The late Palaeozoic to late Mesozoic interval is punctuated by two mass extinctions (the Permian–Triassic (251 Ma) and Triassic–Jurassic (200 Ma); Raup and Sepkoski 1982) and a purported reorganization of marine ecosystems (Vermeij 1977), coupled with environmental perturbations ranging from ocean anoxic events (Toarcian (183–176 Ma), early Aptian (125–112 Ma), and Cenomanian–Turonian (100–89 Ma): Schlanger and Jenkyns 1976; Jenkyns 1988) to rapid changes in global temperatures (Price 1999; Jenkyns 2003). However, the response of fishes to these major climatic and biotic shifts is unclear. Here, we review outstanding patterns that are presently apparent in fish diversity during this lengthy interval and suggest whether these features are likely real or merely artefactual.
The late Mississippian and Permian richness trough: genuine or artefactual?
Marine invertebrate palaeontologists have proposed a bioevent equivalent to the Hangenberg and ecologically more severe than the end-Ordovician at the Visean–Serpukhovian boundary (328 Ma), coincident with the onset of the Late Palaeozoic Ice Age (Bambach 2006; McGhee et al. 2012). However, Sallan and Coates (2010) found jawed fish faunal composition to be stable in the later Mississippian, perhaps in line with the onset of stasis in vertebrate morphological and taxonomic diversity (Sallan et al. 2011; Sallan and Friedman 2012). There is a significant reduction in marine ichthyolith sampling and the number of macrofossil localities beginning at the Serpukhovian (328–318 Ma) and persisting into the later Palaeozoic (Sepkoski 2002; Sallan et al. 2011). However, the Mississippian–Permian trough found in many marine generic diversity curves might be related to a general lack of appropriate marine deposits in Europe (Sepukhovian; McGowan and Smith 2008; McGhee et al. 2012). The absence of fossiliferous marine facies was likely driven by both the destruction of Euramerican coastlines during the formation of Pangaea and regression-driven hiatuses during long glacial cycles (which last up to 150 000 years in the Pleistocene; Falcon-Lang et al. 2009; McGhee et al. 2012). There is also a lack of nonmarine Permo-Carboniferous (c. 318–251 Ma) deposits relative to the temporal span: most productive fish localities represent coal swamps and similar nonmarine habitats which were only widespread during short interglacials (lasting at most 20 000 years as in the Pleistocene) and cyclically replaced by seasonally or perennially dry environments (Falcon-Lang and DiMichele 2010).
Therefore, the late Palaeozoic depletion apparent in Sepkoski’s genus-level data might represent a sampling artefact. However, it does not occur in all data. Serpukhovian vertebrate taxon counts are boosted by the Lagerstätten at Bear Gulch, USA and Bearsden, Scotland, which exhibit a higher taxonomic and morphological diversity of chondrichthyans than might assumed from ichthyolith sites (Sepkoski 2002; Sallan and Coates 2010; Sallan et al. 2011) (Fig. 4). Blieck (2011) showed that Pennsylvanian vertebrate familial diversity rises above Mississippian levels in data from The Fossil Record 2, perhaps driven by the sporadic appearance of members of certain families better known from other Palaeozoic and Mesozoic intervals.
It is also possible that the Permo-Carboniferous trough is driven by the existence of stable cosmopolitan marine and freshwater faunas around Pangaea, rather than abiotic events or rock volumes. Permo-Carboniferous actinopterygian genera, such as Elonichthys, Platysomus, Aeduella, Amblypterus, Acrolepis and Palaeoniscum, seem especially widespread and long-lived, appearing at multiple disparate localities and persisting for tens of millions of years. Likewise, similar chondrichthyan teeth are known from around the Permo-Carboniferous world, with a few ranging through the entire interval (e.g. some petalodonts; Sepkoski 2002). Many of these apparently stable late Palaeozoic taxa have not undergone critical taxonomic revision in decades, with their longevity perhaps more indicative of neglect rather than true stratigraphic duration. However, their ecomorphologies do appear static (L. C. S., pers. obs.) and the same pattern occurs in marine invertebrate data, with Permo-Carboniferous benthic assemblages being particularly stable and conserved over large temporal and geographical scales (Schram 1979; Bonuso and Bottjer 2006). Bonelli and Patzkowsky (2008) noted highly homogeneous faunal composition at a single Serpukhovian site, with similar taxa appearing at all depths along a coastal gradient. In summary, reduced richness of fishes during the Permo-Carboniferous appears attributable to a lack of ecological opportunities and available habitat leading to low origination, perhaps exacerbated by poor sampling (McGowan and Smith 2008; Falcon-Lang and DiMichele 2010; McGhee et al. 2012).
The end-Permian event and Triassic diversification
Although classically regarded as the most catastrophic of Phanerozoic mass extinctions (Raup and Sepkoski 1982; Erwin 1990), the effects of the Permian-Triassic event on fishes remain deeply ambiguous (Janvier 1996; Blieck 2011). This reflects, we suspect, the relatively poor understanding of late Permian fishes (particularly actinopterygians; see discussion in Hurley et al. 2007), combined with a failure to adequately quantify patterns derived from available fossil data. Recent discussion in the literature touching on the end-Permian event as it relates to fishes is generally couched in terms of extinction recovery (Tong et al. 2006; Brinkmann et al. 2010; Hu et al. 2011; Wen et al. 2012). This is largely because Triassic (251–200 Ma) fishes are abundant and well-studied in comparison with the sparse record available for the Permian. The obvious problem is that such a research programme presupposes that patterns apparent among fishes represent recovery from extinction, without having first clearly demonstrated that fishes themselves were affected in such a way that it might be necessary to invoke recovery. We emphasize this point here because palaeontologists studying both elasmobranchs (Mutter et al. 2007; Mutter and Neuman 2008, Mutter 2009) and osteichthyans (Schaeffer 1973), as well as total fish diversity (Janvier 1996; Blieck 2011), have found little evidence for major taxonomic shifts associated with the end-Permian event, and no striking decline in richness is apparent in broader surveys (Fig. 1). Marine conodonts, which have best global record of any vertebrate group, were apparently little affected by the Permo-Triassic apart from a dip in abundance (Clark 1983; Clark et al. 1986; De Renzi et al. 1996). Indeed, the familial data within the Fossil Record 2 show consistent levels of fish diversity through the Permian and into the early Triassic, leading Blieck (2011) to conclude that there was no real loss. Sepkoski’s (2002) data give no indication of elevated extinction in the late Permian (Fig. 2), and his osteichthyan data are so scant that rates cannot be estimated for this major group (Fig. 3). A literal reading of Sepkoski’s data would suggest that the earliest Triassic (Induan; 251–249.5 Ma) was an interval of intensive turnover among fishes (Figs 1–3), perhaps indicative of turbulent postextinction recovery. Here too, small taxonomic samples urge caution: Sepkoski (2002) records only six chondrichthyan and 13 osteichthyan genera from this interval. In the face of such evidence, we question claims that ‘fishes were severely affected by the end-Permian mass extinction’ (Wen et al. in press), at least in aggregate.
However, at least one important segment of Permo-Carboniferous fish diversity is missing from Triassic localities: nonchimaeroid holocephalans (Cappetta et al. 1993; Stahl 1999; Sepkoski 2002). The durophagous holocephalans became particularly diverse in the aftermath of the Hangenberg extinction (Figs 5 and 6), and many assemblages, including petalodonts, cochliodonts, deltoptychiids, pristiodonts, menaspids, and helodonts, persist through the late Palaeozoic (Stahl 1999; Sepkoski 2002; Sallan et al. 2011). The majority of these Palaeozoic holocephalan groups have last appearances in the late Permian. Indeed, petalodont ichthyoliths and even body fossils (e.g. Janassa) were widespread in end-Permian formations from Japan to Germany to Arizona (Goto 1994; Stahl 1999). Many of these holocephalan taxa are effectively repositories for morphologically similar teeth arising in different lineages (Smith and Patterson 1988; Sallan et al. 2011; Finarelli and Coates 2012). However, most represent clades at various levels and may serve as a proxy for ecological or functional diversity (Stahl 1999; Sallan et al. 2011).
In reconciling these losses with the lack of extinction signal for other fishes, it is notable that the vast majority, if not all, of Palaeozoic holocephalan material is marine (Stahl 1999) (Fig. 4). These groups co-existed with, and fed upon, known invertebrate victims of the extinction (Moy-Thomas and Miles 1971; Stahl 1999; Sallan et al. 2011). In contrast, the majority of unaffected elasmobranch and osteichthyan lineages were either euryhaline (e.g. hybodonts) or completely freshwater (e.g. xenacanths) in ecology (contraSchultze 2009) and are well represented in the coal measures, deltas and shallow basins of Palaeozoic–Mesozoic Euramerica (Hook and Baird 1988; Dick 1998; Zajic 2000; Kriwet et al. 2008) (Fig. 6). As exceptions that might prove the rule, several deep-bodied, durophagous actinopterygian lineages widespread in Permo-Carboniferous sediments (e.g. Eurynotus, Amphicentrum; Moy-Thomas and Miles 1971; Dineley and Metcalf 1999), suddenly disappear at or before the end-Permian (Gardiner 1993a). An additional datum supports marine, but not durophage, selectivity: the brush-backed symmoriiform chondrichthyans (stethacanthids) (Fig. 1), nektonic predators once widely dispersed in Palaeozoic seas (Figs 1 and 6), make their last appearance in the late Permian despite high diversity in earlier assemblages (Goto 1994; Ivanov 2005).
It is therefore possible there was a selective loss of marine and/or durophagous fishes between the Permian and Triassic. Whether these extinctions were centred on the end-Permian event or occurred more gradually is another issue. Mapes and Benstock (1988) noted a decline in holocephalan lineages over the later Permian, and Ivanov (2005) suggested that chondrichthyan tooth assemblages from that interval are less diverse than in the Carboniferous. Indeed, compendia show that the last appearances of some holocephalan lineages, such as cochliodonts, deltoptychiids and chondrenchelyiforms, occurred in the early Permian or even the Late Carboniferous (Cappetta et al. 1993; Stahl 1999; Sepkoski 2002).
These last appearances could represent random extinctions expected over any geological interval. After all, other fishes sometimes counted among the victims of the end-Permian event – acanthodians and megaliththyid sarcopterygians – represented depauperate lineages that disappeared in geographically stepwise fashion long before the boundary (Janvier 1996; Mutter and Richter 2007; Sallan and Coates 2010). Alternatively, holocephalan losses before the end-Permian could be due to the Signor-Lipps effect: backsmearing of extinction because of incomplete sampling of the record (Signor and Lipps 1982; Foote 2007), perhaps magnified by the poor condition of the late Permian fish record. Indeed, articulated marine fishes from that interval derive almost exclusively from the Marl Slate and Kupferschiefer of the northern European Zechstein Sea (Dineley and Metcalf 1999; Diedrich 2009) with a few scattered examples from further afield (China: Liu and Wei 1988; Greenland: Stemmerik et al. 2001), and these have been little studied. However, it is clear even from this scant record that many actinopterygian genera typically associated with Triassic age assemblages (Saurichthys: Liu and Wei 1988; Bobasatrania: Stemmerik et al. 2001) have ranges extending into the late Permian.
By contrast, the Triassic is marked by a series of well-documented and widely distributed marine Lagerstätten in Austria, Canada, China, Greenland, Italy, Madagascar, Spitsbergen, and Switzerland, with more minor assemblages in the United States (Tintori 1998; Brinkmann et al. 2010; Hu et al. 2011; Mutter 2011). Such Triassic deposits have been particularly important for calibrating the radiation of neopterygians, the clade that includes nearly all modern ray-finned fish diversity (Nelson 2006). In addition, the early Triassic also seems to record the onset of the neoselachian elasmobranch radiation (Underwood 2006), which includes all living chondrichthyans apart from holocephalans.
Both the neopterygian total group and crown appear to extend well into the Palaeozoic (Hurley et al. 2007), but crown representatives are minor components of faunas of this age, in terms of both richness and abundance (Diedrich 2009). Holosteans (bowfin, gars and their relatives) remain rare and teleosts are absent until the Late Triassic, at which point some localities record a great diversity of trophically divergent crown neopterygians. Particularly, striking is the proliferation of durophagous taxa both among total group teleosts (Pycnodontiformes) and holosteans (Macrosemiidae, Seminotidae) along with incertae sedis neopterygian groups (Dapediidae), occurring subsequent to the last appearances of so many Palaeozoic durophages (Tintori 1998).
In summary, although the magnitude of the end-Permian event for fishes is unclear, there is a possibility of selective extinction of marine (and particularly durophagous) fishes. In contrast, euryhaline elasmobranch and actinopterygian lineages, and marine conodonts, seem to have been largely unaffected, with multiple lineages present in devastated marine ecosystems in the Early Triassic. Just as many groups underwent habitat shifts post-Hangenberg, surviving fish clades might have moved into new marine environments, even though they would have found few resources in the immediate aftermath. Indeed, elasmobranch ichthyoliths from some Early Triassic localities are said exhibit a ‘Lilliput effect’, a reduction in size often noted after mass extinction and associated with poor productivity (Twitchett 2001; Chen et al. 2007; Mutter 2009). However, the significance of this reduction is unclear, because ichthyoliths from a single taxon can be variable, the size of pre-event ancestors is not always known, and oversampling of stressed environments in recovery intervals can affect recorded averages (McGowan et al. 2009). Holocephalans do not reappear in the record until the later Triassic, when they largely exhibit a form very similar to living chimaeroids (Stahl 1999). Mesozoic holocephalans did achieve some degree of disparity, ranging from dorsoventrally flattened skate-like forms in the Early Jurassic (Stahl 1999) and giant, but anatomically more conventional, species in the Late Cretaceous (Cicimurri et al. 2008). However, they never completely refilled lost morphospace or recovered to their Palaeozoic abundance, at least outside of the deep-sea environments that Recent forms inhabit and for which Mesozoic records are poor (Stahl 1999). The apparent diversity patterns discussed previously are therefore suggestive of selective extinction and replacement of fishes at the Permo-Triassic. These are in need of detailed investigation.
Middle and late Mesozoic diversity patterns
The middle Mesozoic commenced in the aftermath of the Triassic–Jurassic extinction, but the effect of that event upon fishes seems minimal (McCune and Schaeffer 1986; Bambach et al. 2004). Not a single osteichthyan family listed in The Fossil Record 2 by Gardiner (1993b) or Patterson (1993a) fails to cross the boundary (Hallam 2002). However, there is one potentially major exception: conodonts (Fig. 2). While Triassic conodont diversity paled in comparison with their Ordovician and Devonian–Missisissippian peaks (Fig. 2), conodont origination preceding the Triassic-Jurassic boundary was greater than in any interval because the Mississippian and their biostratigraphic utility was undiminished until the end of the period (Clark 1983; De Renzi et al. 1996).
Conodonts seem to undergo a long-term decline in the second half of the Triassic (Fig. 2) (Clark 1983; De Renzi et al. 1996; Sepkoski 2002). During this same interval, conodont elements became more ‘generalized’ or homogeneous in form, waned in abundance, were reduced to a single family and were extirpated from faunal regions in stepwise fashion (Trammer 1974; Clark 1983; Hallam 2002; Tanner et al. 2004). The latter trends could be reflective of a Signor-Lipps effect driven by facies change near the extinction boundary (Signor and Lipps 1982; Clark 1983; De Renzi et al. 1996; Tanner et al. 2004). However, the selective disappearance of conodonts by the end-Triassic is not widely attributed to an abiotic marine event, but rather to long-term loss of appropriate environments and greater provincialism because of the break-up of Pangaea (De Renzi et al. 1996). Losses have also been credited to an unfortunate run of random extinction, after-effects of the Permo–Triassic, competition with the modern evolutionary fauna, and even anecdotal scenarios invoking predation by ichthyosaurs (Clark 1983; De Renzi et al. 1996).
It is difficult to favour any single or combination of options because relevant data are largely unavailable, including that for the diversity of other fishes with similar environmental preferences and ecologies. However, the Triassic–Jurassic interval is generally defined by such gradual taxonomic and ecological turnover (Hallam 2002). In fact, the event has been termed a mass depletion without a single cause, akin to the Frasnian–Famennian (Bambach et al. 2004). On that note, Kriwet and colleagues (2009) have suggested that the Early Jurassic radiation of neoselachians reflects opportunistic radiation into ecological roles cleared by extinction, whether sudden or gradual, a repeated pattern by this point in the record.
The Jurassic–Cretaceous interval (200–65.5 Ma) is punctuated by several ocean anoxic events (OAEs; Schlanger and Jenkyns 1976; Jenkyns 1988), but there has been no suggestion that any of these resulted in either major extinction or faunal turnover among fishes. Indeed, some OAEs are flanked by well-studied faunas (e.g. the Hettangian–Sinemurian of Lyme Regis, England and the Toarcian of Yorkshire, England, Germany, and France in the case of the early Toarcian OAE; Wenz 1967; Hauff and Hauff 1981; Dineley and Metcalf 1999), and some even occur within continuous units that have been historically well-sampled for fishes (e.g. the English Chalk in the case of the Cenomanian–Turonian OAE; Dineley and Metcalf 1999).
There are two clear peaks in raw richness trajectories for Mesozoic fishes: one at the close of the Jurassic and another in the early Late Cretaceous (100–65.5 Ma). Both of these correspond to intervals with well-studied exceptional deposits, yielding numerous articulated actinopterygians (Late Jurassic: Cerin, France, and Solnhofen, Germany; early Late Cretaceous: Djebel Tselfat, Morocco, English Chalk, UK, Hakel, Hadjoula, and Namoura, Lebanon; Lambers 1999; Forey et al. 2003). Phylogeny-based techniques indicate that the Late Jurassic peak is probably a preservational artefact, at least for actinopterygians (Cavin 2010). However, the same phylogenetic test suggests that a genuine radiation among actinopterygians occurred during the Cenomanian (100–94 Ma; Cavin and Forey 2007), and Cavin et al. (2007) hypothesized such a pattern might have been driven by high sea surface temperatures.