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Article

The role of bioturbation-driven substrate disturbance in theMesozoic brachiopod decline

Marko Manojlovic and Matthew E. Clapham

Abstract.—Brachiopods dominated the seafloor as a primary member of the Paleozoic fauna. Despite thedevastating effects of the end-Permian extinction, the group recovered during the early Mesozoic only togradually decline from the Jurassic to today. This decline likely had multiple causes, including increasedpredation and bioturbation-driven substrate disruption, but the role of changing substrate is not wellunderstood. Given the importance of substrate for extant brachiopod habitat, we documented Meso-zoic–Cenozoic lithologic preferences and morphological changes to assess how decreasing firm-substratehabitat may have contributed to the brachiopod decline. Compared with bivalves, Mesozoic brachiopodsoccurred more frequently and were disproportionately abundant in carbonate lithologies. Although pat-terns in glauconitic or ferruginous sediments are equivocal, brachiopods became more abundant incoarser-grained carbonates and less abundant in fine-grained siliciclastics. During the Jurassic, brachiopodspecies rarely had abraded beaks but tended to be more convex with a high beak, potentially consistentwith a non-analogue lifestyle resting on the seafloor. However, those highly convex morphotypes largelydisappeared by the Cenozoic, whenmore terebratulides had abraded beaks, suggesting closer attachmentto hard substrates. Rhynchonellides disproportionately declined to become a minor component of Ceno-zoic faunas, perhaps because of less pronounced morphological shifts. Trends in lithologic preferencesand morphology are consistent with bioturbation-driven substrate disruption, with brachiopods initiallyusing firmer carbonate sediments as refugia before adapting to live primarily attached to hard surfaces.This progressive habitat restriction likely played a role in the final brachiopod decline, as bioturbating eco-system engineers transformed benthic habitats in the Mesozoic and Cenozoic.

MarkoManojlovic andMatthew E. Clapham.Department of Earth and Planetary Sciences, University of California,Santa Cruz, Santa Cruz, California 95064 U.S.A. E-mail: [email protected], [email protected]

Accepted: 25 September 2020Data available from the Dryad Digital Repository: https://doi.org/10.7291/D1696V

Introduction

Brachiopods were one of the primary consti-tuents of the Paleozoic Fauna, ecosystems domi-nated by sessile suspension-feeding organismsrather than the motile gastropods, crustaceans,and infaunal bivalves and echinoids that dom-inate today’s seafloor. The transition from thebrachiopod-dominated Paleozoic Fauna to thebivalve-dominated Modern Fauna shaped thetaxonomic composition of present-day oceans(Sepkoski 1981) and was part of a shift tomore motile taxa and greater energetics in themarine biosphere (Bush et al. 2007; Finneganet al. 2011; Payne et al. 2014). Though the Paleo-zoic Fauna was decimated at the end-Permianmass extinction (Gould and Calloway 1980;Fraiser and Bottjer 2007), brachiopods recov-ered and were locally abundant in communitiesfrom the Middle Triassic to Middle Jurassic

(Fig. 1) (Clapham and Bottjer 2007; Greeneet al. 2011). However, by the Late Cretaceousand Cenozoic brachiopods were exceedinglyrare in most shallow-marine habitats, havingundergone a pronounced decrease in abun-dance during the Late Jurassic and Early Cret-aceous (Fig. 1) (Clapham and Bottjer 2007).The causes of this Late Jurassic and Early

Cretaceous brachiopod decline are not wellunderstood, but may have included predation(e.g., Donovan and Gale 1990) and competitionwith bivalves (Steele-Petrović 1979; Thayer1985; Liow et al. 2015), as well as increasing bio-turbation (Thayer 1979) and grazing pressure(Vermeij 1977; Tomašových 2008). Predationis plausible, as the brachiopod decline coin-cided with the Mesozoic marine revolution(Vermeij 1977) and brachiopods can be targetedby predators even if they may not be preferred

Paleobiology, 47(1), 2021, pp. 86–100DOI: 10.1017/pab.2020.50

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prey (Tyler et al. 2013). Competition for space,at least on hard substrates, is also a possibility,as mussels directly dislodge brachiopods incage experiments (Thayer 1985) and brachio-pods appear more vulnerable to disturbanceby grazers or other motile organisms (Tomašo-vých 2008). Finally, increasing bioturbation bydeposit-feeding and other infauna during theJurassic and Cretaceous (Thayer 1979, 1983;

Sepkoski et al. 1991), may also have contributedto the brachiopod decline.Although some extant brachiopods can

occupy soft and even muddy sediments, insome cases attached to small shell fragmentsor rocks (Richardson and Watson 1975; Rich-ardson 1981b; Stewart 1981; Richardson et al.2007), most living shallow-marine populationsinhabit hard substrates, carbonate sediments,and areas of low to moderate sedimentation(Foster 1974; Noble et al. 1976; Witman andCooper 1983; Lee 1991; Kowalewski et al.2002). Brachiopods preferentially occur in suchenvironments because hard and often crypticattachment sites minimize the burrowing, graz-ing, and dislodging activity of other organisms(Witman and Cooper 1983; Tomašových 2008).The history of brachiopod substrate depend-ence extends back to the Mesozoic (Ager 1965;Surlyk 1972; Owen 1978; Alméras and Moulan1983), suggesting that the mid-Mesozoicdecline of brachiopods may have been partiallydriven by enhanced bioturbation that furtherdisrupted firm substrates (Thayer 1983; Sep-koski et al. 1991). Among other invertebrates,infaunal groups with deeper burrowing habitsand/or more intense sediment reworkingmodes diversified in the Mesozoic, consistentwith greater substrate disruption (Thayer1983). Likewise, thin storm-deposited shellbeds were preserved less frequently beginningin the Jurassic and Cretaceous, implyingintensification of the bioturbated mixed layer(Brandt 1986; Sepkoski et al. 1991). As a result,Upper Cretaceous strata often were intenselybioturbated, with complex tiering structuresimilar tomodern sediments (Ekdale andBrom-ley 1991) and evidence for extremely soft tosoupy substrates (Bottjer 1981). Ultimately,increased sediment mixing may have createdsofter substrates that were uninhabitable formany immobile brachiopods (Thayer 1979).To test the hypothesis that substrate changes

contributed to the mid-Mesozoic decline of bra-chiopods, we quantified the shifting substrateaffinities of articulate brachiopods from a globaldatabase of fossil occurrences. We also assessedmorphological changes in terebratulide andrhynchonellide brachiopods, focusing on char-acteristics of the beak and pedicle opening thatpotentially relate to substrate attachment.

FIGURE 1. Devonian–Quaternary trends in the occurrenceand relative abundance of rhynchonelliform brachiopods.A, Number of occurrences in the Paleobiology Database,binned at stage level, showing the gradual mid-Jurassic toearly Cenozoic decline. Occurrence scale is log-transformed.B, Mean proportional abundance in bulk-sampled assem-blage counts, binned at series level, demonstrating thedecline from the Early Jurassic to the Early Cretaceous. Theproportion in each assemblage is calculated as the numberof rhynchonelliform brachiopod specimens divided by thetotal number of brachiopod, bivalve, and gastropod speci-mens. Abbreviations: D, Devonian; C, Carboniferous; P, Per-mian; Tr, Triassic; J, Jurassic; K, Cretaceous; Pg, Paleogene;Ng, Neogene.

BIOTURBATION AND THE MESOZOIC BRACHIOPOD DECLINE 87

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Although themid-Mesozoic decline of articulatebrachiopods likely had multiple causes, ourapproachwill help constrain the role of substratedisruption in the final transition tomodern-stylebenthic communities.

Methods

We first assessed substrate preferences usingglobal occurrence data of Devonian–Pleistocenebrachiopods and bivalves from the PaleobiologyDatabase.We used occurrences identified at anytaxonomic level and retained uncertain genusand species identifications, but excluded anyoccurrence that could not be resolved to stagelevel. The resulting dataset included 108,678brachiopod occurrences and 77,260 bivalveoccurrences. We classified the lithology of eachoccurrence as either carbonate or clastic usingthe primary lithology field; secondary litholo-gies and lithology adjectives (calcareous, argilla-ceous, etc.) were ignored. Mixed lithologies(marl, “mixed carbonate-siliciclastic”) were alsoexcluded.Althoughwe did not use specific lithologies or

lithology adjectives in the main analysis, someprovide additional information about substrateconsistency. For examples, shales (includingmudstones and claystones) are more likely torepresent particularly soft substrates relative toother siliciclastics, whereas glauconitic siliciclas-tics often reflect sediment starvation and firmersubstrates (Van Houten and Purucker 1985).Coarser-grained carbonates (packstones andgrainstones) or reef habitats would likely be fir-mer and would provide more opportunities forbrachiopod attachment relative to lime mud-stonesorwackestones. Similarly, ferruginouscar-bonates can also form during times of slowsedimentation andmay be associatedwith hard-grounds (Van Houten and Purucker 1985), bothsuggesting firmer substrates on average. Wequantified the proportion of both brachiopodsand bivalves that were in shale (relative to othersiliciclastics), level-bottom packstones and grain-stones (relative to carbonate lithologies of limemudstone, wackestone, packstone, grainstone,marl, and chalk), reefal carbonates (excludingthe perireef or subreef lithology, measured rela-tive to all carbonates), glauconitic siliciclastics(relative to other siliciclastics), and ferruginous

carbonates (relative to other carbonates). Becauselithologic adjectives such as glauconitic or ferru-ginousare rare,wegroupedoccurrencesbyseries(Early Jurassic, Middle Jurassic, etc.).Substrate preferences derived from global

occurrence data can be confounded by geo-graphic shifts in the focus of sampling whenwell-sampled regions are dominated by asingle lithology. For an alternative measure ofsubstrate preferences, we also examined bra-chiopod relative abundance in collections thatreport bulk sample counts. To do so, we down-loaded Permian–Cretaceous occurrences of bra-chiopods, bivalves, and gastropods that hadabundance counts. The download was filteredto select collections that could be resolved to asingle stage; contained at least 25 specimens ofbrachiopods, bivalves, and/or gastropods; andincluded counts of the entire shelly fauna ratherthan of a single group. We checked all collec-tions with 25 or more specimens to determinewhether they were bulk-assemblage paleoeco-logical samples, marking unsuitable collectionsas lacking major groups of macrofossils (collec-tion coverage as “some macrofossils”).The morphology of the brachiopod beak and

pedicle foramen also reflects the organism’sinteraction with its substrate (Richardson1979, 1981a). Individuals with an incurvedbeak are more likely to be free-lying, whereasthose with a straight or suberect beak aremore likely to use the pedicle for attachmentto a hard substrate. There are exceptions tothat broad trend (e.g., the extant speciesNeothyris compressa; Chapman and Richardson1981), but a small to minute pedicle foramenand/or thickened posterior shell region mayalso imply a free-lying habit (Richardson andWatson 1975; Chapman and Richardson1981). Some species with an open pedicle for-amen may live either free-lying or attached,and may shift to a free-lying habit after out-growing the attachment surface (Richardson1981b), but close attachment to a hard substratemay be indicated by an abraded, eroded, ortruncated beak (e.g., Hiller et al. 2007). To char-acterize these morphological traits, we mea-sured foramen width, beak height, beak angle(umbo curvature), shell width, and shell height(Fig. 2) from published illustrations of 217 Jur-assic to Quaternary terebratulide species and

MARKO MANOJLOVIC AND MATTHEW E. CLAPHAM88





172 rhynchonellide species, with all linear mea-surements normalized to shell length. Wefocused on the Jurassic–Quaternary, becausethat interval spans the gradual mid- to lateMesozoic decline of articulated brachiopods.We only included species that had a maximumdimension of at least 1 cm, eliminating micro-morphic brachiopods that often had highly dis-tinctive morphologies. Although species haveintraspecific shape variability, we used oneset of foramen and beakmeasurements per spe-cies, basing them on the holotype, if possible, oron a typical individual. Shell width/length andheight/length were calculated as the mean ofmeasurements in the Paleobiology Database.We then used principal component analysis(PCA), based on the correlation matrix becauseof different measurement units for the lineardimensions and beak angle, to create a mor-phospace of shell shapes. Finally, we recordedfrom published descriptions whether the spe-cies had posterior shell thickening suggestiveof a free-lying habit, an eroded or abradedbeak suggestive of an attached habit, or a labi-ate foramen suggestive of a functioning pedicle.

Results

Brachiopod Abundance.—Rhynchonelliformbrachiopods have preferentially occurred in

carbonate lithologies since at least the Devon-ian, but were especially prevalent in carbonatesduring the Jurassic and Cretaceous (Fig. 3). Thetypical proportion of global occurrences in car-bonates increased from about 50% in the Dev-onian and Carboniferous to around 90% inthe Jurassic and Cretaceous, but decreasedsharply to 25% (although with a broad 95%confidence interval from 0% to 60%) by theNeogene andQuaternary. These trends are par-tially controlled by the exposed lithologies inwell-sampled regions (particularly NorthAmerica and Europe), which were predomin-antly carbonates in the Triassic and Jurassicbut predominantly siliciclastics in the Neogene.Nevertheless, the increased preference of bra-chiopods for carbonate substrates is likely areal phenomenon, in excess of shifts in theavailability of carbonate lithologies in well-sampled regions. Epifaunal pteriomorphbivalves typically occurred less frequently incarbonates than brachiopods, especially fromthe Triassic to the Paleogene (Fig. 3), implyingthat brachiopods had a stronger carbonate pref-erence than other epifaunal taxa. In addition,

FIGURE 2. Schematic illustration of a terebratulide shell,indicating the measured dimensions (length, width, andheight) and parameters. Beak height is the distance fromthe posterior end of the dorsal valve to the top of thebeak. Foramen width is the maximum width of the pedicleforamen. Beak angle is the angle between the commissuralplane in lateral view and the orientation of the beak andpedicle foramen.

FIGURE 3. Proportion of rhynchonelliform brachiopod(solid circles) and pteriomorph bivalve (open circles) occur-rences in carbonate lithologies, binned by stage. Shadedfields show 95% confidence intervals on LOESS localregressions (smoothing parameter of 0.5 and weightingobservations by the number of occurrences) for brachiopod(dark gray) and bivalve (light gray) trends, shown only tosmooth sampling-related volatility. Brachiopods typicallyoccurred in carbonates more frequently than bivalves, butthe substrate difference was wider in the Mesozoic andPaleogene. Abbreviations: D, Devonian; C, Carboniferous;P, Permian; Tr, Triassic; J, Jurassic; K, Cretaceous; Pg, Paleo-gene; Ng, Neogene.






the normalized proportion of rhynchonelliformbrachiopod occurrences in carbonates (aftersubtracting the proportion of all marine inverte-brate occurrences in carbonates) indicates greaterpreference for carbonates during the Jurassicand Cretaceous (Fig. 4). The proportion of bra-chiopod occurrences in carbonates was notelevated relative to the overall proportion ofcarbonate occurrences during the Devonian–Permian or during theNeogene andQuaternary.Abundance data from individual collections

avoid many of the complexities of occurrencedata and confirm the preferential occurrenceof Mesozoic brachiopod on carbonate sub-strates. Rhynchonelliform brachiopods wereabundant in both carbonates and siliciclasticsduring the Permian, even more abundant insiliciclastics during the Cisuralian and Lopin-gian (Fig. 5). Brachiopods were extremely rareduring the Early Triassic, but were consider-ably more abundant in carbonate samples dur-ing much of the Triassic and Jurassic, except forthe Late Jurassic and perhaps Middle Triassic.By the Late Cretaceous, brachiopods were rarein both carbonate and siliciclastic collectionsthat had abundance data. Overall, the earlyMesozoic resurgence of rhynchonelliform

brachiopods was driven almost entirely by car-bonate habitats; brachiopods remained rare incollections from siliciclastics, except duringthe Middle Triassic.Evidence from specific lithologies is more

equivocal, however. Among siliciclastic occur-rences, brachiopods were not consistentlyunderrepresented in shales (including mud-stones and claystones) during the Mesozoic(Fig. 6), even though those lithologies aremore likely to represent soft substrates com-pared to coarser siliciclastics. The proportionof brachiopod occurrences in shales was lowerthan the proportion of epifaunal bivalves dur-ing the Late Triassic, Late Jurassic, and possiblythe Late Cretaceous, but higher in the Early Jur-assic and Early Cretaceous, and possibly theMiddle Triassic and Middle Jurassic. However,brachiopods consistently occurred at lower fre-quencies in shales during the Paleogene, Neo-gene, and Quaternary, as compared withbivalves.In level-bottom carbonate habitats, brachio-

pods tended to be overrepresented in coarser-grained packstone and grainstone carbonatesediments in the Late Jurassic, Paleogene, Neo-gene, and Quaternary, and therefore underre-presented in finer-grained wackestone, limemudstone, marl, and chalk (Fig. 7A). The pro-portion of brachiopod occurrences in coarser-grained carbonates was similar to that ofbivalves during most other time intervals,although brachiopods were underrepresentedduring the Middle Triassic. There was less dif-ference in frequency in reef habitats relative toall carbonate occurrences; brachiopods andbivalves had occurred at similar frequenciesin most time intervals (Fig. 7B). The most not-able trend is an increasingly strong under-representation of brachiopods during theNeogene and Quaternary, largely driven by asubstantial proportion of bivalve carbonateoccurrences deriving from reef collections.Glauconite-bearing siliciclastics are more

likely to represent firm substrates during sedi-ment starvation, but brachiopods were onlyoverrepresented relative to bivalves duringthe Late Jurassic and the Late Cretaceous, andunderrepresented in the Paleogene (Fig. 8). Bra-chiopods and epifaunal bivalves had similarprevalence in glauconitic siliciclastics during

FIGURE 4. Proportion of rhynchonelliform brachiopodoccurrences in carbonate lithologies, normalized by sub-tracting the proportion of all marine invertebrate occur-rences in carbonate lithologies. During the late Paleozoic,rhynchonelliform brachiopods occurred in carbonatesabout as frequently as marine invertebrates as a whole,but brachiopods tended to occur in carbonates muchmore frequently from the Triassic to the Paleogene. Abbre-viations: D, Devonian; C, Carboniferous; P, Permian; Tr,Triassic; J, Jurassic; K, Cretaceous; Pg, Paleogene; Ng,Neogene.






the Early Cretaceous, and glauconite was anextremely rare adjective in Paleobiology Data-base collections from the Late Triassic through

Middle Jurassic and in the Neogene and Qua-ternary. Finally, ferruginous carbonates mayalso be more likely to represent sediment star-vation and hardground development, and bra-chiopods may have been overrepresentedrelative to epifaunal bivalves in those environ-ments. Although ferruginous carbonates arerare in Paleobiology Database collections, bra-chiopods were overrepresented in the LateCretaceous and Early Jurassic, and especiallyduring the Middle Jurassic and Early Cret-aceous (Fig. 8). However, during the Late Juras-sic and Paleogene, brachiopods were insteadunderrepresented in ferruginous carbonatesrelative to epifaunal bivalves.

Terebratulide Morphology.—Larger terebratu-lide species (>10mm) with abraded beaksoccur at positive PC 1 values on the morpho-space (Fig. 9). PCA loadings indicate thatthese species are characterized by a smallumbo curvature (beak angle), indicating a sub-erect or even straight beak, and that they alsotend to have larger foramenwidths. In contrast,terebratulides with posterior shell thickeningtend to occur at negative values of PC 1, but

FIGURE 5. Proportional abundance of rhynchonelliform brachiopods in Permian–Cretaceous bulk-sampled assemblages,binned at series level. Circles show proportions for individual assemblages (carbonate in gray; siliciclastic in black), withlarge square symbols indicating the mean proportion by lithology. Rhynchonelliform brachiopods were very rare in silici-clastic assemblages beginning in the Late Triassic, but remained moderately abundant in carbonate assemblages until theMiddle Jurassic.

FIGURE 6. Proportional occurrence of rhynchonelliformbrachiopods and epifaunal (pteriomorph) bivalves inshale, mudstone, or claystone lithology relative to all silici-clastic occurrences, binned by Middle Triassic–Quaternaryseries/periods. The gray line shows a 1:1 trend.






overlap with abraded species at intermediatePC 1 and high PC 2 values. Species with largerumbo curvature are likely to also have posteriorthickening, but thickening can neverthelessoccur in species with suberect to straightbeaks. PCA loadings indicate that specieswith posterior thickening also tend to havemoderate to small foramen widths and lowbeak heights. Finally, species with a labiate for-amen typically occupy an intermediate regionof the morphospace, overlapping with theother two groups at higher PC 2 values butpositioned between abraded and posteriorlythickened species at low PC 2 values. Overall,the PCA results highlight a shift from abraded,through labiate, to posteriorly thickened spe-cies along the PC 1 axis. The trend is present,although with greater overlap among all threegroups, in species with smaller height/lengthratio (lower shell convexity or a more

compressed shape, at higher PC 2 values).However, separation between the three groupsis clearest at negative PC 2 values in specieswith a greater height/length ratio (greatershell convexity or a more inflated shape).During the Early and Middle Jurassic, tereb-

ratulides typically occupied a narrow range inthe central part of PC 1, but a broad rangeacross PC 2 (Fig. 10). A few species exhibitedposterior shell thickening, while only one inthe dataset had an abraded beak. In contrast,species with a labiate foramen were common,particularly in the Middle and Late Jurassic.The centroid in each interval was located atnegative PC 1 and PC 2 values. Between theLate Jurassic and Paleogene, the terebratulide

FIGURE 7. Proportion of brachiopod and epifaunal (pterio-morph) bivalve carbonate occurrences that are in (A)coarser lithologies (packstone and grainstone), and (B)reef environments. The gray lines show 1:1 trends.

FIGURE 8. Proportion of brachiopod and epifaunal (pterio-morph) bivalve siliciclastic occurrences that are from glau-conitic clastics (A) and proportion of carbonateoccurrences that are from ferruginous carbonates (B). Thegray lines show 1:1 trends.






centroid shifted to higher PC 1 and PC 2 values,indicating a transition to smaller height/lengthvalues (lower convexity), and straighter beaks.Overall, beak height and pedicle foramenwidth did not change substantially. However,species with higher beaks and larger foramenwidths tended to have a more incurved umboin the Jurassic, but had a straighter umbo inthe Cenozoic. Shell width/length variedalong PC 3, but there were no temporal trendsin that trait. Although the centroid shifted onaverage to higher PC 1 values, terebratulidesexpanded their morphology both to higherPC 1 values (including species with abradedbeaks) and to lower PC 1 values (more specieswith posterior shell thickening). Althoughmicromorphic brachiopods with a large pedicleforamen and abraded beak were already com-mon in the Cretaceous, larger species withabraded beaks became particularly commonbeginning in the Paleogene.

Rhynchonellide Morphology.—Few rhyncho-nellide species in the dataset are described aspossessing shell thickening (four species) or alabiate foramen (one species), and nonehad an abraded beak. Given the small samplesize, it is difficult to determine whetherrhynchonellides and terebratulides had a simi-lar relationship between shell morphology and

those traits. However, three of the species withshell thickening had small foramen widths andbeak heights, and all four had greater thanaverage umbo curvature (Figs. 11, 12).During the Early Jurassic through Late Cret-

aceous, many rhynchonellide species occupiedthe lower left quadrant of the PC 1 versus PC 2morphospace, indicating more globose shellswith higher width/length and height/length

FIGURE 9. Principal component analysis (PCA) of Jurassic–Quaternary terebratulide shell morphology, based on beakangle (ba), foramen width (fw), beak height (bh), and shellwidth/length (WL) and height/length (HL, or convexity)ratios. Open symbols indicate species with posterior shellthickening; gray symbols indicate species with a labiate ped-icle foramen; and solid black points indicate species with anabraded or eroded pedicle. Gray points without a bordershow species that lack any of those three characteristics.

FIGURE 10. Principal component analysis (PCA) of Jurassic–Quaternary terebratulide shell morphology, based on beakangle (ba), foramen width (fw), beak height (bh), and shellwidth/length (WL) and height/length (HL, or convexity)ratios, and grouped by Mesozoic series and Cenozoic period.Open symbols indicate specieswith posterior shell thickening;gray symbols indicate species with a labiate pedicle foramen;and solid black points indicate species with an abraded oreroded beak. Gray points without a border show speciesthat lack any of those three characteristics. Thewhite polygonindicates the morphospace range occupied by species withposterior shell thickening; the gray polygon indicates themor-phospace range occupied by species bearing an abraded beak.Larger squares are the centroids for each time period.






ratios and smaller beak heights and foramenwidths (Fig. 11). In contrast, that region of themorphospace was nearly empty in the Paleo-gene, Neogene, and Quaternary, similar to theshift to species with narrower and less-inflatedshells among terebratulides. Rhynchonellidesalso exhibited a shift toward straighter beakson PC 3 (Fig. 12), driven primarily by a decreasein forms with larger beak curvature. However,rhynchonellides only moved slightly towardhaving a longer beak or a larger pedicle for-amen, shown best by a shift toward more

positive PC 1 values (Figs. 11, 12). Althoughthe average shift was small, species with alarge foramen width and tall beak tended tohave a more incurved umbo in the Early andMiddle Jurassic, but a straighter umbo in theCenozoic. Despite that, no rhynchonellide spe-cies in the database had an abraded beak, incontrast with the abundance of terebratulideswith abraded beaks during the Cenozoic.Whereas terebratulides evolved into newareas of the morphospace, especially with thedevelopment of forms with a large pedicle

FIGURE 11. Principal component analysis (PCA) of Juras-sic–Quaternary rhynchonellide shell morphology (PC 1vs. PC 2), based on beak angle (ba), foramen width (fw),beak height (bh), and shell width/length (WL) andheight/length (HL, or convexity) ratios, and grouped byMesozoic series and Cenozoic period. Open symbols indi-cate species with posterior shell thickening; gray symbolsindicate species with a labiate pedicle foramen (no specieshad an abraded or eroded beak). Gray points without a bor-der show species that lack any of those three characteristics.Larger squares are the centroids for each time period.

FIGURE 12. Principal component analysis (PCA) of Juras-sic–Quaternary rhynchonellide shell morphology (PC 1vs. PC 3), based on beak angle (ba), foramen width (fw),beak height (bh), and shell width/length (WL) andheight/length (HL, or convexity) ratios, and grouped byMesozoic series and Cenozoic period. Open symbols indi-cate species with posterior shell thickening; gray symbolsindicate species with a labiate pedicle foramen (no specieshad an abraded or eroded beak). Gray points without a bor-der show species that lack any of those three characteristics.Larger squares are the centroids for each time period.






foramen and abraded beak, Cenozoic rhyncho-nellides instead occupied a subset of the mor-phological range found in Jurassic species.

Discussion

Did Brachiopods Preferentially Shift to FirmerSubstrates?—Occurrence and within-collectionabundance patterns, both overall and relativeto epifaunal bivalves, imply that brachiopodslived preferentially in carbonate lithologiesduring the Mesozoic, especially the Jurassicand Cretaceous. Global occurrence patternsare more difficult to interpret, but brachiopodswere more common constituents of bulk-sampled carbonate assemblages during muchof the Mesozoic (Fig. 5). But did their prefer-ence occur because of the firmer consistencyof carbonate substrates? Substrate consistencyis controlled by many parameters but, com-pared with siliciclastics, carbonates tend to bemore prone to early diagenetic cementation,especially in tropical settings and when sedi-mentation rates are slow (Purser 1969; Smithand Nelson 2003). Although firmgrounds candevelop inwinnowed fine-grained siliciclastics,and carbonate sediments can also become softor soupy, on average carbonates should pro-vide firmer substrates for sessile benthicorganisms. Late Triassic and Early Jurassic bra-chiopods could be abundant even in fine-grained carbonates (Fürsich et al. 2001; Toma-šových 2006), but later Jurassic and Cretaceousbrachiopods were often reported at firm-grounds or hardgrounds (Eyers 1992; Ruffelland Wach 1998) and other firmer substratetypes (coarser-grained shallow-water facies,hard reef substrates, or highly glauconitic andcondensed sections), and could be rare in finer-grained and likely softer offshore facies (Ager1965; Owen 1978; Alméras and Moulan 1983).Hardgrounds are not consistently reported inthe taxonomic literature and therefore are prob-ably underrepresented in the PaleobiologyDatabase, but brachiopods do not exhibit con-sistent overrepresentation in ferruginous carbo-nates (Fig. 8), which may often be associatedwith sediment starvation and possibly firm-grounds and hardgrounds. Likewise, brachio-pods are overrepresented in glauconiticsiliciclastics, possibly representing sediment

starvation and firmer substrates, but only insome intervals (Fig. 8). Brachiopods are alsogenerally not overrepresented in reef collec-tions relative to epifaunal bivalves (Fig. 7), des-pite reefs providing abundant hard substratesand despite brachiopod genera preferentiallyoriginating in reef habitats (Kiessling et al.2010). This is not the expectation if substratewas a strong influence on brachiopod habitats,although the discrepancy may have beencaused more by preferential data entry of reef-associated bivalves in the Neogene andQuater-nary, as brachiopods occur frequently in reefcollections in an absolute sense during thoseintervals (14% of carbonate collections in theQuaternary and nearly 22% in the Neogene).However, the preferential occurrence of bra-chiopods in coarser-grained packstones andgrainstones in the Cenozoic is consistent witha substrate firmness prediction.Although brachiopods were overrepresented

in Mesozoic carbonates, most Neogene andQuaternary brachiopod occurrences in thePaleobiology Database are instead from silici-clastic substrates. Those siliciclastic occurrencespartly reflect extensive sampling of predomin-antly siliciclastic European localities, but thereis still little evidence for a carbonate lithologicpreference even after normalizing to the overalldistribution of lithologies (Fig. 4). Does thisimply that substrate had ceased to influencebrachiopod habitat by the Neogene, despitehigh bioturbation intensity that was presumablycomparable to the modern? Although brachio-pods commonly occurred in siliciclastic collec-tions in the Paleobiology Database during theCenozoic, those occurrences are nearly exclu-sively from coarse-grained, often gravel, sub-strates. The underrepresentation of brachiopodsin finer-grained shale, mudstone, and claystonelithologies (Fig. 6) is consistent with the rarityof extant brachiopods in mud-dominated habi-tats (Tomašových and Kidwell 2017) and sug-gests that similar substrate constraints operatedduring the Cenozoic. Many Neogene and Qua-ternary brachiopod occurrences also come fromtemperate latitudes, where early diagenetic lithi-fication would have been less prevalent com-pared with tropical sites (Smith and Nelson2003), potentially reducing substrate differencesbetween carbonates and siliciclastics. Finally,






reduced lithologic preference in PaleobiologyDatabase data may also reflect the abundanceof micromorphic and other small brachiopodssuch as Terebratulina,Argyrotheca,Megerlia,Mega-thiris, and Joania (accounting for 30% of Neo-gene–Pleistocene occurrences) that were able toattach to shell fragments, rocks, or other hardsubstrates, or even to other brachiopods (Thom-sen 2005), increasing their ability to live on silici-clastic or other soft substrates.Although not all substrate indicators fully

align with the habitat preference hypothesis,we argue that the preponderance of evidencesupports a role for changing substrate in thegradual decline of brachiopods. Inconsistentor equivocal relationships tend to occur inrare lithologic categories (e.g., ferruginous orglauconitic sediments) that have small samplesizes and are less likely to be consistentlyreported in taxonomic papers. In contrast, pat-terns from broader lithologic categories that aremore widely reported and have larger samplesizes, such as carbonates/siliciclastics andmudstones/shales, largely support the ideathat expansion of softer substrates increasinglyexcluded brachiopods during the late Mesozoicand Cenozoic.

Potential Effects of Predation.—Increased dur-ophagous predation was also a major macro-evolutionary and ecological force during theMesozoic marine revolution (Vermeij 1977,2008; Monarrez et al. 2017). Other sessilegroups, such as stalked crinoids, declined indiversity and shifted to offshore habitats—both potentially consequences of enhanced pre-dation pressure (Bottjer and Jablonski 1988;Gorzelak et al. 2012). The expansion of infaunain multiple groups, ultimately the cause ofincreased substrate disruption during theMesozoic, likely also represents a response topredatory escalation (Vermeij 2008).Mesozoic brachiopods undoubtedly were

affected by enhanced predation, but predationseems like a less plausible explanation for thespecific brachiopod occurrence and abundancedata documented here. Predatory escalation isthought to have been more pronounced in pro-ductive tropical habitats (Vermeij 2008), yetbrachiopods remained more abundant in car-bonates than in siliciclastics during Mesozoic.Carbonate habitats instead may have served

as refugia where brachiopods could persist onfirmer substrates at greater abundances duringthe late Mesozoic. The locally high abundanceof Jurassic–Cretaceous brachiopods in Europealso contrasts with their rarity in North Amer-ica (Ager et al. 1963; Steele-Petrović 1979),even though both regions occupied similarsubtropical latitudes more consistent withsubstrate differences than with predatory escal-ation. European Jurassic localities often con-tained thin or condensed sections, favoringfirmground or hardground development thatprovided suitable brachiopod habitat (Purser1969; Eyers 1992; Ruffell and Wach 1998),whereas higher sedimentation rates in muchof the North American Mesozoic might haveled to fewer firmgrounds or hardgrounds,thus potentially rarer or more localized bra-chiopod occurrences.

Did Morphology Respond to Changing Sub-strate?—Morphology reflects multiple selec-tive factors, along with constructional andevolutionary constraints, but Mesozoic andCenozoic brachiopods exhibited shifts in traitsthat relate to substrate attachment. Overall,many Jurassic terebratulides occupied regionsof the morphospace distinct from their Ceno-zoic counterparts (Fig. 10), with a combinationof more strongly incurved beaks, larger pedicleforamen openings and beak heights for a givenbeak curvature, and greater shell convexity.Rhynchonellides underwent a similar but lesspronounced shift, also exhibiting more convexshells and greater beak curvature in the Jurassiccompared with the Cenozoic (Fig. 11). Amongterebratulides, the morphological shift wasaccompanied by an increase both in the fre-quency of species with abraded beaks and inthe frequency of species with posterior shellthickening, while a greater proportion of Meso-zoic species had a labiate pedicle foramen.Together, these trends are consistent withincreasing specialization for substrate attach-ment, both closer attachment to hard substrates(straighter and abraded beaks with larger for-amen widths) and adaptations for free-lyinghabits (posterior shell thickening and, in somecases, an incurved umbo with tiny pedicleforamen).However, rhynchonellides underwent less

pronounced morphological shifts compared






with terebratulides, despite exhibiting similartypes of shape change. Rhynchonellides alsotended toward lower shell convexity andstraighter beaks, but none of the Cenozoic spe-cies in the dataset had abraded beaks, eventhough some (e.g., Notosaria nigricans) attachto rock substrates (Lee 1978). The weakerresponse of rhynchonellides could cast doubton the generality of substrate change as amacroecological and macroevolutionary dri-ver. However, rhynchonellides also decreasedfrommore than 40% of brachiopod occurrencesin the Early and Middle Jurassic to only 10% ofCenozoic occurrences (Fig. 13). This dispropor-tionate decline is consistent with the import-ance of substrate, where more pronouncedmorphological shifts among terebratulidesmade that group less susceptible to substratedisruption, while rhynchonellides failed torespond to the same degree and declined inimportance.Many Jurassic brachiopods had morpholo-

gies that are rare or absent among Cenozoicand extant species, most notably highly

biconvex forms with long, incurved beaks andlarger pedicle foramen widths. If substrateattachments played a role in the functionalmorphology, what life habit does that suggestfor these non-analogue forms? Their morph-ology differs from extant free-lying Neothyrisor Anakinetica, suggesting a different attach-ment strategy. Many extant brachiopodsinhabit unconsolidated substrates, but attachvia pedicle to shell fragments, small rocks, orother hard surfaces (Richardson 1981b) orsometimes to tiny grains when the pedicledivides into small rootlets (Rudwick 1961).However, these species tend to be more convexand have straighter and shorter beaks than Jur-assic non-analogue forms. Extant species canalso live attached to larger rock outcrops (Rich-ardson 1981b)—even the characteristically free-lying Neothyris can occasionally be foundattached to rock walls (Chapman and Richard-son 1981). In the extant Magasella sanguinea,populations on unconsolidated substrateshave greater shell convexity (Richardson et al.2007). Given that, the greater convexity typical

FIGURE 13. Proportion of all brachiopod occurrences that belong to the order Rhynchonellida, grouped by series in theJurassic and Cretaceous and by period in the Cenozoic.






ofmany Jurassic forms could be consistent witha primary life habit on firm-substrate habitats,rather than the flexible strategy of modern bra-chiopods that often attach to hard substrates.These morphologies may have maintainedpedicle attachment throughout some of theirontogeny, as suggested by the more frequentoccurrence of large foramen sizes and labiatepedicles, but many may have shifted to anunattached life habit resting on and supportedby the more stable substrate (e.g., Manceñidoand Walley 1979; Feldman et al. 2015) Aninflated shape may have helped to elevate thecommissure above the seafloor even if theshell was primarily supported by resting onthe sediment, analogous to the reclining life-style of similarly shaped gryphaeid bivalves(LaBarbera 1981) and other iceberg strategists(Thayer 1975). Like the gryphaeids, these non-analogue brachiopod morphologies may havedisappeared largely as a consequence ofenhanced bioturbation that disrupted the sub-strates and restricted the surviving taxa to cer-tain habitats and specialized adaptations.

Conclusions

Overall, the occurrence and morphologicaltrends imply that bioturbation-driven substratechanges could have been a major contributorto the Mesozoic–Cenozoic decline of brachio-pods. After living in nearly all habitats in thePaleozoic, Mesozoic brachiopods initiallybecame excluded from siliciclastic environ-ments, especially those with fine grain size,and disproportionately occurred in carbonatelithologies that may have provided firmer sub-strates. There are no clear substrate preferencesin rare lithologies, such as glauconitic or ferru-ginous substrates or reef habitats, but amongmore widely reported lithologies, brachiopodsbecame more common in coarse-grained carbo-nates and rare in fine-grained siliciclastics. Bythe Neogene, brachiopods typically occurred ingravelly siliciclastics, coarse carbonates, andreef habitats, similar to their extant distribution.This represents a significant reduction in habitatavailability, which would have contributed tothe gradual decrease in both diversity and abun-dance since the Early Jurassic.

At the same time as bioturbation likelyrestricted habitat availability for brachiopods,many species, especially among terebratulides,underwent morphological shifts consistentwith changing attachment strategies. Highlyconvex forms in the Jurassic may have partiallyrested on firmer seafloors, but declined andwere replaced by Cenozoic species withabraded or eroded beaks implying attachmentto hard substrates. Rhynchonellides exhibitedsimilar but much less pronounced morpho-logical shifts, and as a result declined dispro-portionately in abundance and diversityrelative to the more successful terebratulides.Although a few brachiopods became adaptedfor a free-living lifestyle and others shifted tolive on hard substrates, the limited availabilityof such substrates contributed to the declineof brachiopods since the Jurassic.The decline in brachiopod diversity and abun-

dance, their near-restriction to hard substrates,and significant shifts in shell morphology weremajor macroevolutionary consequences ofMeso-Cenozoic escalation inmarine ecosystems.Escalation of predatory intensity likely was acontributor, but the occurrence and morpho-logical data also imply a role for substratechanges caused by intensification of bioturb-ation and biological bulldozing.While the initialstep in the demise of brachiopodswas an abruptshock from the end-Permian mass extinction,their final decline was instead a gradual processdriven by biological interactions as increasinglyactive bioturbators transformed the seafloorsinto soft sediments that are largely inhospitableto sessile epifauna such as brachiopods.

Acknowledgments

We thank A. Tomašových, an anonymousreviewer, and Paleobiology editor W. Kiesslingfor valuable feedback. Partial funding wasprovided by the American Chemical Society Pet-roleumResearch Fund, award 54675-ND8. This isPaleobiology Database publication no. 384.

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