Boletín de la Sociedad Geológica Mexicana / 2018 / 187 The rise of a novel, plankton-based marine ecosystem during the Mesozoic: a bottom-up model to explain new higher-tier invertebrate morphotypes René Hendricus Bartholomeus Fraaije, Barry Wilhelmus Martinus Van Bakel, John Wilhelmus Maria Jagt, Pedro Andrade Viegas ABSTRACT René Hendricus Bartholomeus Fraaije ABSTRACT RESUMEN [email protected] Barry Wilhelmus Martinus Van Bakel Major radiation events amongst a range of Los mayores eventos de radiación de la microbiota que Pedro Andrade Viegas phytoplanktonic and zooplanktonic microbiota comprende el fitoplancton y zooplankton, con grupos Oertijdmuseum, Bosscheweg 80, 5283 WB such as calcareous nannofossils, calpionellids, como nanofósiles calcáreos, calpionélidos diatomeas, Boxtel, the Netherlands. diatoms, dinoflagellates, planktonic foramin- dinoflagelados, foraminíferos planctónicos y radiolarios, ifera and radiolarians are characteristic of the fueron característicos del intervalo de tiempo comprendi- Barry Wilhelmus Martinus Van Bakel time interval between the Late Jurassic (c. 160 do entre el Jurásico Tardío (c. 160 Ma) y el Cretácico Naturalis Biodiversity Center, P.O. Box 9517, Ma) and Late Cretaceous (c. 100 – 66 Ma). Tardío (c. 100 – 66 Ma). Tanto de forma directa como 2300 RA Leiden, the Netherlands. Both directly and indirectly, these radiations indirecta, dichas radiaciones en la columna de agua ma- in the marine water column led to a prolifera- rina llevaron a la proliferación de varios grupos bentó- John Wilhelmus Maria Jagt tion of various benthic groups such as burying nicos, tales como los cangrejos infaunales y nadadores, Natuurhistorisch Museum Maastricht, de and swimming crabs and irregular echinoids as equinoideos irregulares, así como grupos nectónicos tales Bosquetplein 6-7, 6211 KJ Maastricht, the well as nektonic groups such as ancyloceratine como los ammonites heteromorfos ancilocerátidos. Para Netherlands. heteromorph ammonites. For each of the in- cada grupo de invertebrados estudiado, hemos grafica- vertebrate groups studied we have plotted all do todos los datos disponibles acerca de su diversidad available data on their diversity through time. a través del tiempo. Los histogramas resultantes cons- The resultant histograms form the basis of our tituyen la base para nuestro nuevo modelo de “relleno” new model of the ‘infill’ of Mesozoic ecosys- de los ecosistemas del Mesozoico. El impacto sobre los tems. The impact on detritus and plankton detritófagos y planctotróficos fue directo a partir del Ju- feeders was direct, from the Late Jurassic on- rásico Tardío, ya que se dió un incremento de partículas wards, in that an increased supply of plankton- nutritivas provenientes del plankton, de tal forma que ic food particles became available. However, la radiación de los cangrejos raninoides infaunales (que the radiation of burying raninoid crabs, which comprendía los más complejos carroñeros/detritívoros), comprised more complex scavengers/detriti- estuvo íntimamente ligada a la explosión de (o parte vores, was intimately linked to the bloom of de) su alimento (i.e., meiofauna marina). Durante el (part of) their food source (i.e., marine meiofau- Periodo Cretácico, surgieron innovaciones y adaptacio- na). During the Cretaceous Period new innova- nes en torno a cambios en composición faunística. Por tions and adaptations brought about additional ejemplo, hubo una transición en los cangrejos rana (Ra- faunal turnovers. For instance, amongst frog ninoidia), entre el tipo palaeocorístido (vía el tipo liréi- crabs (Raninoidia), there was a transition from dido), hacia el tipo ranínido. Otros cambios coetáneos the palaeocorystid type, via the lyreidid type to se han documentado para equinoideos irregulares (i.e., the raninid morphology. Similarly, coeval turn- de Toxasteridae, vía Micrasteridae, a Schizasteridae), y overs are documented for irregular echinoids para ammonites heteromorfos, de Ancyloceratoidea, vía (i.e., from Toxasteridae via Micrasteridae to Turrilitoidea, a Scaphitoidea. Aquí se presenta, por vez Schizasteridae) and for heteromorph ammo- primera, un elaborado modelo a detalle, con el fin de nites: from Ancyloceratoidea via Turrilitoidea explicar el surgimiento y la dispersión en el tiempo, de to Scaphitoidea. Here we present, for the first diferentes grupos de invertebrados, en el rango de los más time, an elaborated bottom-up model to ex- altos niveles tróficos. plain the emergence and dispersion in time of different invertebrate groups at a range of Palabras clave: Mesozoico, ecosistema higher-tier trophic levels. marino, paleoecología, morfotipos de invertebrados. Keywords: Mesozoic, marine eco- system, paleoecology, invertebrate BOL. SOC. GEOL. MEX. 2018 morphotypes. VOL. 70 NO. 1 P. 187 ‒ 200 http://dx.doi.org/10.18268/BSGM2018v70n1a11 Manuscript received: October 20, 2017 Corrected manuscript received: November 10, 2017 Manuscript accepted: November 14, 2017 Novel invertebrate morphotypes in Mesozoic marine ecosystems 188 / Boletín de la Sociedad Geológica Mexicana / 2018 1. Introduction studies between the adaptive radiations observed and a coherent marine food chain revolution that The notion of a tardy, low-diversity recovery from filled an important portion of the modern marine the Permian–Triassic mass extinction event has to ecosystem. The present paper demonstrates, for INTRODUCTION be reconsidered following the paper by Brayard the first time, a bottom-up Mesozoic marine rev- et al. (2017). Outline in that paper was an Early olution model from phytoplankton to diverse nek- Triassic marine ecosystem with a phylogenetical- tonic and benthic invertebrate groups (Figure 1). ly diverse, functionally complex and trophically multi-level marine ecosystem, from primary pro- 1.1. PHYTOPLANKTON ducers to top predators and potential scavengers. Thus, ecosystem balance and optimisation were In order to gauge why several invertebrate groups reached not long after the Palaeozoic Era. How- experienced blooms and proceeded to occupy new ever, this was merely the first part of the transition ecological niches in Early Cretaceous marine as- from the Palaeozoic to the modern marine evolu- semblages, the food web at the time needs to be tionary fauna. A second, essential phase (undevel- studied from the bottom up. In their bottom-up oped during the Palaeozoic) still had to take place, perspective on ecosystem changes in Mesozo- as demonstrated below. To encompass patterns of ic oceans, Knoll and Follows (2016) provided a widespread evolutionary changes among benthic mechanism for the observed evolutionary shifts in invertebrates in the marine realm during the Me- Mesozoic marine biota on the basis of a phyto- sozoic (ca. 252 – 66 Ma), Vermeij (1987) coined plankton radiation and diversification (Figure 2). the term ‘the Mesozoic Marine Revolution’. He Stratigraphically and taxonomically, planktonic focused mainly on extinct molluscs and observed microfossils provide the most complete record of a Mesozoic–Cenozoic radiation of durophagous biodiversity of any group of extinct marine organ- predators. Another, coeval, revolution has been isms. The phytoplankton record is of particular discussed by Knoll and Follows (2016), with ref- significance as it tracked global changes in the ma- erence to marine primary producers, inclusive of rine system and, in turn, had an impact on bio- radiations of photosynthetic dinoflagellates, coc- diversity and productivity of higher trophic levels colithophorids and diatoms. of the biosphere. Coccolithophores and other Mesozoic evolutionary and adaptive radiations in calcareous nannoplankton first appeared in strata invertebrate groups such as echinoids (e.g., Kier, of Late Triassic (c. 210 Ma) age. Rates of specia- 1982; Smith, 1984; David et al., 2009; Kroh and tion at levels significantly above background were Smith, 2010), heteromorph ammonoids (Mikhai- confined to the Late Triassic, Early Jurassic and lova and Baraboshkin, 2009; Lehmann, 2015) and Tithonian–Berriasian intervals (Bown et al., 2004). brachyuran decapod crustaceans (e.g., Karasawa et Another phytoplankton group, the dinoflagellates al., 2014; Schweitzer et al., 2016) have also been (single-celled protists at or near the base of the recorded in considerable detail. However, there food chain), showed remarkable patterns in spe- was no link or overview in these palaeontological cies diversity during the Mesozoic. First appear- ing in the Middle Triassic, they rapidly increased Figure 1 Successive radiations through time within the plankton-based Mesozoic food web. Novel invertebrate morphotypes in Mesozoic marine ecosystems Boletín de la Sociedad Geológica Mexicana / 2018 / 189 INTRODUCTION Figure 2 Radiations of species of photosynthetic coccolithophorids, dinoflagellates and diatoms (data from Knoll and Follows, 2016). to a Late Jurassic maximum of 420 species in the and Sliter, 1999; Bown et al., 2004). Kimmeridgian (157 – 153 Ma). After a minor de- During the Late Palaeozoic and into the Mesozo- cline, diversity rose to an all-time peak of 584 taxa ic, Radiolaria experienced a gradual decline until during the mid-Cretaceous (Albian; see MacRae the end of the Jurassic, at which time there was et al., 1996). A third group of planktonic forms of a rapid diversification. This coincided with a ra- importance comprises the enigmatic calpionel- diation amongst dinoflagellates which may have lids. These marine organisms with calcitic, bell- represented an increased source of food for the