Drifting with trilobites: The invasion of early post-embryonic trilobite stages to the pelagic realm
Graphical abstract
Introduction
The Ordovician Radiation is one of the most significant intervals of marine biodiversity increase during the whole Phanerozoic (Droser et al., 1996; Webby, 2000; Servais et al., 2010; Servais and Harper, 2018; Stigall et al., 2019). In addition to the increase in biodiversity, this radiation also affected the structure of marine ecosystems, leading to a more complex trophic web, increased competition between taxa, changes in reef compositions, and diversification of planktic organisms (Droser and Finnegan, 2003; Servais et al., 2010, Servais et al., 2016; Servais and Harper, 2018). As such, the Ordovician Radiation (or Great Ordovician Biodiversification Event) can be viewed as a long-term cascade of events that led to the establishment of a modern structure of marine ecosystems (Servais et al., 2008, Servais et al., 2010, Servais et al., 2016, Servais et al., 2021; Servais and Harper, 2018; Stigall et al., 2019, Stigall et al., 2020; Harper et al., 2020). However, it is worth noting here that the nomenclature and nature of the Ordovician Radiation and the Great Ordovician Biodiversification Event (GOBE) is still a widely discussed topic (Servais and Harper, 2018; Stigall et al., 2020). We focus herein on describing ecological and evolutionary patterns during the Cambrian and the Ordovician. The observed patterns are interpreted in the general context of changes during these time intervals but are not intended to define the onset(s) and are certainly not sufficient on their own to investigate the root(s) of any of the evolutionary event(s) in the Early Paleozoic.
Trilobites are among the most diverse metazoans inhabiting early Paleozoic seas and the most abundant euarthropods in the fossil record from Cambrian to Devonian strata worldwide. Despite being considered the iconic representatives of the so-called Cambrian evolutionary fauna (Sepkoski, 1981) trilobites were still highly diverse in Ordovician ecosystems (Adrain et al., 1998; Adrain, 2013) and their Ordovician morphological disparity was higher than during Cambrian (Foote, 1991, Foote, 1993; Hopkins, 2014). Moreover, in the Ordovician Period, trilobites adapted to various feeding strategies and modes of life (Fortey and Owens, 1999; Fortey, 2013), including epipelagic and mesopelagic adults (Fortey, 1985), displayed higher diversity of their appendages (Pérez-Peris et al., 2021), and showed otherwise complex behaviours (Drage, 2019; Suárez and Esteve, 2021; Fatka et al., 2021).
The early stages of the Ordovician Radiation are associated with the Plankton Revolution – an ecological shift characterized by a progressive invasion of various organisms into the pelagic realm (Signor and Vermeij, 1994; Nützel and Frýda, 2003; Kröger et al., 2009; Servais et al., 2016). This contrasts with earlier Cambrian communities that were generally restricted to the sea bottom (or living close to it). The beginning of the Plankton Revolution is marked by a major change in the diversity, disparity, and distribution of marine phytoplankton, mainly acritarchs (Servais et al., 2008, Servais et al., 2010, Servais et al., 2016), and can be traced back to the end of the Cambrian Period (Nowak et al., 2015; Servais et al., 2016; Shan et al., 2022; Kroeck et al., 2022). The initial phytoplankton burst was followed by various zooplanktic organisms, such as chitinozoans (Achab and Paris, 2007), graptolites (Cooper et al., 2012), cephalopods (Kröger et al., 2009), as well as some euarthropods (Perrier et al., 2015). Some benthic metazoans evolved planktic larval stages during this period (Peterson, 2005; Nützel et al., 2006), increasing the number of meroplankton (i.e., organisms spending part of their life cycle as plankton) in Ordovician seas. This was the case for trilobites, as planktic larval stages are known to be present in numerous species (Fortey and Chatterton, 1988; Speyer and Chatterton, 1989; Chatterton and Speyer, 1989, Chatterton and Speyer, 1997). It has been suggested that these planktic trilobite stages evolved independently in several clades during the Furongian and Early Ordovician in a response to increased ecological pressure in the early phases of the Great Ordovician Biodiversification Event (Park et al., 2016; Park, 2017). However, this trilobite invasion into the pelagic realm has never been quantitatively evaluated. Consequently, the scale and tempo of this evolutionary and ecological shift in a major euarthropod group remain largely unexplored.
Herein, we provide highly resolved, global, quantitative data on 144 trilobite species, ranging from the Cambrian Series 2 up to the Late Ordovician. We show that Cambrian ecosystems were dominated by trilobites with exclusively benthic early post-embryonic stages, while Ordovician seas comprised a remarkable number of trilobites possessing one or more planktic stages. Both species- and family-level data show a progressive increase in the number of taxa that incorporate planktic stages in their development between the Miaolingian and the Middle Ordovician, corresponding with the Plankton Revolution seen in other organisms.
Section snippets
Trilobite post-embryonic development
Trilobites are among the few Paleozoic metazoan groups with well-known early developmental stages (Chatterton and Speyer, 1997; Hughes et al., 2006; Hopkins, 2017; Lerosey-Aubril and Laibl, 2021). Like many other euarthropods, trilobites show hemianamorphic post-embryonic development, characterized by a sequential increase of the segment number in its early phase and segment stability in its later phase (Chatterton and Speyer, 1997; Hughes et al., 2006; Minelli and Fusco, 2013). By convention,
Data collection, reliability, and analysis
Early post-embryonic developmental stages of trilobites are unique among euarthropods because they possess a biomineralized exoskeleton (Lerosey-Aubril and Laibl, 2021) and are as such abundant in the fossil record, being present in strata spanning from the Cambrian Series 2 (e.g., Geyer, 1996; Dai and Zhang, 2012) up to the Lower Mississippian (Lerosey-Aubril and Feist, 2005b). Data from early post-embryonic stages of Cambrian and Ordovician trilobites were collected from an extensive
Results
All recorded early post-embryonic trilobite stages from the Cambrian Series 2 and Miaolingian generally show an adult-like morphology and thus had exclusively benthic early post-embryonic stages (Fig. 3A). The first nonadult-like planktic trilobite larvae are known from the mid-Furongian (Jiangshanian) strata of North China in three species: Tsinania canens (Tsinaniidae), Akoldinioidia latus, and Koldinioidia choii (Shumardiidae) (Park and Choi, 2009; Park, 2017). However, species with
The ancestral state of early developmental trilobite stages
Stratigraphically, early trilobites show gradual development without metamorphosis (Fortey and Owens, 1997). This is corroborated by our data, which show that trilobite species with exclusively benthic early developmental stages (and without distinct metamorphosis) dominated Cambrian ecosystems (Fig. 3A). The phylogenetic position of species with such stages suggests that this type of development is ancestral to Trilobita (compare with the tree topologies of Paterson et al., 2019). Early
Summary
Stratigraphically and phylogenetically early trilobites were characterized by a gradual development and exclusively benthic early developmental stages. These groups dominated Cambrian ecosystems but were also common during post-Cambrian times. The first trilobite species with planktic larvae are known from the Furongian, but some planktic forms might have been present already in the Miaolingian. The appearance of the first planktic larvae in the fossil record generally coincides with the onset
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This contribution is based on the presentation at the IGCP 635 and 735 workshops, organized by Thomas Servais and Bertrand Lefebvre. The authors are particularly grateful to Nigel C. Hughes, an anonymous reviewer, and to editors Thomas Servais and Shuzhong Shen for their constructive comments that improved the quality of the manuscript. Martin Šafka (https://www.fossilreconstructions.com/) is thanked for creating the 3D models of early developmental trilobite stages under the supervision of L.
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