Paleobiology, 32(3), 2006, pp. 483–510

Diversification of atypical Paleozoic echinoderms: a quantitative survey of patterns of stylophoran disparity, diversity, and geography

Bertrand Lefebvre, Gunther J. Eble, Nicolas Navarro, and Bruno David

Abstract.—The analysis of morphological disparity and of morphospace occupation through the macroevolutionary history of clades is now a major research program in paleobiology, and increas- ingly so in organismal and comparative biology. Most studies have focused on the relationship between taxonomic diversity and morphological disparity, and on ecological or developmental con- trols. However, the geographic context of diversification has remained understudied. Here we ad- dress geography quantitatively. Diversity, disparity, and paleogeographic dispersion are used to describe the evolutionary history of an extinct echinoderm clade, the class Stylophora (cornutes, mitrates), from the Middle Cambrian to the Middle Devonian (about 128 Myr subdivided into 12 stratigraphic intervals). Taxonomic diversity is estimated from a representative sample including 73.3% of described species and 92.4% of described genera. Stylophoran morphology is quantified on the basis of seven morphometric parameters derived from image analysis of homologous skel- etal regions. Three separate principal coordinates analyses (PCO) are performed for thecal outlines, plates from the lower thecal surface, and plates from the upper thecal surface, respectively. PCO scores from these three separate analyses are then used as variables for a single, global, meta-PCO. For each time interval, disparity is calculated as the sum of variance in the multidimensional mor- phospace defined by the meta-PCO axes. For each time interval, a semiquantitative index of paleo- geographic dispersion is calculated, reflecting both global (continental) and local (regional) aspects of dispersion. Morphospace occupation of cornutes and mitrates is partly overlapping, suggesting some mor- phologic convergences between the two main stylophoran clades, probably correlated to similar modes of life (e.g., symmetrical cornutes and primitive mitrocystitids). Hierarchical clustering al- lowed the identification of three main morphological sets (subdivided into 11 subsets) within the global stylophoran morphospace. These morphological sets are used to analyze the spatiotemporal variations of disparity. The initial radiation of stylophorans is characterized by a low diversity and a rapid increase in disparity (Middle Cambrian–Tremadocian). The subsequent diversification in- volved filling and little expansion of morphospace (Arenig–Middle Ordovician). Finally, both sty- lophoran diversity and disparity decreased relatively steadily from the Late Ordovician to the Mid- dle Devonian, with the exception of a second (lower) peak in the Early Devonian. Such a pattern is comparable to that of other Paleozoic marine invertebrates such as blastozoans and orthid bra- chiopods. During the Lower to Middle Ordovician, the most dramatic diversification of stylo- phorans took place with a paleogeographic dispersion essentially limited to the periphery of Gond- wana. In the Late Ordovician, stylophorans steadily extended toward lower paleolatitudes, and new environmental conditions, where some of them radiated, and finally survived the end-Ordo- vician mass extinction (e.g., anomalocystitids). This pattern of paleobiogeographic dispersion is comparable to that of other examples of Paleozoic groups of marine invertebrates, such as bivalve mollusks.

Bertrand Lefebvre, Gunther J. Eble, Nicolas Navarro,* and Bruno David. Centre National de la Recherche Scientifique, UMR 5561 Bioge´osciences, Universite´ de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France. E-mail: [email protected], E-mail: [email protected], E-mail: [email protected] *Present address: Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester M13 9PT, United Kingdom. E-mail: [email protected]

Accepted: 16 March 2006

Introduction eral respects. The Cambrian explosion can now be placed in the broader context of both The early Paleozoic radiations continue to the late Precambrian and the Ordovician fossil galvanize debates concerning the tempo and record, as it involved the origin not only of mode of macroevolution. Such debates, as well most animal phyla, but also of most classes as attendant empirical, theoretical, and meth- and orders. The Cambrian explosion has come odological issues, have in turn matured in sev- to be seen less as a single event and more as

᭧ 2006 The Paleontological Society. All rights reserved. 0094-8373/06/3203-0009/$1.00 484 BERTRAND LEFEBVRE ET AL. an ensemble of Cambro-Ordovician events tive generalizations have emerged (see Foote and processes relatively clustered in time and 1996, 1997; Valentine 2004). manifested as an unprecedented period of On the other hand, although disparity is major morphological innovation in the history now recognized as an appropriately rigorous of animal life. Furthermore, it is realized that measure to test hypotheses of differential con- the Cambro-Ordovician radiations are only straint over time and to address its causes, meaningful in contrast to what happened or geographic correlates of diversification have did not take place afterward, both in the Pa- rarely been incorporated into disparity stud- leozoic and post-Paleozoic. Ecological and de- ies. Theoretically and empirically, the geo- velopmental explanations involving differen- graphic context of morphological diversifica- tial flexibility and enhanced innovation dur- tion presents itself as potentially important in ing the early Paleozoic in particular, and dur- terms of both correlation and causation, and is ing evolutionary radiations in general, have eminently tractable given the paleogeograph- served as contrasting hypotheses for many ic data available. As is already the case with studies, and have been complemented by re- taxonomic diversity (Jablonski 1986, 1987, newed attention to the influence of the context 1993, 1998; Jablonski and Bottjer 1991), the of abiotic environmental change (Valentine possibility of meaningful geographic corre- 2004). lates of disparity dynamics could be condu- Against this backdrop, the quantification of cive to a better and broader understanding of morphological disparity and of morphospace the spatial context of morphological diversi- occupation emerged as a major research pro- fication. In this paper, we explicitly address gram in evolutionary paleobiology (e.g., Foote geography along with diversity and disparity, 1991, 1997; Gould 1991; Briggs et al. 1992; and attempt to develop a quantitative index to Wills et al. 1994; Conway Morris 1998; Valen- facilitate comparisons. In the arena of quantification of morpholo- tine 2004). This alternative view of macroevo- gy itself, Gould’s (1991) compelling case for lution effectively revitalized the practice of ‘‘why we must strive to quantify morpho- evolutionary paleobiology, and represented a space’’ motivated the rigorous characteriza- new ‘‘way of seeing’’ large-scale evolution, tion of morphospaces and of the dynamics of complementary to and enriching of more clas- morphological disparity, understood as a dis- sical taxonomic diversity descriptors of mac- tinct and relatively objective aspect of biodi- roevolutionary patterns and processes. The versity. However, a real challenge persists: study of disparity and morphospaces was making objects and variables commensurate. mainly stimulated by the prospect of more ob- The problem of quantification of data is a jectively characterizing morphological signa- perennial one, having already been recog- tures of diversification. In this context, pat- nized as fundamental 60 years ago, with terns of morphological disparity and taxo- Woodger’s (1945) critique of D’Arcy Thomp- nomic diversity are often discordant and for son’s transformation grids and its limits. More this very reason highly informative (e.g., Foote recently, Bookstein (1994: p. 220) provided this 1993a). assessment regarding morphometric studies Despite its scope, this research program is on macroevolutionary scales: ‘‘No important still a relatively young enterprise, and most evolutionary change can be captured persua- studies have focused on the relationship be- sively in the language of morphometrics.’’ tween taxonomic diversity and morphological Later, referring to ‘‘the incoherence of any leg- disparity through time, and on the ecological ible geometric metaphor for ‘‘morphospace’’ or developmental meaning of morphological above the species level,’’ he states: ‘‘The fun- and taxonomic signatures of evolutionary ra- damental analogy between a morphospace diations and diversification in general. A va- . . . and a vector space of shape descriptors riety of groups (arthropods, echinoderms, quickly becomes untenable as the relevant mollusks, and brachiopods) have been studied range of shapes broadens’’ (Bookstein 1994). in this manner and, inductively, a few tenta- Perhaps the survival of disparity and mor- DIVERSIFICATION OF ATYPICAL ECHINODERMS 485

FIGURE 1. Stylophoran morphology: Phyllocystis blayaci (Cornuta), Early Ordovician, Montagne Noire (France), about ϫ2.2 (redrawn and modified after Ubaghs 1970). A, Upper view. B, Lower view. C, Left lateral aspect. phospace studies lies in the multiple mean- (David et al. 2000). Stylophorans are an extinct ings of ‘‘shape,’’ a nontrivial issue. In any case, class of echinoderms (about 120 species and 66 Gould himself also voiced some doubts (1991: genera) that offers the possibility to illustrate p. 421): ‘‘I do confess some fears that, in toto, the complete evolutionary history of an echi- the question of morphospace may be logically noderm clade, from their initial radiation in intractable, not merely difficult.’’ the Middle Cambrian to their decline and fi- In other words, a variety of groups with nal disappearance in the late Carboniferous. puzzling morphologies discourage quantifi- Stylophorans are a major component of Late cation and do not immediately lend them- Cambrian to Early Ordovician echinoderm selves to a morphometric study with pre- faunas (Guensburg and Sprinkle 2000; Lefeb- scribed methods. Often, even within a higher vre and Fatka 2003). They have been recorded taxon, interspecific variation appears difficult from all around the world, with the exception to quantify and interpret, given the various of Antarctica. A relatively good phylogenetic scales of morphological organization and ho- framework is available for the class, which is mology. Is there a solution? Perhaps, if one is usually subdivided into the two monophyletic willing to consider a pluralistic approach in orders Cornuta and Mitrata (Ubaghs 1968; which several techniques are combined and Parsley 1988; Lefebvre 2001; Sprinkle and pragmatically explored. We argue that one Guensburg 2004). All stylophorans share the can, and must be willing, to abandon the hope same basic anatomical organization, with of uniformly applying one’s favored technique their body consisting of two well-defined re- in some instances, whether traditional, out- gions: the aulacophore and the theca (Fig. 1) line-based, or landmark-based. Instead, we (Ubaghs 1961, 1981; Chauvel 1981; Parsley must strive to be pluralistic and flexible in the 1988; Lefebvre 2001). The aulacophore is a del- methods we apply. Exactly how to do so re- icate, flexible, tripartite appendage.Itisa mains an open question, and there may be functional, composite structure comprising a several answers. Here we provide an empiri- feeding arm (distal regions), and an exothecal cal case study to address the issue in a mac- extraxial extension (proximal portion; David roevolutionary context. et al. 2000). The mouth is located at the base In this paper, the class Stylophora has been of the feeding arm (Ubaghs 1961; Nichols chosen as a model to document the initial di- 1972; David et al. 2000). The theca is a massive, versification of the phylum Echinodermata. flattened, asymmetrical extraxial calcite box, Stylophorans are one of four classes formerly which enclosed most organs in life. This ana- included in the subphylum ‘‘Homalozoa’’ tomical interpretation of stylophorans is root- 486 BERTRAND LEFEBVRE ET AL. ed in the Extraxial Axial Theory (Mooi et al. 1994; Bergstro¨m et al. 1998; David and Mooi 1999; David et al. 2000). However, the results of this paper are not conditioned on this the- ory, and the only prerequisite is that Stylo- phora corresponds to a monophyletic group, which is now widely accepted (e.g., Peterson 1995; Parsley 1997; Sumrall 1997; Ruta 1999a). Number, morphology, and arrangement of thecal skeletal elements (plates) are constant and diagnostic of a given species of stylo- phoran (Lefebvre 2001). A solid, well-estab- lished model of homologies has been pro- posed to identify equivalent skeletal elements FIGURE 2. Stylophoran taxonomic diversity: compari- among stylophorans (Lefebvre et al. 1998; Le- son of sampled and total number of described species. febvre and Vizcaı¨no 1999; Lefebvre 2000a,b, 2001). Such a model of plate homologies al- lows direct interspecific comparisons and the genus Placocystella (following Lefebvre 2001), use of a variety of morphometric methods to even though they were traditionally consid- quantify disparity. Although disparity could ered as belonging to four different genera be quantified in terms of total change with (Caster 1983; Parsley 1991, 1997; Ruta 1999b; phylogenetic measures (Smith 1994; Wills et Ruta and Jell 1999e). In this context, stylo- al. 1994; Wagner 1995; Eble 2000), no mor- phoran disparity has been estimated from the phospace would be made explicit, and its dif- largest possible sample of well-preserved ferential exploration would be difficult to forms, including 88 species and 61 genera, and evaluate in terms of phylogeny alone. In con- corresponding, respectively, to 73.3% and trast, disparity as net change (Foote 1995, 92.4% of all forms described to date. This sam- 1996) emphasizes both actual and possible lo- ple includes the two most primitive known cations of taxa in a multidimensional space of stylophoran species (genus Ceratocystis)and traits. Thus, morphospace itself is made ex- representatives of the two monophyletic or- plicit in discourse, analysis, representation, ders Cornuta and Mitrata. Here we consider and interpretation. The patterns documented cornutes and mitrates as clades, following by using this approach are independent of any phylogenetic analyses by Lefebvre and Viz- given phylogeny and of the phylogenetic po- caı¨no (1999) and Lefebvre (2001). The identi- sition of the Stylophora as a group, whether fication of plate homologies within stylophor- within or outside the echinoderms. ans strongly supports the view that the ‘‘an- kyroids’’ of Parsley (1997) are a polyphyletic Material and Methods assemblage based on superficial similarities Sampling. Data were collected at the spe- (Lefebvre 2001). In our analysis, 38 of 49 spe- cies level, based on a comprehensive, nearly cies (77.5%), and 27 of 30 genera of cornutes complete sample of stylophoran taxa. This (90%), and 48 of 69 species (69.6%), and 33 of choice was motivated by the small number of 35 genera of mitrates (94.3%) have been con- species described so far in the class (about sidered (see supplementary materials online 120), by the presence of great morphological at http://dx.doi.org/10.1666/05044.s1). variation within some genera (e.g., in Scotiae- Thirty-two species (five genera) were ex- cystis), and so as to avoid problems related to cluded from the analysis. However, this did the definition of genera, given that there is not affect the pattern of stylophoran diversity more consensus about the identity of species through time (Fig. 2). Taxa were excluded for than of genera. For example, all workers dis- the following reasons: (1) they are known only tinguish the four species P. africana, P. buretti, from isolated skeletal elements (e.g., the cor- P. flemingi,andP.garratti, included here in the nute Babinocystis dilabidus, most kirkocystid DIVERSIFICATION OF ATYPICAL ECHINODERMS 487 mitrates); (2) they were described from a sin- be neglected in comparison with interspecific gle, incomplete specimen (e.g., the cornutes variation (Chauvel 1941; Ubaghs 1968, 1979; Hanusia obtusa, Thoralicystis zagoraensis, Tri- Jefferies 1984; Ruta 1998; Lefebvre 1999; Ruta gonocarpus singularis); (3) their morphology is and Jell 1999d). Similarly, ontogenetic varia- too poorly known, owing to disarticulation, tion was not considered because it is very lim- poor preservation, and/or difficulty in dis- ited, with isometric growth being character- cerning plate boundaries (e.g., the cornute istic of most stylophorans. Reconstructions of Acuticarpus delticus, the mitrates Dalejocystis stylophorans used in this analysis have been casteri and Mongolocarpos minzhini); (4) there is extracted from the relevant literature (see sup- no reconstruction of their morphology avail- plementary materials). able in the literature (e.g., the mitrates Eno- Choice of Anatomical Scheme. The stylophor- ploura balanoides,and?Mitrocystites styloideus); an theca (Fig. 1) is an extraxial ‘‘box’’ with a (5) they possibly represent junior synonyms of stable plate pattern, made of a reduced num- taxa included in the analysis (e.g., Anomalo- ber of plates but still having the potential for cystites disparilis is a possible junior synonym local variation (extraxial regions are relatively of A. cornutus, after Parsley 1991). Further- free of constructional limitations as compared more, the exclusion of about 26.7% of stylo- to regions associated with the axial compo- phoran taxa for mostly preservational reasons nent [Mooi and David 1998; David and Mooi appears to be unbiased with respect to the 1999]). This stability allows the identification two major stylophoran groups, as comparable of homologous skeletal thecal elements in all proportions of cornutes (22.5%) and mitrates stylophorans (Lefebvre et al. 1998), thus per- (30.4%) were not sampled. However, a closer mitting the comparison of the wide array of examination of excluded taxa suggests that thecal morphologies exhibited by cornutes the occurrence of poorly preserved species is and mitrates. Here, we classically treat the flat not completely random within subgroups: for surface of the theca as homologous in cornutes example, 66.7% of peltocystid mitrates have and mitrates (Ubaghs 1968, 1981; Chauvel been excluded from the analysis, as most of 1981; Parsley 1988, 1997; Lefebvre 2000a, 2001; their species were described on the basis of but see Jefferies 1968, 1999). The aulacophore isolated skeletal elements (e.g., most species of has been discarded from the study for two the genus Anatifopsis). It should be stressed, main reasons: (1) it is the most delicate and however, that the small number of peltocys- brittle portion of the organism, and it is thus tids included in the analysis is not expected to seldom preserved (Lefebvre et al. 1998; Ruta alter the overall pattern of stylophoran dis- 1999a)—the precise length and morphology of parity, as morphologies are very conservative the distalmost portion of the aulacophore has in this group of mitrates. For example, the been only rarely documented (Ubaghs and morphologies of excluded taxa such as Anati- Robison 1988; Ruta and Bartels 1998; Sumrall fopsis balclatchiensis (Upper Ordovician) and and Sprinkle 1999); (2) its morphology, and es- ?Mitrocystites styloideus (Early Devonian) look pecially that of its distal portion (arm), is part- very similar to that of the included species A. ly composed of axial skeleton and thus is trapeziiformis (Early Ordovician). much less variable than the extraxial theca; the Whenever complete specimens were not morphology of the appendage is accordingly available, we relied on composite reconstruc- very conservative and uniform across all sty- tions, which are widely accepted. This was lophorans (Ubaghs 1968, 1981; Lefebvre 2001). necessary because fossil remains of stylophor- Plate Homologies. Three main systems of ans are almost always found more or less dis- plate homologies have been proposed for sty- articulated, distorted, and/or incomplete, so lophorans: the ‘‘calcichordate’’ (Jefferies and that reconstruction of their morphology is fre- Prokop 1972; Jefferies 1986; Cripps and Daley quently based on several individuals. This 1994), the ‘‘ankyroid’’ (Parsley 1997; Ruta was possible because intraspecific morpholog- 1999a), and the ‘‘Ceratocystis’’ models (Lefeb- ical variation, when documented in stylo- vre and Vizcaı¨no 1999; Lefebvre 2000b, 2001). phorans, is in most cases very limited and can The calcichordate system of plate homologies 488 BERTRAND LEFEBVRE ET AL.

FIGURE 3. Theca of the primitive stylophoran Ceratocystis perneri, Middle Cambrian, Bohemia (Czech Republic), about ϫ1.5 (redrawn and modified after Ubaghs 1968). A, B, Identification of plate homologies. A, Upper surface. B, Lower surface. C, D, Surfaces used for morphometric analysis. C, Upper surface. D, Lower surface. See text for abbreviations.

is well suited for recognizing homologies of homologous skeletal elements in both cor- within each stylophoran order, but it fails in nutes and mitrates, whatever their number of identifying equivalent skeletal structures in plates and the shape of their theca (e.g., boot- cornutes and mitrates (Ubaghs 1981; Ruta shaped, heart-shaped). The Ceratocystis model 1999a; Lefebvre 2000a; Marti-Mus 2002). In of plate homologies uses the plate terminolo- turn, the identification of homologous ele- gy first applied to mitrates by Jaekel (1901) ments is sometimes ambiguous in the anky- and later extended to cornutes (Ubaghs 1963). roid system because of superficial similarities In this terminology, the insertion of the aula- in shape and/or position (Lefebvre 2001). In cophore is considered as a reference point, contrast, the Ceratocystis system suggests that such that all marginals (M) and adorals (A) to the identification of homologies can be de- the right of it are designated Mn and An, and duced in all stylophorans from a comparison those to the left of it, M’n and A’n (with n as of their morphology with that of the most a number indicating the position of the plate primitive known member of the class, Cerato- away from the insertion of the aulacophore; n cystis (Fig. 3A,B). This system, which is adopt- ϭ 0 in the case of a plate in central position). ed below, consistently allows the identification However, this terminology was adjusted (fol- DIVERSIFICATION OF ATYPICAL ECHINODERMS 489 lowing Lefebvre and Vizcaı¨no 1999) so that ‘‘LM’’), whatever its number of elementary putatively homologous plates are given the plates and their putative identification. Con- same name. sequently, not only do such groupings of the- Number, morphology, and arrangement of cal elements follow the homology of subsets of thecal plates are constant and diagnostic for plates, but they also dramatically reduce the any given species of stylophoran, but highly sensitivity of the analysis to the adoption of variable from one species to another. A stylo- one particular model of plate homologies. phoran theca basically comprises two infra- All in all, 17 surfaces have been retained for central areas (left and right), one supracentral the analysis (see Fig. 3C,D): (1) thecal outline, Ј area, and 16 major plates, consisting of five TH; (2) M1; (3) M 1; (4) right marginals, RM ϩ ϩ Ј pairs of left and right marginals, three ador- (M2 M3 Mc); (5) left marginals, LM (M 2 ϩ Ј Ј als, one posterior zygal plate (Z), and two pos- M 3); (6) M4; (7) M 4; (8) glossal, G; (9) dig- terior elements (glossal and digital). However, ital, D; (10) posterior zygal plate, Z; (11) pos- ϩ Ј ϩ ϩ additional plates are sometimes present: co- terior marginals, PM (M5 M 5 PP1 PP2); thurnocystid marginal (Mc) in some cornutes, (12) plates of the right infracentral area, RIA; and posterior plates (PP1,PP2) in some mitro- (13) plates of the left infracentral area, LIA; cystitid mitrates. Consequently, the theca of (14) right adoral A1; (15) median adoral, A0; Ј some stylophorans comprises more than 16 (16) left adoral, A 1; and (17) plates of the su- major plates (e.g., 17 in the primitive cornute pracentral area, SA. The central marginal M0 Cothurnocystis fellinensis). Moreover, the right of Ceratocystis has not been considered in the infracentral area and/or several major skele- study because it is an autapomorphy of this tal elements are frequently lost in derived genus. forms, typically characterized by a theca con- The profile of the theca is sufficiently low so sisting of a reduced number of elements (e.g., that it is possible to consider that projections only ten major plates in the cornute Lyricocar- (drawings) of the plate patterns are without pus, and in kirkocystid mitrates). The number distortion. Portions of plates or groups of of plates seems to be particularly reduced in plates shared by both the lower and the upper the most recent stylophoran, Jaekelocarpus okla- thecal surfaces were considered as indepen- homaensis, with only nine major plates and a dent elements in each case and treated sepa- single integumentary area (Kolata et al. 1991; rately. This is justified because in most cases Domı´nguez et al. 2002). their extension is different on the lower and To perform the analysis of stylophoran dis- upper thecal surfaces. The only example of parity optimally, it was necessary to group surfaces showing similar extensions in upper some plates, so as (1) to minimize the effect of and lower views are the glossal (G) and digital large variation in the number of major skeletal (D), where these skeletal elements occur in the elements and integumentary areas in cornutes form of exothecal processes, articulated to the and mitrates, and (2) to reduce the uncertainty posterior end of theca (e.g., in the cornute Co- associated with the identification of some the- thurnocystis, and in most anomalocystitid mi- Ј cal plates. Whatever the adopted model of trates). The three adorals (A1,A 1,A0), and the plate homologies (‘‘calcichordate,’’ ‘‘anky- supracentral area (SA) are restricted to the up- roid,’’ or ‘‘Ceratocystis’’), several thecal ele- per thecal side in almost all stylophorans. Ј Ј ments (e.g., M1, M 1, adorals) are considered However, A1 and A 1 can extend onto the low- as equivalent by most authors (see Marti-Mus er side (e.g., Ceratocystis), and sometimes over- 2002: Fig. 9 for an overview of unambiguous lap the lateral edges of the underlying mar- plate homologies within cornutes). In this ginals (e.g., Anatifopsis, Balanocystites). Exten- study, each region of ‘‘problematic’’ thecal el- sion of supracentrals onto the lower side oc- ements was treated as if it constituted a single curs in the mitrate Lagynocystis. Consequently, thecal plate: for example, the left portion of the so as to avoid redundancy and autocorrelation marginal frame delimited by MЈ1, the left in- related to the extension of surfaces from the fracentral area, and MЈ4 was treated as a sin- upper side toward the lower side of the theca gle morphological unit (‘‘left marginals’’ or (e.g., overlap of marginal elements), no por- 490 BERTRAND LEFEBVRE ET AL.

Ј tionsofA1,A1, and SA located on the lower tion more roughly, but are also more reliable side of the theca have been considered in the at the level of the whole organism. analysis. Morphometric variables were measured us- Quantification of Form. Stylophoran mor- ing the software OPTIMAS (version 6). The phology has been quantified with morpho- measurements chosen were a subsample of metric parameters derived from image anal- the total number available, and the choice was ysis of homologous skeletal regions: plates, on carefully made in light of the stylophoran the one hand, and outlines of the theca, on the body plan. Finally, seven parameters (out of other. The aim is to use the geometry of both about 40) were specifically chosen for their the whole theca and its individual plates as ability to characterize all surfaces concerned. morphological descriptors to measure stylo- Together, they capture distinct yet comple- phoran disparity. This combined approach mentary aspects of plate and thecal morphol- also makes it possible to compare global and ogy. Special emphasis was placed on variables local aspects of stylophoran shape. Stylophor- considered the most pertinent for describing ans constitute an appropriate model for the the large array of plate outlines in stylophor- application of such morphometric methods, as ans (e.g., sub-circular to elliptical, sub-quad- they are a relatively small group with clearly rate to polygonal, rodlike, Y-, T-, or C-shaped). identified plate homologies, and with all spe- Redundant, uninformative, and/or uninter- cies sharing a standard organization. Conse- pretable (from a biological point of view) pa- quently, given the aim of the study and the in- rameters were discarded. Of the seven re- trinsic characteristics of stylophoran mor- tained parameters, four (1 to 4 below) were phology, it appears that morphometric meth- applied to all 17 areas, two (5 and 6 below) ods based on the geometry of both thecal only to the 16 plates and groups of plates, and outlines and homologous individual plates one (7 below) only to the whole theca. Defi- nitions for these variables are as follows: (1) constitute a good compromise approach to Circularity (C) expresses the ratio of the quantify disparity in the group. However, oth- square perimeter divided by the area. Circu- er descriptors of shape could have been used. larity is minimum for a circle (C ϭ 12.57), Procrustes methods based on landmarks, for which represents the smallest perimeter for a example, would have allowed us to estimate given area. Low circularity values correspond morphological variety among stylophorans by to rounded, massive surfaces, and high values comparing actual architectural relationships to long, narrow, and/or digitated surfaces. (2) between sets of plates, rather than on plate-by- Rectangularity (R) corresponds to the ratio of plate geometry per se. However, Procrustes the surface area divided by the area of the methods would not have permitted a compar- square box (parameterized by the major and ison between thecal and plate geometries. minor axes) including it. (3) Relative length Fourier methods are another powerful tool al- major axis (RLMA) is the ratio of the surface lowing precise description of outlines of sur- area divided by the square length of the major faces such as the theca or individual plates, axis of the corresponding surface. (4) Coeffi- but such precision is achieved at a cost of bi- cient of variation of Feret diameters (CVFD) ological interpretability; this is particularly represents the standard deviation as a pro- true in the present situation, where the num- portion of the mean of 16 successive diameters ber of distinct surfaces is considerable, and the measured every 11.5Њ around the surface. (5) too numerous Fourier coefficients would have Relative area (RA) expresses the ratio of a giv- been almost impossible to relate to morpho- en surface area divided by the area of the logical differences. In addition, the presence whole theca. (6) Relative perimeter (RP) cor- of distorted specimens inevitably leads to im- responds to the ratio of a given surface perim- precise reconstructions with uncertain reli- eter divided by the thecal perimeter. (7) Scaled ability of the fine details that Fourier analyses area (SA) is expressed in mm2 (chosen size es- are supposed to capture. Therefore, we pre- timate of the whole theca). ferred to use variables that convey informa- These variables were used to produce three DIVERSIFICATION OF ATYPICAL ECHINODERMS 491 separate raw data matrices: (1) for the whole theca, comprising 88 species and five morpho- metric variables (C, R, RMAL, CVFD, SA); (2) for plates and groups of plates of the lower surface, including 88 species and 72 morpho- metric variables (six variables measured for each of the 12 plates or groups of plates: C, R, RMAL, CVFD, RA, RP); and (3) for plates and groups of plates of the upper surface, includ- ing 88 species and 84 variables (six variables measured for each of 14 plates or groups of plates). Missing plates occasionally reflect imper- FIGURE 4. Diagram illustrating the degree of pairwise independence between the 84 variables of the upper sur- fect preservation of posterior thecal region (D face using Van Valen’s (1974) measure of dimensionality and G), but in most cases they reflect true ab- (D). Mean value of D is shown for each variable, as well sences. Coding in such situations proceeded as the 95% confidence interval. The degree of non-in- dependence is highly significant (p Ͻ 0.0001, sign test as follows. When due to imperfect preserva- with expected null value of 1.5). tion, entries were coded as missing values. When due to true plate absence, entries were coded as zero when logically interpretable sions. In this PCO space, species are naturally (RLMA, CVFD, RA, RP), or as a missing value ordinated in proportion to morphological dis- when this was mathematically impossible (C tance. Here, we treat PCO ordinations as pro- and R). viding a useful graphical representation of the It was not necessary to take into account general patterns of empirical morphospace oc- measurement error given that, at the scale of cupation. this study, observed interspecific differences A separate PCO analysis (using Gower’s are several orders of magnitude larger than distance-transformed coefficient for quantita- those induced by drawing error in the recon- tive characters) was performed on each of the struction of plate architecture. three data matrices referred to above. These To evaluate the persistence of correlations include (1) whole theca, (2) plates of lower the- among the variables considered in the three cal surface, and (3) plates of upper thecal sur- modules, we calculated Van Valen’s measure face. Given that our purpose was to consider of dimensionality or non-redundancy (Van all taxa and all three morphological contexts Valen 1974) for all pairwise comparisons be- together in a single, comprehensive analysis, tween variables pertinent to each of the three we performed a ‘‘meta-PCO’’ (similar to that modules. Figure 4 illustrates the result for the proposed by Klingenberg [1996] for ‘‘meta- upper surface only, but the degree of non-in- PC’’) based on the PCO axes (treated as new dependence is highly significant for the three variables) retained from each of the three modules, although weaker for the theca. analyses above. A meta-PCO allows for a bal- Data Analyses. Gower’s coefficient of simi- ance between the three anatomic modules larity (Gower 1971) and principal coordinates considered (whole theca, upper surface, lower analysis (PCO; Gower 1966) were used to an- surface), although they are each depicted by alyze the data. Although all variables were very different numbers of variables (5, 84, and continuous, Gower’s coefficient and PCO are 72 respectively). The number of PCO axes re- appropriate here so as to allow every species tained was based on the decay of the eigen- to be considered regardless of missing values. values. The quality of the reduced space rep- In addition, given that the variables are not all resentation (analogous to the cumulative pro- strictly commensurate, PCO is the technique portion of variance in principal components of choice. PCO axes were used to project the analysis) was estimated as the ratio of the sum original, raw multidimensional space onto a of the eigenvalues of the retained axes to the smaller, more informative number of dimen- total sum of the eigenvalues. Because of neg- 492 BERTRAND LEFEBVRE ET AL.

TABLE 1. Timescale, total number of stylophoran genera and species, and sample sizes. Age at base of intervals in millions years before present (Ma), and durations in millions of years (Myr) based on data from the International Stratigraphic Chart (Gradstein et al. 2004), and the new Ordovician stratigraphic chart (Webby et al. 2004a). Ab- breviations in parentheses are also used in the figures and the online appendix.

No. of genera No. of species Age at base Duration Stratigraphic interval (Ma) (Myr) Total Sampled Total Sampled Pennsylvanian (Pe) 318.1 19.1 1 1 1 1 Middle Devonian (MD) 397.5 12.2 4 3 4 3 Emsian (Em) 407.0 9.5 7 6 9 7 earliest Devonian (eD) 416.0 9 6 6 7 6 late Silurian (lS) 422.9 6.9 4 3 4 3 early Silurian (eS) 443.7 20.8 2 2 2 2 Ashgill (As) 449 5.3 8 8 11 8 Caradoc (Ca) 460.9 11.9 10 9 18 11 Middle Ordovician (MO) 471.8 10.9 19 19 27 21 Arenig p.p. (Ar) 478.6 6.8 21 19 29 23 Tremadocian (Tr) 488.3 9.7 7 7 9 7 Late Cambrian (LC) 501.0 12.7 6 4 7 4 Middle Cambrian (MC) 513.0 12 4 4 5 5 ative eigenvalues resulting from imbalance in time frame of the analysis (about 215 Myr) en- the distance matrices due to missing values compasses the entire evolutionary history of and non-Euclidean property of the resulting the class Stylophora, from the Middle Cam- distance, these sums were corrected according brian (Archaeocothurnus, Ceratocystis, Ponticu- to the absolute value of the largest negative ei- locarpus, Protocystites), to the Pennsylvanian genvalues (see Legendre and Legendre 1998). (Jaekelocarpus). It is worth pointing out that the Approximately 70% of the cumulative vari- recent discovery of Jaekelocarpus has consider- ance corresponded to most of the structure in ably extended the stratigraphic range of the all three analyses. Therefore, using this crite- class from the Middle Devonian to the late rion, five PCO axes were retained for the Carboniferous (Kolata et al. 1991; Domı´nguez whole theca, eight for the lower surface, and 8 et al. 2002). However, the presence of a single for the upper surface, yielding 21 ‘‘meta-var- species more than 65 million years after the iables’’ for the meta-PCO. In this way, a global Middle Devonian is uninformative. Thus, for morphospace projection reflecting different the purposes of reconstructing disparity his- aspects and scales of stylophoran variation tory, this interval was discarded from the was possible. All retained axes have larger val- study. Even so, the species was retained for its ues than the absolute value of the largest neg- contribution to the total empirical morpho- ative eigenvalues. Therefore, the Euclidean ap- space. The 12 stratigraphic intervals used in proximation of the reduced space is meaning- the analysis represent a compromise between ful (Legendre and Legendre 1998). sample size and time resolution (Table 1). In addition, cluster analysis was used to Ages and durations of time intervals were identify morphological clusters. This analysis based on the IUGS timescale produced by was performed using Euclidean distances and Gradstein et al. (2004), and the revised Or- unweighted pair-group method using arith- dovician stratigraphic chart of Webby et al. metic averages as aggregation rule. A thresh- (2004a). The duration of intervals is between old was identified according to the impor- 5.3 and 20.8 Myr, with a mean value of 10.7 tance of steps on the aggregation graph, and Myr, and duration of 9–13 Myr for 8 of 12 of the fine-scale structure of the dendrogram them. The duration of intervals and the num- was not kept. The resulting 11 morphological ber of taxa per interval (total number and/or groups are hierarchically clustered into three number of sampled taxa) are clearly not cor- main sets (I to III), and were used in turn as related (r2 ϭ 0.198, p ϭ 0.128; Table 1). morphological units in further analyses. Quantification of Geographic Space Occupa- Stratigraphic Intervals and Resolution. The tion. The aim was to define a semiquantita- DIVERSIFICATION OF ATYPICAL ECHINODERMS 493 tive index that could be used to draw curves number of regions ever occupied [NR]). of paleo(bio)geographic dispersion through Therefore, Bi ϭ Co/NC ϩ Ro/NR. time, comparable to curves of taxonomic and All stylophorans included in this study morphological diversity. Specifically, our goal were collected on the continental margins of was to use a biogeographic index that both is three paleocontinents: Baltica (Russia, Scan- relevant for large-scale studies and displays dinavia), Gondwana (Africa, South America, the same degree of generality with which di- Australia, southwestern Europe, Korea), and versity and disparity changes were docu- Laurentia (North America, northern Ireland, mented (only 12 stratigraphic intervals be- Scotland). However, by late Silurian times, tween the Middle Cambrian and the Middle Baltica and Laurentia had collided (Scandian Devonian). Therefore, such an index differs orogeny) to form a single paleocontinent, Lau- from most ‘‘traditional’’ paleogeographic in- russia. The estimate of stylophoran global dis- dices, usually designed for comparison of fau- persion is not affected by the reduction in the nal compositions and/or quantification of bio- number of major continental masses after the geographic affinities between regions. Geo- Silurian, as only one Laurussian species is graphic space occupation was quantified on considered (Anomalocystites cornutus). During both a global and a regional scale. the Ordovician, Avalonia (Belgium, England, The global scale reflects overall colonization most of Nova Scotia and New Brunswick, and dispersion patterns around continental Wales) formed a fourth, separate, short-lived margins, with high precision but low resolu- paleocontinent, which split off from the north- tion, given the relatively small number of sam- western margin of Gondwana (Early Ordovi- pling units (continents). Estimation of global- cian), drifted northward, and finally collided scale dispersion is based on available data with Baltica (Ashgill to early Silurian; Cocks concerning the absence/presence of stylo- et al. 1997; Nance et al. 2002; Verniers et al. phorans around paleocontinents (as defined 2002). Consequently, Avalonian faunas exhibit on paleoreconstructions; e.g., Scotese and strong Gondwanan affinities in the Early Or- McKerrow 1990; Scotese 2001), which reflect dovician, and increasing Baltic influences in general dispersion events. In contrast, the lo- the Late Ordovician (Cocks and Fortey 1990; cal scale expresses the number of distinct re- Cocks et al. 1997). In this study, Avalonian sty- gional occurrences around the same paleocon- lophorans were considered as ‘‘Gondwanan’’ tinent. Although the local approach is more from the Middle Cambrian to the Darriwilian, precise, and conveys more information than and as ‘‘Baltic’’ from the Caradoc to the Mid- the global one, the signal is more influenced dle Devonian. A fifth paleocontinent, Siberia, by preservational biases: the presence of sty- was not considered because the single known lophorans in a regional entity is partly corre- lated to outcrop area (volume and accessibil- stylophoran reported so far from this region ity of rock strata), number of echinoderm Lag- was too poorly preserved to be included (Mon- ersta¨tten, and effort of sampling (see Smith golocarpos minzhini). 1988). Several weighting combinations be- Seventeen distinct regional entities were tween continental and regional entities have considered: (1) eastern North America (Illi- been explored. All combinations are strongly nois, Indiana, Kentucky, Maryland, Missouri, correlated to each other (r2 Ն 0.90) and lead to New York State, Ohio, Oklahoma, Ontario, very similar ‘‘paleogeographic curves.’’ For Quebec, Pennsylvania, Tennessee, Virginia, the purpose of this paper, a ‘‘mixed’’ paleo- Wisconsin); (2) western North America (Ne- geographic index [Bi] was calculated for each vada, Utah); (3) Argentina; (4) Australia (Vic- time interval, as the sum of both relative glob- toria); (5) Bohemia; (6) Brazil (Parana´ Basin); al dispersion (number of distinct ‘‘continen- (7) England (Shropshire and Worcestershire) tal’’ occurrences [Co] divided by total number and Wales; (8) Germany; (9) Ibero-Armorica of paleocontinents [NC] ever colonized) and (western France, Spain, Portugal); (10) Korea; relative local dispersion (number of distinct (11) Montagne Noire (southern France); (12) regional occurrences [Ro] divided by total Morocco (Anti-Atlas); (13) New Zealand; (14) 494 BERTRAND LEFEBVRE ET AL.

Norway; (15) Scotland and Northern Ireland; (16) South Africa; (17) Tasmania.

Results and Discussion Morphospace Ordination. Principal coordi- nate analysis of the 21 ‘‘meta-variables’’ re- veals considerable structure in the data, with about 27.5% of the variation expressed in the first three ‘‘meta-axes.’’ At face value, the amount of information conveyed in this com- pound analysis is smaller than that obtained in each of the three ‘‘source’’ analyses per- formed independently on the theca (63% of the variance in the first three axes), the lower FIGURE 5. Plot of the global morphospace of the 88 surface (51.5% of the variance in the first three sampled stylophoran species on the first two principal coordinates axes of the meta-PCO, with distinction be- axes), and the upper surface (48.2% of the var- tween primitive forms, and representatives of the two iance in the first three axes). Nevertheless, de- main clades, cornutes and mitrates. spite an unavoidable loss of resolution, the meta-PCO analysis has the advantage of con- stituting an integrative and heuristic ap- form, Ceratocystis vizcainoi. The partitioning of proach allowing representation and visuali- the two main clades of stylophorans in this zation, however obliquely and partially, of a morphospace is relatively clear: cornutes ‘‘global’’ morphospace that takes simulta- show great variability along meta-PCO1 but neously into account three different aspects of reduced dispersion along meta-PCO2 (with stylophoran morphology. These three aspects almost exclusively positive values), whereas are here viewed as the relevant organizational mitrates are characterized by great variability and variational modular regions of the phe- along the metaPCO2, and to a lesser extent notype (Eble 2004, 2005), and each modular also along meta-PCO1 (Fig. 5). As plotted, the region in turn can be expressed in terms of a two groups are relatively distinct, although partial morphospace. Combining partial mor- there is a large zone of overlap representing phospaces allows the portrayal of all sampled convergent morphologies among certain mi- species in a single global morphospace, which trocystitid mitrates (e.g., Ovocarpus, Vizcaino- is not the case for the source PCO analyses of carpus) and various derived cornutes (e.g., the lower surface (six missing species) and of Amygdalotheca, Lyricocarpus). It is interesting the upper surface (12 missing species; see sup- to point out that the two primitive forms of the plementary materials). The meta-axes of the genus Ceratocystis appear in a position rough- global PCO analysis reflect a multidimension- ly intermediate between the clouds of points al space in which ordination is possible for all corresponding to cornutes and to mitrates. sampled stylophorans, including partially The partitioning of cornutes and mitrates in preserved forms. this global reference morphospace reflects The projection of this multidimensional quite well the preliminary results previously space in the plane defined by the first two obtained by principal components analyses of meta-axes, i.e., meta-PCO1 (10.5% of the var- the thecal outlines and of the lower surface iance) and meta-PCO2 (9.5% of the variance), (Lefebvre et al. 2003). In fact, those results allows a partial yet still heuristically infor- suggested that although the distinction be- mative and practical visualization of broad tween cornutes and mitrates was very clear morphospace occupation among stylophorans with respect to the morphology of plates in (Fig. 5). Occupation in general is not homo- the lower surface, these two groups could not geneous, with several ‘‘clouds’’ or groupings be distinguished on the basis of their thecal situated at the periphery of an almost empty outlines. This indicates that very similar thecal central ‘‘zone,’’ occupied only by a primitive outlines were independently achieved by the DIVERSIFICATION OF ATYPICAL ECHINODERMS 495 two clades, but with plates having different relatively large thecal width (set III, subsets Ia, morphologies (Lefebvre et al. 2003). Similarly, Ic–Ie, and IIb), from forms with reduced or ab- the existence of a region of overlap between sent integumentary surfaces and with a nar- cornutes and mitrates in the global morpho- rower and more elongated theca (subsets Ib, space defined by the meta-PCO axes can be and IIa, IIc, IId). The third axis of the meta- explained by the fact that variables describing PCO is more difficult to interpret, but it shows thecal outline and variables describing plate a distinction between two ensembles of sub- morphology were both taken into account. In sets: in one case, Ia, Ib, and IIIa (positive val- any case, the present study seems to confirm ues), and in the other case, Ic–Ie, IIb, and IIIb the existence of form convergences between (negative values); the remainder subset, IIa, is the two groups (see Lefebvre 2001). spread all along meta-PCO3 (taking both pos- In order to minimize a priori taxonomic as- itive and negative values). sumptions, and so as to better characterize the Set I comprises 36 stylophorans (10 cornutes heterogeneities in occupation of stylophoran and 26 mitrates), all characterized by massive morphospace (the existence of a large zone of thecae, symmetrical and without outgrowths, superposition between its two component and with integumentary areas at times re- groups suggesting that the classical distinc- duced (subset Ib), but more often relatively tion between cornutes and mitrates is not nec- large (subsets Ia, Ic–Ie). The second set com- essarily the most pertinent for describing dis- prises 38 stylophorans (two primitive forms, parity), several morphological subgroups of 14 cornutes, and 22 mitrates) with an asym- stylophorans were identified a posteriori, on metrical theca, sometimes with extensive out- the basis of hierarchical clustering of all pair- growths and infracentral areas (subset IIb), wise distances. The application of this cluster- but more often reduced (subsets IIa, IIc, IId). ing procedure yielded a dendrogram of dis- Finally, set III comprises 14 cornutes that are tances among different stylophoran species in very strongly asymmetric (boot-shaped the- the multidimensional space defined by the ca), characterized by large integumentary ar- axes of the meta-PCO (Fig. 6). Eleven morpho- eas (subset IIIa) and by large exothecal out- logical subgroups (understood as operational growths (subset IIIb). subsets) were revealed. These 11 subsets can It is interesting to note that the general as- themselves be grouped into three main sets (I, pect of the dendrogram produced by hierar- II, and III), containing five (Ia–Ie), four (IIa– chical clustering for purely operational rea- IId), and two subsets (IIIa, IIIb), respectively. sons resembles the general aspect of the clad- Seven subsets comprise at least six species, but ogram produced by Parsley (1997, 1998). In ef- four subsets are small and contain only one fect, sets I and II bring together the (IIc, IId), two (Id), or three (Ie) taxa. ‘‘ankyroid’’ stylophorans (mitrates and sym- The first axis of the meta-PCO is mainly in- metrical cornutes), whereas set III corre- fluenced by the general morphology of thecal sponds to cornutes with a boot-shaped theca. contours (Fig. 7). This axis discriminates clear- These observations suggest that the phyloge- ly stylophorans belonging to sets II and III, netic tree produced by Parsley (1997, 1998), characterized by very asymmetrical and dig- which takes into account numerous characters itated thecal contours (thecal outgrowths, based on the general morphology and the such as digital, glossal, and spinal; positive asymmetry of the theca, may be more similar values of scores in meta-PCO1), from those in in structure to a dendrogram than to a clad- set I, which have symmetrical and massive ogram (see Lefebvre 2001). thecae, without outgrowths (negative values The existence of convergent morphologies in meta-PCO1). The second axis of the meta- among cornutes and mitrates, for example be- PCO appears to reflect more the relative im- tween mitrocystitids and symmetrical cor- portance of integumentary areas (especially nutes (set I) or between asymmetrical cornutes infracentral; Fig. 7). Meta-PCO2 thus sepa- and mitrates with posterior processes (set II), rates quite clearly forms with large integu- brings to the fore the issue of a possible rela- mentary surfaces and, consequently, with a tion between morphology and mode of life. 496 BERTRAND LEFEBVRE ET AL.

FIGURE 6. Dendrogram resulting from the hierarchical clustering of the global stylophoran morphospace (see Fig. 5), and showing the disconnection into three well-defined main morphological sets (I, II, and III), consisting of five (Ia–Ie), four (IIa–IId), and two (IIIa, IIIb) subsets, respectively. Morphologies included in each subset are illustrated by some significant taxa (all thecae illustrated in lower view, and showing surfaces used for morphometric analysis): 1, Adoketocarpus acheronticus;2,Aspidocarpus bohemicus;3,Chinianocarpos thorali;4,Mitrocystites mitra;5,Ovocarpus moncereti;6,Ateleocystites guttenbergensis;7,Barrandeocarpus jaekeli;8,Eumitrocystella savilli;9,Mitrocystella incipiens; 10, Yachalicystis triangularis; 11, Amygdalotheca griffei; 12, Lyricocarpus courtessolei; 13, Nanocarpus milnerorum; 14, Re- ticulocarpos hanusi; 15, Ampelocarpus landeyranensis; 16, Prochauvelicystis semispinosa; 17, Lobocarpus vizcainoi; 18, Viz- cainocarpus dentiger; 19, Balanocystites primus; 20, Ceratocystis perneri; 21, Diamphidiocystis drepanon; 22, Lagynocystis pyramidalis; 23, Placocystella africana; 24, Arauricystis primaeva; 25, Chauvelicystis spinosa; 26, Hanusia prilepensis; 27, Ponticulocarpus robisoni; 28, Protocystites menevensis; 29, Jaekelocarpus oklahomaensis; 30, Diamphidiocystis sp.; 31, Ar- auricystis occitana; 32, Cothurnocystis fellinensis; 33, Phyllocystis blayaci; 34, Scotiaecystis jefferiesi; 35, Thoralicystis griffei; 36, Cothurnocystis elizae; 37, Galliaecystis ubaghsi; 38, Scotiaecystis collapsa; 39, Scotiaecystis curvata. DIVERSIFICATION OF ATYPICAL ECHINODERMS 497

FIGURE 7. Plot of the global morphospace of the 88 FIGURE 8. Plot of the global morphospace of the 88 sampled stylophoran species on the first two principal sampled stylophoran species on the first two principal coordinate axes of the meta-PCO, with distinction be- coordinate axes of the meta-PCO, with distinction be- tween the 11 morphological subsets identified by hier- tween infaunal and various epibenthic forms. archical clustering (see Fig. 6).

with anchoring by the theca (IIb in cornutes Four major modes of life among stylophorans and IId in mitrates), or else endobenthic (only have been identified (Lefebvre 2003): one is mitrates, IIa). A certain correspondence be- endobenthic (theca buried under the sub- tween thecal morphology and mode of life strate), and three are epibenthic, with the an- could be expected, given that the latter was imal attaching itself to the substrate by means partly deduced from the general aspect of the of thecal protuberances, spines arranged on theca (Lefebvre 2003). However, there is no di- the perimeter of the theca, or the arm. A gen- rect correspondence between thecal morphol- eral relationship seems to exist between mor- phology and mode of life (Fig. 8). In fact, ogy and presumed mode of life, as the latter meta-PCO1 discriminates quite well the epi- was also largely deduced from the morphol- benthic forms anchored with the arm (and ogy of the appendage (Lefebvre 2003), which having a rather symmetric theca; left of dia- is not considered herein. Moreover, several as- gram) from the endobenthic and epibenthic pects of stylophoran thecal morphology are forms clinging to the sediment by means of not correlated with functional morphology the theca (asymmetric forms and/or forms (e.g., asymmetry of lower thecal surface, with having exothecal outgrowths; right of the di- the zygal bar), but possibly reflect construc- agram). Similarly, meta-PCO2 separates quite tional constraints. well, on the right portion of the diagram, the It is also interesting to note that certain epibenthic forms anchored by means of the morphological types were never developed in theca or of spines (large integumentary areas, mitrates (e.g., set I), perhaps because such thecae staggered transversally; positive val- types are associated with a mode of life in- ues on meta-PCO2) from the endobenthic herently uncommon in this clade (epibenthic forms (reduced integumentary areas, thecae with anchoring by the theca; e.g., Diamphidi- staggered anteroposteriorly; negative values ocystis). Likewise, neither of the two main on metaPCO2). Therefore, it is probable that morphological types characteristic of burrow- very similar morphologies, independently ing forms was adopted by cornutes (subsets Ib evolved in some cornutes and mitrates, show and IIa). This suggests the existence, in each very similar modes of life, as exemplified in of the two clades, of functional limits and/or set I (epibenthic mode of life with anchoring structural constraints intrinsic to their body by the arm). On the other hand, in set II the plans, and impervious to convergent evolu- presence of exothecal outgrowths corresponds tion. Thus, although convergence is relatively to two very distinct modes of life: epibenthic common, it is conditioned on the degrees of 498 BERTRAND LEFEBVRE ET AL. freedom established in the history of the phospace previously partitioned in the Tre- clade. madocian. This important Arenigian phase of Spatiotemporal Pattern of Stylophoran Diversi- taxonomic diversification occurred exclusively fication in Morphospace. The spatiotemporal on the north-Gondwanan margin, i.e., the evolution of taxonomic and morphologic di- same paleogeographic region as in the Tre- versity may be followed in simplified fashion, madocian. by representing, for each of the 12 stratigraph- Stylophoran taxonomic diversity steadily ic intervals considered (representing about decreased from the Middle Ordovician to the 128 Myr from the base of the Middle Cambri- end of the Ashgill (Fig. 10). Nevertheless, mor- an to the end of the Givetian), the distribution phological disparity was maintained, with the of various forms in the projection of the global persistence of the three main morphological morphospace and the corresponding paleo- sets even as the number of subsets represented geographic dispersion. Thus, inspection of the regularly declined (eight in the Middle Or- temporal sequence of 12 morphospace projec- dovician, four in the Caradoc, and three in the tions on the meta-PCO1–metaPCO2 plane be- Ashgill) and intermediate forms among the side 12 associated ‘‘snapshots’’ of paleogeo- three sets disappeared. In the Ashgill, these graphic partitioning allows a generalized but three sets were represented only by extreme heuristic assessment of the broad evolutionary morphologies, such as those of the strongly dynamics of this class of echinoderms. A suc- asymmetric cornutes Cothurnocystis elizae or cession of five main phases is apparent and Scotiaecystis curvata. In parallel with the de- explained below. cline in taxonomic diversity and the evacua- Initially, from the Middle Cambrian to the tion of morphospace, stylophorans showed an Tremadocian (Fig. 9), stylophorans under- increase in paleogeographic dispersion from went an apparent increase in disparity, in the Middle Ordovician to the Ashgill, with ex- spite of the relatively small sample sizes. Al- pansion into Avalonia, then Laurentia, and fi- though members of only one main morpho- nally Baltica and the east-Gondwanan mar- logical set (II) were represented in the Middle gin). This paleogeographic expansion was ac- Cambrian (subsets IIa and IIb), they were fol- companied by a decrease in disparity within lowed by two (I and II) in the Late Cambrian the region of origin (the north-Gondwanan (subsets Ic, Ie, and IIb), and finally three (I, II, margin) and by a relatively low disparity and III) in the Tremadocian (subsets Ic, Id, Ie, within each of the different zones occupied at IIa, IIb, and IIIa). Therefore, in less than 35 the end of the Ordovician. It is also apparent Myr, stylophorans occupied all three distinct that one of the three main morphologies re- zones in morphospace; no other main mor- maining in the Ashgill (IIa, anomalocystitids) phological set would appear in the ensuing exhibited a vast paleogeographic distribution 180 Myr. This expansion in morphospace was at lower paleolatitudes, on both sides of the accompanied by an even greater paleogeo- equator. This type of stylophoran dispersion graphic dispersion during the Cambrian, but seems very different from that of the Early it must be emphasized that disparity re- and Middle Ordovician, almost exclusively mained low within each of the three zones limited to high paleolatitudes. The paleogeo- considered. Conversely, in the Tremadocian, graphic expansion toward low paleolatitudes, disparity increased strongly, while paleogeo- observed from the Middle Ordovician, might graphic dispersion was extremely low (re- conceivably correspond to the adaptation of stricted to the northern-Gondwanan margin). certain forms to new environmental condi- During the early and middle Arenig (Fig. tions. 9), stylophorans displayed a marked increase The early Silurian (Fig. 10) was character- in taxonomic diversity, yet disparity remained ized by a profound reduction not only of tax- comparable to that of the Tremadocian, de- onomic diversity, but also of disparity, as there spite the appearance of two additional mor- remained only one morphological type (II), phological subsets (Ia and IIIb). This interval represented by a single subset (IIa). Through seems to correspond to a simple filling of mor- this time interval, by far the longest in this DIVERSIFICATION OF ATYPICAL ECHINODERMS 499

FIGURE 9. Evolution of stylophoran morphospace occupation and paleogeographic dispersion from the Middle Cambrian to the end of the Early Ordovician. 500 BERTRAND LEFEBVRE ET AL.

FIGURE 10. Evolution of stylophoran morphospace occupation and paleogeographic dispersion from the Middle Ordovician to the early Silurian (Llandovery–Wenlock). DIVERSIFICATION OF ATYPICAL ECHINODERMS 501 study (20.8 Myr), paleogeographic distribu- graphic dispersion. This phase was followed tion was also strongly reduced, with one spe- by a slight decrease in diversity and disparity cies from the Llandovery of Tasmania (Placo- (two morphological types each represented by cystella buretti) and one species from the Wen- only one subset) and reduced paleogeograph- lock of England (Placocystites forbesianus). ic dispersion in the Middle Devonian. Also, a These two anomalocystitid mitrates are from second important difference from the Cam- regions then situated at very low paleolati- bro-Tremadocian radiation concerns the pa- tudes and they belong to the same morpho- leogeographic context of the Siluro-Devonian logical type (IIa) as that of Ashgillian stylo- diversification: whereas the former occurred phorans present in those regions. This was essentially in a single region (the northern- also the first time since the Middle Cambrian Gondwanan margin), the latter was character- that stylophorans were absent from the vari- ized by strong paleogeographic dispersion. ous regions of the northern-Gondwanan mar- Spatiotemporal Pattern of Stylophoran Diversi- gin. In fact, in the early Silurian these regions fication: Comparison of Quantitative Indices. were characterized by extensive deposits of The three main aspects of the stylophoran di- black shale, indicating the existence (and per- versification of interest in this study, i.e., tax- sistence) of anoxic oceanic conditions follow- onomic diversity, morphological disparity, ing the major climatic perturbations of the and paleogeographic dispersion, can be ana- end-Ordovician (Cocks and Fortey 1990; Paris lyzed in a more rigorous manner by means of and Le He´risse´ 1992; Storch et al. 1993). It is comparisons through time of quantitative in- therefore possible that the presence of a single dices summarizing the general signal con- stylophoran morphological type in the early veyed by each of these aspects. The taxonomic Silurian signaled not only the disappearance diversity curve expresses temporal variations of types I and III from high paleolatitudes, by in number of species. The morphological dis- virtue of unfavorable environmental condi- parity curve indicates, for each interval con- tions (anoxia), but also the persistence of type sidered, the sum of the variances of the prin- II only at low paleolatitudes, given that pa- cipal coordinates scores as calculated by the leoenvironmental conditions were more favor- software MDA (Navarro 2003). Other relevant able (Cocks and Fortey 1990; Robardet et al. disparity measures, such as the total range, 1990), and given that this type became estab- were explored, but the results did not differ lished in the end-Ordovician. Curiously, the much, or else demanded the use of rarefaction only morphological type that survived the bi- with a baseline sample size too small to allow ological crisis at the end of the Ordovician (set meaningful interpretation, owing to the large II) was precisely the same that was initially error bars. The sum of the variances was present in the Middle Cambrian. therefore chosen as the reference disparity Finally, from the late Silurian to the Middle measure because it is relatively insensitive to Devonian (Fig. 11), stylophorans underwent a sample size differences, and more directly second phase of diversification, which corre- comparable and interpretable with a number sponded to an increase in disparity with the of other studies of disparity in the literature. reappearance of the type I morphology. Con- Error bars for disparity values were estimated sequently, in contrast to the Cambro-Trema- by bootstrapping (Efron and Tibshirani 1993). docian radiation, no fundamentally new For each stratigraphic interval, species coor- forms evolved during the Siluro-Devonian di- dinates on PCO axes were resampled with re- versification—as if somehow mitrates were placement and the sum of variance was cal- limited in their evolution and could only pro- culated. This procedure was repeated 500 duce morphologies of types I and II. This sec- times, and the mean and standard deviation ond phase was characterized by a peak of di- were calculated. Standard deviation of the versity and disparity (two morphological bootstrap samples provides an estimate of the types, represented by three subsets, Ia, Ib, and standard error, which, in paleobiological stud- IIa) in the Early Devonian (Lochkovian to Em- ies, essentially reflects an estimate of analyti- sian), as well as by an increase in paleogeo- cal error (Foote 1993b). Finally, the curve sum- 502 BERTRAND LEFEBVRE ET AL.

FIGURE 11. Evolution of stylophoran morphospace occupation and paleogeographic dispersion from the late Si- lurian (Ludlow–Pridoli) to the Middle Devonian. DIVERSIFICATION OF ATYPICAL ECHINODERMS 503

FIGURE 12. Patterns of stylophoran disparity (thick FIGURE 13. Patterns of stylophoran disparity (thick line) and taxonomic diversity (thin line) from the Mid- line) and paleogeographic dispersion (dotted line) from dle Cambrian to the Middle Devonian. Disparity is mea- the Middle Cambrian to the Middle Devonian. Disparity sured as the sum of variances. Diversity is the number is measured as the sum of variances. Paleogeographic of sampled species. Errors bars on disparity were esti- dispersion measured as indicated in the text. Errors bars mated by bootstrap (500 replications). MC, Middle Cam- on disparity were estimated by bootstrap (500 replica- brian. LC, Late Cambrian. Tr, Tremadocian. Ar, Arenig tions). Abbreviations as in Figure 12. pro parte. MO, Middle Ordovician. Ca, Caradoc. As, Ashgill. eS, early Silurian. lS, late Silurian. eD, earliest Devonian. Em, Emsian. MD, Middle Devonian. parity and paleogeographic dispersion re- veals two distinct diversification phases (Fig. marizing general paleogeographic dispersion 13). During the first phase, which corresponds through time was constructed by calculating to the principal radiation (Middle Cambrian for each stratigraphical interval an index of to Middle Ordovician), the signals of dispar- dispersion reflecting the distribution of both ity and paleogeographic dispersion appear in- global (paleocontinents) and local (regions) versely related: dispersion was maximal when samples (see above). disparity was lowest (Cambrian) and, con- The comparison of diversity and disparity versely, dispersion was minimal when dispar- curves (Fig. 12) quantitatively confirms the ity was highest (Early to Middle Ordovician). various patterns revealed by the qualitative During the second phase (Late Ordovician to examination of the details of morphospace oc- Middle Devonian), the relationship between cupation in the metaPCO1-metaPCO2 projec- the two signals was reversed. tion (Figs. 9–11). A very clear discordance ex- Conclusions isted between disparity and diversity in the first half of stylophoran history, although it The disjunction between the peaks of dis- was manifested in several ways. During the parity and diversity during the initial radia- initial radiation phase (Cambro-Tremado- tion of stylophorans is in itself an interesting cian), disparity greatly increased while diver- result, given that a similar pattern character- sity remained relatively low. From the earliest izes a number of other marine invertebrate Arenig to the Middle Ordovician, disparity clades, including arthropods (Gould 1989; remained elevated and relatively constant, Briggs et al. 1992; Foote and Gould 1992; Wills while diversity strongly increased and et al. 1994), brachiopods (Carlson 1992; reached its peak (Fig. 12). Finally, from the McGhee 1995), gastropods (Wagner 1995), Late Ordovician (Caradoc) to the Middle De- blastozoans (Foote 1992, 1993a), and crinoids vonian disparity and diversity show relatively (Foote 1994, 1995, 1999). Nevertheless, the op- good concordance, with both decreasing mo- posite pattern has also been described, for ex- notonously, despite a second peak in the Early ample in trilobites whose Cambrian diversity Devonian (though much smaller than the Ear- peak clearly preceded the Ordovician dispar- ly to the Middle Ordovician). ity peak (Foote 1991, 1993a). In the case of sty- The comparison between the signals of dis- lophorans, it seems that diversification was 504 BERTRAND LEFEBVRE ET AL. characterized by a relatively rapid saturation (both taxonomic and morphologic) during the of morphospace, with initially few species in initial history of stylophorans runs conversely the Cambro-Tremadocian occupying rapidly to the hypothesis of diffusion on a global but sparsely the main morphospace regions, scale, which entails an expectation of positive later followed, in the Arenig-Middle Ordovi- correlation between the two signals. This re- cian, by an important phase of diversification lationship suggests that the colonization of that nonetheless only filled in an already oc- new geographic areas, and putatively of new cupied morphospace. environments, is not necessary for speciation The macroevolutionary pattern of stylo- and morphological differentiation. The stylo- phorans is quite similar to that documented phoran pattern is reminiscent of other groups for several other marine invertebrate groups, of marine invertebrates, in particular bivalve which began to diversify comparatively slow- mollusks. Bivalves apparently radiated in the ly during the Cambrian, achieving a diversity Cambrian, diversified extensively in the Early peak in the Ordovician, and then declined in and Middle Ordovician, but remained ex- relatively consistent manner until their dis- tremely restricted paleogeographically (Babin appearance during the late Paleozoic (Car- 1993; Cope and Babin 1999; Cope 2004). From boniferous–Permian), but still displayed a sec- the Caradoc onward, bivalves extended their ond disparity peak in the Early Devonian. range toward lower paleolatitudes, where a This is the case of blastozoans (Foote 1992, second major diversification occurred, though 1993a) and orthid brachiopods (Harper and they became rarer and less diverse in the re- Tychsen 2004). The similarity in macroevolu- gion of origin (notably the northern-Gond- tionary patterns might have involved common wanan margin). The similarity of the stylo- causes (e.g., paleoenvironmental) to particular phoran and bivalve macroevolutionary pat- fluctuations and/or reflect more general mac- terns suggests perhaps the influence of com- roevolutionary trends, of intrinsic (increase in mon paleoenvironmental controls of the constraint through time) or extrinsic character paleogeographic dispersion of these two (replacement of the Paleozoic fauna by the groups. modern fauna). Preservational and sampling More generally, results of the threefold ap- biases cannot be completely excluded, notably proach (diversity, disparity, geography) pur- with respect to the strong decline in both tax- sued in this study suggest that the relation- onomic and morphological diversity in the Si- ships among the three signals can be complex lurian and to the diversity peak in the Early and at times too idiosyncratic for simple in- Devonian. Indeed, as with stylophorans, a terpretation. Still, the explicit consideration of number of echinoderm groups relatively com- the geographic context of taxonomic and mor- mon in the Ordovician were virtually absent phological diversification has enhanced our in the Silurian, only to reappear in Lazarus- understanding of the macroevolutionary dy- like fashion in the Early Devonian. This was namics of stylophorans by providing an im- the case, for example, of solutes and of pleu- portant additional perspective for the char- rocystitid rhombiferans. Thus, the rarity of acterization and interpretation of biodiversity. certain echinoderm groups in the Silurian Biodiversity is inherently complex, having may be tied to the lack of preservation (or un- multiple aspects, measures, and contexts. Ac- derrepresentation) of certain types of environ- cordingly, different patterns are likely to be ments or Lagersta¨tten. Finally, stylophorans collectively informative in novel and valuable differ from other groups with an otherwise ways, complementing the rich body of knowl- similar pattern by the fact that their diversity edge stemming from generally accepted stud- clearly peaked earlier: earliest Arenig (‘‘un- ies focusing on a particular aspect, measure, named stage 2’’ [Sprinkle and Guensburg and context. 2004]) instead of Middle to Late Ordovician Although comparisons of diversity and dis- (Foote 1992; Harper and Tychsen 2004). parity have yielded important insights about The apparent inverse relationship between macroevolution, more work is needed because paleogeographic dispersion and diversity generalizations have emerged mostly in an in- DIVERSIFICATION OF ATYPICAL ECHINODERMS 505 ductive fashion, and many groups still await lution and Cognition Research (Vienna, Aus- study. An eventual theory of biodiversity dy- tria), as well as by research grants from the namics cast in terms of diversity and disparity Deutsche Forschungsgemeinschaft to the In- remains possible, but would remain inevitably terdisciplinary Centre for Bioinformatics partial given the heterogeneity of biodiversi- (University of Leipzig, Germany). We thank ty. It may well be that some components of our referees, M. Foote and M. A. Wills, for biodiversity are less informative and of lim- their detailed critique and insightful sugges- ited interest or applicability in paleobiology, tions. yet factors such as biogeography are well es- tablished in their empirical and theoretical Literature Cited value for understanding diversification and its Babin, C. 1993. Roˆle des plates-formes gondwaniennes dans les controls. diversifications des mollusques bivalves durant l’Ordovicien. Biogeography should be more widely con- Bulletin de la Socie´te´Ge´ologique de France 164:141–153. 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List of species included in the analysis, with corresponding taxonomic group, stratigraphic ranges, illustration sources for reconstructions used in morphometric analysis, and studied areas. MC ϭ Middle Cambrian; LC ϭ Late Cambrian; Tr ϭ Tremadocian; Ar ϭ Arenig pro parte (Early Ordovician, stage 2 of Webby et al. 2004); MO ϭ Middle Ordovician (stages 3 and 4); Ca ϭ Caradoc; As ϭ Ashgill; eS ϭ early Silurian (Llandovery and Wenlock); lS ϭ late Silurian (Ludlow and Pridoli); eD ϭ early Devonian (Lochkovian and Praguian); Em ϭ Emsian; MD ϭ Middle Devonian (Eifelian and Givetian); Pe ϭ Pennsylvanian. Abbreviations for bibliographic references are: 1 ϭ Beis- swenger (1994); 2 ϭ Chauvel (1966); 3 ϭ Craske and Jefferies (1989); 4 ϭ Cripps (1988); 5 ϭ Cripps (1989a); 6 ϭ Cripps (1989b); 7 ϭ Cripps (1990); 8 ϭ Cripps and Daley (1994); 9 ϭ Daley (1992); 10 ϭ Gil Cid et al. (1996); 11 ϭ Haude (1995); 12 ϭ Jefferies (1968); 13 ϭ Jefferies (1986); 14 ϭ Jefferies and Lewis (1978); 15 ϭ Jefferies and Prokop (1972); 16 ϭ Jefferies et al. (1987); 17 ϭ Kolata and Guensburg (1979); 18 ϭ Kolata and Jollie (1982); 19 ϭ Kolata et al. (1991); 20 ϭ Lee et al. (2005); 21 ϭ Lefebvre (1999); 22 ϭ Lefebvre (2000b); 23 ϭ Lefebvre (2000c); 24 ϭ Lefebvre and Gutie´rrez-Marco (2003); 25 ϭ Lefebvre and Vizcaı¨no (1999); 26 ϭ Marti Mus (2002); 27 ϭ Parsley (1991); 28 ϭ Ruta (1997); 29 ϭ Ruta (1999a); 30 ϭ Ruta (1999b); 31 ϭ Ruta and Bartels (1998); 32 ϭ Ruta and Jell (1999a); 33 ϭ Ruta and Jell (1999b); 34 ϭ Ruta and Jell (1999c); 35 ϭ Ruta and Jell (1999e); 36 ϭ Ruta and Theron (1997); 37 ϭ Smith and Jell (1999); 38 ϭ Sumrall and Sprinkle (1999); 39 ϭ Ubaghs (1963); 40 ϭ Ubaghs (1968); 41 ϭ Ubaghs (1970); 42 ϭ Ubaghs (1979); 43 ϭ Ubaghs (1983); 44 ϭ Ubaghs (1987); 45 ϭ Ubaghs (1991); 46 ϭ Ubaghs (1994); 47 ϭ Ubaghs and Robison (1988); 48 ϭ Woods and Jefferies (1992). These references are listed in the Literature Cited section. Abbreviations for studied surfaces: TH ϭ Theca; LTS ϭ Lower Thecal Surface; UTS ϭ Upper Thecal Surface.

Species Order Range Refs. Studied areas Adoketocarpus acheronticus mitrate lS 33 TH, LTS, UTS Adoketocarpus janeae mitrate eD 33 TH, LTS Ampelocarpus landeyranensis cornute Ar 25 TH, LTS, UTS Amygdalotheca griffei cornute Tr–Ar 41 TH, LTS Anatifopsis barrandei mitrate MO–Ca 21 TH, LTS, UTS Anatifopsis minuta mitrate MO 23 TH, UTS Anatifopsis trapeziiformis mitrate Tr–MO 21 TH, LTS, UTS Anomalocystites cornutus mitrate eD 27 TH, LTS, UTS Arauricystis occitana cornute Ar 46 TH, LTS, UTS Arauricystis primaeva cornute Ar 41 TH, LTS Archaeocothurnus bifida cornute MC 47 TH, LTS, UTS Aspidocarpus bohemicus mitrate Ca 42 TH, LTS, UTS Aspidocarpus discoidalis mitrate MO 7 TH, LTS, UTS Aspidocarpus riadanensis mitrate Ca 22 TH, LTS Ateleocystites guttenbergensis mitrate Ca 18 TH, LTS, UTS Ateleocystites huxleyi mitrate Ca 40 TH, LTS Balanocystites primus mitrate Ar–MO 23 TH, LTS, UTS Barrandeocarpus jaekeli mitrate Ca 42 TH, LTS, UTS Barrandeocarpus norvegicus mitrate As 3 TH, LTS, UTS Beryllia miranda cornute MO 8 TH, LTS, UTS Bokkeveldia oosthuizeni mitrate Em 36 TH, UTS Ceratocystis perneri primitive MC 40 TH, LTS, UTS Ceratocystis vizcainoi primitive MC 44 TH, UTS Chauvelicystis spinosa cornute Ar 41 TH, LTS, UTS Chauvelicystis ubaghsi cornute Ar 2 TH, LTS, UTS Chauvelicystis vizcainoi cornute Ar 9 TH, LTS Chinianocarpos thorali mitrate Ar 13 TH, LTS, UTS Cothurnocystis courtessolei cornute Ar 41 TH, LTS, UTS Cothurnocystis elizae cornute As 40 TH, LTS, UTS Cothurnocystis fellinensis cornute Tr–Ar 41 TH, LTS, UTS Diamphidiocystis drepanon mitrate As 17 TH, LTS, UTS Diamphidiocystis sp. mitrate MO 23 TH, LTSa Domfrontia pissotensis cornute MO 8 TH, LTS, UTS Drepanocarpos australis cornute LC 37 TH, LTS, UTS Enoploura popei mitrate Ca–As 27 TH, LTS, UTS Eumitrocystella savilli mitrate MO 1 TH, LTS, UTS Flabellicarpus rushtoni cornute Tr 26 TH, LYS, UTS Galliaecystis ubaghsi cornute Ar 41 TH, LTS, UTS Hanusia prilepensis cornute MO 6 TH, LTS, UTS Jaekelocarpus oklahomaensis mitrate Pe 19 TH, LTS, UTS Kierocystis inserta mitrate Ca 27 TH, UTS Kopficystis kirkfieldi mitrate Ca 27 TH, UTS Lagynocystis pyramidalis mitrate Ar–MO 40 TH, LTS, UTS Lobocarpus vizcainoi mitrate LC 22 TH, LTS Lyricocarpus courtessolei cornute Ar 25 TH, LTS, UTS 510

Appendix. Continued.

Species Order Range Refs. Studied areas Milonicystis kerfornei cornute MO 8 TH, LTS, UTS Mitrocystella incipiens mitrate MO 12 TH, LTS, UTS Mitrocystites mitra mitrate MO 40 TH, LTS, UTS Nanocarpus dolambii cornute Ar 45 TH, LTS, UTS Nanocarpus milnerorum cornute As 29 TH, LTS, UTS Nevadaecystis americana cornute LC 39 TH, LTS, UTS Occultocystis koeneni mitrate eD–Em 11 TH, UTS Ovocarpus moncereti mitrate Ar–MO 24 TH, LTS, UTS Paranacystis petrii mitrate Em 40 TH, LTS, UTS Paranacystis simoneae mitrate MD 21 TH, LTS Peltocystis cornuta mitrate Ar 41 TH, LTS, UTS Phyllocystis blayaci cornute Ar 41 TH, LTS, UTS Phyllocystis crassimarginata cornute Tr–Ar 41 TH, LTS, UTS Placocystella africana mitrate Em–MD 36 TH, LTS, UTS Placocystella buretti mitrate eS 30,35 TH, LTS, UTS Placocystella flemingi mitrate Em 30,35 TH, LTS, UTS Placocystella garratti mitrate lS 30,35 TH, LTS, UTS Placocystites forbesianus mitrate eS 14 TH, LTS, UTS Ponticulocarpus robisoni cornute MC 38 TH, LTS, UTS Prochauvelicystis semispinosa cornute Tr 9 TH, LTS, UTS Procothurnocystis owensi cornute MO 48 TH, LTS, UTS Prokopicystis mergli cornute MO 5 TH, LTS, UTS Promitrocystites barrandei mitrate MO 40 TH, LTS, UTS Proscotiaecystis melchiori cornute Ar 43 TH, LTS Protocystites menevensis cornute MC 16 TH, LTS, UTS Protocytidium elliotae mitrate As 32 TH, LTS, UTS Pseudovictoriacystis problematica mitrate eD 34 TH, LTS, UTS Reticulocarpos hanusi cornute MO 15 TH, LTS, UTS Rhenocystis latipedunculata mitrate Em 31 TH, LTS, UTS Scotiaecystis collapsa cornute As 4 TH, LTS, UTS Scotiaecystis curvata cornute As 12 TH, LTS, UTS Scotiaecystis guilloui cornute MO 25 TH, LTS, UTS Scotiaecystis jefferiesi cornute Ca 10 TH, LTS, UTS Sokkaejaecystis serrata cornute LC 20 TH, LTS, UTS Thoralicystis bouceki cornute MO 40 TH, LTS, UTS Thoralicystis griffei cornute Ar 41 TH, LTS, UTS Victoriacystis hulmesorum mitrate eD 34 TH, LTS, UTS Victoriacystis wilkinsi mitrate lS 28 TH, LTS, UTS Vizcainocarpus dentiger mitrate Ar 22 TH, LTS, UTS Vizcainocarpus rutai mitrate Tr 22 TH, LTS Willmanocystis denticulata mitrate Ca 18 TH, LTS, UTS Yachalicystis triangularis mitrate eD–Em 11 TH, LTS, UTS Yachalicystis sp. mitrate MD 21 TH, LTS