Quantitative analysis of substrate preference in Carboniferous stem group echinoids
Introduction
Echinoids, or sea urchins, are a diverse clade that has occupied a range of environments in both modern and ancient ecosystems. In modern oceans, echinoids are abundant in numerous marine habitats (e.g., Kier and Grant, 1965; Nebelsick, 1996) and make up an important part of the ecosystems in which they inhabit (Chesher, 1969; Lohrer et al., 2004; Steneck, 2013). Though members of the modern fauna (Sepkoski, 1981), echinoids first originated in the Ordovician (Pisera, 1994; Smith and Savill, 2001). They were moderately diverse and abundant in the late Paleozoic (Schneider et al., 2008), reaching their peak specific and generic diversities in the Carboniferous (Kier, 1965; Smith, 1984). Paleozoic echinoid faunas differed substantially from post-Paleozoic communities, in part because almost all fossil echinoids known from before the Permian belonged to the echinoid stem group (Thompson et al., 2017; Thompson et al., 2015b). These stem group echinoids displayed a variable number of columns of interambulacral and ambulacral plates in each area (Fig. 1), as opposed to the reduced two ambulacral and interambulacral columns that characterize the crown group (Smith, 1984). Despite having existed throughout the majority of the Paleozoic, the paleoecology and environmental distribution of stem group echinoids is very poorly known. We set out herein to provide a quantitative assessment of the environmental distribution of different families of stem group echinoids during the Carboniferous Period.
Extant echinoids occupy different substrates dependent upon their life modes (Nebelsick, 1992, Nebelsick, 1996; Smith, 1984) and many echinoids have evolved to live on or in particular substrates. Often associated with this environmental specialization is the evolution of novel morphologies suited for life in these environments (Carter et al., 1989; Kanazawa, 1992; Saitoh and Kanazawa, 2012; Smith, 1978a). For example, the atelostomate echinoids are specially adapted to life in fine-grained substrates, and have evolved specialized tube feet to feed in these sediments (Barras, 2008; Smith, 1984). Little is known about echinoid substrate affinities in the Paleozoic, however, and to date there have been no quantitative tests of hypotheses regarding Paleozoic echinoid environmental distribution. The Carboniferous peak in stem group echinoid diversity coincided with peak Paleozoic diversity of echinoids at the family level, and was home to six families including the archaeocidarids, palaechinids, proterocidarids, lepidesthids, lepidocentrids and cravenechinids. Additionally a seventh family, the crown group echinoids of the Miocidaridae, may also have been present (Thompson et al., in review). These families display a wide array of disparate morphologies, and have been postulated to represent different life modes and ecologies based upon functional morphology and studies of local paleoecology (Chesnut and Ettensohn, 1988; Smith, 1984; Thompson and Ausich, 2016). Despite the information gleaned from these local studies, a large-scale analysis of Carboniferous echinoid environmental distribution has been wanting.
The affinity for particular substrates amongst post-Paleozoic echinoids has long been demonstrated based upon the environmental distribution of certain clades and functional morphological studies. The preference for particular substrates is closely related to feeding strategies and food source. Although many post-Paleozoic regular echinoids display a tendency for the hard substrates that they graze upon (Nebelsick, 1995, Nebelsick, 1996), many irregular echinoids deposit feed, relying on nutrients from the sediment (Lohrer et al., 2004). Subsequently, grain size has been demonstrated to play a key role in determining the distribution of modern echinoids (e.g., Ferber and Lawrence, 1976; Gladfelter, 1978; Hendler et al., 1995; Hill and Lawrence, 2003; Ivany et al., 1994; Kier and Grant, 1965; Mooi, 1990; Nebelsick, 1992, Nebelsick, 1995; Pawson and Miller, 1983; Poulin and Feral, 1995; Schinner, 1993; Stanley and James, 1971; Telford et al., 1983; Telford and Mooi, 1986; Walker and Gagnon, 2014), and numerous field-based studies of echinoid-rich Cenozoic stratigraphic successions have shown grain-size to be a determinant in the distribution of clypeasteroids, atelostomates, and regular echinoids (Carter et al., 1989; Carter and Hamza, 1994; Gordon and Donovan, 1992; Kroh and Nebelsick, 2003; Mancosu and Nebelsick, 2016, Mancosu and Nebelsick, 2017).
Aside from study of differential facies distributions, functional morphology has long influenced interpretation of fossil echinoid life modes (Kanazawa, 1992; Nichols, 1959; Saitoh and Kanazawa, 2012; Seilacher, 1979; Smith, 1978a, Smith, 1979, Smith, 1980a) and numerous morphological innovations including test shape (François and David, 2006; Kanazawa, 1992; Saitoh and Kanazawa, 2012; Schlüter, 2016), tubercle and spine shape and structure (Smith, 1980a; Walker and Gagnon, 2014), and the size, shape, and structure of tube feet and their associated ambulacral pores (Smith, 1978b, Smith, 1980b) can be directly linked to environmental correlates. Test shape, for instance, has been shown to control the ability of different spatangoids to burrow and locomote in or on different substrates (Kanazawa, 1992; Saitoh and Kanazawa, 2012). Tubercle and spine morphology and arrangement also have adaptive significance, and in-part control the distribution of echinoids amongst differing grain size regimes (Ferber and Lawrence, 1976; Smith, 1978a, Smith, 1980a).
In addition to grain size, substrate mineralogy has been shown to influence the distribution of extant echinoids. Analysis of the distribution of three Atlantic sand dollars revealed that Leodia sexiesperforata occurred only on biogenic carbonate sediments, while Mellita quinquiesperforata preferred terrigenous siliciclastic sediments. Furthermore, Encope michelini occurred on both siliciclastics and carbonates, and showed no affinity for one over the other (Telford and Mooi, 1986). Mooi (1990) also discussed that different species of cassiduloid echinoids in the Caribbean prefer substrates of differing mineralogies. Cassidulus caribaearum, Echinolampas depressa, and Conolampas sigsbei preferred carbonates, while Eurhodia relicta was found in association with siliciclastics. Despite this apparent preference in some species, there are counterexamples (Guidetti et al., 2004), and though there is much less evidence for mineralogical preference in echinoids than there is with respect to grain size, analyses of the fossil records of marine animals have demonstrated that clear lithological preferences do exist throughout the Phanerozoic (Foote, 2006, Foote, 2014; Hopkins, 2014; Hopkins et al., 2014; Kiessling and Aberhan, 2007; Kiessling et al., 2007; Miller and Connolly, 2001).
Though there has been no rigorous analysis of Paleozoic echinoid substrate affinities, previous workers have speculated about their environmental preference based upon functional morphology and local studies of their distribution. For instance, the proterocidarid echinoids are characterized by their enlarged oral ambulacral pores, which are surrounded by large peripodial rings and may have supported penicillate tube feet (Smith, 1984). Such penicillate tube feet are found in the extant atelostomate echinoids, and have been associated with their ability to colonize fine-grained environments (Barras, 2008; Smith, 1980a, Smith, 1984). The presumptive penicillate tube feet of the Proterocidaridae may also indicate that they were specialized for life on fine-grained substrates. Proterocidarids also have a large, expanded oral surface (Fig. 1E), which bears many more columns of ambulacral plates than the adapical surface, and was presumably associated with food-gathering (Kier, 1965).
Studies of local paleoecology have also informed hypotheses about stem group echinoid environmental distribution. In their study of the echinoderm fauna of the Serpukhovian Pennington Formation of Kentucky, Chesnut and Ettensohn (1988) proposed that the genus Lepidesthes was an epifaunal deposit feeder with affinities for marly, soft substrates. Thompson and Ausich (2016) found the archaeocidarid Lepidocidaris sp. in a siliciclastic green shale facies of the Viséan Fort Payne Formation of Kentucky. This genus is also fairly abundant in the coarse carbonate sediments of the Tournaisian Burlington Limestone (Meek and Worthen, 1869). Furthermore, in the Fort Payne Formation, the archaeocidarid ?Archaeocidaris sp. was found preserved on coarse-grained crinoidal flank beds. Thompson and Ausich interpreted the occurrence of these two genera in diverse environments as evidence that the archaeocidarids likely had a wide tolerance with respect to both grain size and substrate lithology (Thompson and Ausich, 2016). They also found lepidesthid echinoids on firm, packstone and wackestone carbonate buildups, and showed that despite their abundance in fine-grained, siliciclastic environments (Lane, 1973) they were also apparently capable of inhabiting coarser carbonate substrates (Thompson and Ausich, 2016). Donovan and Lewis (2017) examined the distribution of echinoids in the Carboniferous of Derbyshire, U.K. and commented on the limited occurrence of Lepidocidaris in shallow environments relative to the wider occurrence of Archaeocidaris and the palaechinid Melonechinus in shallow and deeper-water carbonate settings.
Despite the utility of these local studies in demonstrating the paleoenvironmental distribution of different taxa, they generally rely on limited sample sizes and short intervals of geological time. To overcome these issues, we examined environmental preferences using a global database of echinoid occurrences spanning the entirety of the Carboniferous. Our database consists of echinoid specimens in museum collections in North America and Europe, and is supplemented by occurrences from the published literature. We used this database to determine if different families showed preferences for particular substrate mineralogies and grain sizes using three distinct analytical metrics. Our aim was to test the hypothesis that different echinoid clades showed a preference for particular substrates. We then use these results to lay out novel hypotheses regarding the role of substrate affinity in stem group echinoid macroevolution.
Section snippets
Echinoid occurrence database
In order to assess substrate affinities in Carboniferous echinoids, a comprehensive database of echinoid occurrences was assembled. The species and genera comprising the seven known families of Carboniferous echinoids occur globally, and with the probable exception of the Palaechinidae, span all stages of the Carboniferous (Jackson, 1912; Kier, 1965, Kier, 1968). After data collection, the Cravenechinidae and Miocidaridae were excluded from our analyses due to their representation in our
Results
As previously mentioned, results using the binomial test and Bayesian inference for lithological comparisons are based on comparisons to PaleobioDB collections. Conversely, the SRA as calculated herein is relative to the database of Carboniferous echinoid occurrences. Because of these differences, results for substrate lithology assessed using Foote, 2006, Foote, 2014 binomial test and the Bayesian approach (Simpson and Harnik, 2009) must be interpreted differently from results of the SRA (
Comparison of results at differing scales
We analyzed our data at three hierarchical scales: the stage level, the subperiod level, and the period level. This was primarily to allow for the inclusion of occurrences whose stratigraphic occurrences were known at the subperiod and period levels, but not the stage level. Results were broadly similar dependent upon scale, however, there were exceptions where results of analyses at one scale differed from those at another. Variation in results when analyses are run at different scales is
Conclusions
Much like many post-Paleozoic sea urchins, the stem group echinoids clearly showed environmental preferences for both substrate lithology and for grain size. In general, most families of echinoids show a broad preference for carbonate environments, which is robust to secular variations in the abundance of carbonate and siliciclastic sediments in the rock record. Furthermore, when measured in a relative framework, different families show differential affinities for substrates of differing
Acknowledgments
This work was funded by the US National Science Foundation Grant IOS1240626 to D.J.B. J.R.T. acknowledges W. I. Ausich, E. Petsios and J. H. Nebelsick for informed discussion which helped to shape the ideas presented in this paper. We are highly indebted to the numerous museum curators, collections managers, and researchers who gave us access to their collections, which made up the bulk of our echinoid occurrence database. These include K. Hollis, D. Levin, M. Florence, and J. Strotman at the
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