Downloaded by guest on September 27, 2021 www.pnas.org/cgi/doi/10.1073/pnas.1717636115 Edie M. Stewart diversity taxonomic major in to losses diversity functional of responses Contrasting ucinldiversity functional loss. future and present, among and past, diversity diversity of functional drivers for taxonomic different consequences in the predict declines help severe can conse- similarly biological contrasting of diversity- strongly aspects quences of reveal different thus operation of biodiversity the analyses of Comparative suggests factors. independent mass two through groups functional the all diversity-dependent almost FE reflect of retention in primarily whereas increase factors, LDG and hypothesize present-day diversity We taxonomic the FE of groups. along in decline functional rise spatial of a rich- the persistence that in functional the resulting in to intensities, declines owing high minor despite only ness of show events extinctions, era-defining and two mass anal- the contrast, the across In , system hemispheres. the model both this of of waters yses polar taxa num- in of even- the functional evenness (FE) maximum the ness in with in groups, decline increase those an a among and distributed by groups the functional accompanied of macroecology, In is ber and trend maximum. macroevolution taxonomic tropical for this its system latitudinal model at the Pacific a is western along , the diversity the hemisphere along from shallow-sea steeply each magnitude where most in of (LDG), gradient poles order diversity an the Novack-Gottshall) nearly M. to Philip by and tropics Bottjer present J. shelf David at invertebrate by reviewed marine declines 2017; benthic 10, October of review diversity for Taxonomic (sent 2017 17, November Valentine, W. James by Contributed and 94720; CA a ucin otnospromneo ri aibe r often are ecological variables of trait framework or common performance a Continuous into function. organisms extant of integration the from and profit can diversity functional dynam- of temporal ics and spatial large-scale of analyses Comparative Diversity Functional of Analyses Comparative two the between declines. outcomes taxonomic and of causes types in illu- differences and significantly the the differ minate reductions, losses diversity diversity severe functional equally of patterns show LDG the extinc- and the tions While the (KPg). (7)—and extinction Eon (PT)— mass Phanerozoic extinction the Cretaceous–Paleogene of mass event in extinction Permian–Triassic diversity largest taxonomic the the in record, drops in fossil temporal seen severe the richness those most taxonomic to the (LDG), in of gradient two pattern diversity spatial latitudinal dramatic the today, most the in sity 4–6). refs. example, (for and implications macroecological macroevolutionary far-reaching changes major have Thus, can 109). diversity p. functional those 2, in ref. of function- paraphrases 742 range p. 3, influence and (ref. that ing” value func- traits “the aspects, organismal as and different defined species these be Of can diversity space. bio- tional and of time maintenance and over origin the aspects diversity into other insight novel to provide phylogenetic— relation can and its functional, morphological, of diversity—e.g., analyses of but currency, common B gradient diversity eateto h epyia cecs nvriyo hcg,Ciao L60637; IL Chicago, Chicago, of University Sciences, Geophysical the of Department eew opr elnsi aooi n ucinldiver- functional and taxonomic in declines compare we Here oi ihesa h ee fseiso eu stemost the is genus or Taxo- species of (1). level currencies the or at dimensions richness nomic many has iodiversity c uemo aenooy nvriyo aiona ekly A94720 CA Berkeley, California, of University , of Museum | a,1 aooi diversity taxonomic ai Jablonski David , | asextinction mass a,1 n ae .Valentine W. James and , | latitudinal 1073/pnas.1717636115/-/DCSupplemental at online information supporting contains article This 1 the under Published interest. of conflict no declare authors The University. Benedictine P.M.N.-G., paper. and the California; Southern wrote J.W.V. of University and D.J.B., D.J., Reviewers: S.M.E., and data; analyzed D.J. and S.M.E. iavs hc aebcm oe ytmfrtesuyof study Marine the 14). for system (13, model cooled a and become geologic warmed have through which climate shallowed (12); bivalves, global groups and currently as biological steepened time most diversity have in trends functional trends these latitudinal and strong diversity show taxonomic Both Diversity Functional and Taxonomic environ- : of Modern modes different change. these under biological and of dynamics mental coupling diversity predic- the of our improve evaluating tions richness will taxonomic but currencies with macroevolutionary studied, FE different little and FR been in tem- FGs have trends among relationships spatial of The and metrics). poral FE number the and (see (FE), FR FGs of evenness the definition among functional and taxa (FR), clade, of or paral- distribution richness biota In a decom- by functional 11). be occupied (10, can into diversity time functional over posed diversity, or taxonomic with latitude turnover lel with compositional e.g., macroecologi- communities scales, at of macroevolutionary functioning ecosystem and can in cal and taxa stability related detect distantly thus even among equivalencies are logical 52 Methods). which and (Materials of intervals states, study our functional in mechanisms, possible realized feeding sepa- 567 and comprising generate fixation, (9) motility, which ecospace tiering, for an axes use rate we Here, classi- (FGs). instead “functional are groups” termed organisms categories difficult discrete where are lower-resolution, record, into approaches fossil fied these the However, in apply 8)]. to 5, (3, and rates metabolic [e.g., growth vertebrates and plants extant for emphasized uhrcnrbtos ...dsge eerh ...adDJ efre research; performed D.J. and S.M.E. research; designed J.W.V. contributions: Author b,c,1 ciaoeu [email protected]. or uchicago.edu, owo orsodnemyb drse.Eal ei@ciaoeu djablons@ [email protected], Email: addressed. be may correspondence whom To esgetta h ifrn eairo hs w bio- the two anticipating biota. these today’s in in losses important of impending of be behavior impacts will differing components the diversity that and contrast, suggest this present understanding we We for events. framework func- conceptual extinction all a the virtually survived whereas in categories groups, drop tional functional concomitant of a number shows the one first the Cretaceous–Paleogene extinctions—only and Permian–Triassic the in temporally in and today declines poles to major equator from three func- diversity—spatially capable taxonomic In are behavior. they or find independent we ecological strikingly but tandem, of their in fall or of be rise might to biodiversity also expected of components but two These species, variety. taxonomic tional of as sum such the of units only not consists biodiversity Global Significance hs ra ucinlctgre atr prxmt eco- approximate capture categories functional broad These b eateto nertv ilg,Uiest fClfri,Berkeley, California, of University Biology, Integrative of Department NSlicense. PNAS . aeil n Methods and Materials www.pnas.org/lookup/suppl/doi:10. NSEryEdition Early PNAS | f6 of 1 for

ECOLOGY macroevolution and macroecology (13, 15, 16), today exhibit an ing adaptive breadth in more seasonal climates appears to be 81–98% decline in bivalve from the tropics to the particularly important (18–20). Thus, species in higher latitudes, poles along major coastlines in the shallow sea, depending on the which must endure seasons of low light and primary productiv- tropical starting point (genera show a similar 80–95% decline; ity, must access a larger proportion of available resource types Fig. 1 A and B). Major coastlines show a range of declines in FR than in lower latitudes and so tend to be more gen- from 45% to 70%, and only 19 and 16 of the 48 tropical FGs per- eralized. A reasonable model is that the number of species that sist into the Arctic and Antarctic, respectively (Fig. 1 C and D can be supported declines with increasing latitude as environ- and Fig. S1). This latitudinal drop in the two currencies, which is mental conditions—particularly lower temperatures and higher seen in other marine groups (17), produces a rise in FE at both seasonality—increasingly favor the and maintenance poles (Fig. 1 E and F and Fig. S1). These patterns differ strikingly of a few gluttons over many epicures. from the taxonomic and functional patterns associated with mass Within this general framework relating richness to seasonality extinctions, as discussed below. and its correlates, the poleward decline in the number of FGs The roster of factors hypothesized to shape spatial gradients and the overall drop in FE values are consistent with the “out- in diversity is long (12, 18), involving such multifactorial features of-the-tropics” dynamic observed for bivalve clades over the past as environmental heterogeneities at many scales, thermal and 12 My (21). The highly uneven FR in the tropics reflects varia- trophic settings, stability of many environmental factors, sizes of tion in taxonomic origination rates among lineages in the differ- areas, the sizes and structures of themselves, ent FGs (21), a “supply-side” effect that is increasingly damped in situ evolution, and geographic range shifts into and out of a as taxonomic richness declines toward the poles. Operating in focal region—almost anything capable of affecting patterns in tandem with this effect was extinction among the FGs that were the numbers of taxa or the numbers of their attributes that can present at high latitudes before refrigeration of the poles dur- be counted. Nevertheless, selection for metabolism-based adap- ing the late (22, 23). The independent or combinatory tation to latitudinal differences in temperature and for promot- action of these processes as they unfold within the environmental




Fig. 1. Present-day taxonomic and functional diversity patterns for marine bivalves along the continental shelf (water depths <200 m). Details of the recent marine bivalve dataset are provided in Recent Marine Bivalve Dataset.(A) Taxonomic richness of marine bivalve genera binned into 111-km2 equal-area grid cells (∼1◦ of latitude at the equator). Global genus richness peaks in the Indo-West Pacific and is the location of the strongest latitudinal gradient across north–south coastlines. (B) Integrated occurrences of distinct genera across 1◦ latitudinal bands reveal a broad richness peak within the tropics; species show a steeper gradient peaking at ∼10◦ N. (C) Functional richness, the number of distinct FGs, of marine bivalves per equal-area grid cell (binned as in A) peaks in the Indo-West Pacific, similar to genus richness in A. (D) Integrated occurrences of FGs across 1◦ latitudinal bands show a global increase in FR from the tropics to the poles, with a fully saturated richness spanning nearly the entire tropics and warm-temperate zones. (E) Functional evenness of bivalve genera per equal-area grid cell measured as the inverse Simpson index and normalized by the number of FGs per cell (Materials and Methods; binned as in A). The lowest evenness occurs in the Indo-West Pacific, the region of highest taxonomic and functional diversity. While tropical regions of other coastlines are less even than the Indo-West Pacific, each coastline exhibits an increase in FE from the tropics to the poles. (F) FE increases globally from the tropics to the poles across 1◦ latitudinal bands at both the genus and species levels.

2 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1717636115 Edie et al. Downloaded by guest on September 27, 2021 Downloaded by guest on September 27, 2021 uvvlo l,o l u n Gwudhv nrae Eunder FE increased have ( would scenario FG realistic the one any but but virtually the all with PT, or combined all, the PT, of the surviving survival across fauna estimate extinction robust bivalve genus a the 76% of calculation for the value undermine sam- evenness Triassic and Early preservation the Poor in 2A). (Fig. pling PT the survive pian sizes. sample smaller to number owing total considered the being reducing FGs for except of con- results, Per- change we latest the not the of Accordingly, do to standpoint mian restricted event. the Analyses from PT fauna. PT bivalve final the Guadalupian of Epoch, the biology functional before Guadalupian the My the sider relatively 8 the in of least was picture at virtu- good fauna last both, our or that unperturbed agree losses, poorly authors substantial was all suffering biota ally global already Permian or 260 Late about the sampled Epoch Whether Guadalupian 32). the ear- of (31, an end Ma with the pulses, at distinct 30) severe two (29, lier of prolonged extinction pattern or major a (28) single to brief decline a geologically a from by ranging preceded PT, event the for framed been marine species-level the the to of magnitude today. composition observed in LDG taxonomic comparable the was unprece- sweeping, biota—and in a “background” was change exclude This to event. dented the aim before they just (27). because extinctions lost boundary these genera fauna even the the and marine of near proportion (27), the all 81–85% underestimate be slightly of to (Permian– estimates estimated genera 61–64% are losses bivalve and Species marine Extinction) of 76% Triassic removed which Ma, PT. eras, postextinction first postextinction the with the comparison bin. of narrow time a phylogenetic faunas in a the than last rather from to the event of relative faunas each perspective, the before analyze intervals we measured well-sampled Accordingly, time intensity currency. postextinction extinction any overestimate immediate in to the inven- tend simple from a will recorded these), interval of survivors taxa all many of likely of more tory (or restriction depleted refugia or failure, localized survivors, to sampling Lazarus of or the populations whether preservation local of from Regardless (12 study). derives (26) this of KPg effect the (15 in around 25) families occurs 24, 78 also (7, but of study) PT this the in around families severe 50 particularly is (24); effect events the extinction this from around disappearing My level several for family record even stratigraphic numer- and genus with the effect,” at “Lazarus taxa ous the by by illustrated complicated are issues, extinctions present- sampling mass the of taxonomic the of analyses the Global bivalves separate LDG. the using day to that here applied framework changes analyze functional faunal we and events which the the Eras, in for Phanerozoic notably responsible most are extinctions, that complex major of during inver- diversification marine occurred in the richness since taxonomic in tebrates losses extreme most The Diversity Functional and Taxonomic Boundaries: Era poles. increase the and to FR tropics decrease the to from FE tend will above described template dee al. et Edie fossil the of out drop FGs (35, 25 PT of the 9 biota, of marine studies entire the previous For with 36). consistent largely are fauna results. the alter respec- significantly feeders, not immobile does suspension as (35), taxa semiinfaunal tively these mobile Reassigning and 34). well epifaunal (33, surviving Megalodontidae, the the Alatoconchi- and inferring into the Permian, in the clades, difficulty in tropical lost the dae, extinct reflects two FG in one photosymbiosis of loss or persistence l,o osbyalbtoe ftebvleFsi h Guadalu- the in FGs bivalve the of one, but all possibly or All, have scenarios different problems, sampling severe of Because h tblt fF n nerdices nF ftesurviving the of FE in increase inferred and FR of stability The h otsvr hnrzi vn a h Taot252 about PT the was event Phanerozoic severe most The i.S2 Fig. B and .Teambiguous The C). h D ntxnmcrcns n Rcntu eattributed be thus can FR and richness taxonomic general- in more LDG 20). require (16, The taxa that fewer accommodates which conditions function, ecological to ized adapting by pro- primary ductivity and climate, seasonality, in gradients environmental functional and taxonomic systems. regulate marine differen- that in to diversity factors related the directly of We effects reason. are tial one patterns than these more for that conse- increase hypothesize functional can different FE that radically and have quences sur- billion can 0.5 fauna loss past bivalve taxonomic magnitudes the similar of the that of suggest in extinctions patterns contrasting mass FGs These greatest . the the of of LDG, all, two modern vived nearly the or along all, richness the whereas taxonomic with concert in indepen- in reduction lost func- strikingly great are and groups taxonomic of Functional common framework. a capable tional in are analyzed curren- when diversity behavior different dent the biological that of show cies here documented patterns The Boundaries Era the and Across LDG Diversity Functional of Responses contained Contrasting that groups for even and LDG, PT taxa. the few the with across compared completely KPg eradicate (Fig. to PT difficult the remarkably of likely level FE the and lost, to S2F are not FGs the although of significantly, this 30) increased of that (2 7% in assuming only record (44)], Even Crimea a discounting (34). [and clade, photosymbiotic Hippuritida) was photosymbiotic clade (order potentially large-bodied, the a entire of the pretation to relative losses estimate across changes we FE so Cenozoic. and and effect FR boundary, Lazarus of a the calculations Paleogene creating direct (26), earliest impeding sampled the poorly and (43); more which be globally ), to sampled (the tends well relatively Cretaceous bivalve the final is use we the Here of loss. survival taxonomic fauna FG large-scale of of generality face the the for in test additional useful a provides (n FGs more were there extinction; genus (64% KPg. tem- among patterns. taxo- comparisons spatial and and direct functional poral allowed consistent that a framework apply nomic to both us in present permitted group present-day major settings to single a relation on its Focusing of and trends. diversity response and PT the extinction the across the in diversity of functional ambiguity effects created assess defined; to intervals were used FGs rediversification measures the the how in in and resolution; taxonomic 235). p. and 37, poral, (ref. taxa” individual few a post by “each only ecosys- ship: a but postextinction manning occupied, crew of was skeleton a status of 37. that functional to ref. the likened tems PT of with the that across 41), increase and 38, an find ours (37, ele- also above FE which addressing loss studies effects, few FR The Lazarus of or estimates did phylogeny their but vated account here, used into that take to not classification functional 40) similar (39, a analyses genuine other used both The to effects. sampling owing and loss variation FR spatial of estimates elevate more to tend a that attributes would used two and (10), ages classification functional different subdivided stud- of finely faunas other Triassic Permian in four single and a seen involved fauna (38) were analysis FR one However, in (38–40). when ies declines substantial the account More through into taken (37). persisted is boundary one, the but across continuity all phylogenetic or all, but record, rmtetoist h oe,tebvlefuarsod to responds fauna bivalve the poles, the to tropics the From inter- the on depends lost FGs of number the PT, the in As tem- spatial, in differences the studies, these of all Among .Uigti igefaeok ecnld htFswere FGs that conclude we framework, single this Using ). h P a essvr hnteP o aiebivalves marine for PT the than severe less was KPg The .Ti asetnto thus extinction mass This 2B). (Fig. 30) = ,but Extinction), Cretaceous–Paleogene NSEryEdition Early PNAS | f6 of 3

ECOLOGY A Permian (Guadalupian) Fauna BCretaceous (Maastrichtian) Fauna 60 60 50 * FG possibly extinct 50 40 genus body size 40 30 median body 30 size for FG 20 20 10 * 10 0 * * 0 5 1 3 6 8 9 4 3 1 5 9 6 8 2 4 17 26 11 49 33 21 19 39 40 32 51 14 49 16 33 11 10 17 13 50 21 27 19 18 23 28 26 38 52 25 29 40 500 500 250 C D 250

(log-scale)100 Genus Richness 100 2 50 50 25 25 10 10 5 5 Body Size mm 5 1 3 6 8 9 4 3 1 5 9 6 8 2 4 17 26 11 49 33 21 19 39 40 32 51 14 49 16 33 11 10 17 13 50 21 27 19 18 23 28 26 38 52 25 29 40 Functional Group Code

Fig. 2. Genus richness of FGs and maximum recovered body sizes of genera from the Guadalupian epoch of the Permian (∼272–260 Ma) and the Maas- trichtian stage of the Cretaceous (∼72–66 Ma). See Table S1 for FG codes plotted along the x axis. Details of the fossil marine bivalve datasets are provided in Era Boundaries Marine Bivalve Dataset.(A) The FE of the Guadalupian fauna was 0.38, similar to the temperate latitudes in today’s diversity gradient. The FG 49 marked as possibly extinct reflects the potential photosymbiosis in the Alatoconchidae (33). (B) The Maastrichtian fauna had 13 more FGs than the Guadalupian, but the FE was very similar at ∼0.39. FGs 49 and 50 marked as possibly extinct reflects uncertainty on photosymbiosis among “rudists” (order Hippuritida) (34, 42). (C) Low-richness Guadalupian FGs contained genera with similar body sizes to the median values of the high-richness genera. (D) As in the Guadalupian, low-richness Maastrichtian FGs were of a similar large-body size to those genera in the high-richness FGs. We did not include body sizes of the FGs composed of exclusively rudist taxa (FGs 49–51), which were known to range in size from a few cm to >1 m in length (42).

to diversity-dependent factors, i.e., those arising from resource “Preadaptation.” The survival of all FGs could reflect the exis- limitation. When conditions disfavor resource partitioning, e.g., tence, within each FG, of taxa that can tolerate the combination under highly variable or seasonal resources, taxonomic diversity of adverse conditions that drove the extinctions. We then might is relatively low, whereas greater resource stability accordingly expect the low-richness FGs to occur, before the extinction, in permits greater partitioning and thus higher taxonomic diversity marine settings where they were “preadapted” to the extinction (9, 45). Of the 26 FGs that occur in the tropics but are absent drivers. That is, few species could tolerate the environmental con- at the poles today, 2 are photosymbiotic and thus probably not ditions of the PT or KPg, but those conditions did not impose viable there given the annual solar cycle, and 17 belong to a sin- selection on the biota along the functional categories used here. gle trophic category, phytoplankton suspension feeding, and so For example, perhaps each FG contained taxa that were relatively are subject to resource limitation in the highly seasonal Arctic robust in pH buffering capabilities or had relatively efficient res- and circum-Antarctic waters. If the trophic dimension were the piratory physiology. To test this interpretation, a more direct win- key diversity-dependent factor, we would expect the exclusion of dow into the paleophysiology of fossil invertebrates is needed to taxa, as in the Arctic, to focus on the feeding axis and to be unse- go beyond the broad-brush inference from extant members at the lective with respect to the other functional attributes, i.e., mobility level of taxonomic class applied to date (46, 47). and substratum relationships, and this appears to be the case (21). In contrast, the PT and KPg events were remarkably indiffer- Asymmetric Functional Selectivity. The mass extinctions might ent to the ecological adaptations encoded in our FGs. Taxonomic have directly disfavored the richest FGs and favored or were neu- diversity was severely reduced but all or nearly all of the func- tral to taxon-poor FGs. For both extinctions, the low-richness tional categories persisted. Such discordance between taxonomic bivalve FGs overlap along all four functional axes with the high- and FR is inconsistent with the factors implicated in the LDG richness groups (both sets include burrowers, suspension feed- such as seasonality and levels of trophic resources (reviews in ers, attached forms, etc.; Fig. 2 A and B). Thus, the selectiv- refs. 18 and 20). Instead, the biotic patterns associated with the ity in this scenario would have to operate on biotic attributes mass extinctions suggest the operation of diversity-independent not incorporated in the scheme used here or on specific com- factors—that is, factors such as temperature that are not parti- binations in a trade-off effect. For example, the eight FGs that tioned by individuals, populations, or taxa (9), although they can are taxon poor in the Guadalupian, and thus are most likely partially govern other factors, such as productivity in the case of to have been lost entirely under adverse conditions, include temperature, that are diversity dependent. Diversity-independent relatively energy-intensive lifestyles such as boring into hard factors have been hypothesized as key drivers for the PT and substrata or short-burst swimming and body sizes comparable KPg events, albeit with different triggers, such as sudden tem- to those seen in the taxon-rich FGs (Fig. 2 A and C) (35). perature perturbations, elevated pCO2, and ocean acidification The same characteristics apply to the Maastrictian fauna as (40, 46–48). well, where the low-richness FGs include large-bodied burrow- Although the operation of diversity-independent factors can ers and suspension feeders (Fig. 2 B and D). Thus, FG survival explain why FGs were not selected against during the PT and is not obviously associated with small body sizes or low-energy KPg, it does not necessarily account fully for the survival of low- lifestyles. richness FGs in the face of such high overall extinction intensities. We can list four hypotheses and potential tests for the seemingly Special Case of Diversity Dependence. The PT and KPg drivers disproportionate survival of FGs. Testing any of these scenarios, were actually diversity dependent, but only within FGs. That or combinations thereof, for the two era-defining events of the is, every FG remained viable under extinction conditions, but Phanerozoic—and in other situations—will be a significant step each could support only a few taxa owing to limited or unsta- toward understanding how specific diversity-independent factors ble resources; this mode of diversity limitation, tightly focused can decouple taxonomic and functional extinction. by FG, is not evident along the modern LDG (22) or along

4 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1717636115 Edie et al. Downloaded by guest on September 27, 2021 Downloaded by guest on September 27, 2021 ihciaecag ie,teciaesit htsae the shaped damped extinction, that of shifts combination a climate via decline the LDG FR [i.e., marine vs extinctions current change con- mass dramatic climate the most across with The constancy spatial FE. FR and of is FR interpretation trast in the dynamics about temporal questions and broader diver- compo- taxonomic raise in two declines sity the major to of diversity responses functional of in nents differences and similarities The Conclusions selectivity. phylogenetic and nar- or ranges, near-exclusive any tropicality, row to near-exclusive owing factors: Hippuritida), these (order of rudists all the extirpation near clade, or single total a the loss of represents the KPg the alataconchids, across Permian FGs the two of with As persist losses. to tend some would all despite they If taxa, 58). wide-ranging (56, few a survival contained FG-specific taxon FGs with or associated often smaller are encountering and refugia of ranges probability geographic the broad increase difficult Alternatively, is biologically. so and interpret Greenland to western to from America and South Europe extinc- northern northwestern lesser to biogeographic Australia defined for from study extending this argued units but (55) (57), analysis poles regional KPg One the the near at scale. tion bivalves (56) marine provincial for or detected been have gia the (47). latitudes harbored high that at filter FGs extinction of an range cur- for full record support Permian no the gives hamper distributions, rently and spatial caution of analyses require robust issues still sampling is poten- effects Although the sampling unclear. within or perhaps Alataconchidae, as photosymbiotic extinction phylo- tially intense a (54), of biota focus global genetic the of homogenization more a spatial this intensity, general extinction Whether in variation (37). spatial extinctions represents distributed pattern mass evenly 52, more both (47, be may following Triassic FR latitudinally observed earliest and the 53), ref. for see low-latitude but hypothesized Severe been identified. been consistent has yet (24), heating be have events refugia extinction would such both biotas no for but global observed effect their Lazarus from the a with FGs harboring of refugia range environmental full or geographical of The existence Size. factors. extinction-resistant other Range on hitchhiked or they because Refugia on Hitchhiking macro- marine among extinction (50), modest (51). most benthos Maximum remarkably the Thermal a but Paleocene– shows at composition, the acidifica- case, atmospheric performed ocean obvious changing be intensifying and/or could warming, (48). global tion patterns KPg of despite nonanalog the episodes persisted, at other similar apparently photosynthesis for FG of inhibition each Tests resources, the over- in for of species the scenarios maintain types one to to the least necessary contributing but at chemosymbionts, intervals, richness, to KPg phytoplankton taxonomic from and in consider- decline PT dropped all the have at may in disappear abundance ably FGs Resource entire (49). where depth gradients, bathymetric modern dee al. et Edie .SesnN,e l 21)Cntnyi ucinlsaears pce richness species a across space functional in Constancy (2016) al. et NG, Swenson pack- 6. and expansion the reveal traits Functional (2016) JA Tobias CH, Trisos AL, Pigot 5. forward. Vill looking and 4. basics to Back diversity: Functional (2006) KJ Gaston OL, Petchey 3. diversity. Functional (2001) D Tilman 2. mismatches and Extensions macroevolution: and interactions Biotic (2008) D Jablonski 1. o h P,weerne ie r etrkon orefu- no known, better are sizes ranges where KPg, the For anomaly. passerine in gradient diversity elevational an birds. underlying space niche ecological of ing geological across biotas marine benthic in time. changes diversity functional reveals niche Lett Ecol 109–120. pp Diego), San demic, levels. and scales across grS oakGtsalP,Mulo 21)Temliiesoaiyo the of multidimensionality The (2011) D Mouillot PM, Novack-Gottshall S, eger ´ clLett Ecol rcRScB Soc R Proc 9:741–758. mNat Am 14:561–568. 187:E83–E92. 283:20152013. Evolution 62:715–739. nylpdao Biodiversity of Encyclopedia G ih aesurvived have might FGs dLvnS(Aca- S Levin ed , 3 rm A(00 vlto ftxnmcdvriygainsi h aieram Evi- realm: marine the in gradients diversity taxonomic of Evolution (2000) JA Crame , gradient: 13. diversity latitudinal the and Evolution (2007) al. et G, diversifi- Mittelbach ecological-functional the 12. Modelling (2012) PM ecological Novack-Gottshall the AM, quantify Bush to ecospace 11. theoretical a Using (2007) PM Novack-Gottshall 10. sdi h grsaedfie in defined are figures the in in Per- used available the are for functional genera Maastrichtian infor- assignments and of missing Functional mian of hierarchy. set extent taxonomic the the common on across depending order, mation most or family the the published for applied attributes previously we lacking information, (iv genera functional For and byssate). deposit/suspension); cemented, (iii photosymbiotic, (unattached, mixed epifaunal); deposit, carnivore, surface nestler, deposit, chemosymbiotic, (i semiinfaunal, subsurface 21: commensal, (suspension, feeding borer, ref. infau- siphonate, of deep/shallow nal siphonate, methodology shallow-infaunal (ii the siphonate, swimming); deep-infaunal following mobile, axes (immobile, mobility functional four across Ecospace. Bivalve Marine Methods and Materials biologi- of currencies diversity. different cal the relating models next of functional the developing generation and for essential taxonomic are here, spatial single provided as a of framework, within analyses patterns temporal Comparative toward and taxa (68–71). of attributes identities and functional numbers recovery the and beyond expanding remediation, accu- are conservation, biotas to and approaches in mulate, alterations irreversible seemingly and as factors, involve diversity-independent to urgency appear and has 67) diversity-dependent (66, decoupled both biota marine be today’s on can Pressures now. diversity functional and onomic infer- misleading 65). strongly 64, to (61, lead ences can application that its temporal show that and so patterns spatial scale, increasing bivalve with the weakens (61–63), extrapolation such situations for proxy conse- some can apparent space in although these time Further, needed. of is scale exploration of that quences along and indicating extinctions mass LDG, the for the true be to appears However, opposite 60). stress- the (59, few predominate a species per- opportunistic and or in drops tolerant decline diversity to taxonomic expected as scales, generally ecosystems local is turbed on FE and events, term pollution short in find the as also In We FE. 22)]. in patterns 16, unexpected (15, immigration damped and origination, eerhFlosi rga n S otrlDsetto Improvement Dissertation S.M.E.). Doctoral (to NSF (DEB-1501880) and Grant Graduate Program the NSF Fellowship and into D.J.) the Research (to thank (EAR-0922156) and entry reviews, (NSF) We (EXOB08-0089) Foundation for Administration Wignall Science Database. for Space National Clapham B. Paleobiology and P. Kidwell Aeronautics M. the sources, National via Chinese and the M. scarce literature stratigraphy, to S. invertebrate Svalbard access Permian and for on Zeng advice Foote H. for and M. Erwin H. suggestions, D. and comments ACKNOWLEDGMENTS. are FE of patterns latitudinal observed the but 21 similar. ref. taxa of that of from (compare gradient distribution differs metric “intuitive the FE single an in a changes provides to using discernable it FGs FGs, maps among because and sample) within by (72) a evenness” taxa normalized in in index FGs of functional Simpson’s of our distribution (inverse number of the the evenness” nature of as discrete measure FE entirely “Simpson’s characterized the we Given place. data, or time given FE. and FR Estimating .EwnD (2006) DH Erwin 7. .VlnieJ (1973) JW gradient. Valentine diversity latitudinal the 9. and space trait Functional (2014) al. et CA, Lamanna 8. ial,adee nesadn fwe n h ossi tax- in losses why and when of understanding deeper a Finally, rcNt cdSiUSA Sci Acad Natl Proc Princeton). Press, Univ (Princeton aino aieMtzao elgcltm scales. time geological on Metazoa marine of cation biotas. marine modern and Paleozoic of diversity NJ). Cliffs, Englewood Hall, ec rmtecmoiino eetbvlefaunas. bivalve recent of composition the from dence biogeography. and extinction xicin o ieo at eryEdd20MlinYasAgo Years Million 250 Ended Nearly Earth on Life How Extinction: vltoayPloclg fteMrn Biosphere Marine the of Paleoecology Evolutionary eetmtdF stenme fdsic G na in FGs distinct of number the as FR estimated We 111:13745–13750. etaktejitDJ–.D rc aoaoyfor laboratory Price D. D.J.–T. joint the thank We easge iav eeat igestates single to genera bivalve assigned We clLett Ecol al S1. Table 10:315–331. i.S1 Fig. irn ifua asiphonate, (infaunal tiering ) Paleobiology n i.1.Ti prahto approach This 1). Fig. and ucinlcodes Functional S1. Dataset ilLett Biol NSEryEdition Early PNAS Paleobiology 8:151–155. 33:273–294. 26:188–214. fixation ) (Prentice- | f6 of 5 ) )

ECOLOGY 14. Powell MG, Moore BR, Smith TJ (2015) Origination, extinction, invasion, and extir- 42. Ross DJ, Skelton PW (1993) Rudist formations of the Cretaceous: A palaeoecological, pation components of the latitudinal biodiversity gradient through the sedimentological and stratigraphical review. Sedimentology Review, ed VP Wright Phanerozoic Eon. Paleobiology 41:330–341. (Blackwell, Oxford), pp 73–91. 15. Jablonski D, Roy K, Valentine J (2006) Out of the tropics: Evolutionary dynamics of 43. Jablonski D (2008) Extinction and the spatial dynamics of biodiversity. Proc Natl Acad the latitudinal diversity gradient. Science 314:102–106. Sci USA 105:11528–11535. 16. Jablonski D, Huang S, Roy K, Valentine JW (2017) Shaping the latitudinal diversity 44. Skelton P, Benton M (1993) : Rostroconchia, Scaphopoda and Bivalvia. The gradient: New perspectives from a synthesis of paleobiology and biogeography. Am Fossil Record, ed Benton MJ (Chapman & Hall, London), Vol 2, pp 237–263. Nat 189:1–12. 45. Valentine JW, Jablonski D, Krug AZ, Roy K (2008) Incumbency, diversity, and latitudi- 17. Stuart-Smith RD, et al. (2013) Integrating abundance and functional traits reveals new nal gradients. Paleobiology 34:169–178. global hotspots of fish diversity. Nature 501:539–542. 46. Knoll AH, Bambach RK, Payne JL, Pruss S, Fischer WW (2007) Paleophysiology and 18. Fine P (2015) Ecological and evolutionary drivers of geographic variation in species end-Permian mass extinction. Earth Planet Sci Lett 256:295–313. diversity. Annu Rev Ecol Evol Syst 46:369–392. 47. Payne JL, Clapham ME (2012) End-Permian mass extinction in the : An ancient 19. Brown JH (2014) Why are there so many species in the tropics? J Biogeogr 41:8–22. analog for the twenty-first century? Annu Rev Earth Planet Sci 40:89–111. 20. Valentine JW, Jablonski D (2015) A twofold role for global energy gradients in marine 48. Vellekoop J, et al. (2014) Rapid short-term cooling following the Chicxulub biodiversity trends. J Biogeogr 42:997–1005. impact at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci USA 111: 21. Berke SK, Jablonski D, Krug AZ, Valentine JW (2014) Origination and immigration 7537–7541. drive latitudinal gradients in marine functional diversity. PLoS One 9:e101494. 49. Rex MA, Etter RJ (2010) Deep-Sea Biodiversity (Harvard Univ Press, Cambridge, MA). 22. Krug AZ, Jablonski D, Roy K, Beu AG (2010) Differential extinction and the contrasting 50. McInerney FA, Wing SL (2011) The Paleocene-Eocene thermal maximum: A perturba- structure of polar marine faunas. PLoS One 5:e15362. tion of carbon cycle, climate, and biosphere with implications for the future. Annu 23. Crame JA, et al. (2014) The early origin of the Antarctic marine fauna and its evolu- Rev Earth Planet Sci 39:489–516. tionary implications. PLoS One 9:e114743. 51. Melott AL, Bambach R (2014) Analysis of periodicity of extinction using the 2012 24. Jablonski D (1986) Causes and consequences of mass extinctions: A comparative geological timescale. Paleobiology 40:177–196. approach. Dynamics of Extinction, ed Elliott DK (Wiley, New York), pp 183–229. 52. Sun YD, et al. (2012) Lethally hot temperatures during the greenhouse. 25. Fraiser ML, Clapham ME, Bottjer DJ (2011) Mass extinctions and changing taphonomic Science 338:366–370. processes fidelity of the Guadalupian, , and early Triassic fossil records. 53. Ramono C, et al. (2017) Marine Early Triassic Actinopterygii from Elko County : Process and Bias Through Time, eds Allison PA, Bottjer DJ (Springer, (Nevada, USA): Implications for the Smithian equatorial vertebrate eclipse. J Pale- Berlin), Vol 32, 2nd Ed, pp 569–590. ontol 91:1025–1046. 26. Sessa JA, Patzkowsky ME, Bralower TJ (2009) The impact of lithification on the diver- 54. Jablonski D (1998) Geographic variation in the molluscan recovery from the end- sity, size distribution, & recovery dynamics of marine invertebrate assemblages. Geol- Cretaceous extinction. Science 279:1327–1330. ogy 37:115–118. 55. Raup DM, Jablonski D (1993) Geography of end-Cretaceous marine bivalve extinc- 27. Stanley SM (2016) Estimates of the magnitudes of major marine mass extinctions in tions. Science 260:971–973. Earth history. Proc Natl Acad Sci USA 113:E6325–E6334. 56. Jablonski D (2007) Scale and hierarchy in macroevolution. Palaeontology 50: 28. Wang Y, et al. (2014) Quantifying the process and abruptness of the end-Permian 87–109. mass extinction. Paleobiology 40:113–129. 57. Vilhena DA, et al. (2013) Bivalve network reveals latitudinal selectivity gradient at the 29. Clapham ME, Bottjer DJ (2007) Prolonged Permian-Triassic ecological crisis recorded end-Cretaceous mass extinction. Sci Rep 3:1790. by molluscan dominance in late Permian offshore assemblages. Proc Natl Acad Sci 58. Jablonski D (2005) Mass extinctions and macroevolution. Paleobiology 31:192–210. USA 104:12971–12975. 59. Gusmao JB, Brauko KM, Eriksson BK, Lana PC (2016) Functional diversity of macroben- 30. Clapham ME, Shen S, Bottjer DJ (2009) The double mass extinction revisited: Reassess- thic assemblages decreases in response to sewage discharges. Ecol Indic 66:65–75. ing the severity, selectivity, and causes of the end-Guadalupian biotic crisis (late Per- 60. Mouillot D, Graham NA, Villeger´ S, Mason NW, Bellwood DR (2013) A functional mian). Paleobiology 35:32–50. approach reveals community responses to disturbances. Trends Ecol Evol 28:167– 31. Stanley SM, Yang X (1994) A double mass extinction at the end of the Paleozoic Era. 177. Science 266:1340–1344. 61. Pickett STA (1989) Space-for-time substitution as an alternative to long-term studies. 32. Bond DPG, et al. (2015) An abrupt extinction in the middle Permian () of Long-Term Studies in Ecology, ed Likens G (Springer, New York), pp 110–135. the realm (Spitsbergen) and its link to anoxia and acidification. Bull Geol Soc 62. Habeeb RL, Trebilco J, Wotherspoon S, Johnson CR (2005) Determining natural scales Am 127:1411–1421. of ecological systems. Ecol Monogr 75:467–487. 33. Asato K, Kase T, Ono T, Sashida K, Agematsu S (2017) Morphology, systematics and 63. Blois JL, Williams JW, Fitzpatrick MC, Jackson ST, Ferrier S (2013) Space can substitute paleoecology of Shikamaia, aberrant Permian bivalves (Alatoconchidae: Ambony- for time in predicting climate-change effects on biodiversity. Proc Natl Acad Sci USA chioidea) from Japan. Paleontol Res 21:358–379. 110:9374–9379. 34. Vermeij GJ (2013) The evolution of molluscan photosymbioses: A critical appraisal. 64. Dobson LL, La Sorte FA, Manne LL, Hawkins BA (2015) The diversity and abundance Biol J Linn Soc 109:497–511. of North American bird assemblages fail to track changing productivity. Ecology 35. Mondal S, Harries PJ (2016) Phanerozoic trends in ecospace utilization: The bivalve 96:1105–1114. perspective. Earth-Sci Rev 152:106–118. 65. Levy O, Buckley LB, Keitt TH, Angilletta MJ (2016) Ontogeny constrains phenology: 36. Erwin DH, Valentine JW, Sepkoski JJ (1987) A comparative study of diversification Opportunities for activity and reproduction interact to dictate potential phenologies events: The early Paleozoic versus the Mesozoic. Evolution 41:1177–1186. in a changing climate. Ecol Lett 19:620–628. 37. Foster WJ, Twitchett RJ (2014) Functional diversity of marine ecosystems after the late 66. Halpern BS, et al. (2015) Spatial and temporal changes in cumulative human impacts Permian mass extinction event. Nat Geosci 7:233–238. on the world’s ocean. Nat Commun 6:7615. 38. Dineen AA, Fraiser ML, Sheehan PM (2014) Quantifying functional diversity in pre- 67. Harnik PG, et al. (2012) Extinctions in ancient and modern seas. Trends Ecol Evol and post-extinction paleocommunities: A test of ecological restructuring after the 27:608–617. end-Permian mass extinction. Earth-Sci Rev 136:339–349. 68. Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: Functional diver- 39. Knope ML, Heim NA, Frishkoff LO, Payne JL (2015) Limited role of functional differ- sity and the maintenance of ecological processes and services. J Appl Ecol 48:1079– entiation in early diversification of animals. Nat Commun 6:1–6. 1087. 40. Petsios E, Thompson JR, Pietsch C, Bottjer DJ (September 12, 2017) Biotic impacts 69. Naeem S, Duffy JE, Zavaleta E (2012) The functions of biological diversity in an age of of temperature before, during, and after the end-Permian extinction: A multi-metric extinction. Science 336:1401–1406. and multi-scale approach to modeling extinction and recovery dynamics. Palaeogeogr 70. Tomasovˇ ych´ A, et al. (2016) Unifying latitudinal gradients in range size and richness Palaeoclimatol Palaeoecol, 10.1016/j.palaeo.2017.08.038. across marine and terrestrial systems. Proc R Soc B 283:20153027. 41. Dineen AA, Fraiser ML, Tong J (2015) Low functional evenness in a post-extinction 71. Perring MP, et al. (2015) Advances in : Rising to the challenges of () paleocommunity: A case study of the Leidapo member the coming decades. Ecosphere 6:1–25. (Qingyan formation), South . Glob Planet Change 133:79–86. 72. Magurran A (2004) Measuring Biological Diversity (Blackwell, Malden, MA).

6 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1717636115 Edie et al. Downloaded by guest on September 27, 2021