Mass Extinctions and Changing Taphonomic Processes

Chapter 16 1

Mass Extinctions and Changing 2

Taphonomic Processes 3

Fidelity of the Guadalupian, Lopingian, 4 and Early Triassic Fossil Records 5

Margaret L. Fraiser, Matthew E. Clapham, and David J. Bottjer 6

Contents

1 Introduction ...... 000 2 Previous Understanding of Biases in the Middle Permian to Early Triassic Fossil Record 000 2.1 End-Guadalupian Extinction and Lopingian Aftermath ...... 000 2.2 End-Permian Mass Extinction and Early Triassic Aftermath ...... 000 3 Methods ...... 000 4 Results ...... 000 4.1 Guadalupian–Lopingian Lazarus Effect ...... 000 4.2 Patterns in Permian Silicification ...... 000 4.3 Early Triassic Lazarus Effect ...... 000 4.4 Patterns in Early Triassic Silicification ...... 000 5 Conclusions ...... 000 References ...... 000

Abstract The biotic crisis of the Middle Permian through Early Triassic is unmatched 7 in the Phanerozoic in terms of taxonomic diversity losses and paleoecological reor- 8 ganization. However, the potential taphonomic bias from post-mortem diagenesis for 9 this crucial time has not been evaluated. We assessed the quality of the fossil record 10 during this interval by quantifying the number of Lazarus taxa using – our own 11 database, data available in the Paleobiology Database and previous compilations. We 12 also quantitatively tested for paleoecological differences between silicified versus 13

M.L. Fraiser ( ) Department of Geosciences, University of Wisconsin-Milwaukee, Milwaukee, WI 53203, USA e-mail: [email protected] M.E. Clapham Department of Earth and Planetary Sciences, University of California Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, USA e-mail: [email protected] D.J. Bottjer Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, USA e-mail: [email protected]

P.A. Allison and D.J. Bottjer (eds.), Taphonomy, Second Edition: Process and Bias Through Time, Topics in Geobiology 32, DOI 10.1007/978-90-481-8643-3_16, © Springer Science+Business Media B.V. 2010 M.L. Fraiser et al.

14 non-silicified faunas. Herein we report that there is no major taphonomic bias due to 15 skeletal mineralogy or fossil preservation affecting the Middle and Late Permian fos- 16 sil record, but that aragonite-shelled molluscs may exhibit a significant Lazarus effect 17 during the Induan. We propose that a variety of mechanisms affected the fossil record 18 of the Paleozoic/Mesozoic transition, including ocean chemistry, paleobiology of the 19 examined groups, and human influences on taxonomic and sampling practices.

20 1 Introduction

21 Mass extinctions are geologically short intervals of time when biodiversity losses 22 are significantly elevated above background rates of extinction (e.g. Jablonski 23 1986a; Sepkoski 1986; Flessa 1990). They are a prominent feature of the fossil 24 record and, along with the rise and fall of the three great evolutionary faunas, 25 shaped the Phanerozoic biodiversity curve (Raup and Sepkoski 1982; Sepkoski 26 1981, 1984; Courtillot and Gaudemer 1996). Mass extinctions are also important 27 agents of macroevolutionary change because they eliminate successful groups of 28 organisms and create new evolutionary opportunities for previously minor groups 29 (Gould and Calloway 1980; Jablonski 1986a, b, 2001, 2005; Raup 1986, 1994; 30 Erwin 2001; Bambach et al. 2002). A complete understanding of the evolutionary 31 role of a mass extinction must include more than just an analysis of the taxonomic 32 crisis because the effects of mass extinctions extend beyond the biodiversity 33 losses: the aftermaths may be as important as the extinctions themselves because 34 the new ecological patterns arising from survivors that interact in new ways in less 35 crowded ecological niches (Droser et al. 1997, 2000; Erwin 2001; Bambach et al. 36 2002; Jablonski 2001, 2002). 37 Proper interpretation of the duration, magnitude, and causes of mass extinctions 38 and the nature of the survival and recovery of organisms during their aftermaths is 39 contingent upon accurate reconstruction of taxonomic and ecological changes. 40 Artifacts of sampling methods or taxonomic practice can obscure the real trends 41 (Sepkoski 1986; Flessa 1990), whereas taphonomic biases inherent in the geologic 42 record, such as mode of organism preservation (Schubert et al. 1997), rock volume 43 (e.g., Crampton et al. 2003), and preferential loss of organisms with aragonitic shell 44 mineralogy (e.g. Cherns and Wright 2000) may also influence observed patterns. 45 Such taphonomic biases may have obscured the true biotic patterns during the 46 Permian–Triassic extinction and its aftermath. These potentially confounding 47 effects have been inferred from the abundance of Lazarus taxa – taxa that temporar- 48 ily disappear from the fossil record but reappear later unchanged (Flessa and 49 Jablonski 1983) – and from a decrease in preservation by silicification (Erwin and 50 Pan 1996; Schubert et al. 1997; Twitchett 2001). Lazarus taxa may be an indicator 51 of the quality of the fossil record if the phenomenon reflects a failure of certain 52 organisms to be preserved through taphonomic effects such as the Signor–Lipps 53 effect, outcrop area bias, paleolatitudinal sampling bias, or reduced preservation 54 quality (Signor and Lipps 1982; Allison and Briggs 1993; Erwin and Pan 1996; 16 Mass Extinctions and Changing Taphonomic Processes

Smith and McGowan 2007). Lazarus taxa abundance may also be due to biological 55 factors such as reduced population size (which may also affect the chance of sam- 56 pling a taxon) or reduced geographic range and migration to refugia. (Jablonski 57 1986a,b; Kauffman and Harries 1996; Wignall and Benton 1999; Twitchett 2001; 58 Rickards and Wright 2002). Taxonomic uncertainty can cause an apparent Lazarus 59 effect (Wheeley and Twitchett 2005). 60 Herein we test two aspects of the quality of the fossil record during the 61 Guadalupian, Lopingian, and Early Triassic. The end-Guadalupian and end-Permian 62 extinctions marked the end of the Paleozoic (Fig. 1) and heralded major changes in 63 benthic marine ecology (e.g. Fraiser and Bottjer 2007; Clapham and Bottjer 2007a, b), 64 but several studies have proposed that taphonomic processes make it difficult to 65 extract real ecological patterns during these key intervals in evolutionary history 66 (e.g. Erwin and Pan 1996; Twitchett 2001). First, we quantified the number of Lazarus 67 taxa among several key taxonomic groups, as an increased number of Lazarus taxa 68 may indicate reduced preservation quality. Second, a potential source of bias in the 69 fossil record for this interval, changes in preservation via silicification, was tested 70 by quantifying the proportion of silicified fossil collections, comparing the alpha 71 diversity of silicified and non-silicified (preserved as molds and casts) collections, 72 and assessing the number of taxa exclusive to silicified collections. Silicification is 73 important because it allows fossils to be acid-etched and freed from calcareous 74 matrix, often preserving very fine morphological details and improving ease of iden- 75 tification by taxonomists (e.g. Holdaway and Clayton 1982). It can also preserve a 76 more faithful record of the original diversity and abundance within an assemblage 77 (Cherns and Wright 2000; Wright et al. 2003, Butts and Briggs, this volume). Results 78 of this test will reveal any temporal trends in silicification and the extent to which 79 silicified faunas preserve a higher fidelity record. Together these tests document the 80

Fig. 1 Geologic timescale of Middle Permian (Guadalupian), Late Permian (Lopingian), and Early Triassic stages. Ch = Changhsingian, Ind = Induan. The lower panel shows the per-capita extinction rates (Foote 2000) for rhynchonelliform brachiopods, bivalves, and gastropods in each stage based on data from Clapham et al. (2009) (Permian invertebrates), Chen et al. (2005) (Early Triassic brachiopods), Gastrobase (Early Triassic gastropods), and the Paleobiology Database (Early Triassic bivalves and gastropods). The per-capita extinction for rhynchonelliform brachiopods is undefined in the Induan because no genera cross both bottom and top boundaries of the stage M.L. Fraiser et al.

81 taphonomic quality of the Permian–Triassic fossil record in greater detail and elucidate 82 the impact of temporal trends of taphonomic bias on the records of the end-Guadalupian 83 extinction, the end-Permian extinction, and their aftermaths.

84 2 Previous Understanding of Biases in the Middle 85 Permian to Early Triassic Fossil Record

86 2.1 End-Guadalupian Extinction and Lopingian Aftermath

87 The end-Guadalupian extinction, at the end of the Middle Permian (Guadalupian 88 Series), was the first phase of the two-stage taxonomic crisis during the Permian– 89 Triassic interval (Jin et al. 1994; Stanley and Yang 1994). Initial estimates suggested 90 that biodiversity loss during the end-Guadalupian event was severe with as many as 91 55–60% of all marine invertebrate and fusulinid genera going extinct (Stanley and 92 Yang 1994). However, more recent studies have shown that extinction rates were 93 actually not elevated during the end-Guadalupian interval among most marine 94 invertebrate groups, including brachiopods, bivalves, and gastropods (Shen et al. 95 2006; Clapham et al. 2009). Nevertheless, the end-Guadalupian extinction remains 96 an especially severe event for fusulinids (Stanley and Yang 1994; Yang et al. 2004). 97 The potential causes of the extinction are unclear, and there may not be a need to 98 invoke serious perturbations given the negligible invertebrate extinctions. 99 Environmental changes during the Guadalupian–Lopingian interval include the 100 Emeishan flood basalts (Wignall 2001), possible climate cooling (Isozaki et al. 101 2007), and the onset of deep-marine anoxia (Isozaki 1997). Despite the minimal [AU1] 102 effects on global invertebrate biodiversity, environmental stress during the 103 Guadalupian–Lopingian interval caused profound changes in the habitat distribu- 104 tion of bryozoans during the Lopingian (Powers and Bottjer 2007), shifts in the 105 relative abundance of rhynchonelliform brachiopods and molluscs in offshore habi- 106 tats (Clapham and Bottjer 2007a, b), and a dramatic reduction in the number and 107 size of reefs in the Wuchiapingian (Weidlich 2002; Weidlich et al. 2003). 108 The potential influences of taphonomic bias on the apparent severity of the end- 109 Guadalupian extinction were first investigated by Stanley and Yang (1994). They 110 applied three tests and concluded that the end-Guadalupian extinction peak did not 111 result from a poor Lopingian fossil record. The preferential extinction of large, 112 complex fusulinid genera, the inconsistency between observed patterns of extinction 113 and predicted Signor–Lipps effects, and a strong excess of originations relative to 114 extinctions in the Wuchiapingian and early Changhsingian all suggest that tapho- 115 nomic biases only had minor effects on the end-Guadalupian extinction (Stanley 116 and Yang 1994). However, other taphonomic effects, including changes in the abun- 117 dance of silicified fossil collections or reductions in preserved rock volume, may 118 have exacerbated the severity of the end-Guadalupian extinction without producing 119 a spurious Signor–Lipps effect or completely masking the Lopingian radiation. 16 Mass Extinctions and Changing Taphonomic Processes

2.2 End-Permian Mass Extinction and Early 120 Triassic Aftermath 121

The end-Permian mass extinction, approximately 252 million years ago, was the 122 largest biotic crisis of the Phanerozoic (Bambach et al. 2004; Henderson 2005) with 123 78% of marine genera going extinct (Clapham et al. 2009). For up to 5 million years 124 during the Early Triassic aftermath of the end-Permian mass extinction, benthic 125 marine paleocommunities were characterized by low biodiversity and low ecologi- 126 cal complexity compared to pre-extinction Permian and later Triassic paleocom- 127 munities (e.g. Fraiser and Bottjer 2005b; Lehrmann et al. 2006). Macroevolutionary 128 changes in benthic marine ecology, such as a shift from primarily non-motile organ- 129 isms to self-mobile taxa and a switch from rhynchonelliform brachiopod-dominated 130 to bivalve-dominated paleocommunities, were triggered by the end-Permian mass 131 extinction (Bambach et al. 2002; Wagner et al. 2006; Fraiser and Bottjer 2007). 132 Sedimentological and geochemical evidence indicate that much of the latest 133

Permian through the Early Triassic had an atmosphere with elevated CO2 and low 134

O2, and an ocean rich in H2S and depleted in O2; these conditions were ultimately 135 linked to extensive volcanism and the supercontinent configuration of Pangea (e.g. 136 Wignall and Twitchett 1996; Wignall 2001; Berner 2004; Grice et al. 2005; Huey 137 and Ward 2005; Sephton et al. 2005). 138 It has been reported that a large portion of Early Triassic taxa are Lazarus taxa 139 (Batten 1973; Erwin and Pan 1996; Twitchett 2001). For example, there are esti- 140 mates that 69% of gastropod genera are Lazarus genera during the Griesbachian 141 (Erwin 1996), and that 90% of sponge families are Lazarus taxa during all stages 142 of the Early Triassic (Twitchett 2001). Though the Early Triassic Lazarus phe- 143 nomenon heretofore had been examined for gastropods and sponges only (e.g. 144 Erwin 1996; Erwin and Pan 1996; Twitchett 2001, Wheeley and Twitchett 2005), 145 it has been implied that the Lazarus effect was very large for all groups of skele- 146 toned benthic marine invertebrates during the Early Triassic (e.g. Twitchett 2001; 147 Erwin 2006). 148 An absence of faunas preserved by silicification has been proposed as a major 149 cause of the Early Triassic Lazarus phenomenon and for the apparent delayed 150 biotic recovery following the end-Permian mass extinction (Erwin 1996, 2006; 151 Erwin and Pan 1996; Kidder and Erwin 2001). This hypothesis is based on studies 152 indicating that silicified faunas have a higher fidelity of fossil preservation than 153 non-silicified faunas preserved as casts and molds (Cherns and Wright 2000; 154 Wright et al. 2003). Furthermore, it has been proposed that the post-Paleozoic 155 fossil record suffers from a taphonomic “megabias” because of low numbers of 156 silicified faunas compared to the Paleozoic (Schubert et al. 1997). Previous 157 studies of the fidelity of the fossil record following the end-Permian mass extinc- 158 tion have focused on only one group of benthic marine organisms (e.g. gastro- 159 pods, Erwin and Pan 1996; or echinoids, Smith 2007), or have examined data 160 from the Triassic period as a whole (Smith 2007), obscuring any processes that 161 may have been unique to the aftermath of the end-Permian mass extinction. 162 M.L. Fraiser et al.

163 The extent of silicification during the Early Triassic has not been quantified 164 previously, and the characteristics of silicified faunas have not been statistically 165 compared to those of non-silicified ones.

166 3 Methods

167 We compiled a database of Roadian (Middle Permian) through Anisian (Middle 168 Triassic) rhynchonelliform brachiopod, bivalve, gastropod, and demosponge fossil 169 occurrences. This was used to examine two additional taphonomic metrics that test 170 the fidelity of the Permian–Triassic fossil record and its potential influence on the 171 end-Guadalupian and end-Permian extinctions. The dataset includes (1) more than 172 53,321 Permian marine invertebrate fossil occurrences, including records of all 173 marine invertebrate groups, from 9863 collections (the database used in Clapham 174 et al. 2009); (2) Triassic gastropods modified and updated from Gastrobase, a data- 175 base of published occurrences of gastropod genera at the stage and substage levels 176 for the Permian and Triassic periods (http://www.earth.cardiff.ac.uk/people/sum- 177 maries/GASTROBASEdoc.htm); (3) Triassic bivalves and sponges, and Anisian 178 brachiopods, from the Paleobiology Database (www.paleodb.org); and (4) Early 179 Triassic rhynchonelliform brachiopods (Chen et al. 2005). Though the PBDB is not 180 flawless, it is the most complete database available for comparing benthic marine 181 organisms from the Lopingian, Early Triassic, and Middle Triassic. Taxonomic 182 assignments were corrected when necessary and possible. 183 First, the number of rhynchonelliform brachiopod, bivalve, gastropod, and 184 sponge Lazarus taxa in each stage from the Roadian to Anisian was quantified to 185 test for poor preservation, especially in the Wuchiapingian stage immediately fol- 186 lowing the traditional end-Guadalupian extinction interval and the Induan and 187 Olenekian stages following the end-Permian extinction (Appendix A). The signifi- [AU2] 188 cance of differences between the proportions of Lazarus taxa between stages was 189 determined using a two-tailed t-test. 190 Second, the number of Permian and Early Triassic silicified collections was 191 tallied using the Clapham et al. (2009) database, 211 Paleobiology Database 192 collections, and 358 additional Induan and Olenekian collections culled from the 193 primary literature to determine whether a reduction in silicification, particularly 194 due to the loss of the rich record from western North America, affected diversity 195 and extinction (Appendix B). Included in the analyses were benthic marine inver- 196 tebrates from level-bottom marine communities; planktonic, nektonic, and reef 197 collections were excluded in the Triassic but not in the Permian data. Species 198 richness (alpha diversity) of each silicified collection was determined and com- 199 pared to the richness of non-silicified collections. The number of brachiopod, 200 bivalve, and gastropod genera unique to silicified collections was also quantified 201 to determine the influence of silicification on large-scale compilations of taxo- 202 nomic diversity. 16 Mass Extinctions and Changing Taphonomic Processes

4 Results 203

4.1 Guadalupian–Lopingian Lazarus Effect 204

During the Guadalupian and Lopingian, the prevalence of Lazarus taxa varied 205 significantly among different taxonomic groups. At the genus level, a substantial 206 percentage of gastropod taxa in a given stage, up to 38% of the total genus rich- 207 ness, are actually Lazarus taxa (Fig. 2a). In contrast, only 20–25% of all bivalve 208 genera (Fig. 2b) and 18–20% of all rhynchonelliform brachiopods (Fig. 2c) are 209 Lazarus taxa. Lazarus abundance is calculated by dividing the number of Lazarus 210 taxa by the total diversity (Lazarus taxa plus taxa sampled within the stratigraphic 211 interval) in each stage. Despite the pronounced difference between clades, the pro- 212 portion of Lazarus taxa within most clades typically exhibits little variation (Fig. 2). 213 There was no statistically significant change in the percentage of gastropod Lazarus 214 taxa from the Roadian through Wuchiapingian stages (varying between 33.3% and 215 38.6%). Likewise, the number of bivalve Lazarus taxa remained statistically 216 unchanged at 19.6–25.2% from the Roadian to the Wuchiapingian. Both aragonitic 217 bivalves and those with a calcite shell layer (pterioids, pectinoids, and mytiloids) 218 displayed statistically similar patterns and there is no systematic variation in the 219 number of Lazarus genera between the two mineralogies, suggesting that the num- 220 ber of Lazarus taxa is most strongly controlled by the abundance of a group rather 221 than its skeletal mineralogy. Lazarus taxa accounted for 18.4–20.8% of total rhyn- 222 chonelliform brachiopod diversity in the Roadian–Capitanian interval, with a 223 significant decrease to 10% in the Wuchiapingian (Z = 3.03, p = 0.002). However, 224 in notable contrast to the other groups, demosponges exhibit dramatic variation in 225 the percentage of Lazarus taxa in a given stage (Fig. 2d). Lazarus genera account 226 for 50.9% of all present or inferred sponges during the Wuchiapingian, but only 227 10.2% in the Wordian and 17.0% in the Changhsingian. 228 Although there are few changes in the percentage of Lazarus taxa from the Roadian 229 to Wuchiapingian, all investigated groups have substantially fewer Lazarus genera 230 in the Changhsingian stage (Fig. 2). The percentage of gastropod Lazarus taxa 231 decreased from more than 37% in the Wuchiapingian to only 18.8% in the 232 Changhsingian (Z = 2.73, p = 0.006), bivalve Lazarus taxa decreased from 19.6% 233 to only 4.9% (Z = 2.90, p = 0.003), rhynchonelliform brachiopods decreased from 234 10% to 0% in the Changhsingian (Z = 4.85, p < 0.001), and demosponges from 235 50.9% to 17.0% (Z = 3.69, p < 0.001). However, this dramatic reduction in the 236 percentage of Lazarus taxa does not imply a pronounced increase in the quality of 237 the fossil record or the fidelity of sampling during the Changhsingian. Rather, it 238 reflects edge effects due to the severe taxonomic impact of the end-Permian extinc- 239 tion. Because so many Permian genera became extinct (51% of gastropod genera, 240 65% of bivalves, and 96% of rhynchonelliform brachiopods, with the remaining 241 brachiopods disappearing in the Griesbachian), the likelihood of Permian taxa 242 occurring in the Triassic was greatly reduced and the latest Permian Changhsingian 243 M.L. Fraiser et al.

a 90 80 70 60

50 Genera 40 50 40 30 20 10 Lazarus Genera (%)

b 120 100 80

60 Genera 40

Aragonitic 40 Calcitic 30 20 10 Lazarus Genera (%) 400 c 300 200

100 Genera 0

10 Lazarus Genera (%)

90 d 80 70 60 50

40 Genera 30 20 100 75 50 25 Lazarus Genera (%)

Roadian Wordian Capitanian Wuchiaping Changhsing Induan Olenekian Anisian

Fig. 2 Total (within-bin and Lazarus) diversity and percentage of Lazarus taxa for gastropods (a), bivalves, with aragonitic and calcitic forms plotted separately (b), rhynchonelliform brachiopods (c), and sponges (d) in Middle and Late Permian and Early Triassic stages. Error bars indicate 95% confidence interval for Lazarus percentage 16 Mass Extinctions and Changing Taphonomic Processes

Stage has anomalously low numbers of Lazarus taxa compared to more typical 244 Permian values. For example, there are no rhynchonelliform brachiopod Lazarus 245 genera in the Changhsingian stage due to the extreme severity of the end-Permian 246 extinction event. 247 The striking stability in the percentage of rhynchonelliform brachiopod, 248 bivalve, and gastropod genera represented by Lazarus taxa during the Roadian– 249 Wuchiapingian interval, and especially across the end-Guadalupian extinction, 250 implies that the quality of the benthic invertebrate fossil record remained consis- 251 tent across the Guadalupian/Lopingian boundary. Demosponges may be an excep- 252 tion and the significant increase in Lazarus taxa across the end-Guadalupian 253 extinction, from 22.5% in the Capitanian to 50.9% in the Wuchiapingian (Z = 254 −3.49, p < 0.001), could either reflect poor preservation of sponges or small 255 sponge population sizes in the Wuchiapingian. The Wuchiapingian has few demo- 256 sponge occurrences compared to the well-sampled surrounding intervals; only 103 257 generic occurrences of sponges compared to 1,513 in the Capitanian and 223 in the 258 Changhsingian. In addition, the Wuchiapingian is a time of turnover or crisis in the 259 reef ecosystem, and the number of preserved reefs is low compared to the Wordian, 260 Capitanian, or Changhsingian (Weidlich 2002). Thus, the high number of sponge 261 Lazarus taxa is primarily a result of actual decreases in population size rather than 262 taphonomic biases due to poor preservation. The overall lack of substantial varia- 263 tion in the abundance of Lazarus taxa across the end-Guadalupian extinction is 264 consistent with the conclusions of Stanley and Yang (1994) that taphonomic biases 265 did not substantially influence the observed pattern of extinction during the end- 266 Guadalupian crisis. 267

4.2 Patterns in Permian Silicification 268

Although variations in Lazarus taxa abundance are not consistent with major 269 taphonomic biases during the Guadalupian–Lopingian interval, shifts in the amount 270 of silicification may have independently affected diversity patterns. Early diagenetic 271 silicification can preserve a higher fidelity record of a fossil assemblage because 272 of enhanced aragonite preservation (Cherns and Wright 2000; Wright et al. 2003, 273 Butts and Briggs, this volume) and temporal variations in the amount of silica- 274 replaced fossils have been argued to influence diversity patterns and extinction 275 estimates (Schubert et al. 1997). To evaluate the potential effects of silicification 276 on the end-Guadalupian extinction, we calculated the percentage of collections 277 with silica-replaced fossils in each Permian stage, quantified the difference in 278 alpha diversity between silicified and non-silicified assemblages, and counted the 279 number of genera that are uniquely found in silicified collections. 280 Diagenetic silica replacement is thought to be a common phenomenon during 281 much of the Permian, as exemplified by famous silicified localities from Thailand, 282 the Salt Range in Pakistan, and especially from the Glass and Guadalupe Mountains 283 M.L. Fraiser et al.

284 in the United States, among others (e.g. Cooper and Grant 1972; Grant 1968, 1976). 285 However, the number of silicified fossil collections in each stage is actually quite 286 variable (Fig. 3); for example, 7.5% of the 1,280 Wordian collections contain silica- 287 replaced fossils whereas 18.1% of the 1,444 collections in the Capitanian have been 288 silicified. In contrast to the Guadalupian, silicification is much less widespread in 289 the Lopingian. Only 3.3% of the 1,241 Wuchiapingian collections and 1.5% of the 290 983 Changhsingian collections have been silicified, suggesting that the substantial 291 decline in the proportion of silicified fossils across the end-Guadalupian boundary 292 may contribute to apparent elevated extinction rates. 293 Collections with silica-replaced fossils also have consistently higher sampled 294 alpha diversity than non-silicified collections (Fig. 4). Note that overall mean alpha

10 N = 1419 N = 1444 N = 455 5 2 N = 880 N = 1241 6 1

N = 983 N = 1211 = N = 1280

N = 950 N = 354 N Silicified Collections (% of total) Assel Sak Art Kung Road Word Cap Wuch Chang Induan Olenek

Fig. 3 Percentage of fossil collections containing silicified fossils in each Permian and Early Triassic stage. Assel: Asselian; Sak: Sakmarian; Art: Artinskian; Kung: Kungurian; Road: Roadian; Word: Wordian; Cap: Capitanian; Wuch: Wuchiapingian; Chang: Changhsingian; Ind: Induan; Ole: Olenekian. The n values indicate the total number of collections from each stage

35 Silicified Collections Non-Silicified Collections 30

Mean Species Richness 10

Roadian Wordian Capitanian Wuchiapingian Changhsingian Induan Olenekian

Fig. 4 Mean species richness for collections containing silicified fossils (solid line and square symbols) and non-silicified fossils (dashed line and open circle symbols) in Middle Permian, Late Permian, and Early Triassic stages. Error bars are 95% confidence intervals 16 Mass Extinctions and Changing Taphonomic Processes diversity values are a function of the nature of reporting in the published literature 295 and are not representative of actual alpha diversity; many papers are taxonomic 296 descriptions and only consider a single taxonomic group and record one or a few 297 new species of interest from a given locality. In particular, the large discrepancy 298 between silicified and non-silicified alpha diversity in the Middle Permian is pri- 299 marily a result of the large taxonomic lists reported from the extraordinarily large 300 silicified collections from west Texas. Nevertheless, apparent changes in sampled 301 alpha diversity, whether real biological phenomena or due to changes in the number 302 of taxa actually reported for a collection in published papers, still affect our percep- 303 tion of diversity and extinction in the fossil record. During the Roadian and 304 Wordian, mean silicified alpha diversity is 24.4 species and 14.6 species per collec- 305 tion, compared to only 3.0 and 3.65 species in non-silicified collections from the 306 same stages. The difference between silicified and non-silicified alpha diversity is 307 statistically significant during the Guadalupian, but not in the Lopingian stages (4.5 308 vs 3.95 species in the Wuchiapingian, p = 0.51; 5.95 vs 4.4 species in the 309 Changhsingian, p = 0.18). Although the difference in alpha diversity is not always 310 statistically significant, the consistently higher values in silicified collections may 311 have acted in conjunction with the significant decrease in the amount of silicifica- 312 tion to exacerbate apparent diversity loss and increase calculated extinction rates. 313 However, the major decrease in alpha diversity in silicified collections occurs from 314 the Roadian to Capitanian stages (Fig. 4), earlier than the traditionally recognized 315 end-Guadalupian extinction. There is a minor but significant decrease in silicified 316 alpha diversity across the Guadalupian/Lopingian boundary (7.4–4.5 species; p = 317 0.05) but non-silicified alpha diversity actually increases significantly (3.45–3.95 318 species, p = 0.02). 319 Although there were substantial changes in the extent of silicification during 320 the Permian, and silicification may preserve a better record of alpha diversity and 321 relative abundance (Cherns and Wright 2000; Wright et al. 2003), it is not clear to 322 what extent it affects global diversity patterns. If many genera are known exclu- 323 sively from silicified collections, silica-replacement may exert an important con- 324 trol on global diversity patterns. In contrast, if most genera from silicified 325 assemblages are also found in non-silicified assemblages, the implication is that 326 silicification itself is not important for reconstructing diversity. During the 327 Permian, the percentage of genera uniquely known from silicified assemblages in 328 a given stage is influenced by the percentage of collections that are silicified, and 329 can be as high as 23% of bivalves, 33% of brachiopods, and 60% of gastropods, 330 all during the Roadian Stage. However, overall only a small number of genera are 331 known only from silicified specimens, as many found in silicified collections from 332 one stage are then recorded from non-silicified assemblages at another time. Only 333 3.2% of Permian bivalves (6 of 190 genera) are exclusive to silicified collections, 334 while 17.4% of gastropods (31 of 178 genera, although several of those may be 335 known from non-silicified collections in the Carboniferous) and 12.9% of brachio- 336 pods (94 of 727 genera) are uniquely found in silicified assemblages. Total genus 337 richness is only 5–25% higher when silicified collections are included, compared 338 to the value obtained solely from non-silicified fossils. However, calculated 339 M.L. Fraiser et al.

340 extinction and origination rates vary by no more than 5% if silicified collections 341 are excluded. These results indicate that silicification itself is not necessary for 342 preserving a good record of diversity during the Guadalupian–Lopingian interval 343 and that the severity of the end-Guadalupian extinction is not biased by changes 344 in silicification.

345 4.3 Early Triassic Lazarus Effect

346 Only 18.8% of gastropod genera during the Changhsingian and 26.9% during the 347 Anisian stage are Lazarus taxa, while 34.9% of Induan and 37.2% of Olenekian 348 gastropod diversity are Lazarus taxa (Fig. 2a). The differences between the propor- 349 tion of Lazarus gastropod genera from the Changhsingian to Induan is statistically 350 significant (Z = −2.00; p = 0.045) but the other differences are not significant at 351 p = 0.05. The proportions of gastropod Lazarus taxa are also lower than those previ- 352 ously published (Erwin and Pan 1996). Though the proportions of gastropod 353 Lazarus taxa during the Induan and Olenekian are similar to those of the Middle 354 Permian (Fig. 2), the predicted proportion of Lazarus taxa in the Induan would be 355 lower because of extinction edge effects, as in the Changhsingian when less than 356 20% of taxa were Lazarus genera. The proportion of bivalve Lazarus taxa was 22% 357 in the Induan and 11.3% in the Olenekian. The differences in the proportion of 358 bivalve taxa are not statistically significant between the Induan and Olenekian or 359 from the Olenekian to Anisian, but the change from the Changhsingian to Induan, 360 is (Z = −2.88, p = 0.004: Fig. 2b). Aragonitic bivalves had a higher proportion of 361 Lazarus taxa compared to calcitic taxa during the Induan (40% versus 13.3%), but 362 the difference is not significant due to the small sample size, especially of arago- 363 nitic taxa (Z = 1.82, p = 0.07). There was also little difference between aragonitic 364 and calcitic mineralogy during the Olenekian. The proportions of Lazarus arago- 365 nitic genera were significantly different between the Changhsingian and Induan and 366 the Induan and Olenekian (Z = −3.65, p < 0.001; Z = 2.01, p = 0.04). The proportions 367 of calcitic Lazarus taxa did not differ significantly between the Changhsingian 368 through Anisian stages. There are no rhynchonelliform brachiopod Lazarus genera 369 during the Early Triassic stages. One hundred percent and 95.8% of demosponge 370 genera were Lazarus genera during the Induan and the Olenekian, respectively, 371 while many sponges remained known only as Lazarus taxa in the Anisian.

372 4.3.1 Controls on Early Triassic Lazarus Taxa

373 Potential controls on the occurrence of Lazarus taxa during the Early Triassic 374 include taphonomic processes, sampling, environmental conditions, paleobiology 375 of the organisms, and taxonomic practices, or a combination thereof. 376 The Early Triassic Lazarus phenomenon among bivalves and gastropods may 377 have resulted from taphonomic bias related to their aragonitic composition. 16 Mass Extinctions and Changing Taphonomic Processes

Aragonitic shells typically dissolve during meteoric or burial diagenetic processes 378 during early diagenesis because aragonite is less stable than calcite at surface 379 temperatures and pressures, even during “aragonite seas” (e.g. Tucker and Wright 380 1990). These diagenetic processes may have been compounded by increased acid- 381 ity and CaCO3 undersaturation of seawater caused by elevated atmospheric CO2 382 levels during the Early Triassic (Berner 2004). Thus, the large proportion of ara- 383 gonitic Lazarus taxa could reflect post-mortem taphonomic processes in a high 384

CO2 world. Similar processes have been proposed to explain Triassic–Jurassic 385 boundary patterns (e.g. Hautmann 2004; Hautmann et al. 2008a), and are observed 386 in the modern ocean and predicted for the future (e.g. Feely et al. 2004). 387 Alternatively, low levels and depth of bioturbation during the Early Triassic (e.g. 388 Twitchett 1999; Pruss and Bottjer 2004; Fraiser and Bottjer in press) may have 389 buffered some shell dissolution during the Early Triassic. Shell dissolution is high 390 in areas with well-developed infaunal benthic communities because biogenic 391 reworking of sediments increases oxygen levels in the mixed layer and promotes 392 oxidative decay of organic matter, thereby increasing acidity near the sediment– 393 water interface and causing pore waters to become undersaturated with respect to 394 both aragonite and calcite (Aller 1982; Walter and Burton 1990). Sediment 395 reworking by infaunal organisms also disrupts mold space left after shells dissolve 396 (Cherns and Wright 2000). Even if after death benthic calcareous shells were dis- 397 solved on the seafloor in some regions due to a lowered carbonate saturation state 398 of seawater (Berner 2004; Feely et al. 2004), the reduction in bioturbating activity 399 that characterized much of the Early Triassic may have prevented molds from 400 being disturbed. 401 Sample size, either as a result of actual sampling effort or of true population size, 402 is another potential contributor to the Early Triassic Lazarus phenomenon. A good 403 correlation between a group’s abundance, the number of occurrences, and the num- 404 ber of Lazarus taxa can be observed in Middle Permian rhynchonelliform brachio- 405 pods, bivalves, and gastropods, confirming the importance of sampling on Lazarus 406 abundance. Reduced Early Triassic sampling between two well-sampled stages 407 tends to increase the number of Lazarus taxa. Very low levels of sampling in the 408 Early Triassic (378 Induan occurrences and 673 Olenekian occurrences of rhyncho- 409 nelliform brachiopods, gastropods, and bivalves) relative to the Changhsingian 410 (4,755 occurrences) and Anisian (2,439 occurrences) may be influenced by sam- 411 pling effort but more likely reflect reduced marine invertebrate abundance due to 412 environmental stress following the end-Permian mass extinction (e.g. Fraiser and 413 Bottjer 2007). A specimen of a Griesbachian Lazarus gastropod taxon was found 414 recently in a newly discovered Tethyan section (Wheeley and Twitchett 2005), 415 further highlighting that low numbers of some gastropod taxa contributed to the 416 Lazarus phenomenon (sensu Wignall and Benton 1999) and suggesting that more 417 sampling of Lower Triassic strata, especially in largely ignored regions, could aid 418 in finding missing gastropod taxa that migrated to refugia or that were low in abun- 419 dance. Future work on physiological and ecological characteristics of Lazarus 420 gastropod genera could determine the extent to which Early Triassic environmental 421 conditions contributed to the low numbers of certain gastropod taxa. The prevalence 422 M.L. Fraiser et al.

423 of sponge Lazarus taxa is also likely tied to sampling; namely, the lack of reef sites 424 during the Early Triassic (a metazoan “reef gap”, Flügel and Stanley 1984). 425 Permian–Triassic sponge occurrences are strongly covariant with times of wide- 426 spread reef-building in the Wordian–Capitanian, Changhsingian, and Late Triassic. 427 Stages with low reef abundance between those reef episodes have many demo- 428 sponge Lazarus taxa – e.g. the Wuchiapingian (50.9%), Anisian (the beginning of 429 the Triassic reef recovery, but still with 53.3% Lazarus taxa), and to an extreme 430 degree the Induan and Olenekian. As the Early Triassic reef gap may have been due

431 to elevated atmospheric CO2 and ocean acidification that prevented metazoan reef 432 organisms from forming skeletons (Stanley et al. 2007), extinction-related environ- 433 mental factors may have contributed to the reduced sampling through reduced 434 population size. 435 Biological factors may have facilitated the Lazarus effect among some Early 436 Triassic taxa. Most of the aragonitic Induan Lazarus genera had infaunal or 437 semi-faunal lifestyles. During the end-Triassic mass extinction, aragonitic infau- 438 nal bivalves suffered greater extinctions than epifaunal bivalves (Hautmann 439 et al. 2008b), and it has been proposed that this pattern indicates a reduction in 440 primary productivity as epifaunal bivalves have physiological characteristics 441 that enabled them to fare better during conditions of reduced food availability 442 (McRoberts and Newton 1995). A decrease in primary productivity has also 443 been proposed for the Early Triassic (Twitchett 2001). It is unclear whether the 444 Lazarus pattern among Early Triassic bivalves resulted more from diagenetic 445 processes or from biological reasons, but both mechanisms were linked to Early

446 Triassic environmental conditions (elevated CO2). Furthermore, the reason that 447 the Lazarus effect among aragonitic bivalve taxa is more pronounced in Induan 448 versus Olenekian age strata is unknown. However, this temporal pattern supports 449 the argument for environmental conditions contributing to the Lazarus effect 450 because it could reflect an amelioration of some aspect of the global environ- 451 ment later in the aftermath. 452 Poor taxonomic practice is a plausible hypothesis to part explain the Early 453 Triassic Lazarus phenomenon among some groups. For example, partial preserva- 454 tion has made it difficult to definitively identify some Early Triassic gastropod taxa 455 (Wheeley and Twitchett 2005). The small size of Early Triassic gastropods could 456 make it difficult to determine gastropod taxonomy; many Early Triassic gastropods 457 are microgastropods <1cm in height (Fraiser and Bottjer 2004; Fraiser et al. 2005), 458 and needles have been required to prepare them to expose areas for proper identifi- 459 cation (Batten and Stokes 1986). Some Middle Triassic gastropods have been incor- 460 rectly identified as Elvis taxa (Wheeley and Twitchett 2005), taxa that were 461 misidentified as having re-emerged after their presumed extinction, but are not 462 actually descendants of the original taxa (Erwin and Droser 1993). More accurate 463 gastropod taxonomy across the P/T boundary and into the Middle Triassic could 464 determine the extent to which the Lazarus effect among gastropods is real and 465 significant. 16 Mass Extinctions and Changing Taphonomic Processes

4.4 Patterns in Early Triassic Silicification 466

Contrary to previous reports that shell replacement by silica is absent among Lower 467 Triassic faunas (e.g. Erwin and Pan 1996; Kidder and Erwin 2001; Twitchett 2001), 468 5% of Early Triassic collections contain fossils preserved via silicification (Fig. 3). 469 Silicified Early Triassic faunas have been reported from Oman, China, and the 470 U.S.A. Although this value likely represents a maximum estimate due to the easily- 471 accessible literature on silicified faunas, the value is broadly similar to the proportion 472 of silicification in Permian stages, in the Lopingian in particular. Of the Early 473 Triassic benthic collections with preservation via silica replacement, 30% are from 474 Induan and 70% are from Olenekian age strata (Fig. 3). Olenekian U.S.A. collections 475 comprise 70% of the silicified collections. 476 The mean alpha diversity of PBDB Early Triassic collections preserved via 477 silicification is 7.86 for Induan collections, 2.63 for Olenekian collections, and 4.19 478 for the series. An independent groups t-test of means indicates that the difference 479 between the mean alpha diversities of silicified Induan and Olenekian collections is 480 significant (t = 5.20, p < 0.0001). Non-silicified Induan collections have a mean 481 alpha diversity of 3.18, and Olenekian ones have a mean alpha diversity of 4.14 482 (Fig. 4). The mean alpha diversity for all Early Triassic collections preserved 483 as casts and molds is 3.67. The difference between the means for non-silicified 484 Induan and Olenekian collections is statistically significant (t = 2.50, p = 0.013). 485 The difference between means of silicified and non-silicified Induan collections is 486 statistically significant (t = 4.87, p < 0.0001), but there is no significant difference 487 between the means for silicified and non-silicified Olenekian collections (t = 1.49, 488 p = 0.14), or between the means for silicified and non-silicified Early Triassic 489 collections (t = 0.696, p = 0.49). 490 Fourteen gastropod genera (Ananias, Anomphalus, Bellerophon, Chartronella, 491 Coelostylina, Donaldina, Jiangxispira, Laxella, Naticopsis, Omphaloptycha, 492 Platyzona, Streptacis, Strobeus, and Worthenia) are found in Induan silicified col- 493 lections, but all but two of those (Jiangxispira, Laxella) also occur in non-silicified 494 collections at another time. No Olenekian gastropods are known exclusively from 495 silicified faunas. No Induan bivalve genera are known exclusively from silicified 496 faunas. At least eight bivalve genera (Elegantinia, Entolioides, Eumorphotis, 497 Leptochondria, Neoschizodus, Pegmavalvula, “Pleuronectites”, Placunopsis) are 498 known from Olenekian silicified collections, but Pegmavalvula is the only one of 499 46 Olenekian bivalves exclusively found in silicified localities throughout its entire 500 range. No rhynchonelliform brachiopods are known only from shells preserved via 501 silicification. Therefore, most Early Triassic genera are known from fossil casts 502 and molds. 503 Documentation of silicified fossil collections from Lower Triassic strata refutes 504 the hypothesis that there is a “complete absence of silicified faunas” during the 505 Early Triassic (Twitchett 2001). Silicified Induan and Olenekian collections are 506 rare in comparison to some Permian stages, but actually occur as frequently as 507 M.L. Fraiser et al.

508 silicified collections in the Wuchiapingian or Changhsingian stages of the Late 509 Permian. There is no change in silicification across the Permian–Triassic boundary, 510 indicating that changes in preservation style are not the primary contributor to the 511 unusual Early Triassic record. 512 The statistically significant differences between silicified Induan and Olenekian 513 collections and between non-silicified Induan and Olenekian collections supports 514 previous findings that diversity increased through the Early Triassic (e.g. Schubert 515 and Bottjer 1995) and could be an indication of biotic recovery following the end- 516 Permian mass extinction. That there is no statistically significant difference 517 between silicified and non-silicified Olenekian collections does not support the 518 hypothesis that silicified faunas record more information than non-silicified ones. 519 Furthermore, Lazarus taxa have been found in non-silicified collections 520 (Hautmann and Nützel 2004). The statistically significant difference between silici- [AU3] 521 fied and non-silicified Induan collections could reflect a real difference in the 522 amount of data preserved in silicified and non-silicified collections. However, 22% 523 of silicified faunas are from one recently discovered Griesbachian-age section in 524 Oman, and these collections have a mean alpha diversity of 8.5 that skews the mean 525 alpha diversity for Induan silicified faunas. When these collections are removed 526 from the analysis, there is no statistically significant difference between the mean 527 alpha diversities of silicified and non-silicified Induan collections. More sampling 528 of Lower Triassic sections around the world would probably lead to the discovery 529 of more silicified faunas. 530 Only a very small percentage of gastropod, bivalve, or brachiopod genera are known 531 exclusively from silicified collections, whether in the Permian or in the Early Triassic. 532 The impact of silicification, or the lack thereof, on global diversity compilations is 533 therefore minimal. 534 Differences between silicified and non-silicified collections were likely influ- 535 enced more by worker-introduced bias and not taphonomic processes. One source 536 of bias could potentially be the focus of many Early Triassic studies. Publications 537 of taxonomic lists from Lower Triassic strata commonly report only one higher 538 taxonomic group, e.g., rhynchonelliform brachiopods (Perry and Chatterton 1979), 539 ostracodes (Crasquin-Soleau and Kershaw 2005), or pectinoid bivalves (e.g. Newell 540 and Boyd 1995), even when other taxa have been collected in the field (D.W. Boyd, 541 pers. comm.). Furthermore, authors commonly report only higher taxa rather than 542 detailed lists of genera or species. Incompletely reported taxonomic lists mean that 543 the alpha diversities of both silicified and non-silicified Induan and Olenekian col- 544 lections are likely underestimates. Bias also could be introduced by the methods in 545 which data are collected (D.W. Boyd pers. comm.). If only silicified faunas are 546 searched for and collected from the field for analysis, any data from fossils that are 547 not silicified are omitted. It is important to note that the only known Smithian (early 548 Olenekian) collections are from non-silicified collections. Though silicified shells 549 are easily extracted from their encompassing matrix with weak acids (such as 550 hydrochloric or acetic acid), acids also cause the dissolution of any non-silicified 551 material in the sample. Incomplete and incorrectly entered data in the PBDB, i.e., 552 preservation entered as silicification when fossils were not actually silicified, incorrect 16 Mass Extinctions and Changing Taphonomic Processes

and outdated taxonomy, and omitted publications, prevent many collections 553 and taxa (e.g., sponges) from being downloaded when certain searches are per- 554 formed. Outdated taxonomy, incomplete taxonomic lists, and under-sampling 555 likely exert a stronger influence on understanding of Early Triassic ecology than 556 taphonomic processes. 557

5 Conclusions 558

A full accounting of the effects of taphonomic biases during mass extinction inter- 559 vals is critical in any attempt to extract meaningful biological signals from the fossil 560 record during a biotic crisis and its aftermath. Changes in the fidelity or dominant 561 style of fossil preservation can have a substantial impact on the composition and 562 diversity of marine fossil assemblages, and it has been proposed, based on an abun- 563 dance of Lazarus taxa and a reduction in silicification, that such taphonomic 564 changes irreparably bias the fossil record of the Permian–Triassic mass extinction. 565 A new tabulation of the proportion of Lazarus genera in the major Permian–Triassic 566 taxonomic groups suggests that there was no major bias or change in taphonomic 567 style in the Late Permian but that aragonitic taxa (gastropods and some, primarily 568 infaunal, bivalves) may have suffered from reduced preservation in the Induan. 569 Comparisons between silicified and non-silicified faunas indicate there was little 570 change in the amount of silicification across the Permian–Triassic boundary; 571 regardless, silicification is unlikely to be a major taphonomic bias in global compi- 572 lations because few taxa are known exclusively from silicified collections. 573 Documentation of Lazarus taxa does not necessarily indicate that the fossil record 574 is biased. Indeed, taxon outages are a common phenomenon in the fossil record and 575 are caused by a variety of mechanisms. Rickards and Wright (2002) suggest that the 576 concept of a Lazarus taxon is not useful as a taphonomic indicator because it repre- 577 sents nothing more than a taxon’s low abundance during a given interval. The 578 Permian–Triassic pattern of Lazarus taxa documented here is partially consistent 579 with this concept; the Early Triassic Lazarus effect is a function of sampling effects, 580 biological and environmental factors, and actual taphonomic degradation. 581 Though more sampling and refined taxonomy will improve the reconstruction of 582 the end-Permian extinction and its unusual aftermath, our current understanding of 583 the Early Triassic fossil record likely reflects a primary ecological signal (to the 584 extent that any Paleozoic or Mesozoic fossil assemblage reflects a primary biological 585 [AU4] signal) (Fig. 5). Taphonomy remains an important factor that must be assessed in 586 each fossil assemblage, but analysis of the Permian–Triassic record of Lazarus taxa 587 and silicification demonstrates that the fossil record of the end-Permian extinction 588 and the Early Triassic aftermath is not completely obscured by a taphonomic mega- 589 bias due to skeletal mineralogy or fossil preservation. Instead of being solely an 590 indication of the poor quality of the fossil record (e.g., Twitchett 2001; Smith 591 2007), Lazarus taxa could also provide clues about the environmental conditions 592 during deposition. 593 M.L. Fraiser et al.

Fig. 5 Preservation of Early Triassic fossils. (a) Silicified microgastropods, Virgin Limestone Member, Moenkopi Formation. (b) Internal molds of microgastropods, Campil Member, Werfen Formation. (c) Silicified Promyalina, upper member, Thaynes Formation. Scale in mm. From D. Boyd collection. (d) Internal molds of bivalves (Unionites), Siusi Member, Werfen Formation (Modified from Fraiser and Bottjer (2005a)

594 References

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