http://dx.doi.org/10.18268/BSGM2018v70n1a11 P. 187‒200 VOL. 70NO. 1 BOL. SOC.GEOL.MEX.2018 Netherlands. Bosquetplein 6-7, 6211 KJMaastricht, the Natuurhistorisch MuseumMaastricht, de John Wilhelmus MariaJagt 2300 RALeiden,theNetherlands. Naturalis Biodiversity Center, P.O. Box 9517, WilhelmusBarry Martinus Van Bakel Boxtel, theNetherlands. Oertijdmuseum, Bosscheweg 80, 5283WB Pedro AndradeViegas WilhelmusBarry Martinus Van Bakel [email protected] René HendricusBartholomeus Fraaije Pedro Andrade René Hendricus Bartholomeus morphotypes Mesozoic: abottom-up model to explain new higher-tier invertebrate The rise of a novel, plankton-based marine ecosystem during the Manuscript November accepted: 14,2017 Corrected manuscript received: November 10, 2017 Manuscript received: October20,2017 Viegas Fraaije morphotypes. paleoecology,system, invertebrate Keywords: Mesozoic, marineeco higher-tier trophic levels. different invertebrate groups at a range of of plain the emergence intime and dispersion time, anelaborated bottom-up model to ex to Scaphitoidea. Here we present, for the first nites: from Ancyloceratoidea via Turrilitoidea Schizasteridae) and for ammo heteromorph ( overs are documented for irregular echinoids the raninid morphology. Similarly, coeval turn type,the palaeocorystid via the lyreidid type to (Raninoidia),therea transition from was faunal turnovers. For instance, amongst frog tions and adaptations brought about additional na). DuringtheCretaceous Period newinnova (part of) their food source ( vores, wasintimately linked to the bloom of comprised more complex scavengers/detriti buryingraninoid crabs, which the radiation of ic food particles became available. However, plankton wards, inthat anincreasedof supply direct,was feeders fromthe Late Jurassicon tems. impactondetritus and plankton The Mesozoic ecosys the ‘infill’ of new model of our of the basis form resultantThe histograms available data on their diversitythrough time. vertebrate groupsstudied we have plotted all the in ammonites.heteromorph For each of well nektonic groupsas such asancyloceratine and swimmingcrabsirregular echinoidsas various benthic groups such asburying tion of in the marine water columnled to a prolifera Both directly and indirectly, these radiations Ma) andLate ( time interval between the Late ( the ifera and radiolarians are characteristic of diatoms, dinoflagellates, planktonic foramin such ascalcareous nannofossils, calpionellids, phytoplanktonic andzooplanktonic microbiota Major radiation events amongst a range of ABSTRACT , Barry Wilhelmus, Barry Martinus i.e. , from Toxasteridae via Micrasteridae to Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín i.e. c , marine meiofau . 100–66Ma). c Van Bakel . 160 ------do entre elJurásico Tardío (c. 160Ma)yelCretácico de tiempo comprendifueron característicos del intervalo dinoflagelados, foraminíferos planctónicos y radiolarios, como nanofósiles calcáreos, calpionélidos diatomeas, comprende elfitoplancton y zooplankton, con grupos Los mayores deradiación de lamicrobiota eventos que RESUMEN invertebrados. marino, paleoecología,morfotiposde Palabras clave: Mesozoico, ecosistema tróficos.altos niveles de invertebrados,diferentes enelrango de los más grupos y la dispersión el surgimiento explicar en el tiempo, de primera, unelaborado modelo adetalle, conelfinde Turrilitoidea, Aquí se presenta, a Scaphitoidea. por vez para ammonites heteromorfos, de Ancyloceratoidea, vía de Toxasteridae, vía Micrasteridae, aSchizasteridae), y (i.e., se han documentado para equinoideos irregulares dido), hacia eltipo ranínido. Otros cambios coetáneos ninoidia), entre eltipo palaeocorístido (vía el tipo liréi ejemplo, rana hubo unatransición (Ra en los cangrejos a cambios en composición faunística. Pornes entorno Periodo Cretácico, surgieron innovaciones y adaptacio de) su alimento (i.e., meiofauna marina). Durante el de (oparte ligada íntimamente a laexplosión estuvo comprendía los más complejos carroñeros/detritívoros), raninoidesla radiación infaunales de los cangrejos (que que nutritivas provenientes del plankton, de tal forma rásico Tardío, yaincremento quesedió un de partículas y planctotróficos detritófagos fue directo a partir del Ju de los ecosistemas del Mesozoico. Elimpacto sobre los tituyenla base para modelo de “relleno” nuestro nuevo a través del tiempo. resultantes cons Los histogramas do todos los datos disponibles acerca de sudiversidad deinvertebrados estudiado, hemos grafica cada grupo como los ammonites heteromorfos ancilocerátidos. Para nectónicos tales así como grupos equinoideos irregulares, nicos, infaunales y nadadores, tales como los cangrejos bentó rina llevaron alaproliferación de varios grupos indirecta, dichas ma radiacionesla en columna deagua Tardío (c. 100–66Ma).Tanto directa como de forma , John Wilhelmus Maria /2018 Jagt 187 , ------

Novel invertebrate morphotypes in Mesozoic marine ecosystems ABSTRACT Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION 188 188 1. Introduction Figure 1 Triassicmarine ecosystemwithaphylogenetical et al. be reconsidered following the paper byBrayard the –Triassicextinction mass event has to atardy, notion of low-diversityThe recovery from was no link or overviewlink no was these palaeontological in recorded in considerable detail. However, there al. brachyuran decapod ( lova and Baraboshkin,2009;Lehmann,2015) and (Mikhai ammonoids Smith, 2010),heteromorph 1982; Smith, 1984; David invertebrate groups such asechinoids( Mesozoic evolutionary andadaptive radiations in colithophorids anddiatoms. coc dinoflagellates, photosynthetic of radiations erence producers, to marine primary inclusive of bydiscussed Knolland Follows (2016), with ref predators. Another, coeval, revolutionbeen has durophagous a Mesozoic–Cenozoic radiation of focusedon extinct mainly and observed molluscs ‘the Mesozoic Marine Revolution’.the term He sozoic ( invertebrates in the marine realm during the Me widespread evolutionary changes among benthic as demonstrated below. Toof patterns encompass oped during the Palaeozoic) still had to take place, essential phase(undevelsecond, fauna. A tionary from the Palaeozoic marine evolu to the modern , the transition this was merely the first part of reached not longafter the PalaeozoicEra. How Thus, balance ecosystem and optimisation were to toppredators ducers and potential scavengers. multi-level marine ecosystem, from pro primary ly diverse, functionallycomplex andtrophically / Successive radiations through timewithintheplankton-based Mesozoicfood web. Successive , 2014;Schweitzer Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín (2017).Outline inthat paperanEarlywas ca . 252 – 66 Ma), Vermeij (1987) coined et al ., 2016)have also been et al ., 2009;Kroh and e.g. , Karasawa e.g. , Kier, et ------/2018 1.1. PHYTOPLANKTON studied from the bottom up. Intheir bottom-up semblages, the food web at the time needs to be ecological niches inEarly Cretaceous marine as experienced bloomsand proceeded to occupynew In order why to gauge several invertebrate groups tonic andbenthicinvertebrate groups (Figure 1). olution model from phytoplankton to diverse nek rev marine Mesozoic bottom-up a time, first the presentThe ecosystem. paper demonstrates, for marine modern the of portion important an filled and acoherent marine food chain revolution that studies between the adaptive radiations observed ing inthe Middle ,they rapidly increased cies diversity duringthe Mesozoic. appear First food chain), showed remarkablein spe patterns the protists(single-celled at or near the base of dinoflagellates the group, phytoplankton Another intervalsTithonian–Berriasian (Bown and Early Jurassic Triassic, Late the to confined were above background significantly levels at tion Late Triassic( of strata in appeared first nannoplankton calcareous the biosphere. Coccolithophores andother of higher trophic levels diversity andproductivity of hadanimpactonbio rine and,inturn, system significance as it trackedglobal changes in the ma particular isms. phytoplankton The recordof is extinct marine organ any group of biodiversity of microfossilsprovide the most complete record of andtaxonomically,Stratigraphically planktonic plankton radiation anddiversification (Figure 2). aphyto Mesozoic marinebiota of on the basis mechanismfor the observed evolutionaryin shifts ic oceans, KnollandFollows(2016) provided a perspective on ecosystemchanges inMesozo c 1 a g.Rtso specia . 210Ma)age. Rates of et al ., 2004). ------1.2. ZOOPLANKTON Figure 2 ln,dvriyrs oa l-iepa f584taxa cline, diversityrose toanall-time peak of Kimmeridgian (157–153Ma).After a minorde 420speciesinthe to a Late Jurassic maximum of ( crease from the Tithonian tothe Late Cretaceous abundance and diversity and a phytoplankton in ton ( record there isastrikinglinkbetween zooplank recorded ( responsesto phytoplankton bloomshave been seasandoceansdistinctzooplankton In modern documented (Figure 3). phytoplanktonicdiversity,food been itemshas of a marked increase,and overall bothinnumbers Late Jurassic(Tithonian, 152–145Ma)onwards (Reháková andMichalík, 1997). Thus, from the environments, from the Tithonian to the Albian shaped testsranged, particularly inmore basinal lids.with calcitic, bell- marine organisms These the importance enigmaticcomprises calpionel et al. during the mid-Cretaceous (Albian; seeMacRae e.g. Radiationsof speciesofphotosyntheticcoccolithophorids, and dinoflagellates diatoms(datafromKnoll and Follows,2016). , Erbacher and Thurow, 1997; Premoli Silva 96.Atidgopo pakoi om fof forms planktonic third, 1996).A group of i.e., planktonic foraminifera and radiolarians) e.g. , Atkinson et al. , 1996).Inthe fossil Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín - - - - 1.3. HETEROMORPH AMMONITES ewe h rlfrto fplanktonic groups between the proliferation of the early Paleocene. Although the link the start of the late Maastrichtian (69–66Ma)or the end of early late Hauterivian ( inate in numerous faunal assemblages from the role duringtheearliest Cretaceous, theypredom ammonitesplayWhile heteromorph almost no place. ganisms, collectively known asmeiofauna, to take smallbenthicor available to allow aradiation of food particles were heim, 2005),largeof amounts settings, from the Tithonian onwards( offshore in floor sea the to remains planktonic of the increased, continuous ‘snowfall’ As a result of Radiolaria (Olney, 2002). food for the represented an increased source of have may which dinoflagellates amongst diation ra a with coincided This diversification. rapid a the Jurassic, at which time there was the end of decline until ic, Radiolaria experienced a gradual During the Late Palaeozoic andintothe Mesozo and Sliter, 1999;Bown et al c. 130Ma)onwards, until ., 2004). /2018 e.g. , Rück 189 189 - - - - -

Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION 190 190 fig. 8). Figure 3 into the earliest Paleocene (Landman semblages right uptothe latest Maastrichtian and Middle and Late Cretaceous ammoniteas of twoThese groups remained important elements (Mikhailova morphs 2009). andBaraboshkin, previouslyhad been the predominant hetero which Ancyloceratina the replaced and versified superfamilies Scaphitoidea and Turrilitoidea, di ammonitesthat comprisedthe Ma), agroup of During the Albian (mid-Cretaceous, 113–100 4). ( the waterin the planktonic‘clouds’ within column cyloceratine ammonites that fed directly on and an nektonic foremost, and first were, radiation plankton total the from benefited that vertebrates involved (Lehmann are still debating the diverse ecological constraints quite obvious,appears many ammonite workers / e.g. Radiationofzooplankton (planktonicforaminifera) relatedtotheradiation of phytoplankton(modifiedafter Bown Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín , Mikhailova and Baraboshkin,2009) (Figure et al. , 2015).Larger-sized in et al. , 2014, - - - - - /2018 plankton as discussed herein. the discussed plankton as Understanding newgroupsof with the radiationconjunction of ammonites duringthe Jurassic andCretaceous, in the so-called aptychophoran led to the radiation of thisplankton-feeding strategy appearance of The living by exemplified as floor, ocean the on prey large water rathercolumn, than capturing and eating these ammonites fed in the on smallorganisms remains insidethe buccalmakes it mass likely that possible prey jaws andradula and the presence of the of similar feeding habits. morphology The them had adopted similarity that all of suggests apparatus inthese ammonites have revealed a the buccal Three-dimensional reconstructions of described in detail ( ammonites haveand turrilitoid scaphitoid been In recent years, well-preserved buccalof masses 2015). Nautilus Linnaeus, 1758(Kruta e.g. , Kruta et al. , 2011,2013). et al et al ., 2011). ., 2004, 1.4. IRREGULARECHINOIDS from Rückheim,2005;Mikhailovaand Baraboshkin, 2009). Figure 4 uasc swl steretnto tteedo Jurassic,wellas their asextinction at theendof web providesinto their radiationinsights inthe the newMesozoic theseammonitesin food role of hsagetn h ag fecological niches thus augmenting the range of shoreface environments, and shallow waters of sequently, variouswarm colonised derived forms offshorewere environments.characteristic of Sub representatives ( that interval ( the group during uous developmental trend of Cretaceous Period. Studies have shown a contin entire the during diversification experienced and early Berriasian, Spatangoids (‘heart urchins’)originated during the (Monks, 1999). loceratoidea and the latter from the Turrilitoidea letic group, derived from withthe former Ancy and Scaphitoidea together comprise a monophy have morphology established that Turrilitoidea the ontogeny andsutural Phylogenetic studies of (Kruta the Cretaceous or during the earliest Paleogene Successive radiationintimeof numbers Successive of planktonic foraminiferal genera and ofancyloceratine ammonite families(data et al. , 2011;Landman e.g. , Villier and Eble, 2004). The first first VillierEble, , The and 2004).

i.e. Number of genera / families 10 12 14 16 c. 0 2 4 6 8 145Ma(Masrour pce fthegenus of , species plan et al. k tonic , 2014,2015).

et al. foramin Toxaster , 2004) i fera Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín - - - - ) Age ancyl o h aletmmeso the the earliestof members with adaptive strategies to improve exchange gas – the early each Aptian, shallow waters by the end of al spatangoid throughout ( the Aptian and remained the commonest andmostdiverse late Barremian andearly ( Aptian muchmore diverse andwidespread duringthe the Urgonian facies. margins of logical niches inshallow-water along the platforms ty. neweco coeval was This tothe colonisation of abili burrowing better and exchange gas efficient specialisationsulted from for more morphological western the re success in adaptive Tethys.fied Its the Hauterivian toBarremian, thisgenusdiversi carbonate platforms. From the development of realms and newpalaeogeographical onisation of diversification that can be correlated to the col of Humbert, 1976). orbitoline-rich marls andlimestones(Masse shoreface settingsthat are representedby mainly Tethys Ocean, inhabiting upper offshore and lower the commonest heart urchin along the margins of interval, the genusian-Aptian occupied by spatangoids. Duringthe Hauteriv ce ., 2016). However,2016). ., differentiated in lineages new ra tine

amm o n ites showed several phases Macraster Heteraster Heteraster c /2018 . 126–123Ma) e.g. / , Yavari Douvillaster was the was became 191 191 et ------

Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION 192 192 and ofspatangoid echinoid genera (datafrom Villier Figure 5 and younger Cretaceous spatangoid communities shallow-waterin environments. Late Cenomanian cient structuresfor exchange gas andburrowing effi more evolved that schizasterids diversifying might have been initiated bycompetition with the Schizasteridae – the familiesMicrasteridae, Hemiasteridae and of representatives primitive of differentiation clear a distributed but forms, the Albian was marked by villaster Micrasteridae ( clade ( h eieo demiseof The era time, diversityof became the major spatangoid group. Atthe same manian, the Schizasteridae rapidly diversified and waters. Intheearlyshallow andwarmer Ceno ( shallow-water carbonates, whereas schizasterids cool, to and settings offshore in substrates muddy Hemiasterids ( spatangoid echinoids. groups of modern / Mecaster Successive radiation and peaks in time of numbers of planktonic foraminiferal genera, of ancyloceratine ammonite families foraminiferalancyloceratine ammonite genera,ofplanktonicnumbers of of in time radiation andpeaks Successive Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín Heteraster Number of genera / families and i.e. 10 12 14 16 0 2 4 6 8 , , Periaster Douvillaster convexus and Tithonia Macraster Hemiaster Macraster Epiaster polygonus Macraster Douvillaster plan i.e. and n h aletmmeso all , the earliest of members k remainedwidely themost tonic B ) became specialised to , Polydesmaster e r Douvillaster went extinct.

riasia foramin dropped andthe gen n fthe family ) andof n ). i fera V Heteraster alanginia and ) adapted to et al. Heteraster n s pa , , 2004;Rückheim, 2005;Mikhailovaand Baraboshkin, 2009). Hauter Dou t a ng - - - - /2018 o

i ivia d

echinoids n Age 1.5. MEIOFAUNA B a r remian tine ammonites(Figure 5). planktonicforaminifera and ancylocera bloom of spatangoid echinoids directly followed the ation of plate compounding.time, In theradi adoption of and, hence, pore pair crowding, necessitating the denser tube feet ing required the development of the history in the clade. feed ecological shift to graze This of time first the for feeding deposit During thistime, irregular echinoidsswitched to (Saucède andVillier, 2005). zone ronments, andmicrasteridsinthe mid-shelf hemiasterids in upper offshore and shoreface envi were structured asfollows:schizasterids andsome Today, meiofauna constitutes the most abundant entire lifespan or justtemporarily (Vincx, 1996). meiobenthic representatives, either during their 33animalphyla have manysettings as 23 of as element amongst marine biota – inpresent-day size (42 – 1000 μm). These are the most diversified the benthos, defined by body zoan components of meta ‘meiofauna’ refers to a range of term The ancyl Aptian o ce ra tine

amm Albi o a n n ites Ceno m a ni a n

- - - - - 1.6. RANINOIDIANCRABS and niches to occupy, first in shelf settings and settings later alsoinmore basinalenvironments. shelf in first occupy, to niches and sources food new offered components two these ‘snowfall’ zooplankton. uninterrupted of The of the phytoplankton radiation generated a bloom food. Inshort, ageneral of lack ments becauseof environ offshore inhabit to unable been viously benthicgroupsthat hadpre amongst arange of led toaradiationand increased areal distribution Late Jurassic–Cretaceous plankton bloom, inturn meiofauna, triggered bythe dance anddiversityof al (Watzin, 1983;Wägele, 1989;Kalogeropoulou iments) and diverse metazoan meiofauna taxon sed meiofauna, up to > 90 per cent in deep-sea total is the most plentiful (often > 50 per cent of the oceans. phylum The Nematoda, meanwhile, shell-bearing micro-organismsin most diverse of tozoans, foraminifera areand thecommonest the benthic system. Amongstmeiobenthic pro of to be intimately linked to other faunal components benthic group inthe marine realm,thought and is 2012). sisted by pleonal locking mechanisms(Luque as legs, the between fit that pleon a and sternum (necrocarcinid-type) and hadabroader thoracic carapaces that wereornamented widerthanlong with different, morphologically were nopleurans ing) lifestyle. Nevertheless, the most basalgym specialisedburyingto their(back-burrow cryptic which are well suited and paddle-like limbs, all of apleon that is partially exposed sternum, dorsally corystid-lyreidid-raninid type), anarrow thoracic are characterised by carapace (palaeo a fusiform which extant members brachyuransof group of is, Raninoidia),also known asfrog a crabs, form (Jagt habitatsous cryptic withinthese environments thenumer the Late Jurassic,good useof making the TethysOcean during margin of northern environments alongthe crobial andcoral-reef sponge-mi in brachyurans,flourished the among Prosopids andallied crabs, the most primitive ., 2010; Balsamo et al. , 2015). The clade Gymnopleura (that, 2015).The et al. , 2012). The rise in abun, 2012). The et al. Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín et ------, Extant softsediments). (burying withinfine-grained, morphotype palaeocorystid arose the fusiform inhabitants) (shallow-marine reef nid morphotype (pers. obs.). Fromhexagonal abasic necrocarci Štramberk, Czech Republic reefal limestones of ian known Jurassicto date fromis the uppermost raninoid first The globe. the across regions itude a widebathymetric range, fromtropical tolow-lat adapted to inhabitsoftandsandysediments across the majorbrachyurangroupsto have one of was Luque settings), a buryinglifestyle a prerequisite was for places for crabsto hide in(such asthose inreefal thatshale-like deposits lacked crevices and other deeper-marine environments withpredominantly thefactthat thenewnicherelativelyin was of life. Inview terised bya back-burrowing modeof was the mostspecialised family that was charac Lőrenthey tidae al. toids have recently beenrevisedby Van Bakel palaeocorys phylogeneticThe relationshipsof explain thesechanges hasnotyet beenproposed. over gymnopleurity time, amodel to increase of the successive diversity peaks(Figure 6), andan the various morphotypes, appearance of order of the earliest have gymnopleurans recognised the shale-richdeposits. Althoughnumerousstudies on and inlargecurred globally numbers, mostlyin Luque, 2014).Duringthe Albian bothtypesoc appearedrystoid in Colombia (Luque Schweitzer distributed worldwide ( necrocarcinidswere alreadydiverse andwidely near Auxerre (Yonne, France). During the Aptian, Migraine, Straelen, 1936 from the Hauterivian of ran was that of Until recently, a gymnopleu the oldest record of 1851). and Bemvenuti (2005) showed that meiofauna fauna) (Soto and Escobar-Briones, 1995). Rosa invertebrates (meio food acquisitionof mode of the burrowing by affected negatively was structure community (2012), who concluded that the Palaeocorys et al. Raninoides lamarcki et al (2012) noted that the Gymnopleura ., 2016), whereas the first palaeoco in Paranecrocarcinus hexagonalis Lőrenthey and Beurlen, 1929 Beurlen, and Lőrenthey Chasmagnathus granulata Chasmagnathus e.g. stillshowsa scavenger , Van Bakel /2018 et al. et al ., 2012; (Dana, , 2012; Van 193 193 et ------

Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION 194 194 Van Bakel Figure 6 replacement events overtime. replacement events (most conspicuous gymnopleurity; D),documenting niche- via lyreidid(increased gymnopleurity; C)toraninidmorphotype Figure 7 / Frompalaeocorystoid(no externalgymnopleurity; A,B), radiationintimeofnecrocarcinid- Successive and palaeocorystid-type crabgenera (numbers) (data from Luque Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín et al

., 2012;Karasawa Number of genera 10 0 1 2 3 4 5 6 7 8 9 Tithonia n et al B ., 2014,Schweitzer e r riasia n V alanginia necrocarcinids et al n Hauter ., 2016;pers. obs.). /2018 ivia Age n pala B a e r respect. 5) inthatwas mostsuccessful on thoracic sternite abdominal holding(adoubleconspicuous peg of and loss the cephalothorax) posed pleurae of (reduced branchiostegitesgymnopleurity and ex had tobeimproved. Apparently, theincrease of hiding/burying predator-pressure, the mode of bythis Driven increased. ammonites and fishes niche marine new worldwide, this the predator-pressure by, for example, filling and lifestyle ing After havingadapted been to abury successfully rites) (Figure 7). the pleu in a more axial position and exposure of arthrodial cavities surface,sternal development of the body, the posterior thoracic minimisation of coherent adaptations (a narrowing of a series of life involved was advantageous to such a mode of developing in survival.major step A ashapethat o remian cor y sti ds Aptian Albi a n Ce no m a ni a n et al ., 2012; - - - echinoid genera and of palaeocorystid crabgenera (data fromVillier Figure 8 1.7. ETYIOIDCRABS Luque an–Cenomanian) tosmoothercarapaces( carapaces ( time amongst etyioidsfrom more ornamented widely spacedorbits.a general There is trend in rounded anterolateral marginsand withlarge, is wider than long, withmultiple spines onsub that carapace flattened dorsally thin, a following: features are moststrikingmorphological the The quite possible (compare Wright and Collins, 1972). crabs (portunids), an ancestral relationship seems logical similarity of the morpho carapace features. Inviewof basis of genus (1991) even1996a, b).Bishop transferred the taxa were able( to swim quent studies it has been inferred that etyioid crab derived from a necrocarcinid ancestor. Insubse Förster (1968, p. 190)postulated that etyioidswere et al. Successive radiationintimeof numbers Successive offoraminiferal planktonic genera, ofancyloceratine ammonitefamilies,ofspatangoid , 2012,VanBakel Number of genera / families Xanthosia 10 12 14 16 0 2 4 6 8 plan e.g. k Tithonia , tonic Bell, 1863 to the Portunidae on the Steorrosia

foramin et al. Xanthosia n , 2012;Karasawa e.g. (Rathbun, 1935);Albi B e i fera r , Bishop, 1991;Fraaye, riasia to extant swimming n s pa V t alanginia a ng et al o i d

echinoids e.g. ., 2014;Fran n , the Hauter Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín Ţ ţƫƮțȶ - - - - ivia pa Age n escu et al laeoc B a ., 2004;Rückheim,2005;Mikhailova and Baraboshkin,2009; et al r remian rcso damage on scaphitids are not uncom traces of ing been produced by predatory crabs. Similar them as havscaphitid ammonitesandinterpreted latest Maastrichtian that pierced the shells of punctures paired documented (1996) Radwański mainte acontinued nektoniclifestyle. the nance of to finally and prey) of (capture ing feed natatory capabilities improved to periods of predators.time, In the reactionsavoidance in of connected toescape mode amongstetyioidswas It is most likely that the first stage in the swimming see Fraaye, 2012; 1996b, p. 275)(Figure 8). Klompmaker, and Franţescu mann, and earlyPaleocene late Maastrichtian CretachlorodiusFraaye, 1996a in Maastrichtianin fromscaphitids North America, 10per cent account for an average incidence of indicated byrepaired damage matureon shells, (Takeda North America mon inthe Upper Cretaceous of or y ., 2016). s tid

crabs et al. Aptian , 2016). Externally inflicted injuries, inflicted Externally 2016). , ancyl o ce Albi Faksecarcinus ra tine a n

amm Ce no o n m Schweitzer, Feld ites a /2018 ni a n 195 195 - - - - -

Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION Novel invertebrate morphotypes in Mesozoic marine ecosystems INTRODUCTION 196 196 2. Conclusions Schweitzer Figure 9 eouinr’ecp fnatant etyioids at the end ‘evolutionary’ escapeof by, for instance, ammonites, mighthave led to an the predation pressure ondecapodcrustaceans 1986). Fraaye (1996b)subsequentlypostulated that ries approach 40per cent (Landman andWaage, est latest Cretaceous levels where scaphitidinju young the stratigraphically with the exception of wards, the impactonmarineinvertebrate detritus and nektonicgroups. Fromthe Late Jurassicon various marine benthic evolutionary radiation of newecological niches and,concomitantly, rise of biota triggered, bothdirectly and indirectly, the among marinephyto- andzooplanktonic micro Major Mesozoic evolutionary andradiation events settings. radiationnon-reefal in documented examples of two first the are 9) (Figure etyioids and raninoids overecosystem engineers time. evolution The of thatcontracted, suggesting reefsmay have acted as followedand was bya severe diversityas reefsloss expansion pod crustaceans coincidedwith reef deca of the Mesozoic. diversification the that in concluded They groups decapod different for presented genus- andspecies-level diversitycurves recent studyby Klompmaker through time were virtually unknown until the decapodbiodiversity Quantitativeof patterns the Paleogene (Fraaye, 1996b). portunids during a faunal replacement event in monites.were Etyioids ousted bybetter-adapted a new andabundant food source –scaphitidam the Cretaceous. these etyioids met with In turn, of / Successive radiation intimeof numbers Successive of necrocarcinid, palaeocorystidand etyidcrabgenera (data fromLuque Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín et al ., 2012;VanBakel et al. , 2012;Karasawa et al . (2013),who et al. , 2014;Schweitzer ------/2018 References Acknowledgements is presented here. diverse nektonicandbenthicinvertebrate groups, sozoic marine revolution, from phytoplankton to first time, a coherent bottom-up model for the Me echinoids ammonites.and heteromorph For the brachyuranas decapod crustaceans, irregular tional distinctive faunal turnoversin such groups innovations andadaptations brought about addi meiofauna). During the Cretaceous Period new (part of) their food source ( bloom of decapod crustaceans) were intimately linked to the scavenger/detritivore ( patterns direct.was and planktonfeeders More complex Balsamo, M.,Semprucci, F., Frontalini, F., Shreeve,A., Atkinson, R.S., Pakhomov, E.A., thetypescript. an earlier version of anonymousreviewer for pertinent comments on tional Research Institute, Kraków, Poland) and an Institute–Na Geological (Polish Krobicki Michał literature andDr Berkeley)California, for itemsof We thank DrAdiël A. Klompmaker(University of et al for marine ecosystem biomonitoring, a tool R., 2012,Meiofauna as Coccioni, 195–210. Progress Series,Marine Ecology 144, bloom near South Georgia, Antarctica: Zooplankton response to a phytoplankton Priddle, J., Blight, S.P., Ward, P., 1996, ., 2016). e.g. , brachyuran i.e. et al , marine ., 2012; in - - -

Brayard, A., Krumenacker, L., Botting, J.P., Jenks, Bown, P.R., Lees, J.A., Young, J.R., 2004, Bishop, G.A., 1991, the fossilBell, T., of 1863, A monograph Erbacher, J., Thurow, J., 1997, Influence of Influence 1997, J., Thurow, J., Erbacher, David, B., Mooi,R.,Néraudeau, D., Saucède, Dana, J.D., 1851,Crustacea , Palaeontographical1863, Society London, the of Greensand. London, Monographs the Gault and Britain. Part II. Crustacea of Great malacostracous Crustacea of InTech Publisher, 4,77–104. Cruzado, A.(ed.), Marine Ecosystems: Micropalaeontology, 30,139–158. Tethys:Atlantic and western Marine mid-Cretaceous Radiolaria in the north oceanic anoxic events onthe evolution of Rendus Palevol, 8,189–207. adaptatives chez leséchinides: Comptes T.,Villier, L.,2009,Évolution et radiations Philadelphia, 5,247–254. Natural Sciences of the Academy of descriptsit J.D. Dana:Proceedings of Reipublicae Foederatae Duce, lexit et circumnavigatione, Carolo Wilkes e classe Crustacearum quae in OrbisTerrarum (Cyclometopa, Conspectus Edwardsii): fauna: ScienceAdvances 3,e1602159,11p. evolutionary themodern and theriseof Unexpected Early Triassicmarine ecosystem D.A., Thomazo, C.,Escarguel, G., 2017, L., Thuy, B., Hautmann,M.,Stephen, Charbonnier, S., Romano, C.,Doguzhaeva, Olivier, N., Goudemand,N., Saucède, T., J.F, Bylund, K.G., Fara, E., Vennin, E., Springer. 481–508. molecular process impact. Berlin, to global Young, J.R. (eds.), Coccolithophores: from diversitythrough time, Calcareousevolution nannoplankton and Biology, 11,305–314. the Western Interior: Journal of Shale of two Late Cretaceous crabsfromthe Pierre 1985, and viii +1–40p. Xanthosia spinosa Xanthosia occidentalis in Thierstein, H.R., Thierstein, newspecies, Bishop, Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín Förster, R., 1968, Jagt, J.W.M.,Van Bakel,B.W.M.,Guinot, D., Fraaye, R.H.B., 1996b, Late Cretaceous swimming Fraaye, R.H.B.,new Tethyan 1996a,A migrant: Knoll, A.H.,Follows, M.J., 2016,Abottom-up Klompmaker, A.A.,Schweitzer, C.E.,Feldmann, Kier, P.M.,1982, Rapidevolution echinoids: in Karasawa, H,Schweitzer, C.E., Feldmann, R.M., Kalogeropoulou, V., Bett, B.J., Gooday, A.J., 269–278. extinction: Acta Geologica Polonica, 46, crabs: radiation, competition, and migration, Paleontology,area: Journal 70,293–296. of ), fromthe Maastrichtian type Cretachlorodius enciensis 167–195. Paläontologie und historische Geologie, 8, aus der Bayerischen Staatssammlung für Calappidae in der Kreide: Mitteilungen sp. (Decapoda) und die Entwicklung der org/10.1098/rspb.2016.1755, 10p. (London) B283:20161755, http://dx.doi. the Royal Society oceans, Proceedings of perspectivechange onecosystem in Mesozoic crustaceans: Geology, 41,1179–1182. Mesozoic marine reefs onthe rise of of influence The 2013, Kowalewski,M., R.M., Palaeontology, 25,1–9. CrustaceanBiology, 34,216–272. Journal of Raninoida (Decapoda: Brachyura): of Luque,J., Phylogenyclassification 2014, and 1383–1395. ResearchNE Atlantic: Deep-Sea Part II, 57, assemblages on the Porcupine AbyssalPlain, metazoan1999) indeep-sea meiofaunal Vanreusel, A., 2010, Temporal changes (1989- Lampadariou, N., Martinez-Arbizu, P., Brachyura (Part 1).LeidenBrill,847–920. the Traité de Zoologie, 9(C) (I), Decapoda: the volumes translated from the French of to Crustacea, complementary Biology—The Treatise onZoology—Anatomy, Taxonomy, D., Schram, F., Von Vaupel Klein, C. (eds.), Brachyura, Fraaije, R.H.B., Artal, P., 2015,Fossil in Castro, P., Davie, P.J.F., Guinot, Paranecrocarcinus libanoticus n.gen., n. sp. (Crustacea, /2018 197 197 n.

Novel invertebrate morphotypes in Mesozoic marine ecosystems REFERENCES Novel invertebrate morphotypes in Mesozoic marine ecosystems REFERENCES 198 198 Kruta, I., Landman, N.,Kruta, I.,Landman, Rouget, I., Cecca,F., Kroh, A.,Smith, A.B., phylogeny 2010,The and Lehmann, J., Ifrim, C., Bulot, L., Frau, C., 2015, J.,Lehmann, 2015,Ammonitebiostratigraphyof Landman, N.H., Goolaerts, S., Jagt, J.W.M., Landman, N.H., Goolaerts, S., Jagt, J.W.M., Jagt- Landman, N.H., Waage, K.M.,1986,Shell Kruta, I., Landman,N.H., Rouget, I., Cecca, / Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín in the Mesozoic marine food web revealed by ammonites of role The Tafforeau, 2011, P., 147–212. systematic Palaeontology,Journal of 8, echinoids: post-Palaeozoic of classification Heidelberg, 229–257. in Geology, 43/44]. Springer, Berlin/ macroevolution to paleogeography[Topics fromammonoids, paleobiology: Ammonoid Early Cretaceous Paleobiogeography of Heidelberg. 403–429. in Geology, 43/44]. Springer, Berlin/ macroevolution topaleogeography[Topics (eds.),R.H. from paleobiology: Ammonoid Korn, D., De Baets, K.,Kruta, I., Mapes, the Cretaceous – anoverview, Heidelberg. 497–553. in Geology, 43/44]. Springer, Berlin/ macroevolution topaleogeography[Topics (eds.),R.H. from paleobiology: Ammonoid Korn, D., De Baets, K.,Kruta, I., Mapes, Paleogene (K/Pg) boundary, Order Ammonoidea at the Cretaceous/ diversity, the abundance, of andecology extinction: Ammonites onthe brink of Jagt-Yazykova,Machalski, E.A., 2015, M., Geology, 42,707–710. the Cretaceous: nautilid survival at the end of M.M., 2014, Ammonite extinction and Yazykova, E.A.,Machalski,Yacobucci,M., Lethaia, 19,211–224. in scaphitidammonites. abnormalities Palaeontology, 56,9–14. of Rhaeboceras halli radula The the Late Cretaceous ammonite scaphitid 2013, P., Tafforeau, F., jaw preservation: Science, 331,70–72. (MeekandHayden, 1856). in in Klug, C., Klug, C., /2018 uu,J,21,Anwgnsadseiso Luque, J., 2014,Anewgenus andspeciesof fossilen Die 1929, K., Beurlen, E., Lőrenthey, Linnaeus, C., 1758, Systema naturae per regna tria Mikhailova,E.Yu.,Baraboshkin, I.A., 2009, Masse, J.-P., Humbert, S., 1976,Leséchinidesdu Masrour, M.,Aoutem, M., Atrops, F., 2004, MacRae, R.A.,Fensome, R.A.,Williams, Luque, J., Feldmann,R.M., Schweitzer, C.E., M., Jagt, J.W.M., Krobicki, M.,Van Bakel, South America, Colombia, from the Lower Cretaceous of raninoidian crab(Decapoda, Brachyura) Palaeontologica, 3,1–420. Krone: Series Geologica Hungarica, Decapoden der Länder der Ungarischen p. Tomus I,Laurentius ,824 Stockholm, differentiis, characteribus, synonymis, locis. Editiodecima,reformata. cum species, naturae, secundumclasses, ordines, genera, fthe suborder Ancyloceratina Wiedmann: of Early Cretaceousmonomorph ammonites and the heteromorph evolutionThe of 3, 45–56. et paléoécologie: Géologie Méditerranéenne, Crétacé inférieur provençal. Biostratigraphie 595–617. Geobios,et intérêt stratigraphique: 37, atlantique (Maroc); révisionsystématique du Crétacé Inférieur dans le Haut Succession des peuplements d’échinides of Botany,74, 1687–1694. Journal Canadian significance: diversity, originations, and extinctions and their dinoflagellate Fossil 1996, G.L., Biology, 32,405–420. Crustacean South America: Journal of northern Raninoida) from of the Aptian oldest frog crabs(Decapoda: Brachyura: Jaramillo, C.,Cameron,C.B., 2012,The Geologica, 147,27–34. to Pál Mihály Müller, Poland 2013,Scripta decapod crustaceans, Krakow [sic],a tribute on MesozoicSymposium andCenozoic B.W.M. the 5th (eds.), Proceedings of in raj, ... Hyžný, R.H.B., Fraaije, Rathbun, M.J., the 1935,Fossil Crustacea of and upon, predation The 1996, A., Radwański, Premoli-Silva, I.,Sliter, W.V., 1999,Cretaceous Olney, M.,2002,Radiolaria, UniversityCollege Albian Monks, N.,of 1999,Cladistic analysis Saucède, T., Villier, environmental L.,2005,The planktic Rückheim, S., onset of 2005. The of Effects 2005, C.E., Bemvenuti, L.C., Rosa, Reháková, D., Michalík, J., 1997,Evolution ucl.ac.uk/GeolSci/micropal/radiolaria.html MicropalaeontologyLondon, Unit, www. 907–925. Palaeontology,ammonites: heteromorph 42, Paleontological Journal, 43,527–536. N., Zghal, I.(eds.), Global events during 267–274. andTechnology, Biology Archives of 48, Patos Brazilian Lagoon. Southern habitats of estuarine intertidal (Dana) on meiofauna of Acta GeologicaPolonica, 46,117–135. the Middle Vistula Valley, Central Poland: constrictus Hoploscaphites the ammonite species populations of the extinction of, the latest Maastrichtian 301–328. America, Special Paper, 332, Society of Cretaceous ocean-climate Geological system: the Johnson,C.C. (eds.), Evolution of foraminiferal evolution, paleoceanography: evidence from planktonic (accessed March 15,2018). Cretaceous, Echinoidea) evolution inthe Early andMid spatangoid (Echinodermata: context of Bochum, unpublished PhDthesis, 82p. für Geowissenschaften, Ruhr-Universität Boreal Realm. Bochum,Germany, Fakultät the foraminifera in the mid-Cretaceous of the burrowing crab Cretaceous Research, 18,493–504. Cretaceous Tethyan microplankton: Lower most characteristic constituents of calpionellids–the and distribution of America,SpecialPaper, 2,1–160. Society of Coastal Plain: Geological Atlantic and Gulf in Arnaud-Vanneau, A., Arndt, Chasmagnathus granulata Chasmagnathus (J. Sowerby, 1817)from in Barrera, E., Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín

Smith, A.B., 1984,Echinoid palaeobiology,. Schweitzer, C.E.,Karasawa, H.,Luque, J., Franţescu, R.M., Feldmann, C.E., Schweitzer, Soto,Escobar-Briones, L.A., E.,1995,Coupling Villier, L.,Eble, G.,the robustness 2004,Assessing Vermeij, G.J., 1987,Evolution and escalation: an Van Straelen, V., 1936,Crustacés décapodes Van Bakel, B.W.M., Guinot, D., Artal, P., Fraaije, Takeda, Y., Tanabe,T., K.,Sasaki, Landman, Crustacean Biology, 36,338–372. two newgenera: Journal of description of 1968 (Brachyura: Raninoida) with the Förster, Necrocarcinoidea of classification Feldmann, R.M., 2016, Phylogeny and 129–155. Paleontology,Brachyura). Journal 86, of Etyidae Guinot andTavares, 2001(Crustacea: O.D., Klompmaker, 2012, Revision A.A., of Excursions”, 6,59–61. Géologie Alpine, Série spéciale “Colloques et the quiet Aptian-Turonian Superchron: taxonomiclevel in spatangoid echinoids: scheme,morphometric temporal scale, and disparity estimates: theimpactof of Jersey, PrincetonUniversity Press, 527p. life, Princeton, New of ecological history d’Histoire naturelle deBelgique, 12,1–50. Crétacique: Bulletin du Muséeroyal nouveaux ou peu connus de l’époque 1–216. Brachyura, Podotremata): Zootaxa, 3215, raninoidiancrabs(Crustacea, Decapoda, of the Palaeocorystoidea andthe phylogeny R.H.B., Jagt, J.W.M., 2012,Arevisionof Lethaia, 49,28–42. North America: Western Interior Seaway of in the scaphitid ammonoids Late Cretaceous N.H., 2016, Durophagous predation on Olsen, Fredensborg, 233–244. 1993, Iraklion,Crete:Symposium Olsen & the 28th European Marine Biology of Ansell, A.D., Smith, C.J. (eds.), Proceedings Mexico, of the SW Gulf mechanismsrelated to benthic production in Allen&Unwin,London,190p. in Eleftheriou, A., /2018 199 199

Novel invertebrate morphotypes in Mesozoic marine ecosystems REFERENCES Novel invertebrate morphotypes in Mesozoic marine ecosystems REFERENCES 200 200 Vincx, M.,1996,Meiofauna in marine and Villier, L.,Néraudeau, D., Clavel, B., Neumann, äee JW, 99 O te nlec o fishes of influence the On 1989, J.W.,Wägele, / Boletín de la Sociedad Geológica Mexicana Geológica Sociedad la de Boletín Palaeontology, 47,265–292. Echinoidea)taxonomic and implications: Cretaceous spatangoids (Echinodermata: Early C., David,B., 2004,Phylogenyof Paleobiology, 30, 652–665. Evolutionsforschung, 27,297–309. Zeitschrift fürzoologische Systematik und benthic crustaceans: on the evolution of Wallingford,International, 187–195. diversity insoilsand sediments, CAB organismal Methods for the examination of freshwater sediments, in Hall, G.S. (ed.), /2018 Yavari, M., Yazdi, M.,Gahalavand, H.,Kamyabi Wright, C.W., Collins, J.S.H., 1972, British meiofauna of effects The 1983, M.C., Watzin, Geology, 16(26),615–632. de Géologie/Notebooks of Iran:Carnets of Heteraster fromsouth ZagrosBasin, the High Early Cretaceous toxasterid echinoid Shadan, H., Adabi, M.H., Villier, L.,2016, (533), 114p. Palaeontographical126 Society London, the of Cretaceous crabs: Monographs Oecologia, 59,163–166. structure macrofaunal communities: on settling macrofaunal meiofauna may