of the reflecting a rapidly changing environment. In this sense, these Meishan D section. They thought that the depth of deposition of bed conodonts did respond to the P–T mass extinction. The temporal 24d was about 20–60 m, while that of bed 24e was about 30–40 m. pattern of the conodont size variation is also coincident with some Bed 25, the “white clay bed”, is composed of montmorillonite–illite 182 G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187

Fig. 7. Columnar section and some important changes in the Permian–Triassic boundary beds of the Meishan Section in Changxing Country, Zhejiang Province, South China (references see the text). 1, clay; 2, calcareous mud; 3, argillaceous limestone; 4. mud bearing limestone; 5, mud and silicious-bearing limestone; 6, boidetrital limestone; 7, high temperature quartz; 8, zircon; 9, microsphere; 10, horizontal bed; 11, microwave bed; 12, inversely graded bed. All the conodont specimens are magnified by 44.4. claystones with subordinate kaolinite, and is of volcanic origin (Yin papers that discuss this question. Li and Zhou (2002) found pyrite in et al.,1992; Yin and Zhang,1996). Bed 26 is a finely laminated, organic- bed 24d at the Meishan section and concluded that the anoxic event of rich, dark mudstone with fossils dominated by pelagic types mainly the end Permian started at bed 24d. In the present study, a lot of pyrite consisting of ophiceratid ammonites and abundant prasinophyte has also been found in bed 24d, but most grains are radiating or cubic algae (Yin et al., 1992). A few dysaerobic benthic taxa are present in aggregates. Some scholars supposed that the framboid pyrite with the this bed, including non-fusulinid foraminifera and tiny, thin-shelled diameter about 4–6 μm indicates that the sedimentary environment brachiopods. Bed 27 is a 16 cm thick grey, argillaceous micrite with was anoxic (Wignall and Twitchett, 2002). The authors argue that this scattered pyrite grains and a pervasively burrowed fabric, and the P/T type of pyrite is syngenetic and formed at the redox boundary. Also, boundary lies in the middle. Based on analysis of the microfacies and Huang et al. (2007) studied the ratio of Pr/Ph which reflects the redox faunal characters, Lai and Zhang (1999) speculated that the deposi- state of the bottom water. Based on Huang's data, it is evident that the tional depth of bed 27 was about 90 m. Bed 28 is a 4 cm thick illite– bottom water was oxygenated because the value of Pr/Ph was larger montmorillonite mixed claystone, with abundant framboidal pyrite than 1, although it fluctuated slightly stratigraphically. Furthermore, crystals and less bioturbation. Bed 29 is grey, medium-bedded, the presence of abundant and diverse representatives of the conodont dolomitic calcimicrite with minor mud and silt. It yields abundant genus Neogondolella in bed 24d also provides evidence against specimens of Ophiceras, Claraia and thin-shelled brachiopods. bottom-water anoxia at this horizon. Grice et al. (2005) concluded In summary, from the end of the Late Permian (bed 24) to earliest that the photic zones during deposition of beds 24 and 27 were anoxic Triassic, the sea-level underwent a regression until the base of bed 25, based on the study of Chlorobiaceae at the Meishan section. But followed by a rapid transgression. Wignall and Hallam (1993) also restudy on the biomarker during this time at Meishan Section thought that there was a transgression at this level and suggested that indicated that bed 24 was marked by brief episodes of anoxia the greatest deepening was represented in the upper part of bed 28. (Huang et al., 2007). Zhang et al. (1996) suggested that the anoxic event at the end Permian commenced at bed 24e, while Wignall and 5.2.2. Oceanic oxygenation Hallam (1993) and Wignall et al. (1996) considered that the anoxia As one of the main proposed causes of the mass extinction during started at bed 25 with abundant chalcophile-enriched pyrites the P/T transition, the anoxic event is very important. There are many reflecting anoxic conditions (Chai, 1992). G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187 183

Different opinions also exist about the redox conditions repre- 5.2.3. Palaeoproductivity sented in beds 25 and 26. Most previous authors have interpreted It is possible that oceanic productivity was reduced during the beds 25 and 26 as anoxic, particularly bed 26 (He,1989; Chai,1992; Yin Early Triassic, as indicated by the widespread sparsity of radiolarians, et al., 1992; Wignall and Hallam, 1993). However, new studies of lipids which are regarded as an indicator of oceanic productivity (Isozaki, during the P/T transition show that both of these beds were not truly 1997; Hollis, 2002; Wang and Abelmann, 2002; Ivanova et al., 2003; anoxic (Grice et al., 2005; Wang et al., 2005; Huang et al., 2007). The Danelian et al., 2004), and the lower value of δ13C in the Early Triassic latest studies have shown that bed 27 was anoxic in both bottom (Baud et al., 1989; Magaritz et al., 1992; Cao et al., 2002). 13 waters (Huang et al., 2007) and the photic zone (Grice et al., 2005), At the Meishan Section, in bed 24e, the negative shift of δ Ccarb is particularly beds 27c and 27d (Huang et al., 2007). Deepening of often accepted as one line of evidence for a reduction of productivity anoxia is purported to have led to euxinia and a buildup of dissolved (Cao et al., 2002; Wang et al., 2005). The same also holds for the 13 13 gases (i.e., H2S, CO2), in deep-water masses which then resulted in a negative shift of both δ Corg and δ Ckero in bed 26, negative shifts of 13 13 13 massive upwelling of H2S and CO2 (Knoll et al., 1996; Kump et al., δ Ccarb and δ Corg in bed 27c, as well as the negative shift of δ Ckero 2005). Riccardi et al. (2006) conjectured that the anoxic gas upwelled in bed 29. Many workers have accepted the idea that the main cause of into the upper water which might have caused the upper water to the negative excursion was a reduction of productivity in the oceans, 13 become anoxic. Because of the upwelling of H2S into the photic zone although the same negative trend of δ Ccarb could be explained by (Fig. 8; see also Kakuwa and Matsumoto, 2006), Chlorobiaceae became other factors (e. g. Berner, 2002). Another indicator is the concentra- enriched in the photic zone (Grice et al., 2005). In bed 28 and the tion of Ba, a trace element affected by palaeoproductivity (Dymond bottom of bed 29, the bottom water was slightly anoxic because the et al., 1992; Thomson et al., 1995; Wehausen and Brumsack, 1998; ratio of Pr/Ph is about 1 (Wang et al., 2005); while in the upper part of Warning and Brumsack, 2000). Ba is very low during the P/T bed 29, the bottom water was oxygenated as suggested by the ratio of transition, in most cases lower than 200 ppm, except in bed 26 Pr/Ph being greater than 1 (Huang et al., 2007). The photic zone at the where it is 310 ppm (Zhang et al., 2005). These Ba values are much time of deposition of these two beds may have been oxygenic, given lower than the average value of shale, 580 ppm (Wedepohl, 1991). Ba the evidence of the lower abundance of Chlorobiaceae (Grice et al., concentrations in beds 24e, 27c and 29 are lower than in their 2005). overlying and underlying beds. The comparatively higher value of Ba

Fig. 8. Speculative pattern of anoxia distribution in beds 26 and 27c of the Meishan Section. 1: Conodont Hindeodus–Isarcicella; 2: Pyrite; 3: Organic material. In bed 26, both the bottom water and upper water was oxygenic, while in bed 27c, not only the bottom water was anoxic, but also did the upper water in the photic zone(Grice et al., 2005; Huang et al., 2007). In bed 27c, the terrestrial organic matter was increase (Xie et al., 2007), with decomposition of sinking organisms consuming oxygen in the water and reductive gases, such as

H2S, and CO2 upwelling. 184 G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187 concentration in bed 26 may have been caused by a high intensity of than in shallow water and it was deeper in Shangsi than in Meishan at microbial activity (Xie et al., 2005). Also, lots of the corals, fusulinids and the time of the Permian–Triassic transition. ammonoids, deep-water radiolarians and many Permian brachiopods disappeared during the transition of bed 24d/24e, and lots of the skeletal 5.3.2. Anoxia fragments of major benthos disappeared in bed 24e (Kaiho et al., The anoxic event is thought to be one of the main causes of the 2001; Yin et al., 2007b). Further losses occurred in beds 25 and 28. mass extinction during the P/T transition (Wignall and Hallam, 1993; Isozaki, 1997; Li and Zhou, 2002; Grice et al., 2005; Huang et al., 2007). 5.3. Possible causes of the size reduction As discussed above, the photic zone was anoxic (Grice et al., 2005), even in bed 27c and 27d.

Research on biotic miniaturization (including the size reduction) Because the photic zone was anoxic and filled with abundant H2S, during the Permian–Triassic biotic crisis is in its infancy. Elucidation of this must have constituted a major threat to the survival of Hindeo- the causes of miniaturization would provide a further understanding dus–Isarcicella living in the same zone. Thus, one could expect a link of the mass extinction as well as the ensuing recovery. Previous between the onset of anoxic conditions in the photic zone and the size research on this topic based on fossil data from the Lower Triassic has reduction of the conodonts. suggested numerous possible causes, including extinction and preservation selectivity, fluctuating temperatures, decreased food avail- 5.3.3. Sea-level changes ability, fluctuating sea-level, changes in oceanic oxygenation including Although food shortage and anoxia are herein regarded as the a reduction in oxygen level, abnormal salinity, changes in oceanic main causes of the size reduction of Hindeodus–Isarcicella,the turbidity, exposure to waves, high population densities, and unfavor- contribution of sea level changes can not be ignored. In general, able substrate conditions (Hallam, 1965; Price-Lloyd and Twitchett, transgression would not directly have affected the size of Hindeodus– 2002; Twitchett, 2005a; He et al., 2007). Twitchett (2005a) suggested Isarcicella because they were pelagic elements. A major transgression that neither extinction selectivity nor preservation selectivity could event, however, might have triggered some other environmental account for the Lilliput effect, while increased temperature, decreased changes, such as anoxia and water quality, which in turn could have food supply, and changes in the duration of the colonization windows retarded the growth of conodonts across the PTB. For example, Luo between anoxic intervals could have been responsible for some of the et al. (2006) forwarded an increase in turbidity of the sea-water as one Lilliput effects. Luo et al. (2006) suggested that the reduction of food of the possible causes responsible for the size reduction of Neogon- supply, increase in the turbidity of the sea water and the shallowing of dolella. However, this interpretation should not be extrapolated to the sea water were the main causes of the size reduction of conodont explain the size reduction of Hindeodus–Isarcicella, as this clade was Neogondolella at the end Permian at the Meishan section. As probably less affected by turbidity than Neogondolella Nicoll et al. mentioned by Twitchett (2005a), the effect of many of these causes (2002). For example, the sizes of Hindeodus–Isarcicella from beds 25 has not been adequately addressed and even questioned. Here, we will and 28, two volcanic ash beds (hence, higher turbidity), are actually discuss the possible causes of the size reduction of Hindeodus–Isarci- larger than their counterparts from other beds of non-volcanic origin. cella during the Permian–Triassic transition. The physiology, development and evolution of organisms are 5.4. The relationship between size reduction and mass extinction affected by their living environment. There is not any one factor that can explain all the episodes of size reduction phenomenon well. There There is a coincidence between the horizons where size reduction may be different dominant factors for each of the size reduction of conodonts occurred and the horizons where mass extinctions of episodes. Given the relationship between the size variation of Hin- other taxa are found, so the two are clearly related. The size reduction deodus–Isarcicella and indicators of palaeoenvironmental change of Hindeodus–Isarcicella took place in four main episodes: in beds 24e, during the P/T transition, as well as the palaeoecology of Hindeodus– 26, 27c and 29; one of these (bed 24e) is synchronous with the first Isarcicella (as outlined above), the authors consider that the main mass extinction point of the three-episode extinction model, and the factors accountable for the size reduction of the studied conodonts are timings of two others (beds 26 and 29) are slightly offset against the the anoxic event and a sharp decline in food resources. remaining two main extinction levels of the three-episode extinction model. These differences in timing are probably related to different 5.3.1. Food shortage extinction processes and mechanisms. The extinction at bed 24e From the above discussion, productivity apparently decreased appears to be one of catastrophic nature, with a decrease of δ34S during each of the transitions between beds 24e/24d, 26/25, 27c/27b (Kaiho et al., 2001) and sudden disappearance of numerous organisms and 29/28. Previous work has suggested that the transition between (Yin et al., 2007b). As a consequence, not only did the elements of the beds 24d/24e corresponds to one episode of mass extinction during conodonts Hindeodus–Isarcicella and Neogondolella show a distinct the P/T transition (Wu et al., 1988; Yin and Tong, 1998; Kaiho et al., size reduction, so do the fish teeth (unpublished data). At beds 26 and 2001); the same is also true for beds 25 and 28, which correspond to 29, the two size reduction events of the Hindeodus–Isarcicella slightly two major extinction levels (Wu et al., 1988; Jin et al., 2000; Fang, lagged behind the corresponding two mass extinction points; 2004a; Xie et al., 2005). The size reductions in beds 26 and 29 however, both of the size reduction events coincide with the coincided closely with the expansion of cyanobacteria plankton, expansion of microbes (cyanobacteria) (Xie et al., 2005). suggesting a great simplification of the food web as might be expected As discussed above, the main reasons of the size reduction of with major productivity collapse. conodont Hindeodus–Isarcicella are likely to be a sharp decline of food So food production at the times of deposition of beds 24e, 26, 27c resources and the onset of anoxic conditions. As the evidence available and 29 must have been very low. Hindeodus–Isarcicella was a carnivore for anoxia in bed 24e is conflicting, the main reason for the size reduction or scavenger (Purnell, 1993), so when the biomass was suddenly and of conodonts in this bed may be attributed to a shortage of food caused sharply reduced, its food resources for would have declined sharply, by the mass extinction. A severe food shortage in both bottom and upper leading to a higher juvenile mortality. Particularly interesting, the waters in bed 24e may also explain why the mass extinction at this level mean size of Hindeodus–Isarcicella P1 elements at the Meishan Section was the largest during the P–T transition. It is also in accord with the was larger than that for the Shangsi Section. This may be due to sharp and large decline of fossil fragments Kaiho et al. (2006) and the differences in the availability and in the abundance level of food sharp decline of sulfate isotope (Kaiho et al., 2001) in this bed. resources between their different localized living environments. The size reduction in bed 26 corresponds with the main extinction Obviously, in general food resources are more limited in deep water level proposed by Yin and Tong (1998), but lags behind the main G. Luo et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 264 (2008) 176–187 185 extinction point (bed 25) advocated by Jin et al. (2000), Wignall and (2) A sharp decline of food coupled with the onset of an anoxia are Hallam (1993), Fang (2004a) and Xie et al. (2005). In view of the considered to be the most likely triggers. In addition, relationship between the size reduction and the mass extinction, it is transgression may have played a role. plausible that the second episode of mass extinction started at the (3) Based on the relationship between size reduction of Hindeo- time of deposition of bed 25, and peaked at the time of bed 26. dus–Isarcicella and different episodes of mass extinction Because of the mass extinction and the expansion of cyanobacteria in proposed by previous authors, it is suggested that there were bed 26, the food source for Hindeodus–Isarcicella declined sharply, at least three episodes of extinction during the P/T transition. consequently leading to the size reduction of the elements. On the These three episodes are represented in beds 24e, 26 and 28 other hand, we can not exclude the possibility that the extinction just respectively, with the main extinction level possibly at bed 24e. took place in bed 25, while bed 26 represents an ‘organism winter’ Another extinction also appears likely at the transition of bed after the mass extinction, just like the size reduction of bed 29. 27c/27b. Likewise, the size reduction of specimens in bed 29 lags a little behind the mass extinction of bed 28, but it was coupled with a major Acknowledgements expansion event of cyanobacteria Xie et al. (2005). From the palaeoenvironmental viewpoint of this bed (as discussed in 4.2.2), the authors This work was supported by the Natural Science Foundation of consider that the anoxic extent of bed 29 was not as strong as in bed 28, China (grant Nos 40621002, 40232025) and by the Program for although some authors have suggested that bed 29 is also anoxic, maybe Changjiang Scholars and Innovative Research Team. LXL acknowl- more so than bed 28 Wang et al. (2005). The mass extinction took place edges the Royal Society, NERC and “111” project of Chinese State in bed 28, and bed 29 could represent another “organism winter”after Administration of Foreign Experts Affairs (grant No. B08030) for the mass extinction. Because of the extinction, the grazing pressure funding this international collaboration. GRS acknowledges continu- during bed 29 declined, so the cyanobacteria once again expanded. In ing support from the Australian Research Council (ARC P0772161) and the wake of the mass extinction of bed 28, the decline of food in bed 29 a research grant from the Chinese Academy of Science (2006-1-16). caused the size reduction of Hindeodus–Isarcicella. Thanks due to Prof. Richard J. Aldridge for his significant comments on In addition to the three episodes of size reduction mentioned this manuscript. The authors also would like to thank Dr. Robert Nicoll above, there was also a distinct size reduction in bed 27c. The bottom for his valuable suggestion on distinguishing the juvenile and of bed 27c records the first appearance of H. parvus, marking the start dwarfism element, and Yali Jin, Hua Huang and Zhihong Li for their of the Triassic. The significance of the transition from bed 27b to 27c field assistance and laboratory dissolution of samples. The paper was has only received limited attention. For example, Zhang et al. (1996) improved by constructive comments from Dr. Charles Henderson and pointed out that the bottom of bed 27c is an important biological an anonymous reviewer. event surface. Cao et al. (2002) also showed a negative shift of both δ13 δ13 fl Δ13 δ13 −δ13 Corg and Ccarb, and strong uctuations in C(= Ccarb Corg) References across this transition, More recently, Grice et al. (2005) also reported that the photic zone at the time of deposition of bed 27 was anoxic, Aldridge, R.J., Smith, M.P., Norby, R.D., Briggs, D.E.G., 1987. The architecture and function and Huang et al. (2007) concluded that the bottom water of this bed of Carboniferous polygnathacean conodont apparatuses. In: Aldridge, R.J. (Ed.), was anoxic based on the ratio of Pr/Ph. Xie et al. (2007)showed that Palaeobiology of conodonts. Ellis Horwood press, Chichester, England, pp. 63–75. Bambach, R.K., Knoll, A.H., Wang, S.C., 2004. 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