OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

CHAPTER 5 Lessons from the fossil record: the Ediacaran radiation, the Cambrian radiation, and the end-Permian mass extinction

S tephen Q . D ornbos, M atthew E . C lapham, M argaret L . F raiser, and M arc L afl amme

5.1 Introduction and altering substrate consistency (Thayer 1979 ; Seilacher and Pfl üger 1994 ). In addition, burrowing Ecologists studying modern communities and eco- organisms play a crucial role in modifying decom- systems are well aware of the relationship between position and enhancing nutrient cycling ( Solan et al. biodiversity and aspects of ecosystem functioning 2008 ). such as productivity (e.g. Tilman 1982 ; Rosenzweig Increased species richness often enhances ecosys- and Abramsky 1993 ; Mittelbach et al. 2001 ; Chase tem functioning, but a simple increase in diversity and Leibold 2002 ; Worm et al. 2002 ), but the pre- may not be the actual underlying driving mecha- dominant directionality of that relationship, nism; instead an increase in functional diversity, the whether biodiversity is a consequence of productiv- number of ecological roles present in a community, ity or vice versa, is a matter of debate ( Aarssen 1997 ; may be the proximal cause of enhanced functioning Tilman et al. 1997 ; Worm and Duffy 2003 ; van ( Tilman et al. 1997 ; Naeem 2002 ; Petchey and Gaston, Ruijven and Berendse 2005 ). Increased species rich- 2002 ). The relationship between species richness ness could result in increased productivity through (diversity) and functional diversity has important 1) interspecies facilitation and complementary implications for ecosystem functioning during resource use, 2) sampling effects such as a greater times of diversity loss, such as mass extinctions, chance of including a highly productive species in a because species with overlapping ecological roles diverse assemblage, or 3) a combination of biologi- can provide functional redundancy to maintain cal and stochastic factors ( Tilman et al. 1997 ; Loreau productivity (or other aspects of functioning) as et al. 2001 ; van Ruijven and Berendse 2005 ). species become extinct (Solan et al. 2004 ; Petchey The importance of burrowing organisms as eco- and Gaston, 2005 ). system engineers that infl uence ecosystem proc- esses in the near-seafl oor environment has gained 5.2 Strengths and limitations increasing recognition (e.g. Thayer 1979 ; Seilacher of the geological record and Pfl üger 1994 ; Marinelli and Williams 2003 ; Solan et al. 2004 ; Mermillod-Blondin et al. 2005 ; Ieno The fossil record provides an unparalleled, nearly et al. 2006 ; Norling et al. 2007 ; Solan et al. 2008 ). 600 million year-long history of changing diversity Increased bioturbation infl uences the benthic eco- in marine animal ecosystems. This extensive deep- system by increasing the water content of the upper- time history provides a series of natural experi- most sediment layers, creating a diffuse mixed layer ments in changing biodiversity, ranging from rapid

Marine Biodiversity and Ecosystem Functioning. First Edition. Edited by Martin Solan, Rebecca J. Aspden, and David M. Paterson. © Oxford University Press 2012. Published 2012 by Oxford University Press. OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 53 diversifi cation during the radiation of metazoans Proxies for ecosystem functioning may be more in the Ediacaran and the Cambrian explosion to diffi cult to obtain, however, and there are several extensive species losses during mass extinctions factors that complicate reconstruction of the pro- such as the Permian-Triassic crisis. The fossil ductivity-diversity relationship in nearly all fossil record is also the only source of potential ana- assemblages. Most experimental analyses of the logues to challenges facing the biosphere in the productivity-diversity relationship are conducted near future. Situations such as ice-free climates, in assemblages of primary producers (terrestrial rapid greenhouse gas emission and global warm- plant assemblages); thus, productivity can be meas- ing, or the extinction of nearly 80% of marine ured directly as biomass or the rate of biomass accu- invertebrate genera are not available for study on mulation (e.g. Tilman et al . 1997 ; Worm and Duffy the modern Earth, yet are all represented in the 2003 ). We will use this defi nition of productivity fossil record. throughout the chapter. In contrast, the marine Despite incomplete preservation, most notably of fossil record, at least in the Phanerozoic (the time species that lack hard parts like shells or bone, the of conspicuous animals, since the Cambrian fossil record retains a recognizable signal of changes Explosion), is dominated by heterotrophic, prima- in biodiversity. Measures of diversity are particu- rily suspension- and deposit-feeding, invertebrates. larly reliable in exceptionally preserved localities Because they are not primary producers, their diver- (Lagerstätten) containing soft tissue preservation, sity is unlikely to have direct effects on primary such as the Cambrian Burgess Shale or Chengjiang production as postulated for plant assemblages Fauna (Allison and Briggs 1993 ; Dornbos et al. 2005 ) ( Tilman et al. 1997 ; Worm and Duffy 2003 ; van or the latest Precambrian Ediacara biota ( Clapham Ruijven and Berendse 2005 ). The combined biomass et al. 2003 ; Droser et al. 2006 ), but localities with typ- of heterotrophic invertebrates is presumably infl u- ical hard part-only preservation can still provide enced to some degree by food supply, however, useful data, although with more caveats (Kidwell, suggesting that biotic or stochastic factors (e.g. facil- 2002 ; Tomašových and Kidwell , 2010 ). The loss of itation, niche complementarity, sampling effects; soft tissues, along with preservation biases against Tilman et al. 1997 ; Loreau et al . 2001 ) could similarly certain types of shell mineralogy ( Cherns and infl uence the biomass-diversity relationship. Wright 2009 ), precludes comparison of shelly fossil Although food supply is infl uenced by primary collections with extant communities but does not productivity, it is diffi cult to relate primary produc- prevent comparison among different fossil assem- tivity to nutrient levels, which are more commonly blages. The typical shelly fossil assemblage contains inferred through geological proxies, because of the a mixture of individuals that originally lived over a complicated controls on primary production span of decades to millennia (‘time averaging’), not ( Braiser 1995 ). Even nutrient levels themselves are preserved in life position but mostly derived from diffi cult to assess in the ancient record. First, quan- within a particular habitat (‘spatial mixing’). Time titative geochemical proxies for paleoproductivity, averaging infl ates species richness relative to any such as accumulation rates of the mineral barite single life assemblage (Kidwell 2002 ), a problem ( Dymond et al. 1992 ; Paytan and Griffi th 2007 ) or that becomes increasingly pronounced with increas- trace metal (Cd, Cu, Ni, Zn) concentrations (Piper ing temporal scales of time averaging ( Tomašových and Perkins 2004 ; Piper and Calvert 2009 ), rely on and Kidwell 2010 ). These effects introduce random accurate age models of sedimentation rates that are noise to the biodiversity signal, reducing the preci- typically only available in deep-sea sediment cores sion of potential analyses and conclusions. or other fi ne-grained mudrocks ( Paytan and Griffi th Biodiversity changes can nevertheless be resolved 2007 ). However, nearly all sedimentary deposition and other ecological attributes, such as the relative- on the continental shelf, the depositional environ- abundance structure of the shell-bearing taxa within ment for almost all invertebrate fossil localities, is a community, are preserved with greater fi delity episodic and punctuated by numerous hiatuses of ( Kidwell 2002 ). unknown but typically geologically short duration. OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

54 MARINE BIODIVERSITY AND ECOSYSTEM FUNCTIONING

Second, total organic carbon (TOC) concentrations Functional diversity is diffi cult to quantify even refl ect a complex signal of not only primary pro- in modern settings (Petchey et al. 2004 ), and it is ductivity but also dilution by accumulating inor- unlikely that the biological requirements and eco- ganic sediment particles such as clay minerals, logical contributions of extinct taxa can be known preservation versus degradation in surface sedi- with similar precision. Paleontologists have a long ments ( Calvert et al. 1992 ; Lee 1992 ; Ganeshram history, however, of grouping extinct taxa into et al. 1999 ), and subsequent alteration during deep broader functional guilds using attributes such as burial (e.g. Pell et al. 1993 ). Although quantitative life position—e.g. benthic versus planktonic, epi- geochemical proxies are not available, time-aver- faunal versus infaunal—motility, and trophic mode aged estimates of productivity can be obtained (e.g. Bambach, 1983 ; Bambach et al. 2007 ; Bush and from calculations of biomass (e.g. Clapham et al. Bambach 2011 ; Bush et al. 2011 ). These characteris- 2003 ) or trends in shell abundance or body size of tics can be reliably determined for the vast majority marine invertebrates (e.g. Fraiser and Bottjer 2004). of fossil taxa, even for extinct groups such as trilo- Shell abundance is affected by the same factors that bites ( Fortey and Owens 1999 ), and provide a coarse complicate geochemical proxies (sediment dilu- proxy for functional diversity. Additional aspects of tion, shell destruction), and body size may refl ect functional diversity have been described in terms of other infl uences, such as greater juvenile mortality tiering—sometimes called stratifi cation in the bio- or shortened lifespans due to harsh environmental logical literature—the vertical subdivision of epi- conditions. Nevertheless, the density and/or size faunal or infaunal habitat space, presumably of fossil taxa provide a reasonable proxy for bio- indicative of niche partitioning (—e.g. Ausich and mass, which itself is related to productivity ( Waide Bottjer 1982 ; Clapham and Narbonne 2002 ). et al. 1999 ). In this chapter, we explore three of these critical Evidence for burrowing activity in marine sedi- biodiversity changes: 1) the Ediacaran radiation of ments, or bioturbation, is readily observable in the large multicellular eukaryotes, 2) the Cambrian fossil record through preserved trace fossils (also radiation of complex bilaterian-grade animals, and called ichnofossils). Although the uppermost lev- 3) the end-Permian mass extinction, the largest els of the mixed layer are rarely preserved, except known extinction event in Earth history. For each of when marine substrates were fi rmly consolidated these events, we examine how changes in bio- ( Droser et al. 2002 ), maximum burrow depth and diversity were related to various factors involved in burrow diameters can readily be measured from ecosystem functioning such as productivity, biotur- preserved trace fossils ( Droser and Bottjer 1988 ; bation (biogenic mixing depth), and functional Droser et al. 2002 ; Marenco and Bottjer 2011 ). The diversity. intensity of sediment mixing can be measured independently using the semi-quantitative ichno- 5.3 Ediacaran ecosystems fabric index method, which scores sedimentary beds on a scale of 1–5 depending on the amount of For the fi rst three billion years of its existence, life disruption to original depositional features (Droser on Earth was dominated by microorganisms. The and Bottjer 1986 ). An ichnofabric index of 1 corre- appearance in the latest Ediacaran (578–542 Mya) of sponds to absent—or extremely minimal—biotur- large, soft-bodied, and structurally complex multi- bation, such that original layering and features are cellular eukaryotes colloquially called the Ediacara preserved, whereas ichnofabric index 5 corre- biota marked a fundamental change in the way eco- sponds to complete homogenization of the layer. systems are built and sustained ( Narbonne 2005 ; Thus, ichnofabric index measures and quantifi ca- Xiao and Lafl amme 2009 ). Despite sharing a similar tion of burrow size and depth provide a good age and mode of preservation, most Ediacara biota proxy for sediment mixing rates and the ecosys- represent an assemblage of unrelated organisms. tem functions—such as nutrient recycling—associ- Some Ediacaran fossils represent the oldest animals ated with bioturbation. and perhaps root stock to modern faunas (Fedonkin OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 55 and Waggoner 1999), while others represent extinct stones that has been (contentiously) interpreted as clades lying outside of crown Metazoa (Narbonne an oxidation of a large deep ocean dissolved organic 2004 ; Xiao and Lafl amme 2009 ). Despite this taxo- carbon pool ( Rothman et al. 2003 ; Fike et al. 2006) . nomic uncertainty, temporal, biogeographic, and 3) The Nama assemblage (550–541 Mya) of species-diversity patterns in Ediacaran localities Namibia marks a further step in the progression highlight the existence of three assemblages towards modern ecosystems with the advent of bio- characterized by distinct evolutionary innovations logically mediated secretion of calcium carbonate ( Waggoner 2003 ): skeletons ( Figure 5.1 ; Grotzinger et al . 1995 ).

1) The Avalon assemblage of Mistaken Point in The underlying cause for the segregation of the Newfoundland and Bradgate Park in England Ediacara biota into three assemblages is diffi cult (578–560 Mya) is an entirely deep-water assem- to isolate ( Waggoner 2003 ; Grazhdankin 2004 ; blage, having formed several hundred meters below Narbonne 2005 ) and could have been infl uenced, at storm wave base and the photic zone (Wood et al. least in part, by important differences in the way 2003 ; Wilby et al. 2011 ). As a result, the Ediacara fossils were preserved in each locality ( Narbonne biota from these localities could not utilize sunlight 2005 ). Biological responses to limiting factors asso- as their primary source of energy. The Avalon ciated with changes in bathymetry could also assemblage is dominated by rangeomorphs, an explain the diversity pattern, as the Avalon assem- extinct clade of organisms constructed almost blage represents a deep-water community, while entirely from repeatedly branched (fractal) units the most diverse and fossiliferous White Sea and and temporally restricted to the Ediacaran ( Figure Nama assemblages occupied signifi cantly shal- 5.1 ; Narbonne 2004 ; Narbonne et al. 2009 ; Brasier lower water settings. Most intriguingly, however, and Antcliffe 2009 ). This fractal branching allowed the increased diversity and ecological complexity the rangeomorphs to attain high surface-area to vol- could instead refl ect evolutionary advances from ume ratios necessary for diffusion-based feeding, the oldest Avalon assemblage, through the younger termed osmotrophy (Sperling et al. 2007 ; Lafl amme White Sea assemblage containing the fi rst mobile et al. 2009 ). In the absence of metazoan zooplankton bilaterians, to the youngest Nama assemblage with and macropredators in the Ediacaran, and as a its biomineralizing taxa (Xiao and Lafl amme 2009 ; result a lack of sloppy feeding and egestion, a Brasier et al. 2010a ). greater portion of labile dissolved organic carbon The unusual style of fossil preservation in was able to reach the deep ocean to be consumed by Ediacaran communities allows potential relation- osmotrophes ( Sperling et al. 2011 ). Trace-fossils from ships between diversity and ecosystem functioning, the Avalon assemblage are rare and restricted to the including productivity, bioturbation, and functional surface (Liu et al. 2010 ), while carbonate skeletons diversity, to be examined more rigorously. In con- are unknown. trast to virtually all other fossil assemblages, which 2) The White Sea assemblage (560–550 Mya), best are time-averaged and have undergone some degree known from the Flinders Ranges in South Australia of spatial mixing, most Ediacaran assemblages and the White Sea coast of Russia, marks a signifi - record a snapshot of the original in situ community cant step in metazoan evolution, with the fi rst of soft-bodied organisms as it appeared at the appearance of likely bilaterians (Fedonkin and moment of death ( Seilacher 1992 ; Gehling 1999 ; Waggoner 1997; Fedonkin 2007 ) and a diverse array Clapham et al. 2003 ). Any dead specimens ( Liu et al. of novel trace fossils. The highest diversity of fossils 2010 ) would decay within days to weeks (Allison from the White Sea assemblage occurs in rocks that 1988; Brasier et al. 2010b ; Darroch et al . submitted), were deposited in well-lit and energetically active orders of magnitude smaller than typical time aver- shallow water (Gehling 2000 ). The White Sea assem- aging in shelly communities (several hundred years; blage postdates a major change in the stable carbon Kowalewski et al. 1998 ), and on the same timeframe isotope composition (ratio of 13 C to 12 C) of lime- as modern ecological census population studies. OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

56 MARINE BIODIVERSITY AND ECOSYSTEM FUNCTIONING

12 Trepassey Mistaken Point 10 Briscal Drook

8 D

SP 6 LBW LMP E Areal Cover (%) Areal 4 BC G 2 PC SH 2 4 681012 Form Richness

Figure 5.1 Richness-areal coverage relationship for Ediacaran communities from the Avalon Assemblage, Newfoundland. Genus richness is approximated by form richness, although informal groups such as ‘dusters’ may actually include several genera. The probable microbial structures Ivesheadia and the informally named ‘lobate discs’ are excluded. Areal coverage is a proxy for three-dimensional biomass and is measured as the percentage of the rock outcrop covered by fossil impressions, also excluding the area accounted for by Ivesheadia and ‘lobate discs.’ Although areal coverage in the most diverse surfaces is lower than the peak value, maximum likelihood estimation strongly supports a linear model fi t (Akaike weight 0.91, compared to0.055 for Gaussian and 0.035 for quadratic fi ts).

This nearly unique style of preservation allows ( Calver 2000 ), and < 0.1 wt % in Namibia ( Kaufman investigation of ecological questions that may be et al. 1991 ). Although paleoproductivity cannot be obscured in the younger fossil record. For example, quantifi ed in any Ediacaran fossil assemblage, the did more productive Ediacaran communities have unusual preservation of the autotrophic (likely higher species richness? What effects did the onset osmotrophic) fossils as ‘snapshots’ of the living of bioturbation have on diversity in younger community does allow estimation of standing bio- Ediacaran communities? Was there positive feed- mass, analogous to ecological approaches (e.g. back between increasing functional diversity and Tilman et al. 1997 ), and its relationship to diversity higher species richness, in the form of facilitation or ( Clapham and Narbonne, 2002 ; Clapham et al. 2003 ; niche partitioning (Lafl amme and Narbonne Droser et al. 2006 ; Wilby et al . 2011 ). As productivity 2008b )? is the rate of biomass creation, biomass measures provide an approximation of time-averaged pro- ductivity over the lifespan of the organisms ( Waide 5.3.1 Productivity–biodiversity relationship et al. 1999 ), although biomass and productivity at Using organic carbon (TOC) as a proxy for produc- any given instant may themselves be interrelated tivity in Ediacara biota assemblages is not possible ( Guo 2007 ). Because the three-dimensional shape because of complications from dilution by sedi- and material properties are unknown for most ment input and degradation during burial of the Ediacaran fossils, biomass can only be approxi- sedimentary strata, as discussed above. In addi- mated by calculating the percentage of the rock tion, TOC levels in fossiliferous Ediacaran units are surface covered by fossils—percent areal cover uniformly low: < 0.2 weight % in Newfoundland ( Clapham et al. 2003 ). Areal cover is compared ( Canfi eld et al. 2007 ), < 0.2 wt % in South Australia with ‘form diversity,’ an approximation of species OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 57 diversity that takes the presence of undescribed therefore also were more productive, although the taxa—such as ‘dusters’, which may represent sev- existence or directionality of causation (whether eral genera (Clapham et al. 2003 )—into account. productivity led to greater diversity or vice versa) Taxa such as Ivesheadia and the undescribed ‘lobate cannot be determined. disc’ were included in the areal coverage calcula- tions in Clapham et al. ( 2003 ) but are excluded 5.3.2 Infl uence of bioturbation on ecosystem here—except for Long Beach West (LBW) and functioning Spaniard’s Bay (SP) surfaces as taxon-specifi c areal coverage data are not available for those localities— The Ediacaran interval marks the onset of animal because those taxa likely represent microbial mat bioturbation and its ecological effects: infaunal bio- structures rather than multicellular eukaryotes turbation is absent in the oldest Ediacaran commu- (Lafl amme et al. in press; although see Liu et al. nities (Avalon assemblage) and simple horizontal 2010 ). The exclusion of ivesheadiomorphs from the traces are fi rst found in the younger White Sea analysis also eliminates some of the time-averaging assemblage (Seilacher et al. 2005 ; Jensen et al. 2006 ). issues raised by Lui et al. 2011. The fi rst appearance of trace fossils in the White Sea Sample size is small and the data are noisy, assemblage corresponds with an increase in eco- but there is a weakly signifi cant positive relation- logical complexity and the appearance of a variety ship (r = 0.68, p = 0.04) between form richness— of new functional groups, including mobile grazing ‘diversity’—and areal cover—‘biomass’—in Avalon metazoans, but does not correspond with an assemblages at Mistaken Point (Figure 5.1 ). increase in within-community richness (Narbonne Although there is a signifi cant linear correlation, 2005 ; Bottjer and Clapham 2006 ; Droser et al. 2006 ; peak areal coverage does not occur at maximum Shen et al. 2008 ). A causal relationship between the form richness (Figure 5.1 ), potentially suggestive of two events is unlikely, however, because Ediacaran a unimodal—‘hump-shaped’—relationship com- bioturbation was extremely sparse and entirely rep- monly, but not always, observed in modern com- resented by surfi cial traces that did not rework the munities (e.g. Waide et al. 1999 ; Worm and Duffy sediment (Seilacher et al. 2005 ; Jensen et al. 2006 ). It 2003 ; van Ruijven and Berendse 2005 ; Guo 2007 ). is more likely that the appearance of new functional Maximum likelihood estimation was used to fi t and groups, including mobile animals, refl ects some compare linear, Gaussian, and quadratic models to combination of permissive environmental condi- discriminate between linea-r and unimodal-rich- tions—such as an increase in oxygen levels—eco- ness areal cover relationships at Mistaken Point. logical feedbacks, or simply continuing biological The linear model receives the substantial propor- evolution. Frondose taxa, which had been highly tion of model support (Akaike weight 0.91), whereas dominant in the oldest Avalon assemblage Gaussian (Akaike weight 0.055) and quadratic ( Lafl amme et al. 2004 ; 2007 ; Narbonne et al. 2009 ) (Akaike weight 0.035) models are poor fi ts to the and were highly adapted to fi rm microbial sub- data. However, Ediacaran communities span a lim- strates ( Seilacher 1999 ; Lafl amme et al. 2010 ), were ited range of richness values—less than 10 form also less important constituents of the White Sea taxa per site—and could potentially occupy one assemblage (Bottjer and Clapham 2006 ; Droser et al. limb of a larger unimodal trend. Ongoing paleoeco- 2006 ). Frondose taxa and mobile grazers appear to logical research in the Flinders Ranges, South have been largely segregated in White Sea assem- Australia (White Sea Assemblage; Droser et al. 2006 ) blage communities ( Droser et al. 2006 ), suggesting may also help extend and clarify trends interpreted that the decline of erect frondose forms may have from Avalonian assemblage communities at resulted from sediment disturbance by mobile mat- Mistaken Point. Nevertheless, the correlation based grazers and/or burrowers. However, bioturbation on existing data tentatively suggests that richer did not have a signifi cant vertical component that Ediacaran communities had greater biomass, would lead to appreciable sediment reworking until OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

(a) (b) (d)

(b)

(e)

(c)

(f)

(g) (h) (i)

(j) (k) OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 59 the Cambrian (Droser and Bottjer 1988 ; Droser et al. their body into a separate food-gathering apparatus 2002 ), at which point it did exert an important con- and elevating stem ( Lafl amme et al. 2004 ; Lafl amme trol on marine ecosystems ( Bottjer et al. 2000 ). and Narbonne 2008a , 2008b ). Well-developed epi- faunal tiering also resulted in a much more precise subdivision of the vertical habitat: the D surface 5.3.3 Species richness–functional diversity community at Mistaken Point contained Fractofusus relationship in the lowest tier, Bradgatia at an intermediate level, Ediacaran communities display a trend of increas- Pectinifrons at greater heights, and Beothukis in the ing species richness from the earliest Avalonian upper level at heights of nearly 30 cm ( Figure 5.2 ; examples to the White Sea assemblage, accompa- Clapham and Narbonne 2002 ; Lafl amme and nied by a corresponding trend towards greater Narbonne, 2008b ). Comparison of the ecological functional diversity. Ediacaran functional diversity structure of low- and high-diversity Avalon com- cannot be quantifi ed due to the uncertain life habits munities indicates that high-diversity communities of many of the taxa (Xiao and Lafl amme 2009 ), but had a broader range of organism heights subdi- it is possible to make some qualitative generaliza- vided into a more complex and regular tiering tions regarding changes in the types of functional structure. Thus, the positive relationship between groups represented. Early Avalon assemblage com- species richness and functional diversity was plau- munities, in the Drook and Briscal Formations, had sibly driven by niche partitioning and development low species richness (3–5 form species present) and of a more fi nely subdivided tiering structure in also had low functional diversity and poorly devel- Avalon assemblage communities. oped epifaunal stratifi cation (referred to as tiering In the White Sea assemblage, fronds still domi- in the paleontological literature). The two dominant nated the upper tiers while the lowermost tiers were taxa in the Pigeon Cove community—Charnia and colonized by attached epibenthic recliners such as Thectardis—were both relatively unspecialized erect Tribrachidium , Arkarua , Parvancorina ( Figure 5.2 ), mid-to-upper-tier feeders (Clapham and Narbonne, and Phyllozoon ( Droser et al . 2006 ). Mobile Kimberella 2002 ; Lafl amme et al. 2007 ; Sperling et al . 2011 ). The (Figure 5.2 ; Fedonkin and Waggoner 1997; Fedonkin third, Ivesheadia , is unlikely to be a metazoan ( Liu 2007 ; Ivantsov 2009 ) and Dickinsonia ( Figure 5.2 ; et al. 2010 ; Lafl amme et al. in press). The younger Gehling et al. 2005 ; Sperling and Vinther 2010 ), both Bristy Cove community was nearly exclusively of which grazed on abundant microbial mats, also populated by low-tier rangeomorphs (e.g. make their appearance in the White Sea assemblage; Fractofusus , Beothukis) that fed from the basal few as the fi rst mobile, non-suspension feeding (or centimeters of the water column. In contrast, rich- absorbing) taxa, they indicate a major increase in ness and functional diversity were both higher in functional diversity. However, this increase in func- later Avalonian communities, especially in the tional diversity—perhaps the most signifi cant eco- Mistaken Point Formation. Although those commu- logical change within the Ediacaran—was not nities were still dominated by rangeomorphs, taxa accompanied by an increase in within-community began to display morphological adaptations for species richness, or morphospace expansion (Shen subdividing ecospace such as a differentiation of et al. 2008 ), although the regional species pool was

Figure 5.2 Diversity of Ediacaran organisms. (a–f) represent various members of the rangeomorpha from Newfoundland. (a) Avalofractus abaculus from the Trepassey Fm. at Spaniard’s Bay, with long stem and close-up (b) of a fractal, rangeomorph frondlet. (c) Beothukis mistakensis (NFM F-758) from the Trepassey Fm. at Spaniard’s Bay. (d) Fence-shaped Pectinifrons abyssalis from the Mistaken Point Fm. at Mistaken Point North. (e) Cabbage-shaped Bradgatia linfordensis (ROM36500) from the Mistaken Point Fm. ‘d’ surface at Mistaken Point. (f) Spindle-shaped Fractofusus misrai from the Mistaken Point Fm. ‘e’ surface at Mistaken Point. (g) Frondose Charniodiscus spinosus from the Mistaken Point Fm. ‘e’ surface at Mistaken Point. (h–k) Assortment of classic Ediacaran organisms from the Flinders Ranges in South Australia. (h) Two specimens of the probable sponge Palaeophragmodictya reticulata (P32352a–f). (i) Probable stem-group mollusk Kimberella quadrata (P23532). (j) Bilaterally-symmetrical Spriggina fl oundersi (P12771) with anterior-posterior differentiation. (k) Probable placozoan Dickinsonia costata (P18888). Scale bars 1 cm or 1 cm increments. OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

60 MARINE BIODIVERSITY AND ECOSYSTEM FUNCTIONING substantially larger in the White Sea assemblage. et al. 2000 ; Bengtson 2002 , 2004 ; Plotnick et al. 2010 ; Richness and evenness values in White Sea commu- Callow and Brasier 2009 ). It was indeed a time of nities from Australia—mean richness of 5.25 species rapid restructuring of marine ecosystems. per bedding plane—are not signifi cantly different Lagerstätten deposits, which provide the highest from those in Avalon communities from defi nition view of animal life during the Cambrian Newfoundland ( Droser et al. 2006 ). radiation due to their preservation of soft tissues, Increased functional richness in younger White are particularly abundant during the early and mid- Sea assemblage Ediacaran communities, even dle Cambrian, and then fade into comparative rar- though assemblage-level species richness was simi- ity through the remainder of the Phanerozoic Eon lar to the older Avalon assemblage, implies that (Allison and Briggs 1993 ). Two of the most well Australian communities had lower functional studied Lagerstätten assemblages are the early redundancy. Australian assemblages also had more Cambrian Chengjiang biota of Yunnan Province, variable species composition and relative abun- China, and the middle Cambrian Burgess Shale dances ( Droser et al. 2006 ), whereas Mistaken Point biota of British Columbia, Canada. Priapulid worms communities contain many of the same species, and arthropods are dominant in the Chengjiang albeit at different abundances, over more than 10 biota, and arthropods dominate the Burgess Shale million years of their history ( Clapham et al. 2003 ). biota (Dornbos et al . 2005; Caron and Jackson 2008 ; Community stability in the Avalon assemblage may Zhao et al. 2009 ). refl ect the stabilizing role of functional redundancy, allowing maintenance of community structure dur- 5.4.1 Productivity–biodiversity relationship ing disturbances ( Naeem 1998 ). However, it is dif- fi cult to defi nitively reconstruct the true relationship The rapid early Cambrian diversifi cation and radia- between stability and functional redundancy tion of phytoplankton fossils provides evidence for because of the overprint of environmental parame- a dramatic increase in primary productivity during ters such as the frequency of disturbance. The the Cambrian radiation (e.g. Butterfi eld 1997 ). These signifi cantly different habitats of the two assem- fossils consist of small acanthomorphic arcritarchs, blages—deep marine continental slope for the thought to be fossil remnants of planktonic eukary- Avalon assemblage, coastal shallow marine for the otic algae ( Butterfi eld 1997 ). These fossils are accom- White Sea assemblage—may instead be primarily panied by the fi rst evidence for mesozooplankton, responsible for increased volatility in community consisting of minute feeding structures preserved composition in the Australian examples. alongside the acritarchs ( Butterfi eld 1997 ). The development of multiple trophic levels in the 5.4 Cambrian ecosystems planktonic realm was an important characteristic of the Cambrian radiation (Butterfi eld 1997 ), and most Ecosystems continued to increase in complexity likely would have facilitated the further revolution during the Cambrian radiation (starting at 542 of suspension-feeding benthic organisms, as con- Mya). This event involved the geologically rapid solidated organic particles became more common diversifi cation of marine animal life into relatives of in marine waters. It is also likely that the evolution nearly all modern phyla. This increase in diversity of zooplankton led to the restriction of a large per- was coupled with increasing ecological complexity centage of primary productivity, and as such labile as active animals began interacting with each other dissolved organic carbon (DOC), to the surface on a large scale. Although their precursors might lie ocean where it is rapidly consumed and recycled in the Ediacaran, it is in the Cambrian that we fi nd through the microbial loop ( Azam et al. 1983 ; the fi rst defi nitive evidence for predation, the fi rst Pomeroy et al. 2007 ). Furthermore, the evolution of widespread biomineralization, the fi rst macroscopic fecal pellets clumped organic waste into ballasted sensory organs, and the fi rst development of the packages that could travel through the water col- seafl oor mixed layer through bioturbation ( Bottjer umn to accumulate as detritus on the seafl oor OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 61

(Logan et al. 1995). As such, the deep oceans likely Examination of the substrate adaptations of ses- became impoverished in labile DOC, which sile benthic suspension feeders in the early would have had a dramatic effect on deep ocean Cambrian Chengjiang biota supports the pattern osmotrophic Ediacarans which relied on DOC seen in early echinoderms. From the perspective of and could not capture and process larger particu- both generic diversity and relative abundance, lates favored by fi lter-feeding cnidarians and forms adapted to fi rm unlithifi ed sediments domi- sponges (Sperling et al. 2011 ). The increasing com- nate the Chengjiang biota ( Dornbos et al . 2005 ; plexity that developed near the base of the marine Dornbos and Chen 2008). This would be expected trophic web during the Cambrian radiation given the early Cambrian age of the fossil assem- clearly played a role in the dramatic increase in blage, as mixed layer development was only begin- biodiversity that is one of the signatures of this ning. Direct examination of the sediments in which critical event in the evolutionary history of these fossils are preserved indeed reveals that bio- animals (Butterfi eld 2009 ). turbation levels were minimal (Dornbos et al. 2005 ). Similar data from the Burgess Shale biota is lim- ited, but suggests that fewer sessile suspension- 5.4.2 Infl uence of bioturbation on ecosystem feeding genera were adapted for direct substrate functioning interaction (Dornbos et al. 2005 ). Trace fossil taxa diversifi ed rapidly during the The increasing bioturbation depth and intensity Cambrian radiation, refl ecting the increasing com- through the Cambrian clearly was one critical factor plexity of animal behavior (e.g. McIlroy and Logan in shaping ecosystem functioning. Sessile benthic 1999 ; Droser et al. 2002 ). Bioturbation depth and taxa were placed under strong selective pressure intensity increased accordingly within a broad spec- to adapt to increased sediment mixing, resulting in trum of Cambrian depositional environments the evolution of new attachment structures and (Droser 1987). Evidence for a well-developed mixed strategies. layer in the upper few centimeters of the seafl oor is found for the fi rst time in the Cambrian, and pale- 5.4.3 Species richness–functional diversity oecological studies of benthic suspension feeders relationship indicates that it had a profound effect on ecosystem functioning ( Seilacher 1999 ; Bottjer et al . 2000 ; There was a remarkable increase in animal species Dornbos 2006 ). richness from the Ediacaran into the Cambrian. This Echinoderms are among the earliest skele- increase in richness was also associated with a tonized sessile benthic suspension feeders in the marked increase in functional diversity, as meas- Phanerozoic, and have therefore been the focus of ured by ecospace occupation (e.g. Bambach et al. many studies aimed at understanding the evolution- 2007 ). When comparing ecospace occupation dur- ary response of benthic organisms to mixed layer ing the Ediacaran and Cambrian Periods, it becomes development during the Cambrian. Early and mid- clear that a major shift took place from relatively dle Cambrian echinoderms include many genera large, mostly immobile animals in the Ediacaran, to adapted to living directly attached to, or inserted in, somewhat smaller but more mobile animals in the fi rm unlithifi ed sediments (Bottjer et al . 2000 ; Dornbos Cambrian (Bambach et al. 2007 ; Xiao and Lafl amme 2006 ). By the late Cambrian, however, all sessile ben- 2009 ). Most of the immobile Ediacaran animals thic echinoderms lived attached to hard substrates, were most likely absorbing dissolved organic car- either rare carbonate hardgrounds or loose shell bon from the seawater, while the smaller immobile material. This trend away from direct interaction Cambrian animals are interpreted as suspension with unlithifi ed sediments and toward hard sub- feeders on organic particles. Mobile Cambrian ani- strate attachment through the Cambrian is consist- mals occupied a wide range of ecospace compared ent with an evolutionary response to the development their mobile Ediacaran counterparts (Bambach et al . of the mixed layer in marine sediments. 2007 ), which were also much more rare. OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

62 MARINE BIODIVERSITY AND ECOSYSTEM FUNCTIONING

Indeed, it is during the Cambrian in which we 5.5.1 Environmental changes during the late fi nd the fi rst defi nitive evidence for macrophagous Paleozoic to early Mesozoic predation, widespread skeletonization, macro- By the Late Carboniferous to Early Permian, Earth’s scopic sensory organs, and intense bioturbation of major continents were confi gured as the supercon- the seafl oor ( Bottjer et al. 2000 ; Bengtson 2002 , tinent Pangea (Scotese 1997). Atmospheric carbon 2004 ; Plotnick et al. 2010 ). Evidence for these eco- dioxide levels were low during the Permo-Carbon- logical changes is found throughout the early and iferous, while atmospheric oxygen levels were at middle Cambrian fossil record, but is even more their zenith in the Early Permian (Berner 2004). The apparent in deposits of exceptional preservation, precise cause of the end-Permian mass extinction such as the Chengjiang and Burgess Shale biotas. remains controversial, but it is generally well- The older Chengjiang biota is particularly inform- accepted that the ultimate cause of the extinction ative because of its early Cambrian age, which was massive volcanism leading to a cascade of places it during the heart of Cambrian radiation. environmental effects (Riccardi et al . 2007). Some In this assemblage, we fi nd the oldest evidence for combination of hypercapnia (carbon dioxide toxic- the largest known Cambrian predators, the well- ity), hydrogen sulfi de toxicity, and climate change, known stem group arthropods known as the triggered or catalyzed by the eruption of the anomalocaridids (e.g. Whittington and Briggs Siberian Traps, appears to be the most likely kill 1985 ). Well-developed eyes and mechano- and mechanism (Kump et al. 2005; Knoll et al. 2007). chemosensory organs are also found preserved in Deep-water anoxic and euxinic conditions devel- many Chengjiang taxa, indicating the importance oped in the Middle (Isozaki 1997) and Late Permian of navigating the Cambrian marine landscape in (Nielsen and Shen 2004), indicating that environ- search of prey, mates, or protection from predators mental stress that led to the Paleozoic-Mesozoic ( Plotnick et al. 2010 ). biotic crisis was likely to have been initiated sev- eral million years before the end-Permian mass 5.5 The end-Permian mass extinction extinction. Geochemical and sedimentological data and its aftermath also indicate that anoxia, euxinia, and high CO2 concentrations in the oceans persisted at least inter- The Great Ordovician Biodiversifi cation Event mittently through the Early Triassic (Pruss et al. (GOBE) 485–460 Mya exhibited a greater increase 2006; Takahashi et al. 2009). in biodiversity at the family, genus, and species levels than the Cambrian Explosion, and was asso- 5.5.2 Permian–Triassic marine nutrient levels ciated with increases in tiering, epifaunal modes of and primary productivity life, and bioturbation (Servais et al. 2010). The GOBE established the Paleozoic Evolutionary Modeling supports the hypothesis that global Fauna that was dominant approximately 488–251 warming during the Permian through Triassic Mya (Ogg et al. 2008), and characterized as having would have decreased the equator to pole tempera- intermediate-diversity communities, common epi- ture gradient, thereby lowering wind velocities, faunal suspension feeders, developing tiering, and thermohaline circulation, upwelling intensities, intermediate complexity food webs (Sheehan transport of nutrients to the deep ocean and to sur- 1996). The end of the Paleozoic era and the domi- face waters, and thus primary productivity (Kidder nance of the Paleozoic Evolutionary Fauna were and Worsely 2004). However, some sedimentologi- marked by the end-Permian mass extinction ~252 cal and geochemical proxies indicate that nutrient Mya. This extinction was the largest mass extinc- levels and primary productivity may have fl uctu- tion since the Cambrian radiation, whereby 78% ated spatially and temporally during the late of marine genera, and 49% and 63% of marine Permian through Early Triassic. and terrestrial families disappeared (Raup and Hypotheses have been proposed for both Sepkoski 1982; Clapham et al. 2009). enhanced and decreased input of continental OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 63

nutrients into the marine realm during the Late was a time of very little biogenic chert production Permian to Early Triassic. Modeling suggests that and/or preservation around the world, termed the because mountain building had ceased, silicate Early Triassic Chert Gap (ETCG) (Racki 1999; weathering decreased, and thus nutrient input into Beauchamp and Baud 2002; Kidder and Worsely, the oceans was minimal and led to a crash in pri- 2004; Takemura et al . 2003). Sluggish thermohaline mary productivity in the Late Permian (Kidder and circulation caused by global warming, and low bio- Worsley 2004). On the contrary, the extinction of available nutrients that must be present in suffi cient land plants, the occurrence of pedoliths, and a rise amounts for biogenic siliceous sediments to in strontium isotopic values through the Early precipitate during the Early Triassic may have Triassic indicate that terrestrial primary productiv- caused a breakdown in the conditions favorable for ity decreased rapidly, soil erosion was drastic, and chert production, accumulation, and preservation continental weathering increased (Korte et al. 2003; (Laschet 1984; Racki 1999; Gammon et al. 2000). Sephton et al. 2005; Sheldon 2006; Hu et al . 2008; Alternate hypotheses for the ETCG include a Huang et al. 2008; Sedlacek et al. 2008; Ward et al. decrease in biogenic silica due to the extinction of 2005; Retallack et al. 2005). The increased transport some sponge groups (Kato et al. 2002; Sperling and of terrestrial sediments and nutrients into the Ingle 2006) and a poor record of radiolarians (De marine realm is proposed to have facilitated Wever et al. 2006). eutrophication, possibly increasing primary pro- Extensive pyrite deposition is another character- ductivity in the ocean (Sephton et al. 2005). istic feature of rocks deposited during the end-Per- The Early Triassic has a unique sedimentological mian mass extinction and post-extinction aftermath record for the Phanerozoic that can also serve as a (Grasby and Beauchamp 2009). Prominent pyrite proxy for nutrient levels (e.g. Pruss et al . 2006). deposition suggests euxinic conditions that would There is little documented organic matter in Lower have stripped essential bioavailable trace elements Triassic strata, despite conditions that would have from the seawater (Grasby and Beauchamp 2009) contributed to organic matter production and pres- that would have stressed marine primary produc- ervation—including low oxygen conditions, the ers (Anbar and Knoll 2002). phosphate cycle, and low bioturbation (e.g., Berner Phosphorites are rare during the Early Triassic, and Canfi eld 1989; Wignall and Twitchett 1996). possibly indicating decreased nutrient input and Organic-rich black shales have been found in south- upwelling intensity (Trappe 1994; Kidder and west Japan, Australia, and the Sverdrup basin in Worsely 2004). The distribution of phosphorites in northern Canada, and are hypothesized to have mid-high latitudes suggests that there may have resulted from increased nutrients via rivers or been a shift in ocean productivity to high latitudes upwelling, or enhanced preservation under anoxic because of changes in chemical weathering patterns conditions (Suzuki et al . 1998; Thomas et al. 2004; (and the resultant P-fl ux to the ocean) due to the hot Grasby and Beauchamp 2009). The possibility exists and arid climate (Trappe 1994) and wind-driven that high TOC was recorded in some Lower Triassic upwelling. Modeling by Hotinski et al. (2001) show strata that has not yet been discovered (Suzuki et al . that nutrients in high latitudes must have been high

1998; Golonka et al. 1994; Thomas et al . 2004). in order for H2 S and CO2 to build up in the ocean. Prior to the end-Permian mass extinction, there Permian-Triassic sections around the world was a long episode of global chert accumulation record several negative and positive excursions in termed the Permian Chert Event (PCE) (Isozaki d 13C (Corsetti et al. 2005 and references therein; 1994; Beauchamp and Baud 2002). It is proposed Kaiho et al. 2005; Galfetti et al. 2007; Haas et al. 2007; that the PCE was facilitated by upwelling of nutri- Hays et al. 2007; Grasby and Beauchamp; 2009), ent- and silica-rich water along north-western which refl ect, in part, fl uctuations in primary pro- Pangea as seasonal melting of northern sea ice led ductivity (Suzuki et al. 1998; Berner 2002; Payne to circulation of these waters (Beauchamp and Baud and Kump 2007). A drop in marine primary pro- 2002; Kidder and Worsely 2004). The Early Triassic ductivity has been proposed as one major cause of OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

64 MARINE BIODIVERSITY AND ECOSYSTEM FUNCTIONING the negative shifts (e.g. Grard et al. 2005; Rampino Riding 2000) and other microbially mediated struc- and Caldeira 2005; Haas et al. 2006, 2007). In eux- tures (such as wrinkle structures) are widespread inic settings, trace metals become scarce and lead geographically and occur throughout the Early to severe nitrogen limitation, which could reduce Triassic (Pruss et al. 2006; Baud et al. 2005). The fab- primary productivity (Anbar and Knoll 2002). That rics and frameworks of most Early Triassic microbi- euxinia is recorded in strata immediately before the alites were most likely to have been built by negative shift in C-isotopes strongly suggests that a calcifi ed coccoid and fi lamentous cyanobacteria global euxinic event may have had a signifi cant (Lehrmann 1999; Thomas et al. 2004; Hips and Haas negative impact on bioavailable nutrients required 2006; Jiang et al. 2008). The proliferation of benthic to support ocean primary productivity during the primary producers is hypothesized to have been Late Permian (Grasby and Beauchamp 2009). Δ34S facilitated by decreased bioturbation, and upwelling and Δ13C values are interpreted in some strata to of supersaturated, nutrient-rich anoxic marine record a crash in primary productivity in the Late water (e.g. Pruss et al. 2006; Kershaw et al. 2007). Permian perhaps of up to 50% (Algeo et al. 2010). The anoxic conditions that would have facilitated 5.5.3 Productivity–biodiversity–biomass decreasing primary productivity would have also relationship increased it through phosphorus recycling, since phosphorus is a key nutrient driving productivity Approximately 78% of marine invertebrate genera (Payne and Kump 2007). A productivity bloom dur- went extinct at the end of the Permian period ing the Permian-Triassic interval would have (Clapham et al. 2009). Molluscs, brachiopods, echi- occurred when autotrophs recovered, creating a noderms, bryozoans, and Porifera are the only positive excursion in the C-isotope record (Grard higher taxa with known macroscopic benthic fossil et al. 2005). Thus productivity crashes were likely to representatives in the Early Triassic (Griffi n et al. have been followed by productivity blooms that 2010); 143 genera of bivalves, gastropods, and bra- could have been major factors in causing the delayed chiopods have been identifi ed (Fraiser et al. 2010). biotic recovery by consuming oxygen in the photic The mean alpha diversity of Early Triassic collec- zone and reducing Earth’s capability of CO2 draw- tions of skeletonized benthic organisms ranges from down (Winguth and Maier-Reimer 2005; Suzuki 3.67 to 4.19 depending on the preservation style of et al. 1998; Kidder and Worsely 2004). the fossils (Fraiser et al. 2010). The diversity of trace Direct evidence of productivity is indicated by fossils, the tracks and trails of organisms, was also fossils of planktonic and benthic producers. Early- low, ranging from 0–11 ichnogenera (Fraiser and Middle Triassic phytoplankton assemblages were Bottjer 2007). The end-Permian extinction has been characterized by low biodiversity and widespread correlated with a decline in primary productivity. blooms of opportunistic acritarchs and prasino- Some nektonic organisms, like cephalopods, diver- phytes that were likely to have formed the base of sifi ed quickly after the extinction, and may indicate Early Triassic marine ecosystem (Eshet et al. 1995; an increase in diversity and abundance of primary Krassilov et al. 1999; Afonin et al. 2001; Grice et al . producers (Brayard et al. 2009). 2005; Payne and van de Schootbrugge 2007). Decreases in bioturbation, animal size, and the Intermittent euxinic surface water and nitrogen abundance of fossil grains in thin- sections suggest limitation could have facilitated the blooms of that a decrease in animal biomass occurred across cyanobacteria recorded in Lower Triassic strata, as the Permian-Triassic boundary and persisted nearly they are able to fi x nitrogen (Anbar and Knoll 2002; to the end of the Early Triassic (e.g. Payne et al. Xie et al . 2005; Grice et al. 2005). 2006; Fraiser and Bottjer 2007). Tallies from bulk Calcareous algae are rare in the benthic samples and analysis of fossil accumulations indi- realm during the Early Triassic (see Payne and Van cate that bivalves and microgastropods—gastro- de Schootbrugge 2007). However, microbialites pods with greatest dimension less than (microbially mediated calcareous structures, sensu 1 cm—comprised the majority of animal biomass OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

LESSONS FROM THE FOSSIL RECORD 65 during the Early Triassic (Fraiser and Bottjer 2004, Some changes in community structure persisted 2007; Fraiser et al. 2005). It has been proposed that only during the Early Triassic, while other aspects reduced Early Triassic animal biomass can be of benthic level-bottom shallow marine communi- attributed to increased global temperatures, small ties were permanently altered. A decrease in biodi- body sizes, and decreased growth effi ciency of bac- versity, the numerical dominance of a few taxa, and terial heterotrophs that could not sustain large the proliferation of microbially-mediated structures numbers of molluscs with high metabolic demands represent perhaps the most signifi cant short-term (Payne and Finnegan 2006). Opportunistic blooms changes in ecosystem functioning that lasted up to of cyanobacteria did not necessarily facilitate ani- 5 million years (Pruss et al. 2006; Fraiser and Bottjer mal diversifi cation or an increase in biomass 2008; Alroy et al. 2008). Some short-term changes, because they are not as effective of a food source as such as a decrease in bioturbation and the prolifera- eukaryotic algae (see references in Payne and tion of microbial structures, resemble Cambrian Finnegan 2006). ecosystems (Bottjer et al. 1996; Fraiser and Bottjer Yet a decline in abundance and quality of primary 2007). Examples of lasting changes in ecosystem productivity cannot explain why organisms with function related to the end-Permian mass extinction low growth effi ciency (i.e. molluscs), instead of and its aftermath include the switch in taxo- those with high growth effi ciency (i.e. brachiopods), nomic and ecologic dominants (Fraiser and Bottjer proliferated around the globe during the aftermath 2007) and a shift to more complex ecosystems of the end-Permian mass extinction. Fraiser and (Bambach et al. 2002; Wagner et al. 2006). Some of Bottjer (2007) proposed that microgastropods and the short-term changes may have facilitated the bivalves were able to survive the chemically and/or long-term changes: bivalves may have been aided physiologically harsh environmental conditions by fi rm, microbially mediated substrates onto which during the Early Triassic better than most skele- they could byssally attach (Fraiser and Bottjer 2007). tonized benthic marine invertebrates because of A complex interplay of environmental mechanisms their distribution in shallow marine environments directly and indirectly caused the extinction and and their physiological attributes. Thus, though delayed biotic recovery. diversity was very low, some taxa were present in very high numbers likely because they were able to 5.6 Conclusions cope with the environmental conditions (e.g. Fraiser and Bottjer 2004). The biodiversity changes associated with the Ediacaran radiation, the Cambrian radiation, and the end-Permian mass extinction provide natural deep- 5.5.4 Discussion time experiments on the impact of such biodiversity Though fl uctuations in nutrient levels and primary shifts on ecosystem functioning, informing our study productivity contributed to the biotic crisis during of the modern biodiversity crisis. The biodiversity the Late Permian through Early Triassic, it is more increases associated with the Ediacaran and likely that other factors were more important Cambrian radiations show that ecosystem function- infl uences on the extinction and its recovery. ing is enhanced by such changes, making ecosystems Environmental conditions, such as euxinia, most more complex and stable in a series of positive feed- likely directly caused extinctions among both back loops that increase productivity, bioturbation microscopic primary producers and macroscopic levels, and functional diversity. The opposite is true organisms (Bottjer et al. 2008). Conversely, nutrient of the dramatic loss of marine biodiversity associated levels and primary productivity could have been with the end-Permian mass extinction. Ecosystem affected by the decline in biodiversity and biomass instability lasted for up to 5 million years following as well. Low bioturbation levels might have this extinction event, with large crashes and blooms reduced nutrient recycling in the water column in productivity, decreased bioturbation of marine (e.g. Thayer 1983). sediments, and sharply decreased functional diver- OUP CORRECTED PROOF – FINAL, 06/21/12, SPi

66 MARINE BIODIVERSITY AND ECOSYSTEM FUNCTIONING sity. These patterns validate the modern emphasis on Bengtson, S. (2004) Early skeletal fossils. In: Neopro- protecting marine biodiversity, as its decline can fos- terozoic-Cambrian Biological Revolutions. Lipps, J.H. ter devastating ecosystem instability that can last far and Waggoner, B.M. (eds), The Paleontological Society beyond human timescales. Special Papers 10: 67–77. Berner, R. A. and Canfi eld, D. E. (1989) A new model for atmospheric oxygen over Phanerozoic time. American References Journal of Science 289: 333–381. Berner, R.A. (2002) Examination of hypotheses for the Aarssen, L. W. (1997) High productivity in grassland eco- Permo-Triassic boundary extinction by carbon cycle systems: Effected by species diversity or productive modeling. Proceedings of the National Academy of Science species? Oikos 80:183–4. USA 99: 4172–4177. Afonin, S. A., Barinova, S. S., and Krassilov, V. A. (2001) A Berner, R.A. 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