evolutionary history of cambrian spiculate sponges - GeoScienceWorld

PALAIOS, 2008, v. 23, p. 124–138 Research Article DOI: 10.2110/palo.2006.p06-089r

EVOLUTIONARY HISTORY OF CAMBRIAN SPICULATE SPONGES: IMPLICATIONS FOR THE CAMBRIAN EVOLUTIONARY FAUNA MARCELO G. CARRERA1* and JOSEPH P. BOTTING2 1

Universidad Nacional de Co´rdoba, CIPAL (Centro de Investigaciones Paleobiolo´gicas), Facultad de Ciencias Exactas, Fı´sicas y Naturales, Av. Velez Sarsfield 299 (5000) Co´rdoba, Argentina; 2Leeds Museum Discovery Centre, Carlisle Road, Leeds LS10 1LB, UK e-mail: [email protected]

ABSTRACT Broad-scale analyses of Cambrian spiculate sponges are scarce. The apparent differences between Cambrian and Ordovician sponge faunas were included in Sepkoski’s concept of evolutionary faunas; in these, sponges were regarded as minor contributors to the Paleozoic and modern faunas and insignificant in the Cambrian Evolutionary Fauna. More recent published occurrences of Cambrian and Ordovician spiculate sponges and the inclusion of archaeocyaths in the phylum Porifera, however, have altered our understanding of the significance of sponges among Cambrian faunas. The majority of Cambrian occurrences appear to be segregated into two major associations: lower Cambrian sponges in China, and middle Cambrian sponges in North America, primarily British Columbia and Utah. The main associations of spiculate sponges are in siliciclastic deposits from middle-to-deep muddy shelf and basin environments, whereas orchoclad demosponges are associated with shallow carbonate environments. Four main aspects of sponge biology are considered potential factors dictating the distribution of sponges in the Cambrian: their trophic requirements, hydrodynamic constraints, possible biogeochemical constraints, and the sponge-sediment relationship. A series of critical steps in sponge evolutionary history occurred during the interval from the Proterozoic-Cambrian boundary to the middle– late Ordovician. The lower–middle Cambrian faunas are considered to be a Cambrian evolutionary sponge fauna, with archaeocyaths and diverse monaxonid demosponges as distinctive components. There was a transitional fauna in the upper Cambrian–Lower Ordovician, with orchoclad lithistids dominating shallow environments. Hexactinellids began to colonize nearshore siliciclastic settings during this time. The third interval, Middle–Upper Ordovician, corresponds to the Paleozoic Evolutionary Fauna, which is the interval during which lithistids diversified in several suborders and families and the stromatoporoid and sphinctozoan calcified sponges experienced their first radiation.

sons between the middle Cambrian Burgess Shale Formation and Stephen Formation and to the lower Cambrian Chengjiang faunas (Debrenne and Reitner, 2001; Rigby and Collins, 2004; Dornbos et al., 2005; Steiner et al., 2005; Xiao et al., 2005). Previous attempts to differentiate between Cambrian and Ordovician sponge faunas were integrated at the time of Sepkoski’s proposal of evolutionary faunas (Sepkoski, 1981). Sponges were excluded from the Cambrian Evolutionary Faunas both because archaeocyathan affinities were not clear and because of the scarcity of taxonomic studies on other sponge groups (Sepkoski and Sheehan, 1983). Sponges were also regarded as minor contributors to the Paleozoic and modern faunas. Most spiculate sponges have a very intermittent record owing to the fragility of their skeleton, although they have a continuous history from the Late Neoproterozoic. The record of some groups with coherent or rigid skeletons is good. Isolated spicules are abundant and widely distributed, but faunas of complete nonlithistid sponges are very rare, and the record of sponge diversity is certainly extremely incomplete. Despite this, their record is becoming better known, and database-style compilations of published occurrences provide a useful summary of present knowledge, which converges toward reality through time. New published occurrences of Cambrian and Ordovician spiculate sponges have allowed the compilation of an updated database. This new database shows that spiculate and calcified sponges were much more diversified in the Cambrian than recognized previously. Ordovician occurrences and their distribution patterns were compiled recently by Carrera and Rigby (2004), although this does not include the diverse faunas recently described by Botting (2004, 2005). DATABASE CHARACTERISTICS

* Corresponding author.

The majority of Cambrian occurrences are segregated into two major associations (Figs. 1 and 2): lower Cambrian sponges in China (Chen et al., 1989, 1990; Mehl and Reitner, 1993; Rigby and Hou, 1995; Wu et al., 2005; Xiao et al., 2005) and middle Cambrian sponges of North America, notably from British Columbia (Walcott, 1920; Rigby, 1986a; Rigby and Collins, 2004), Utah (Rigby and Gutschick, 1976; Rigby, 1978, 1980, 1983a; Rigby and Church, 1990; Rigby and Gunther, 2003), Vermont and Pennsylvania (Walcott, 1886; Resser and Howell, 1938), Wyoming and Nevada (Howell and van Houten, 1940; Okulitch and Bell, 1955), Texas and Colorado (Wilson, 1950), and Idaho (Church et al., 1999). Lower Cambrian occurrences of sponges in North America are very scarce with only three described species (Rigby, 1987). Other minor associations of Cambrian sponges occur in Australia (Kruse, 1983, 1987; Picket and Jell, 1983; Mehl, 1998), Siberia (Ivantsov et al., 2005), Spain (Sdzuy, 1969; Garcia-Bellido Capdevila, 2003), Germany (Sdzuy, 1969), Argentina (Beresi and Rigby, 1994), Greenland (Rigby, 1986b), Iran (Mostler and Mosleh-Yazdi, 1976; Hamdi et al., 1995), Wales (Salter, 1864), and Ireland (Rushton and Phillips, 1973). Isolated spicules have been recorded elsewhere in the Cambrian (see Zhang and Pratt, 1994; Debrenne and Reitner, 2001), but only those occurrences of isolated spicules with generic designation are included in

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INTRODUCTION In this paper the main features of early sponge evolution are identified and discussed, particularly the main factors involved in their Cambrian and Ordovician radiation. New ideas and previous interpretations explaining the distribution of Cambrian sponges are considered in the light of new database compilations, in an attempt to provide a coherent initial framework for early Paleozoic sponge evolution. Integrated analyses of Cambrian sponges are scarce and restricted mainly to studies of archaeocyath paleogeography and diversification (Zhuravlev, 1986, 2001; Wood et al., 1992; Debrenne and Reitner, 2001). Broad-scope analyses and discussions of Cambrian spiculate sponges are even more limited (Finks 1970; Reitner and Mehl, 1995; Mehl-Janussen, 1999; Carrera, 2005; Botting, 2007), and most are confined to compari-

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EVOLUTIONARY HISTORY OF CAMBRIAN SPICULATE SPONGES

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FIGURE 1—Cambrian paleogeographic map showing distribution of main groups of spiculate sponges and archaeocyaths. Relative size of pie charts represents the number of species.

the database. Some important occurrences of spicules, however, yield significant information for the reconstruction of sponge evolutionary history; these are summarized here. Reitner (in Reitner and Wo¨rheide, 2002) recorded the oldest spicules with demosponge affinities from Nevada (ca. 750 Ma) and in the Cloudina reefs of Namibia (ca. 555 Ma). The first record of tetractinellid spicules is from the base of the Cambrian Flinders Ranges, Australia (Bengtson et al., 1990). Late Neoproterozoic hexactinellids have been reported in China (Tang et al., 1978; Xing et al., 1985; Steiner et al., 1993; Wu et al., 2005; Xiao et al., 2005) and in Mongolia (Brasier et al., 1997), although some of these have been questioned. A complete Ediacaran spongelike organism, Palaeophragmodictya reticulata Gehling and Rigby, 1996, has been interpreted as a hexactinellid or a stem-group sponge (Mehl, 1998). Dispersed hexactinellid spicules are common in the Nemakit-Daldynian–Tommotian rocks (Ding and Qian, 1988; Rozanov and Zhuravlev, 1992; Qian, 1999). There is now general consensus regarding the inclusion of archaeocyaths into a separate group of calcified aspiculate sponges (Debrenne and Vacelet, 1984; Kruse, 1990; Debrenne and Zhuravlev, 1994; Debrenne and Reitner, 2001). Archaeocyaths are restricted to the lower and middle Cambrian and are only conspicuous in the lower Cambrian. They appeared in the Tommotian, progressively colonized Atdabanian and Botomian carbonate platforms, and declined in the Toyonian. Only a few forms persisted into the middle and late Cambrian. Archaeocyaths were adapted to restricted conditions of temperature, salinity, and depth and were limited to tropical and subtropical seas (Zhuravlev, 1986; Debrenne

and Coujault-Rade´, 1994; Debrenne et al., 1999; Debrenne and Reitner, 2001). The paleoenvironmental setting and paleogeographic location is considered in the database for each sponge record (see Supplementary Data1). Most localities have fairly clear sedimentological features that allow for confident paleoenvironmental analysis, including the major associations of China and Utah. The environmental settings of one of the major sponge localities, the Burgess Shale Formation and Stephen Formation, however, are still partially unresolved. Briggs et al. (1994) suggested the parautochthonous burial of the association in the Burgess Shale and Stephen formations from the adjacent carbonate escarpment (i.e., Cathedral Formation). In contrast, Rigby and Collins (2004) analyzed in detail the geographic and stratigraphic distribution of sponges within the Burgess Shale and Stephen formations. Their analysis also considered the taphonomic characteristics and taxonomic composition of each sponge locality and suggested that they were communities and not just assemblages; some can clearly be considered in situ communities. They found that some communities could live on the deep carbonate shelf or talus and others in the deep muddy shelf or basin. In this survey, the Burgess Shale locality is taken as a deep shelf environment, a generalization that clearly differentiates the fauna from the shallow shelf and shallow carbonate shelf environments, at the scale of this analysis. 1

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FIGURE 2—Similarity dendrogram in Q mode for the main Cambrian spiculate sponge assemblages.

METHODS A database was constructed of all sponge descriptions in the global literature that classified the taxa to the level of species or genera (see Supplementary Data1). The entries include details of stratigraphic position as far as possible, in the older Cambrian subdivisions of Lower, Middle, and Upper. Rather than creating ambiguities by converting records to the modern stratigraphy (International Commission on Stratigraphy, n.d.), we have retained the older divisions but leave them uncapitalized in acknowledgment of their now unofficial status. A conversion diagram between the traditional and modern timescales is provided in Figure 3. Data were also included for the geographical area and paleoenvironment. The data for three regions with diverse faunas (Burgess Shale Formation and Stephen Formation sponges, South China associations, and the Wheeler Shale communities of Utah) were compared using the Simpson similitude coefficient. This particular method of analysis was used in order to test statistically the degree of paleogeographic difference among localities in the same continent and between continents and was implemented using PAST (Hammer and Harper, 2004). More detailed discussions of the diversity trends of individual elements of the fauna follow below. RESULTS The cosmopolitan occurrence of the main representative sponge genera and broad paleogeographic distribution of sponge associations in the Cambrian allow a global-scope analysis. The Chinese associations, the British Columbian faunas, and the Utah sponge biotas in total constitute 70% of the described Cambrian sponge species. Only these localities have sufficient species to be considered statistically significant for comparative analysis. For these regions, the similitude coefficient is near 0.7 for the Burgess-Utah pair and 0.4 between the Burgess-Utah pair and China. Although, similarity in taxonomic composition is relatively high between the main associations (Fig. 2), the proportion of endemic taxa is also

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significant (20%–45%). Dissimilarity, as expected, is high only in the more geographically distant associations of British Columbia and China. The Burgess Shale and Stephen formations of British Columbia have produced 26 genera, of which 12 are endemics and 9 are shared with China; China has also yielded 26 genera including 12 endemics. Utah has 12 genera of which 6 are shared with China, 8 are shared with British Columbia, and 2 are endemic. Among the common taxa of these regions are widespread genera such as Protospongia and Leptomitus, which also occur in such minor associations as those in Spain, Vermont, Pennsylvania, and Wales. Among other faunal links between regions, Diagoniella is found in Siberia and Argentina, Choia and Vauxia in Greenland in addition to the primary areas, and Kiwetinokia in Argentina and Quebec. The Cambrian sponge record is limited compared with Ordovician occurrences—139 species of spiculate sponges are recorded in the Cambrian, and more than 300 in the Ordovician. Seventy-five genera are recorded in the Cambrian, consisting of 20 protomonaxonid demosponges with 43 species, and 28 hexactinellids with 46 species. The rest are distributed among heteractinids (Calcarea) with nine genera, anthaspidellids (demosponges) with six genera, and Verongida with one record. The distribution of the main groups of spiculate sponges through the Cambrian and Lower Ordovician is shown in Figure 3. Sclerosponges are represented by three genera of sphinctozoan grade, and the stromatoporoids are also barely represented (Reitner and Wo¨rheide, 2002; Flu¨gel and Singh, 2003). The main associations of Cambrian spiculate sponges are in siliciclastic deposits from middle-to-deep muddy shelf and basinal environments. These relatively deep environments yield only demosponges, hexactinellid sponges, and a few heteractinids. The record of geological settings in the database shows that 69 species were recorded in deep-shelf-to-talus environments and 39 species in deep basin settings (Fig. 4). The spiculate sponge record in carbonate platform settings includes 29 species in shallow carbonate platforms and 14 in deep carbonate shelves. Most species recorded in these carbonate environments belong to orchocladine demosponges, mainly restricted to upper Cambrian records, and calcareous heteractinid and sphinctozoan sponges recorded in the lower and middle Cambrian. Many lower and middle Cambrian sponge localities occur in siliciclastic deposits, such as the Chengjiang associations (Chen et al., 1989, 1990; Rigby and Hou, 1995), the Niutitang of Sansha in Hunan (Steiner et al., 1993), South Anhui (Wu et al., 2005; Xiao et al., 2005), British Columbia (Walcott, 1920; Rigby, 1986a; Rigby and Collins, 2004), Greenland (Rigby, 1986b), Siberia (Ivantsov et al., 2005), Spain (Sdzuy, 1969; Garcia-Bellido Capdevila, 2003), Ireland (Rushton and Phillips, 1973), and Vermont and Pennsylvania (Walcott, 1886; Resser and Howell, 1938). Environmental settings of these associations are included in the Supplementary Data.1 A particular environment is recorded for most of the sponges recorded in Utah. The association occurred in two different deep or quiet-water environments: the Wheeler Shale Formation in the House Range (Rigby and Gutschick, 1976; Rigby and Church, 1990; Rigby and Gunther, 2003), and the silty calcareous deposits of the Marjum Limestone Formation (Rigby, 1987). The Marjum Limestone Formation is considered to have been deposited in deep shelf environments. Although mainly associated with deep environments, monaxonid and hexactinellid sponge distributions show slight variations through the Cambrian (Figs. 4B–C). There is a more conspicuous occupation by both groups of deep basin environments in the lower Cambrian, whereas middle Cambrian records are somewhat more closely associated with deep shelf, including talus, and deep carbonate shelf environments. Shallow carbonate environments were dominated by archaeocyaths, although they are found associated with calcareous and demosponge spicules (Debrenne and Reitner, 2001). Heteractinids and sphinctozoans occur in the lower and middle Cambrian calcareous rocks of Australia (Pickett and Jell, 1983; Kruse, 1987, 1996) but are never abundant. Exceptionally, hexactinellid spicules were recorded in lower Cambrian archaeocyath reefs of Siberia (Kruse et al., 1995), and monaxon (hexactinellid or de-

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FIGURE 3—Species distribution of the main spiculate sponge groups through the Cambrian and Lower Ordovician.

mosponge) spiculites occur in lower–middle Cambrian mixed carbonatesiliciclastic, shallow water deposits of Spain (A´lvaro and Vennin, 1997). Records of early lithistid demosponges are limited and are concentrated in the late Cambrian. Only one group of lithistids, the orchoclad anthaspidellids, has been recorded; this group is mostly restricted to shallow carbonate platforms. In addition to two anthaspidellids recorded in the Burgess Shale Formation and Stephen Formation, Fieldospongia and Capsospongia, other genera (Rankenella, Gallatinospongia, and Wilbernicyathus) are recorded from Australia, Iran, Texas and Colorado, Wyoming, Nevada, and California. All are from shallow carbonate rocks, and most are associated with reef settings (Shapiro and Rigby, 2004; Johns et al., 2007). Fragmentary or complete anthaspidellid specimens (as yet undescribed) have also been reported from Argentina (Beresi and Rigby, 1994), Altai Sayan (Zhuravleva, 1960), and in reef associations of Texas (Spincer, 1996) and Russia (Teslenko et al., 1983). The Early and Middle Ordovician record (see Carrera and Rigby, 2004) shows a different taxonomic distribution. Anthaspidellids dominate with 36 genera, whereas monaxonids decreased to 8 genera and hexactinellids

retained their diversity with 15 genera in Lower and Middle Ordovician rocks. The Ordovician records (Carrera and Rigby, 1999, 2004) come from more globally widespread sites than the Cambrian associations, and the level of endemism varies through the period. Around 30%–50% of genera were endemic in Early Ordovician localities. The Late Ordovician faunas record a considerable increase in diversity and provinciality (Carrera and Rigby, 2004). Among lithistid demosponges, anthaspidellids are still important, but new suborders appeared, and the sphinctozoan calcareans diversified remarkably. Although preservation could be affecting the record of spiculate sponges—the more preservable lithistids dominate platform areas—a significant number of records of nonlithistid demosponges have been found, sometimes in association with lithistids and with the similar high degree of preservation. Well-preserved, shallow water monaxonids and hexactinellids have been found in carbonate and siliciclastic environments in Ordovician associations (Carrera, 1994, 1998; Botting, 2005, 2007). In Tremadoc–Arenig siliciclastics of Morocco, monaxonid demosponges

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glutinating and lithistid demosponges, and rare heteractinids (Botting, 2005). In terms of dominance, the expansion of lithistids in the Ordovician is likely a real phenomenon, considering that few lithistids were recorded in the late Cambrian in more or less the same shallow carbonate environments in which they later diversified. A decreased diversity of nonlithistid demosponges in the Ordovician is more difficult to establish, however. Although this is a clear pattern among published records (Carrera and Rigby, 2004), new data (Botting, 2004, 2005, 2007) have shown that nonlithistid demosponges were more diversified in the Ordovician than has been recognized up to now. SPONGES IN THE CONTEXT OF EVOLUTIONARY FAUNAS

FIGURE 4—Species distribution of spiculate sponges through different environmental settings, including all groups (A) or divided into protomonaxonids (B) and hexactinellids (C).

dominated the sponge biota of the middle shelf, with isolated spicules of an asthenospongiid-like hexactinellid (Botting, 2007). In the lower Llanvirn of Wales, diverse shallow water communities in coarse-grained sandstones include a variety of thick-walled hexactinellids, monaxonid, ag-

Sepkoski’s model of evolutionary faunas is still the large-scale model on which many evolutionary interpretations of marine invertebrates are based, although simplification is inevitable when attempts are made to generalize on this scale. Sepkoski’s Cambrian Evolutionary Fauna includes, in descending order of importance, the Trilobita, Linguliformea, Hyolitha, Tergomya, and Eocrinoidea (Sepkoski and Sheehan, 1983). New discoveries and continuous advances in sponge studies allow a reconsideration of the importance of sponges to the Cambrian Evolutionary Fauna. Figure 5 shows the relative abundance of sponge families, including archaeocyaths, and their contribution as reef builders. The inclusion of archaeocyaths, with approximately 120 families (Rigby et al., 1993), radically affects the perceived status of sponges. Another potentially misleading point is the consideration of demosponges as a uniform group of sponges. We show that the protomonaxonids were the dominant group of demosponges in the Cambrian, while a completely different group of demosponges (lithistids) diversified in the Ordovician and remained an important group for the rest of the Paleozoic. Placing more emphasis on sponges in the context of evolutionary faunas allows the division of the early Paleozoic sponge fauna into three main intervals that emerge from this analysis (see Fig. 6): The lower– middle Cambrian interval can be considered the Cambrian Evolutionary Fauna as originally defined—archaeocyaths and monaxonid demosponges being distinctive components of the sponge fauna. A second interval, the upper Cambrian–Lower Ordovician, represents a transitional fauna in which orchoclad lithistids became the dominant group in the preserved sponge fauna. After the final demise of archaeocyaths in the middle Cambrian (they were nearly extinct by the end of the Toyonian), a reorganization period incorporating the late Cambrian and Tremadocian occurred, with orchoclads recreating the shallow-shelf, reef-type ecosystem that had been absent since the extinction of archaeocyaths. Upper Cambrian and Tremadocian sponge records are limited compared with lower and middle Cambrian occurrences. Sponges in this interval appear to have been differentiated into orchoclads in shallow water carbonates and dominantly hexactinellids in deep water environments. The Tremadocian still shows an upper Cambrian aspect with an increase of orchoclads in carbonate platforms, and records of hexactinellids and monaxonids in deep water environments. There are also records of Lower and Middle Ordovician hexactinellids and monaxonids in shallow water, siliciclastic settings, however (Carrera, 1998; Botting, 2007). The third, Middle–Late Ordovician interval can be regarded as the Paleozoic Evolutionary Fauna, in which lithistids diversified into several suborders and families, and the stromatoporoid and sphinctozoan calcified sponges experienced their first radiation. These faunas lead to the Late Ordovician–early Silurian patch reef ecosystems in which sponges of various types, along with corals, played a critical constructional role. The hexactinellid record shows the least obvious changes through the Cambrian–Ordovician interval, but the changes are nonetheless profound. Like other sponge groups at this time, the evolutionary emphasis appears to have been on strengthening the skeleton and occupying more turbulent, shallow water environments while remaining dominant in deep water settings (Finks, 2003a; Botting, 2004). Rather than becoming hypercalcified,

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FIGURE 5—Relative abundance of sponge families, including archaeocyaths and their contribution to reefs (modified from University of California Museum of Paleontology, n.d.).

or developing lithistid-like or fused skeletons, hexactinellids developed thick but unconsolidated walls of large spicules, which disaggregated rapidly on death. Large hexactinellid spicules, including monaxons, are abundant in many Middle Ordovician shallow water deposits, although complete sponges are rarely preserved (Botting, 2005). The earliest known true dictyosponges with relatively rigid, thin walls also occurred at this time and should have a better record in suitable environments than is currently known. Hexactinellids in deeper water facies developed a range of strategies for strengthening the body wall, including the evolution of multiple spicule layers, woven strands of hexactines, and parietal gaps. Numerous forms of spicule modification were also developed during this interval. Polyactinellid spicules and heteractinids are well developed in the Cambrian (see Mehl-Janussen, 1999; Pickett, 2002, for reviews). The lower Cambrian Polyactinellidae most commonly occurs in archaeocyathancalcimicrobial reef environments such as those of the Siberian Platform (Dzik, 1994; Kruse et al., 1995) or the Australian Flinders Ranges (Reitner and Mehl, 1995). Polyactinellidae commonly occur in shallow, nonagitated environments during the middle and upper Cambrian (Mostler, 1985). Heteractinid sponges are normally found in marly or argillaceous facies (Rigby, 1983b) and never occur in nearshore, turbulent siliciclastic environments at this time. Ordovician polyactinellids and heteractinids are associated with carbonate platform facies of the Argentine Precordillera (Carrera, 1994; Mehl and Lehnert, 1997). These groups show very few changes in their distribution and abundance through the Cambrian–Ordovician transition. Only during the Middle and Late Ordovician do the heteractinids show a significant increase in the number of genera and families (Rigby, 1991; Carrera and Rigby, 2004). Several authors have noted the strong paleogeographic overprint in the patterns predicted by Sepkoski’s model and the decoupled temporal pat-

terns in the installation of evolutionary faunal components (Miller, 1997; Waisfeld et al., 1999). Disparities in ecological and taxonomic diversification between paleocontinents are not so evident in sponges. Lower Ordovician sponges are well dispersed in all continents, although they are not abundantly preserved. This analysis shows that the appearance of orchoclads in the middle–upper Cambrian was a continuous and widespread event, in which they diversified to become the dominant sponges in platform areas. ECOLOGICAL PROPERTIES OF CAMBRIAN AND PALEOZOIC SPONGES Factors affecting the taxonomic composition and distribution of sponge faunas through the Cambrian may also have affected the biota as a whole (i.e., broad-spectrum factors) or may be specific factors relating only to sponge requirements. Aspects of sponge organization, physiology, and ecology that have been considered as important constraints governing early sponge evolution are discussed here, in the context of the Cambrian world. The Trophic Aspect Cambrian spiculate sponges, represented mainly by monaxonids and hexactinellids, are structurally simple, extremely thin walled forms in which the spicules form essentially a single layer. Elongated, cup-shaped, or palmate forms predominate in either shallow or deep water, low-energy environments. These characteristics can be considered an adaptation of filter feeders in quiet water (for reviews, see Warburton, 1960; Trammer, 1983; Palumbi, 1984; Finks, 2003b). In complex skeletons, the passage of water through more complicated channels and cavities minimizes the destructive effects of strong currents in agitated waters. This is a primary condition for being an efficient filter feeder in shallow water

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FIGURE 6—Schematic reconstruction of successive changes among dominant sponge groups in relation to a bathymetric profile, from nearshore reef mounds to deep shelf and basin.

environments. Early Ordovician, shallow water sponges share these characteristics with the independently derived orchoclad structure. Examples of complex morphologies and innovations in Early Ordovician sponges include solid encrusting forms, globose or conical forms without central cavities, and increased importance of multioscular sponges. Brunton and Dixon (1994) proposed a slightly different view, suggesting that intervals with high diversification of siliceous sponges in platform settings correspond to periods of high nutrient influx in shallow environments. Although similar arguments are frequent in the paleontological literature, there is no obvious mechanism for a causative correlation. In fact, it contradicts modern ecological studies in which episodes of elevated nutrient input encourage low diversity and high abundance— not high diversity (for a review, see Rosenzweig, 1995, p. 39–45). The only exceptions are in areas that were initially nutrient starved, for example, deserts and the abyssal plain, which does not seem to have been the case for Cambrian–Ordovician shelf environments. Zhuravlev (2001) suggested that the trophic nucleus of Cambrian communities consisted of what he termed passive filter and suspension feeders, represented mainly by archaeocyaths, spiculate sponges, radiocyaths, hyoliths, brachiopods, early mollusks, and echinoderms. Zhuravlev (2001) also thought that there was a shift in dominance and composition among filter and suspension feeders in the Ordovician. The trophic nucleus was composed instead of crinoids, stromatoporoids, pelecypods, and bryozoans, which are active filtrators. Passive suspension feeders depend mainly on ambient currents, whereas active filtrators create their own currents, allowing them to utilize more dispersed resources. In this sense, sponges, including stromatoporoids, are active filtrators and create their

own current through choanocyte-flagellar movement, and they physically induce water flow through their canals. Similar effects have also been seen in models of archaeocyaths (Vogel, 1978). Brachiopods also create their own current through their lophophore structure and represent another exception to Zhuravlev’s (2001) distinction. Distinctions among organisms with suspension-feeding habits could be made instead between those that isolate food directly from the water column and those that are true filter feeders with water passing through their bodies. Crinoids and corals belong to the first group, and sponges to the second. Another possible distinction involves the type of primary food that organisms were able to utilize. Corals, bryozoans, and pelmatozoans were suspension-feeding collectors whose primary food source was probably zooplankton. Except for a few highly specialized forms, sponges today are unable to utilize zooplankton and larger phytoplankton; it is assumed that early Paleozoic forms of sponges were also mainly dependent on bacteria, dissolved organic matter, and small phytoplankton (Berquist, 1978; Vacelet, 1978; Finks, 2003a). In addition, most modern tropical sponges host bacteria as photosymbionts (see Vacelet, 1978; Wilkinson, 1978). Such distinctive characteristics in sponges argue for no direct competitive interaction for food between sponges and the other suspension-feeding groups. The Hydrodynamic Aspect Lower and middle Cambrian sponges were clearly divided into two associations: the carbonate platform archaeocyath communities in the lower Cambrian and the siliciclastic, deep shelf or basin spiculate sponge

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communities throughout the interval. Early Cambrian reef communities were formed by relatively small, solitary or low modular forms that anchored in soft sediments (Wood et al., 1993; Kruse et al., 1995), although modularity increased during the interval. Archaeocyaths commonly played only a subordinate role in reef building (Wood et al., 1992; Debrenne and Reitner, 2001). The Ajacicyathida were mainly solitary, although catenulate, branching, and pseudocereoid forms have been described. They normally inhabited low-energy, soft-bottom environments, commonly at the reef periphery, but many examples of hard-substrate encrusters are also known, with some frame-building potential. The Archaeocyathida had a higher degree of integration and modularity and produced abundant secondary skeletal projections that enhanced framebuilding ability. They settled on solid surfaces after stabilization of the soft bottom. These also played a secondary role in reef construction, however, with cement and calcimicrobes fulfilling the primary construction role (Pratt et al., 2001). The contribution of archaeocyathans to such buildups would have been primarily in creating a cavernous architecture. The earliest fossil demosponges and hexactinellids were adapted to quiet-water environments. Saclike, tubular, or palmate sponges generally dominate over discoidal or globose forms. Spiculate sponges in the early– middle Cambrian were constructed from slender monaxons held together by spongin or from a single layer of parallel hexactine-based spicules— hexactines, stauractines, or derivatives. This apparently primitive condition of thin-walled, unfused spicular skeletons dominated during the Cambrian but became less significant during the Ordovician. Although the appearance of thicker-walled and more robust hexactinellids is associated with the rise of more preservable lithistid sponges in shallow water, deep water faunas were still dominated by thin-walled forms of various spiculate types (e.g., Botting, 2004). The relative weakness of thin-walled hexactinellid or monaxonid skeletons in turbulent water regimes is not a disadvantage in nutrient-rich, quiet waters. The first whole fossil lithistids appeared in the middle Cambrian, but the group only became common in upper Cambrian and Lower Ordovician shallow water limestones. Interlocking spicules in triangulated nets and cemented attachments were their main adaptations for inhabiting shallow environments, including reef settings (Finks, 2003b). In the Cambrian and Early Ordovician, the anisotropic triangulated skeletons (triangles parallel to the surface) predominate, as in the orchoclad lithistids— particularly the Anthaspidellida (Finks, 2003b). Such a structure was able to maintain rigidity in agitated waters, even in anthaspidellids with elongate tubular or conical shapes. These sponges invaded reef environments in the late Cambrian after the demise of archaeocyaths (Hamdi et al., 1995; Spincer, 1996; Mrozek et al., 2003; Dattilo et al., 2004; Shapiro and Rigby, 2004; Johns et al., 2007) and, more conspicuously, in the Early Ordovician (compiled in Carrera and Rigby, 2004). A new stage in lithistid evolution occurred in the Middle and Late Ordovician, with the appearance of the isotropic triangulated net (triangular in all directions) seen among the hindiids and astylospongiids (Finks, 2003b). Overall, the trend toward more resistant skeletons, associated with colonization of more turbulent environments through the Cambrian– Ordovician, appears to have been one of the dominant factors in early sponge evolution. The Geobiochemical Aspect Sponges and radiolarians were the main organisms responsible for silica depletion in Paleozoic oceans. There is sedimentological and biological evidence that sponges controlled the Si cycling in neritic environments until the Cretaceous–Paleogene burst of diatoms (Hartman, 1981; Maliva et al., 1989; Schubert et al., 1997; Maldonado et al., 1999; Racki, 1999). The Cambrian–Ordovician transition shows the first evidence of the contribution of radiolarians to the skeletal plankton in deep-sea sediments and their significant involvement in the silica cycle with the concomitant rise in offshore, bedded chert (Racki, 1999; Tolmacheva et al., 2001). Radiolarian skeletons are abundant only in sediments that accu-

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mulated under areas of coastal or open-ocean upwelling (Tolmacheva et al., 2001), whereas sponges were locally abundant in almost all marine environments by the Ordovician. The delicate nature of most early and middle Cambrian sponge spicules has been suggested to reflect the relative scarcity of dissolved silica in seawater (Finks, 2003b). The availability of silica in such settings has been postulated as the main condition for the invasion of orchoclads into late Cambrian and Early Ordovician shallow water environments. In the absence of silica-secreting organisms, silica was abundant in the ocean during the Precambrian, and early diagenetic cherts formed abundantly in peritidal marine environments (Maliva et al., 1989). The initial invasion of lithistid demosponges in the lower Paleozoic apparently had no significant effect on chert distribution (Stanley, 2006). The initial radiation of radiolarians combined with the rise in demosponges in the Ordovician apparently prevented formation of early diagenetic chert in shallow water, peritidal settings (Maliva et al., 1989). Cherts continued to form abundantly in subtidal environments from the Silurian through the Early Cretaceous. The argument for silica limitation in the Cambrian, and its subsequent availability in the upper Cambrian–Lower Ordovician, does not appear to be valid. Not only is there is no evidence for silica limitation, but we would expect dissolved Si to be very high, given the lack of organisms removing it and continuous hydrothermal input to the oceans. The colonization of shallow water facies by upper Cambrian and Lower Ordovician sponges occurred in several lineages independently, using different evolutionary innovations. In fact, at the time when silica limitation is alleged to have driven sponges onto the shallow shelves, we see the first development of sponges with large, complex skeletons, often in dense communities. Abundant sponge faunas also persisted in deeper water environments. The Sponge-Substrate Relationship Another particular feature that potentially differentiates Cambrian and Ordovician sponges is the way they interacted with bottom sediment and other substrate conditions. Dornbos et al. (2005) pointed out different adaptations of sponges to Proterozoic-style and Phanerozoic-style soft sediments, basing their analysis on previous work that recognized a remarkable increase in bioturbation activity at the beginning of the Phanerozoic (Thayer, 1983; Droser and Bottjer, 1988; Seilacher and Pflu¨ger, 1994). The Cambrian is considered a transition period from the Proterozoic matgrounds to Phanerozoic mixgrounds with high levels of horizontal and vertical bioturbation (Seilacher and Pflu¨ger, 1994; Bottjer et al., 2000; Dornbos et al. 2005). In this context, Cambrian and Ordovician sponges should have been adapted in their form of attachment to these different sediment characteristics. Although sponge forms are influenced by such other environmental characteristics as water energy and sedimentation rate, a comparison of several localities worldwide with different environmental conditions may have significant value. A previous paleoecological analysis considering sponge-sediment relationships was restricted to the lower Cambrian Yu’anshan Member in China and the middle Cambrian Burgess Shale Formation (Dornbos et al., 2005). This study recognized different adaptations of sponges based on form and structural characteristics, some of them taken from previous analyses (Thayer, 1975, 1983; Seilacher, 1999). Immobile benthic suspension feeders that were well adapted to typical Proterozoic-style, bacterially bound sediments were grouped by Dornbos et al. (2005) into (1) shallow sediment stickers and (2) sediment resters. Shallow sediment stickers have only a small lower end that is inserted into the sediment, whereas sediment resters live freely on the seafloor with their lower surface resting flat on the sediment. Phanerozoic-style adaptations included (1) attachment to hard surfaces, (2) a snowshoe strategy, (3) rootlike adaptations, (4) deep sediment stickers, and (5) increased body size. A variety of suspension-feeding groups adapted to hard-substrate attachment, particularly in the late Cambrian

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TABLE 1—Attachment style for the Cambrian spiculate sponges. PC ⫽ Precambrian style; F ⫽ Phanerozoic style; Sss ⫽ shallow-sediment stickers; Sr ⫽ sediment resting; Hs ⫽ hard surface attachment; Rlh ⫽ rootlike attachment; Sno ⫽ snowshoe strategy; Ice ⫽ iceberg strategy (see text).

Style

Attachment

PC PC F F F F Precambrian style Phanerozoic style

Sss Sr Hs Rlh Sno Ice

Lower Cambrian

Middle Cambrian

Upper Cambrian

12 10 2 2 2 — 22 (78%) 6 (22%)

22 7 8 5 8 4 29 (53%) 25 (47%)

1 — 2 — 1 — 1 3

and Early Ordovician. For example, echinoderm (Sprinkle and Guensburg, 1995) and demosponge (Carrera and Rigby, 2004) occurrences are associated with the availability of widespread hardgrounds in carbonate platforms, as are some early Cambrian bioconstructors such as calcimicrobes and some archaeocyathans. Because the increase in available hard surfaces has been related to changes in seawater chemistry (calcite seas; see Sandberg, 1983), this type of substrate colonization is only applicable to carbonate facies. The snowshoe strategy is a form of sediment resting that is adapted to particularly soft substrates and involves benthic organisms that broadly distributed their body mass on the seafloor, commonly achieved by having a wide, thin body (Thayer, 1975). Rootlike adaptations in sponges involved anchoring in soft sediment by individual elongated spicules, or tufts of spicules. Deep sediment stickers use a large part of the organism or a substantial skeletal element inserted into the seafloor for stabilization (the iceberg strategy of Thayer, 1975). Increase in body size was another effective strategy for survival on a Phanerozoic-style, soft seafloor. Although Dornbos et al.’s (2005) analysis considered all benthic suspension feeders in their study, sponges formed the largest component of the benthic fauna, and so their results relating to sponges are considered here. In that study, the lower Cambrian association of the Yu’anshan Member in China shows 88% of the fauna well adapted to Proterozoicstyle seafloors, while in the Middle Cambrian Burgess Shale Formation, only 62% of the fauna is considered to have Proterozoic-style attachment. The sponge database analyzed here allowed a worldwide comparison of sponge-seafloor relationships. A reevaluation of sponge characteristics was necessary in light of new Burgess Shale Formation and Stephen Formation sponge descriptions (Rigby and Collins, 2004) and our own interpretations of sponge-seafloor adaptations. The analysis was based on sponge localities in siliciclastic rocks with a variety of environmental settings (Table 1) and does not include hard-substrate attachment. The changes in percentages recorded here between early and middle Cambrian sponges with Proterozoic or Phanerozoic adaptations is similar to the results of Dornbos et al. (2005). Sponge adaptations became more suited for survival in increasingly bioturbated, mixed bottom sediment. Although Proterozoic-style attachments did not diminish in the middle Cambrian, there is a small increase in the sediment-sticker type. Their percentage diminished with the emergence of Phanerozoic-style attachments, all types of which became more abundant through time (Table 1). Unfortunately, described late Cambrian and Early Ordovician sponges come mainly from carbonate environments that are unsuitable for these comparisons. The increase in sponge adaptation to hardgrounds is obviously important in this interval. A PHYLOGENETIC FRAMEWORK FOR EVOLUTIONARY INNOVATIONS Evolutionary innovations and external factors that may have induced the diversification of sponges can be further constrained by understanding

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their phylogeny. The broad phylogeny of major (i.e., abundant or widespread) Cambrian–Ordovician groups of demosponges and hexactinellids shows multiple, apparently independent adaptations in a wide range of lineages (Fig. 7), involving a range of modifications for inhabiting more turbulent conditions. Such a pattern strongly suggests that the parallel development of these novel morphologies is related to a definite, temporally controlled trigger. It is more difficult to assess whether this was dominantly a physiochemical environmental factor or an ecological escalation produced by the influence of some sponge groups or other groups on the viability of the other lineages. There is disagreement and ambiguity over many aspects of early sponge phylogeny. For this reason, the emphasis here is on the separation of lineages rather than sister-group relationships; there is little disagreement in the literature over the broad outline of lineage evolution. Similarly, the classes are considered separately, despite some recent and, as yet, controversial work that attempts to clarify class-level relationships from paleontological data (e.g., Botting, 2003; Botting and Butterfield, 2005). A consensus is also beginning to emerge among molecular studies (Medina et al., 2001; Thiel et al., 2002) that siliceous sponges are sister groups and that calcareans may be most closely related to Eumetazoa. Our knowledge of the timing of separation of lineages is probably also extremely incomplete at this stage. In this paper, however, we are interested in the time at which each group became prominent rather than in the precise timing of their originations. Among hexactinellids, early–middle Cambrian faunas are, for the most part, conservative. The earliest faunas from China are among the most diverse, including a variety of forms with a poorly ordered, thin-walled mesh of hexactines and simple derivatives. There are such early dictyosponge-like variations as Quadrolaminiella (Chen et al., 1990), but such forms are apparently local rarities and do not appear to represent successful, widespread groups. Other lineages include Diagoniella, Protospongia sensu stricto, the Dierespongiidae, and Hintzespongiidae, each of which has a relatively wide distribution, but none extend far beyond the Cambrian, if at all. Despite their distinctive structural features, these are all relatively fragile, thin-walled groups with limited or nonexistent attachment structures. These lineages represent the archetype of the Cambrian Evolutionary Fauna. Few, if any, of the most prominent members of this fauna show clear descendent lineages. (See Rigby and Collins, 2004, for an interpretation of the phylogenetic importance of Hintzespongia, and Botting, 2004, for the alternative view followed here.) Several major Paleozoic lineages were already established by the Late Ordovician. The Brachiospongioidea, Dictyospongiidae, and Pyritonemidae were established in some nearshore siliciclastic facies of Wales by the Llanvirn (Botting, 2005); their distribution after this time is unclear because of the low preservation potential of sponges in this facies. In offshore facies, a different assemblage became dominant during the Early Ordovician and perhaps the late Cambrian. The Asthenospongiidae, Cyathophycus, and a range of complex reticulosan-like forms with relatively thick walls appeared during this time and continued as major components of these faunas until at least the Devonian (Rigby and Mehl, 1994). These show some structural novelties and complexity, such as prominent prostalia, and all have discrete attachment structures of various forms. Another fundamental change from the earlier reticulosan faunas is in the much more robust spicules supported by the thicker walls in many species of these groups. Overall, there appear to be recognizable Cambrian and Paleozoic evolutionary faunas and an intermediate assemblage that dominated at least offshore communities during the transitional period. The Paleozoic fauna, characterized particularly by nearshore taxa, shows several types of adaptation in different lineages, all of which appear to have been derived independently from various members of the transitional fauna. The phylogenetic origins of these groups appear to lie among various members of a broad group of hexactinellids that still occur in offshore settings during the Ordovician (Botting, 2004) and that can be traced to the simplest reticulosan morphologies. These relatively delicate putative

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FIGURE 7—Schematic history of the main lineages of Cambrian–Ordovician hexactinellids (left) and demosponges (right), showing longitudinal section of body form, detail of spicule form, and arrangement in each case. Lineages with dotted shading are Cambrian Evolutionary Fauna; those with no shading are Paleozoic Evolutionary Fauna (or modern fauna, in the case of agglutinating demosponges); and those with hatched shading are interpreted here as transitional.

ancestors of brachiosponges, dictyosponges, and the living hexactinellid subclasses all share some skeletal modifications with later Paleozoic reticulosans but are not prominent components of the early–middle Cambrian faunas. The simpler reticulosans in general do not appear to have been prominent members of later Paleozoic faunas, although there are several moderately diverse Devonian assemblages described (e.g., Rigby et al., 1991; Rigby and Mehl, 1994). Demosponge phylogeny is even more problematic. Among the numerous genera described from Burgess Shale–type faunas, it is possible to identify structural similarities apparently defining some groupings (Rigby and Collins, 2004). Beyond this, however, precise evolutionary sequences are rather tenuous. The situation is not aided by the rarity of monaxonid demosponges in upper and post-Cambrian strata, with only a very few species described. Those known from offshore deposits are primarily close relatives of such Cambrian groups as piraniids, hazeliids, and choiids and represent the declining Cambrian Evolutionary Fauna (Botting, 2007). It is notable that the most prominent post-Cambrian examples of this group are those with unusual modifications from the basic hazeliid body plan. None attain any great prominence, and they are relatively minor components of their respective faunas. Some of these modified skeletal architectures, particularly the piraniid structure, with similarity to Saccospongia, at least offer possible avenues for deriving the more complex, later demosponge groups.

Familiar Cambrian nonlithistid demosponges are absent from nearshore deposits during the Ordovician. Instead, the extremely rare known faunas show a much more modern aspect, including agglutinating taxa (Botting, 2005) and forms with complex plumose skeletons (Finks, 1967). The origins of these groups are presently obscure, both in phylogeny and timing, although there are some similarities between Saccospongia and the Piraniidae. Aside from the piraniids, there is no trace of similar forms in even the shallowest of the early–middle Cambrian faunas. Lithistid phylogeny might be expected to be somewhat clearer, owing to a better record and better-defined spicule arrangements. Hypotheses are still controversial, however, and the scenarios proposed are often complicated; numerous groups are described from the Ordovician (Pisera, 2002; Finks and Rigby, 2004), but the relationships between them are largely obscure. Perhaps the most widely cited discussions of demosponges in general, and lithistids in particular, are those of Finks (1967, 1970) and Reid (1970, 2003). Finks (1967, 1970) argued that orchoclads and rhizomorines were derived from a form similar to Archaeoscyphia, based on skeletal structure among monaxon-based lithistids. Archaeoscyphia was derived in turn from Hazelia-like ancestors. The hindiid and astylospongiid lineages, although assumed to derive from monaxonid precursors, were considered to be more obscure. Reid (1970) emphasized the role of tetraxons in reconstructing demosponge phylogeny and speculated that the origins of the various demosponge spicule types were in

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multiple microspiculate forms. This would imply an independent skeletal origin of the different lithistid lineages. Of the two, Finks’s (1970) view has more support (van Kempen, 1978; Webby, 1984; Finks, 2003c). In the absence of a clear lineage leading to the astylospongiids, however, the phylogenetic relationships of the various lithistid groups are still contentious. There is little to be said of heteractinid evolution during this interval, beyond that in Rigby and Collins (2004). The Cambrian is populated exclusively by thin-walled forms, but thick-walled taxa appeared during the Ordovician, followed by encrusting and massive morphologies. Thinwalled forms (eiffellids) continued until at least the Carboniferous, but they are rare and restricted to offshore, quiet-water settings. The evolutionary sequence of increasing morphological complexity is apparently quite continuous, and it is difficult to suggest divisions between evolutionary faunas. It is notable, however, that the first thick-walled forms occur through the Early–Middle Ordovician interval; this group was presumably ancestral to the later, most complex, forms. The Cambrian, Paleozoic, and transitional faunas identified here can be recognized either by the temporal range in which they are significant faunal components or through morphological characteristics. The Cambrian faunas include some lineages that continued through much of the Paleozoic, but invariably in offshore settings. They are thin-walled, relatively simple forms with some modifications that are of little use in colonizing turbulent-water habitats. Early members of the traditional Paleozoic fauna are such thick-walled, robust taxa as various lithistids, various nonlithistid demosponge and hexactinellid groups, and the later stromatoporoids. All occupied carbonate platforms or nearshore siliciclastic environments. The transitional fauna, as recognized here, includes lineages that appear in the middle–late Cambrian or Early Ordovician. Early lithistids, asthenospongiids, and the more complex reticulosan hexactinellids usually possessed novel features of skeletal architecture or spicule development that allowed colonization of somewhat more nearshore environments. The environmental range of representative taxa in this group is wide, including deep water black mudstones and offshore carbonates, but despite such modifications as increased mesh rigidity or anchoring structures, most appear to have been too fragile to colonize extremely turbulent-water facies. These modifications occurred in a large number of lineages independently, as seen most clearly amongst the hexactinellids. Among sponges, the transition from the Cambrian to the Paleozoic fauna can be regarded as the transition from quiet-water, soft-bottom taxa to a community capable of living in the most turbulent water environments. The transitional fauna included a wide range of morphologies that appeared diachronously but during the same broad interval, including innovations subsequently modified to allow the appearance of taxa recognizable as the Paleozoic Evolutionary Fauna. Interestingly, members of the transitional fauna, in general, gave rise to members of the Paleozoic Evolutionary Fauna, rather than these later forms having a direct origin in members of the Cambrian Evolutionary Fauna (see Fig. 7). The parallel nature of these innovations implies that they occurred as part of a widescale ecological development and were not restricted to the phylum. We should, therefore, expect to recognize similar intermediate stages in the history of at least some other groups. DISCUSSION A series of critical steps for the sponge evolutionary history occurred from the Proterozoic-Cambrian boundary to the Middle–Late Ordovician interval. It is fairly clear that sponges possess a long record back to the Proterozoic, represented in the Ediacara fauna. Such indirect methods as biomarkers and molecular clocks (for a review, see Debrenne and Reitner, 2001) suggest that the origin of sponges may extend back to the late Paleoproterozoic. If true, it is not surprising that in the early Cambrian all the sponge classes had already diversified significantly. Wu et al. (2005) suggest a transition of hexactinellid sponges from

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shallow-to-deeper water environments during the early–middle Cambrian, based on records of isolated hexactinellid spicules in the late Proterozoic and lowermost Cambrian. Isolated spicules of hexactinellids occur in shallow water facies of south China and Siberia in the Nemakit-Daldynian (Qian and Bengtson, 1989; Rozanov and Zhuravlev, 1992) and whole sponge bodies in the lower Cambrian of China (Yuanshan Formation; Zhu et al., 2001). The rest of the lower–middle Cambrian sponges lived in outer shelf environments or deep basins. The skeletal architecture apparently changed from thick-walled networks of hexactines, diactines, and stauractines to thin-walled, regular frameworks of stauractines (Wu et al., 2005). This is an interesting point because it implies that hexactinellids show an offshore pattern decoupled from the demosponge development that occurred later in the middle–upper Cambrian, and from upper Cambrian–Ordovician hexactinellids, in which multiple independent lineages evolved to colonize nearshore environments. Late Proterozoic– lowermost Cambrian occurrences of shallow water hexactinellids, are, however, too scarce to make any conclusive statements, and the shallow water environments represented in South China are still ambiguous. They do not appear to include littoral deposits, for example, and sponges represented in the faunas may not have been strong enough to survive in such nearshore settings. It is possible that these are early colonizers of the inner shelf, but that they are not specialized shallow-water sponges. Instead, there are clear trends showing the reverse, offshore-onshore range expansion among later Cambrian–Ordovician faunas reported by Carrera and Rigby (2004) and Botting (2005, 2007), and confirmed in this analysis. Following the thin-walled, hexactinellid, and monaxonid faunas that dominate nonarchaeocyathan sponge faunas in the lower Cambrian, the more derived groups of sponges developed in a two-step sequence. In the middle–early late Cambrian, the first representatives of the intermediate evolutionary fauna appeared, including the first orchocladine lithistids: Capsospongia in the Burgess Shale and Rankenella in limestone deposits of Australia and Iran. It is still unclear whether the orchoclad origin was related to adaptations for invading shallow platform settings from deep environments (hazeliid origin; Finks, 1970, 2003c; van Kempen, 1978; Webby, 1984), or whether they evolved from sponges that actually inhabited shallow areas such as the archaeocyathan reefs; isolated spicules with hadromerid, axinellid, or tetractinellid affinities are known from such settings (Reitner and Wo¨rheide, 2002). Whatever the origin of orchoclads, the skeletal architecture of their ancestors was certainly different to the derived orchoclad spicular network. Orchoclads diversified in the late Cambrian as the main metazoan constituents of reef settings after the demise of archaeocyathans. The change in apparent dominance from thin-walled Cambrian monaxonids and hexactinellids to thick-walled Ordovician anthaspidellids appears to have been an adaptive process for the occupation of shallow, high-energy settings. Lithistid skeletons do not constitute the only evolutionary development of this type, with hexactinellids and some nonlithistid demosponges also beginning to occupy shallow-water environments (cf. Botting 2005), but they were the most preservable group and, perhaps, the most successful in the long term. A third step in sponge development involved diversification of the orchoclad lithistids in the Lower Ordovician (Carrera and Rigby, 2004). The anthaspidellid orchoclads that appeared in upper Cambrian shallow water environments were represented by only a few genera of simple cylindrical to obconical forms. They rapidly diversified at species, genus, and family level and occupied a variety of shallow to deep platform environments during the Lower and Middle Ordovician. In the Middle and Upper Ordovician, the main stage of sponge diversification took place (Carrera and Rigby, 2004), at least among those groups with a good fossil record. The main appearances occur among lithistids, with the first record of several orders and suborders. This interval also witnessed the beginning of domination of stromatoporoids and sphinctozoans among sponges in shallow reef settings (Carrera and Rigby, 2004; Webby, 2004).

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CONCLUSIONS Sponges played a significant role in the evolutionary faunas of Sepkoski’s model, although their importance has not previously been appreciated. The inclusion of archaeocyaths in the phylum radically alters the role of sponges in the early part of the Cambrian Evolutionary Fauna and forces a distinct ecological shift at the end of the lower Cambrian, with their near-total disappearance at that time. Aside from archaeocyathans, the lower–middle Cambrian interval conforms, for sponges, to the traditional view of the Cambrian Evolutionary Fauna. The upper Cambrian– Lower Ordovician interval, however, represents a transitional stage where one of the main components of the Paleozoic sponges—the orchoclad lithistids—radiate from simple forms in shallow water settings to widespread and more complex forms that became an important component of carbonate shelf communities. Sponge communities of the traditional concept of the Paleozoic Evolutionary Fauna certainly appeared by the Middle–Upper Ordovician, when lithistids, stromatoporoids, and sphinctozoans established their dominance and continued over the rest of the Paleozoic. Another additional aspect to the standard evolutionary model is the trend shown by hexactinellids in the Cambrian–Ordovician transition, from delicate to stronger skeletons associated with an inshore migration of various lineages with thicker-walled morphologies (Botting, 2004, 2007). Monaxonid demosponges probably followed a similar trend; they occur widely in deeper water deposits in the Cambrian and Ordovician. The data from Ordovician nearshore facies relating to nonlithistid demosponges, however, are still limited. New findings (Botting, 2005) suggest that nonlithistid demosponges also acquired morphological innovations that permitted their development in such settings. In summary, the concept of distinct evolutionary faunas can be clarified when applied in detail to sponges. A complex suite of factors affected community evolution and ecology, but it is interesting that members traditionally assigned to the Paleozoic Evolutionary Fauna originated from a subset of the Cambrian Evolutionary Fauna, and that this subset can be regarded as intermediate in structure and autecology. With this level of detail, it is possible to trace the origins of the Paleozoic fauna back into the upper Cambrian. It may be useful, both with sponges and other groups, to consider the upper Cambrian–Lower Ordovician interval as a transitional phase distinct from, but critical to, the later part of the Ordovician Radiation. ACKNOWLEDGMENTS MGC acknowledges financial support from Consejo Nacional de Investigaciones Cientı´ficas y Tećnicas (CONICET) and Agencia Nacional de Promocioń Cientı´fica y Tecnolo´gica (ANPCYT). JPB’s research is aided by long-term visitor status at the Natural History Museum, London. Dorte Janussen and an anonymous referee improved the manuscript with constructive reviews. Thanks also to Lucy Muir for proofreading the manuscript and for transliterating Russian and Chinese editor names. This is a contribution to the International Geological Correlation Program (IGCP) 503 project. REFERENCES A´LVARO, J.J., and VENNIN, E., 1997, Episodic development of eocrinoid-sponge meadows in the Iberian Chains (NE Spain): Facies, v. 37, p. 49–64. BENGTSON, S., CONWAY MORRIS, S., COOPER, B.J., JELL, P.A., and RUNNEGAR, B.N., 1990, Early Cambrian fossils from South Australia: Association of Australasian Palaeontologists, Memoir, v. 9, p. 1–364. BERESI, M., and RIGBY, J.K., 1994, Sponges and chancelloriids from the Cambrian of western Argentina: Journal of Paleontology, v. 68, p. 208–217. BERGQUIST, P.R., 1978, Sponges: University of California, Berkeley, 268 p. BOTTING, J.P., 2003, Cyathophycus and the origin of demosponges: Lethaia, v. 36, p. 335–344. BOTTING, J.P., 2004, An exceptional Caradoc sponge fauna from the Llanfawr Quarries, central Wales, and phylogenetic implications: Journal of Systematic Palaeontology, v. 2, p. 31–63.

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