Journal of Asian Earth Sciences 36 (2009) 413–419

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Journal of Asian Earth Sciences

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Behavior of lophophorates during the end-Permian mass extinction and recovery

Catherine M. Powers *, David J. BottjerDepartment of Earth Sciences, University of Southern California, ZHS 117, 3651 Trousdale Pkwy, Los Angeles, CA 90089-0740, USA

a r t i c l e i n f o

Keywords:Early TriassicBrachiopodsBryozoansDiversityEnd-Permian

1367-9120/$ - see front matter � 2008 Elsevier Ltd. Adoi:10.1016/j.jseaes.2008.05.002

* Corresponding author. Tel.: +1 626 807 6656; faxE-mail address: jamet@usc.edu (C.M. Powers).

a b s t r a c t

The end-Permian mass extinction devastated most marine communities and the recovery was a pro-tracted event lasting several million years into the Early Triassic. Environmental and biological processesundoubtedly controlled patterns of recovery for marine invertebrates in the aftermath of the extinction,but are often difficult to single-out. The global diversity and distribution of marine lophophorates duringthe aftermath of the end-Permian mass extinction indicates that stenolaemate bryozoans, rhynchonelli-form brachiopods, and lingulid brachiopods displayed distinct recovery patterns.Bryozoans were the most susceptible of the lophophorates, experiencing relatively high rates of extinc-tion at the end of the Permian, and becoming restricted to the Boreal region during the Early Triassic. Therecovery of bryozoans was also delayed until the Late Triassic and characterized by very low diversity andabundance. Following the final disappearance of Permian rhynchonelliform brachiopod survivors, EarlyTriassic rhynchonelliform brachiopod abundance remained suppressed despite a successful re-diversifi-cation and a global distribution, suggesting a decoupling between global taxonomic and ecological pro-cesses likely driven by lingering environmental stress.In contrast with bryozoans and rhynchonelliforms, lingulid brachiopods rebounded rapidly, colonizingshallow marine settings left vacant by the extinction. Lingulid dominance, characterized by low diversitybut high numerical abundance, was short-lived and they were once again displaced back into marginalsettings as environmental stress changed through the marine recovery. The presence in lingulid brachio-pods of the respiratory pigment hemerythrin, known to increase the efficacy of oxygen storage and trans-port, when coupled with other morphological and physiological adaptations, may have given lingulids asurvival advantage in environmentally stressed Early Triassic settings.

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1. Introduction

The documentation of global faunal patterns during extinctionintervals and their subsequent survival and recovery phases pro-vides invaluable insight on the processes driving ecological catastro-phes. Although some studies have tried to correlate extinctionpatterns with attributes such as geographic range (Jablonski, 1986)or larval types (Valentine and Jablonski, 1986), most have often fo-cused on the response of individual groups without incorporatinginformation about their ecological and environmental context (i.e.,Kier, 1973; Taylor and Larwood, 1988; Pan and Erwin, 2002; McGo-wan, 2004). Assessing the ecological behavior of related groups ofmarine invertebrates in the immediate aftermath of mass extinc-tions offers new opportunities to identify attributes, whether eco-logical or biological, that may have helped certain taxa to surviveand thrive during times of increased environmental stress.

By means of recently published data, we reviewed and com-pared the environmental distribution and ecological attributes ofmarine brachiopods and stenolaemate bryozoans during their

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recovery from the end-Permian mass extinction. Both groups aresessile members of the Paleozoic Fauna (Sepkoski, 1981) and sharea lophophorate filter-feeding life habit, passive respiratory system,and low basal metabolic rate (Knoll et al., 1996). Along with sus-pension feeding crinoids and corals, lophophorates were preferen-tially affected by the end-Permian extinction event (Knoll et al.,1996, 2007). Regardless, several brachiopod and bryozoan taxasurvived into the Early Triassic and ultimately re-diversified. Giventheir similar physiology and ecological requirements, Early Triassicbrachiopods and bryozoans might be expected to have analogousrecovery patterns. A decoupling of these patterns could indicatethat factors controlling the survival and recovery of marine inver-tebrates in the wake of the largest Phanerozoic extinction weremore complex than originally inferred.

2. The end-Permian mass extinction and the Early Triassicrecovery

The end-Permian mass extinction (252 Ma, Mundil et al.,2004), one of the most devastating biotic crises of the Phanero-zoic, is marked by the disappearance of about 80% of marine

414 C.M. Powers, D.J. Bottjer / Journal of Asian Earth Sciences 36 (2009) 413–419

species and 49% and 63% of marine and terrestrial families,respectively (Raup and Sepkoski, 1982; Stanley and Yang,1994; Benton, 1995). Hypothetical causal mechanisms for theend-Permian extinction include a range of gradual and cata-strophic processes: widespread oceanic and atmospheric anoxia(Wignall and Twitchett, 1996; Isozaki, 1997; Huey and Ward,2005), hypercapnia (Knoll et al., 1996), euxinia (H2S poisoning)(Nielsen and Shen, 2004; Grice et al., 2005; Kump et al., 2005),massive volcanism and global warming (Renne et al., 1995;Kamo et al., 2003), methane oxidation (Krull and Retallack,2000; Ryskin, 2003), and a meteorite impact (Becker et al.,2001). The fundamental kill mechanism remains unclear and islikely a combination of several of the aforementioned processes(Erwin, 2006). Whereas evidence for a catastrophic extraterres-trial scenario is not compelling (Isozaki, 2001; Farley et al.,2005), geochemical, sedimentological, and paleontological datasuggest that the end-Permian crisis was the result of a prolongedinterval of environmental degradation caused by widespreadeuxinia triggered by massive volcanism and global warming(i.e., Renne et al., 1995; Grice et al., 2005; Ward, 2006; Claphamand Bottjer, 2007a; Powers and Bottjer, 2007).

The subsequent marine recovery in the Early Triassic was de-layed by several million years. Metazoan reefs of any kind were ab-sent for most of the Early Triassic and many groups of organismsdid not fully recover until the Middle Triassic (Stanley, 1988; seeHallam and Wignall, 1997 and references therein). Early Triassicmarine invertebrate faunas were depauperate and dominated bya few abundant and cosmopolitan species of ammonoids, bivalves,gastropods, and lingulid brachiopods (Schubert and Bottjer, 1995;Rodland and Bottjer, 2001; Fraiser and Bottjer, 2004, 2005). Sus-tained environmental instability throughout the Early Triassic,documented by unusual sedimentary features (i.e., large sea-floorcarbonate precipitates, flat-pebble conglomerates, wrinkle struc-tures, and microbial buildups in normal marine settings) and re-peated large-scale disturbances in the carbon isotopic record,likely contributed to the low marine diversity and delay in recov-ery (i.e., Schubert and Bottjer, 1995; Baud et al., 1996; Woods etal., 1999; Lehrmann et al., 2001; Payne et al., 2004; Pruss et al.,2004, 2006).

3. Lophophorates

The lophophorates are a sessile, filter-feeding group of aquaticinvertebrate organisms that includes Bryozoa and Brachiopoda, de-fined by the use of an extensible cilia-bearing organ, the lopho-phore, for feeding and respiration. Members of both

PermianE M

Rhy

ncho

nellif

orm

bra

chio

pods

Orthotetidina

Sten

olae

mat

es FenestrataCryptostomata

CystoporataTrepostomataCyclostomata

ProductidaOrthida

RhynchonelleaSpiriferidaArthyridita

Terebratulida

Fig. 1. Schematic illustrating the range of stenolaemate bryozoans and rhynchonelliformPachut (2008) and Williams et al. (1996).

lophophorate phyla are abundant in marine settings today andshare a long and rich fossil record from level-bottom communities;brachiopods first appeared in the Cambrian and bryozoans ap-peared in the Ordovician (Williams et al., 1996; Taylor and Ernst,2004).

Phylum Bryozoa consists of two marine classes, Stenolaemataand Gymnolaemata, and the freshwater class Phylactolaemata.Stenolaemate and gymnolaemate bryozoans were important con-tributors to Phanerozoic marine diversity, but the diversity of gym-nolaemates prior to the Jurassic was negligible. Paleozoic andTriassic bryozoan faunas were dominated by five orders, only oneof which went extinct at the end of the Permian (Fig. 1) (Taylorand Larwood, 1988). Brachiopods are more taxonomically diverseand are grouped into the three subphyla Rhynchonelliformea, Lin-guliformea, and Craniiformea. Rhynchonelliforms, the largestgroup with 19 orders, dominated most post-Ordovician Paleozoicbrachiopod faunas and lost three orders during the end-Permianextinction interval (Fig. 1) (Williams et al., 2000).

Bryozoans and brachiopods differ in their morphology. Bryozo-ans are colonial organisms composed of genetically identical func-tional units called ‘zooids’ that secrete a calcium carbonateskeleton in most species. They have a variety of growth forms con-trolled by the arrangement of the zooids and their environmentalsetting (Hageman et al., 1998). Conversely, brachiopods are solitaryshelled organisms. Unlike bivalves, their valves are bilaterally sym-metric and most live attached to hard substrates on the seafloorusing a fleshy appendage called a pedicle. The Lingulidae (OrderLingulida, subphylum Linguliformea) are the only infaunal groupof brachiopods (Emig, 1997).

4. Early Triassic stenolaemate bryozoans

Stenolaemate bryozoan diversity steadily declined throughoutthe Late Permian, culminating in the extinction of 73.5% of steno-laemate genera (Powers and Pachut, 2008), including all membersof the Order Fenestrida (Schäfer and Fois, 1987; Taylor and Lar-wood, 1988). Early Triassic bryozoan faunas were depauperate,geographically restricted, and solely composed of trepostomes;taxa belonging to the other surviving orders did not reappear untilthe Middle and early Late Triassic (Powers and Pachut, 2008). Ind-uan bryozoan faunas were composed of three species belonging toPaleozoic trepostome survivors Pseudobatostomella and Paraliocl-ema. These species are reported from nearshore and multiple off-shore habitats at three locations in Svalbard and one location inSiberia (Lazutkina, 1963; Nakrem and Mork, 1991). Paleogeo-graphic reconstructions of the Early Triassic indicate that these

TriassicE ML L

brachiopods through the Permian/Triassic extinction interval. Data from Powers and

C.M. Powers, D.J. Bottjer / Journal of Asian Earth Sciences 36 (2009) 413–419 415

faunas were restricted to the Boreal region along the northwesterncoast of Pangea (Fig. 2). Diversity increased in the Olenekian withthe appearance of two new Triassic genera Arcticopora in the Borealregion and Dyscritellopsis in eastern Panthalassa (Fritz, 1962; Schä-fer et al., 2003). To date, no Early Triassic bryozoans have been doc-umented from the Tethys Ocean. The recovery of bryozoanscontinued into the Middle Triassic when they increased their geo-graphic range to several localities around the world, includingwithin the Tethys Ocean. However, bryozoan assemblage genericrichness and numerical abundance remained depleted throughoutthe Early and Middle Triassic and only gradually increased duringthe Late Triassic (Powers and Bottjer, 2007). The recovery of bry-ozoans was considered complete with the rapid diversification ofgenera and species in the early Late Triassic, coupled with anexpansion across shallow onshore to deep offshore environments(Powers and Bottjer, 2007; Powers and Pachut, 2008).

5. Early Triassic brachiopods

An estimated 87–90% of brachiopod genera became extinct atthe end of the Permian and the surviving rhynchonelliform gen-era died-out in the early Induan (Carlson, 1991; Shen and Shi,2002; Chen et al., 2005a). Early Triassic brachiopod assemblagesare composed of three elements – Permian rhynchonelliformbrachiopod survivors, new ‘‘Mesozoic-type” brachiopods, andlingulids (Rodland and Bottjer, 2001; Boyer et al., 2004; Chenet al., 2005a,b).

5.1. Permian survivors

Some of the earliest faunas documented from strata immedi-ately above the extinction horizon are composed of rhynchonel-liform brachiopods that survived the extinction. They include102 species belonging to 43 genera dominated by productids,orthids, spiriferids, and orthotetids (Chen et al., 2005a). Thesefaunas are recorded from multiple localities in the Tethyan,Peri-Gondwanan, and Panthalassan regions (see Fig. 1 in Chenet al., 2005a), and were most abundant in open platform and off-shore settings. The survival of these Permian rhynchonelliformbrachiopods has been attributed to their small size, cosmopolitanbehavior, and broad environmental tolerances (Chen et al.,2005a). However most died off rapidly during the second extinc-tion pulse associated with the end-Permian event, less than amillion years following the first pulse at the boundary (Xie etal., 2005).

Panthalassa

Ocean Pangea

BoreaOcea

Fig. 2. Paleobiogeographic distribution of Early Triassic bryozoans. White stars: InduanIsland, western United States, and Svalbard. Modified from Powers and Pachut (2008).

5.2. Rhynchonelliform brachiopods

The taxonomic recovery of rhynchonelliform brachiopods, de-fined by the origination of new higher taxa, was initiated in themid- to late Induan and continued throughout the Olenekian (Chenet al., 2005b). The new fauna, composed of 32 species from 20 gen-era of rhynchonellids, terebratulids, spririferinids and athyridids, isreported from various locations around the Tethyan, Boreal, andGondwanan regions (Fig. 3) (Chen et al., 2005b). Despite their widegeographic distribution, Early Triassic rhynchonelliform brachio-pods exhibited a high degree of endemism and several biogeo-graphic provinces can be distinguished (Chen et al., 2005b). Thetiming of the recovery of rhynchonelliform brachiopods betweenthese regions was not simultaneous and appeared to have hap-pened in two steps. A preliminary recovery took place in themid- to late Induan in South China; however these genera diedoff rapidly and failed to initiate a successful re-diversification.More successful genera evolved in several other regions duringthe late Induan and early Olenekian, spurring the rapid diversifica-tion of more than fifty brachiopod genera during the Middle Trias-sic (Dagys, 1993; Hallam and Wignall, 1997; Chen et al., 2005b).Early Triassic rhynchonelliform brachiopods were nonethelessrarely abundant in marine communities, which were instead dom-inated by abundant bivalves and gastropods (Fraiser and Bottjer,2004; Clapham and Bottjer, 2007a; Fraiser and Bottjer, 2007a).

5.3. Lingulid brachiopods

Lingulids, represented by the genus Lingularia, proliferated dur-ing the Griesbachian (Xu and Grant, 1994). They were numericallyabundant and dominated many onshore (nearshore to middleshelf) communities from several regions (South China, WesternAustralia, East Greenland, western United States, Japan, Pakistan,Europe, Iran, Russia) (Fig. 4) (Schubert and Bottjer, 1995; Boyeret al., 2004; Chen et al., 2005a; Fraiser and Bottjer, 2005; Peng etal., 2007 and references therein). Early Triassic lingulids were com-monly associated with the equally dominant bivalves Claraia andPromyalina and have been considered both a disaster taxon andan ecological opportunist (Rodland and Bottjer, 2001; Zonneveldet al., 2007). Disaster taxa, which normally thrive in stressed mar-ginal environments and are characterized by a long evolutionaryhistory, frequently colonize and dominate normal marine settingsleft vacant in the wake of an environmental crisis before being dis-placed again as the recovery progresses (Hallam and Wignall,1997; Bottjer, 2001). Conversely, ecological opportunists are regu-

Tethys

Ocean

ln

assemblages (Siberia and Svalbard); Black stars: Olenekian assemblages: Ellesmere

Panthalassa

Ocean Pangea

Tethys

Ocean

BorealOcean

Fig. 3. Early Triassic rhynchonelliform brachiopod faunas. New Early Triassic brachiopod genera first evolved in South China in the late Induan (white star) but rapidly wentextinct. More successful genera evolved during the Olenekian at several locations (black stars), initiating the re-diversification of rhynchonelliforms. Modified from Chen et al.(2005b).

Panthalassa

Ocean Pangea

Tethys

Ocean

BorealOcean

Fig. 4. Paleobiogeographic distribution of lingulid brachiopod assemblages during the early Induan. Modified from Peng et al. (2007).

416 C.M. Powers, D.J. Bottjer / Journal of Asian Earth Sciences 36 (2009) 413–419

lar components of normal marine communities which then prolif-erate when other more dominant taxa become extinct during massextinction intervals (Harries et al., 1996; Zonneveld et al., 2007). Inthe case of the end-Permian mass extinction, lingulids rapidlyoccupied and proliferated in the newly vacated eco-space. Theprominence of lingulids in Early Triassic communities was short-lived; their abundance had declined significantly by the end ofthe Griesbachian as the recovery of marine organisms progressedand environmental conditions ameliorated (Schubert and Bottjer,1995; Rodland and Bottjer, 2001; Fraiser and Bottjer, 2005).

6. Recovery patterns, timing, and tempo

Despite their similar physiology and ecological requirements,rhynchonelliform brachiopods and stenolaemate bryozoans dis-played distinctive patterns of survival and recovery from theend-Permian mass extinction (Fig. 5).

The first rhynchonelliform brachiopod and bryozoan faunasdocumented in the immediate aftermath of the end-Permianextinction were composed of survivor genera. But whereas therhynchonelliform brachiopod survivors died shortly after theextinction interval (�0.7 Ma, Chen et al., 2005a), bryozoan survi-vor genera Paralioclema and Pseudobatostomella continued todiversify during the Triassic and did not become extinct untilthe Late Triassic. Trepostomes were in fact the most successful

bryozoans in the Triassic, accounting for 81% of all reported Tri-assic stenolaemate species (Schäfer and Fois, 1987; Powers andPachut, 2008).

New rhynchonelliform brachiopod and bryozoan genera ap-peared during the late Induan and the Olenekian seeding therecovery and successful re-diversification of both groups. However,the timing and tempo of their recovery differed. The taxonomicrecovery phase of articulate brachiopods was initiated in the lateInduan and completed by the Middle Triassic. Conversely, bryozo-ans recovered more gradually during the Early and Middle Triassic,although they remained uncommon in most Triassic communities.Ecologically, rhynchonelliform brachiopod abundance rose duringthe Middle and Late Triassic, but their breadth across marine com-munities was more restricted than during the Paleozoic and con-tinued to decline throughout the remainder of the Phanerozoic(Clapham et al., 2006). Additionally, rhynchonelliforms becamesubordinate members of Mesozoic and Cenozoic communitiesnow dominated by mollusks (see Fig. 2 in Fraiser and Bottjer,2007a).

Although the success of several bryozoan Paleozoic holdoversseems to suggest otherwise, differences in the ecological behaviorof bryozoans and brachiopods and a decoupling in the timing andtempo of their recoveries suggest that bryozoans may not havebeen as well equipped as brachiopods to cope with the environ-mental effects of the end-Permian mass extinction.

Indu

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EarlyTriassic

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End-Permianmass extinction

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yozo

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aleo

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Fig. 5. Early Triassic timescale showing the range and characteristics of rhynch-onelliform brachiopod, lingulid, and stenolaemate bryozoan faunas during therecovery interval of the end-Permian mass extinction. L P, Late Permian; G,Griesbachian; M Tr, Middle Triassic.

C.M. Powers, D.J. Bottjer / Journal of Asian Earth Sciences 36 (2009) 413–419 417

7. Biological and ecological attributes for survival

In a review of extinction intensity and selectivity among marineinvertebrates at the end of the Permian, Knoll et al. (2007) placedrhynchonelliform brachiopods and stenolaemate bryozoans inthe most vulnerable category, based on their tendency to secreterobust calcium carbonate skeletons with minimal physiologicalbuffering. Organisms from this group, that also includes suspen-sion-feeding rugose corals and crinoids, lost 86% of their generaduring the end-Permian extinction, as compared to 5% for thegroup with no or little calcium carbonate in their skeleton, towhich lingulids belong. Knoll et al. (2007) argued that elevatedconcentrations of CO2 in the photic zone during the Late Permianwould have induced hypercapnic stress in marine invertebrates,reducing the ability of their respiratory pigments to carry oxygenand disrupting the biomineralization of their skeletons throughoceanic acidification (Knoll et al., 1996; Caldeira and Wickett,2003; Raven et al., 2005; Fraiser and Bottjer, 2007b; Knoll et al.,2007). Marine invertebrates like stenolaemate bryozoans andrhynchonelliform brachiopods that secrete massive skeletons andshells and are unable to buffer against changes in seawater chem-istry would have therefore been unable to survive and thus expe-rienced high rates of extinction during the end-Permian event.Yet, the difference between their extinction rates (about 20%)and the duration of their recovery (one vs. multiple stages) implies

that other biological (i.e., pre-adaptations, skeletal mineralogy,morphological complexity, bacterial chemosymbiosis, or reproduc-tive strategies) or ecological (i.e., environmental range) factorsinfluenced the survival of these lophophorates during the Perm-ian–Triassic interval (for more in-depth discussion of attributesof selectivity during extinction see Anstey, 1978; Jablonski, 1986;Kitchell et al., 1986; Harries et al., 1996).

Nonetheless the recovery of rhynchonelliform brachiopodsand stenolaemate bryozoans contrasts sharply with the ecologi-cal behavior exhibited by lingulids during the Early Triassic.Lingulids dominated a range of localities and habitats in theimmediate wake of the end-Permian crisis, thriving in areas thatwere subjected to extreme environmental stress during theextinction. Induan assemblages with abundant lingulids havebeen reported from seven localities (western Australia, EastGreenland, Pakistan, Iran, South China, Italy, and eastern Europe)where sedimentological and geochemical data support the pres-ence of photic zone anoxic to euxinic conditions through thePermian–Triassic extinction interval (Wignall and Twitchett,1996; Newton et al., 2004; Grice et al., 2005; Wignall et al.,2005; Kakuwa and Matsumoto, 2006; Summons et al., 2006).A few rhynchonelliform brachiopods are able to survive in lowoxygen conditions, but lingulids display a much greater toler-ance for anoxic settings and may even be able to survive sulfidicconditions (Brunton, 1982; Kammer et al., 1986; Bailey et al.,2006; Knoll et al., 2007). Lingulid brachiopods use the non-heme iron protein hemerythrin to carry and store oxygen (Man-well, 1960c; Hammen et al., 1962). Hemerythrin is analogous tothe respiratory pigment hemoglobin, but is only known to occurin lingulid brachiopods and sipunculid, priapulid, and annelidworms (Manwell, 1960b,c). Unlike other respiratory pigments,hemerythrin in species of lingulids has a low oxygen affinityand increases the Bohr effect, facilitating oxygen transport andenabling lingulids to tolerate low oxygen conditions (Manwell,1960a). This biological attribute likely provided lingulids withthe necessary mechanism to proliferate during the earliest Trias-sic. Peng et al. (2007) ascribed the success of lingulids in theaftermath of the end-Permian event to several pre-adapted mor-phological traits (small body size and a phosphatic shell miner-alogy) that they were able to modify further (elongation andflattening of the shells and reduction in shell thickness) to moreefficiently survive in the decreased oxygen levels of the photiczone. The reduction in shell thickness would have facilitatedoxygen exchange directly through the shell, which in turnwould have been more efficiently distributed by the hemery-thrin (Manwell, 1960a; Peng et al., 2007). The mineralogicalcomposition of lingulid shells provided one further advantageby allowing lingulids to withstand the elevated concentrationof oceanic CO2 (hypercapnia) during the end-Permian event(Knoll et al., 1996, 2007). Lingulid shells are phosphatic and, un-like the calcareous rhynchonelliform brachiopods and stenolae-mate bryozoans, would not have been affected by theundersaturation of calcium carbonate in Late Permian and EarlyTriassic seawaters (Fraiser and Bottjer, 2007b). Hypercapnia ispostulated to be one of the principal sources of environmentalstress in shallow marine communities during the end-Permianextinction and a likely contributor to the patterns of selectivitydocumented in many marine groups during that interval (Knollet al., 1996, 2007). Although infaunal tiering was reduced duringthe Early Triassic (Ausich and Bottjer, 2002; Pruss and Bottjer,2004), the typical burrowing behavior of lingulids throughoutthe Phanerozoic may have put them on an adaptive trajectorythat, coupled with their phosphatic shell mineralogy, led to anenhanced ability to use oxygen and tolerate H2S, which maybe the key to their success in anoxic to sulfidic settings sincethe Cambrian.

418 C.M. Powers, D.J. Bottjer / Journal of Asian Earth Sciences 36 (2009) 413–419

8. Conclusions

The diversity, distribution, and abundance of lophophoratesduring the end-Permian extinction and subsequent aftermath re-veal distinct patterns of survival and recovery. Stenolaemate bry-ozoans were the most susceptible of the lophophorates,experiencing relatively high rates of extinction at the end of thePermian, followed by very low diversity and abundance duringthe Early Triassic. Early Triassic bryozoans were also restricted tothe Boreal region where evidence has shown that environmentalconditions after the mass extinction ameliorated more rapidly(Wignall et al., 1998). Rhynchonelliform brachiopods seemedslightly less sensitive than bryozoans to the deleterious environ-mental conditions of the Permian–Triassic interval, and althoughonly rarely abundant in Early Triassic communities, they wereglobally distributed. Finally, lingulids were the least susceptibleto the end-Permian event, proliferating in vacated Griesbachiansubtidal habitats.

The success of lingulids, known for their ability to thrive instressed marginal environments often characterized by low oxygenconditions, and the lack of rhynchonelliform brachiopods andstenolaemates bryozoans, suggest that shallow subtidal settingsin the earliest Triassic were not suited for the development of nor-mal marine communities and supports geochemical and sedimen-tological evidence of sustained environmental degradation duringthe Early Triassic (i.e., Payne et al., 2004; Pruss et al., 2006). Addi-tional evidence of sustained environmental stress during the earli-est Triassic comes from size data of microgastropods and Permiansurvivor rhynchonelliform brachiopods (Fraiser and Bottjer, 2004;Chen et al., 2005a; Payne, 2005; Twitchett, 2005). Early Triassicmicrogastropods were opportunistic taxa that, like lingulids, prolif-erated in empty subtidal habitats in the aftermath of the end-Permian extinction. And the survival, albeit short-lived, of Permianrhynchonelliform brachiopods during the extinction was attrib-uted to their broad environmental adaptations and small body size,which may have allowed them to live in settings still affected byanoxia and euxinia. No reduction in zooid and colony size has beennoted for Early Triassic bryozoans, which may explain why, unlikerhynchonelliform brachiopods survivors, Permian bryozoan hold-overs were not globally distributed.

The re-diversification of rhynchonelliform brachiopods duringthe Early Triassic was not accompanied with an increase in theirabundance in marine communities, suggesting a decoupling be-tween taxonomic and ecological processes likely driven by linger-ing environmental instability. Divergence between globaltaxonomic diversity and abundance at times of elevated environ-mental stress or in the aftermath of mass extinctions has beennoted in the Late Permian and the Early Cenozoic (Danian Stage)(McKinney et al., 1998; Clapham and Bottjer, 2007b).

The taxonomic and ecological behavior of lophophorates duringthe end-Permian mass extinction interval suggest that the environ-mental effects of this mass extinction were both protracted andmore complex than originally inferred and imply that decouplingbetween taxonomic and ecological processes is prevalent duringextinction intervals.

Acknowledgements

We thank Matthew Clapham for helpful reviews and discus-sions. We also thank two anonymous reviewers for constructivecomments. This research was supported by a USC WiSE grant toD.J.B. and grants from the Geological Society of America, The Pale-ontological Society, the American Museum of Natural History, theYale Peabody Museum, and the USC Department of Earth Sciencesto C.M.P.

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