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Effects of the early Toarcian Oceanic Anoxic Event on ichthyosaur body size and faunal composition in the Southwest German Basin

Published online by Cambridge University Press:  06 November 2015

Erin E. Maxwell  and
Peggy Vincent
Erin E. Maxwell
Affiliation:
Staatliches Museum für Naturkunde, Rosenstein 1, 70191 Stuttgart, Germany. Email: erin.maxwell@smns-bw.de, pvincent@mnhn.fr.
Peggy Vincent
Affiliation:
Staatliches Museum für Naturkunde, Rosenstein 1, 70191 Stuttgart, Germany. Email: erin.maxwell@smns-bw.de, pvincent@mnhn.fr.
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Abstract

The Early Jurassic Toarcian Oceanic Anoxic Event is considered one of the most dramatic environmental perturbations of the Mesozoic. An elevated extinction rate among marine invertebrates accompanied rapid environmental changes, but effects on large vertebrates are less understood. We examined changes in ichthyosaur body size in the Posidonia Shale of the Southwest German Basin spanning the extinction interval to assess how environmental changes and biotic crisis among prey species affected large reptiles. We report no species-level extinction among the ichthyosaurs coinciding with peak invertebrate extinction. Large ichthyosaurs were absent from the fauna during the extinction interval, but became more abundant in the immediate aftermath. Stenopterygius quadriscissus, the most abundant species during the extinction interval, increased in body size after the biotic event. Rapid invasion by large taxa occurred immediately following the extinction event at the end of the first ammonite zone of the early Toarcian. Greater mobility permitting exploitation of ephemeral resources and opportunistic feeding behavior may minimize the impacts of environmental change on large vertebrates.

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Type
Articles
Information
Paleobiology , Volume 42 , Issue 1 , February 2016 , pp. 117 - 126
Copyright
Copyright © 2015 The Paleontological Society. All rights reserved 

Introduction

The Toarcian Oceanic Anoxic Event (T-OAE; ~183 Ma) is considered to be one of the most dramatic environmental perturbations of the Mesozoic. This event was characterized by widespread deposition of organic carbon-rich shales in epicontinental seas (Jenkyns and Clayton Reference Jenkyns and Clayton1986; Jenkyns Reference Jenkyns1988; Jenkyns and Clayton 1997; Suan et al. Reference Suan, Nikitenkoc, Rogov, Baudin, Spangenberg, Knyazev, Glinskikh, Goryacheva, Adatte, Riding, Föllmi, Pittet, Mattioli and Lécuyer2011), accelerated hydrological cycle (Bailey et al. Reference Bailey, Rosenthal, McArthur, Schootbrugge and Thirwall2003; Cohen et al. Reference Cohen, Coe, Harding and Schwark2004; Hesselbo and Pieńkowski Reference Hesselbo and Pieńkowski2011), development of euxinic conditions in the photic zone (Schouten et al. Reference Schouten, van Kaam-Peters, Rijpstra, Schoell and Damste2000; Pancost et al. Reference Pancost, Crawford, Magness, Turner, Jenkyns and Maxwell2004), and a marked rise in seawater temperature (~5–8°C: Bailey et al. Reference Bailey, Rosenthal, McArthur, Schootbrugge and Thirwall2003; Rosales et al. Reference Rosales, Quesada and Robles2004; Gómez et al. Reference Gómez, Goy and Canales2008). These abiotic changes are generally considered to have been caused by the massive injection of isotopically light carbon to the atmosphere, as reflected by the prominent negative carbon isotope excursion (CIE; ~5–7‰) recorded by inorganic and organic material across the upper part of the Dactylioceras tenuicostatum Zone to the middle of the Harpoceras falciferum Zone (e.g., Küspert Reference Küspert1982; Jenkyns and Clayton Reference Jenkyns and Clayton1986, 1997; Schouten et al. Reference Schouten, van Kaam-Peters, Rijpstra, Schoell and Damste2000; Röhl et al. Reference Röhl, Schmid-Röhl, Oschmann, Frimmel and Schwark2001; Cohen et al. Reference Cohen, Coe, Harding and Schwark2004; Kemp et al. Reference Kemp, Coe, Cohen and Schwark2005; Hesselbo et al. Reference Hesselbo, Jenkyns, Duarte and Oliveira2007; Suan et al. Reference Suan, Pittet, Bour, Mattioli, Duarte and Mailliot2008; Suan et al. Reference Suan, Nikitenkoc, Rogov, Baudin, Spangenberg, Knyazev, Glinskikh, Goryacheva, Adatte, Riding, Föllmi, Pittet, Mattioli and Lécuyer2011). Proposed sources of isotopically light carbon include massive gas hydrate dissociation, volcanic-induced thermal metamorphism of organic-rich strata, or volcanogenic CO2 (summarized by Bond and Wignall Reference Bond and Wignall2014).

An elevated extinction rate during the late Pliensbachian–early Toarcian interval accompanied these environmental changes, beginning in the late Pliensbachian with a major pulse at the boundary between the tenuicostatum and falciferum ammonite zones corresponding to the initiation of the negative CIE (Raup and Sepkoski Reference Raup and Sepkoski1984; Hallam Reference Hallam1986; Sepkoski and Raup Reference Sepkoski and Raup1986; Jenkyns Reference Jenkyns1988; Little and Benton Reference Little and Benton1995; Hallam and Wignall Reference Hallam and Wignall1997; Harries and Little Reference Harries and Little1999; Macchioni and Cecca Reference Macchioni and Cecca2002; Aberhan and Baumiller Reference Aberhan and Baumiller2003; Cecca and Macchioni Reference Cecca and Macchioni2004; Wignall et al. Reference Wignall, Newton and Little2005; Boomer et al. Reference Boomer, Lord and Crasquin2008; Gómez et al. Reference Gómez, Goy and Canales2008; Caswell et al. Reference Caswell, Coe and Cohen2009; Morten and Twitchett Reference Morten and Twitchett2009; Dera et al. Reference Dera, Neige, Dommergues, Fara, Laffont and Pellenard2010). Many of the studies examining the biotic event focus on changes in taxonomic diversity to understand the magnitude, timing and geographical extent of the extinction episode (e.g., Hallam Reference Hallam1987; Little and Benton Reference Little and Benton1995; Harries and Little Reference Harries and Little1999; Aberhan and Fürsich Reference Aberhan and Fürsich2000; Macchioni and Cecca Reference Macchioni and Cecca2002; Aberhan and Baumiller Reference Aberhan and Baumiller2003; Cecca and Macchioni Reference Cecca and Macchioni2004; Boomer et al. Reference Boomer, Lord and Crasquin2008; Gómez et al. Reference Gómez, Goy and Canales2008; Caswell et al. Reference Caswell, Coe and Cohen2009). Few examine ecological effects associated with extinction (Hallam Reference Hallam1998; Caswell et al. Reference Caswell, Coe and Cohen2009; Morten and Twitchett Reference Morten and Twitchett2009; Dera et al. Reference Dera, Neige, Dommergues, Fara, Laffont and Pellenard2010; Fraguas and Young Reference Fraguas and Young2011; Danise et al. Reference Danise, Twitchett, Little and Clémence2013); however these effects are important in understanding the biotic response to environmental change that may be decoupled from diversity dynamics (McGhee et al. Reference McGhee, Sheehan, Bottjer and Droser2004; Dera et al. Reference Dera, Neige, Dommergues, Fara, Laffont and Pellenard2010). Ecological questions are of particular interest in the context of the significant abiotic changes over the T-OAE, and may be easier to detect than large diversity fluctuations given the relatively small number of extinctions of higher taxonomic groups during this event.

Due to their high trophic position, marine reptiles have an important role to play in understanding the early Toarcian biotic event. No family-level extinctions are reported for the group between the late Pliensbachian and early Toarcian, suggesting that higher-level taxonomic diversity was unaffected by the rapid abiotic changes (Little and Benton Reference Little and Benton1995). However, the ecological effects of the early Toarcian biotic event have not previously been investigated in vertebrates. Ichthyosaurs are the most abundant group of early Toarcian marine reptiles, occupying several trophic levels including apex predator (Sander Reference Sander2000). We examine the influence of the extinction episode in ichthyosaurs from the perspective of body size, an important parameter in trophic structure (Woodward et al. Reference Woodward, Ebenman, Emmerson, Montoya, Olesen, Valido and Warren2005) that is strongly correlated with extinction dynamics (e.g., McKinney Reference McKinney1990; McKinney Reference McKinney1997; Harries and Knorr Reference Harries and Knorr2009). We measure changes in body size in Stenopterygius quadriscissus (Quenstedt Reference Quenstedt1856), a common Toarcian species with a stratigraphic range spanning the extinction interval, and also examine changes in relative abundance of the ichthyosaur fauna as a whole during the T-OAE.

Institutional abbreviations

GPIT, Geologisch-Paläontologisches Institut und Museum, Universität Tübingen; MHH, Urwelt Museum Hauff; SMF, Senckenberg-Museums Frankfurt; SMNS, Staatliches Museum für Naturkunde Stuttgart.

Methods

Geology

The lower Toarcian Posidonia Shale Formation spans three ammonite zones in the Southwest German Basin (Dactylioceras tenuicostatum, Harpoceras falciferum, and Hildoceras bifrons; ~2.70–2.88 Myr [Boulila et al. Reference Boulila, Galbrun, Huret, Hinnov, Rouget, Gardin and Bartolini2014]), and thus includes the extinction and survival intervals of the early Toarcian extinction (Harries and Little Reference Harries and Little1999). Locally termed the Lias Epsilon (ε), the Posidonia Shale is regionally subdivided into three sections of unequal thickness designated by Roman numerals: εI–εIII. The sections are then further divided, designated by subscript. Localities in this basin comprise the most productive Toarcian fossil vertebrate sites in the world, and key among these are quarries concentrated around the village of Holzmaden (Fig. 1). Ichthyosaurs are found in all three sections, but the most productive layer is εII3 (Dactylioceras tenuicostatum Zone, Dactylioceras semicelatum Subzone; Riegraf et al. Reference Riegraf, Werner and Lörcher1984). We use the total number of fish specimens in the collection of the SMNS (n=343) as a measure of overall preservation and recovery potential of vertebrate fossils (Fig. 2).

Figure 1

Map showing the extent of Posidonia Shale exposure (black shading) in the Southwest German Basin. The most productive fossil vertebrate localities are situated in and around the village of Holzmaden (modified from Röhl et al. Reference Röhl, Schmid-Röhl, Oschmann, Frimmel and Schwark2001).

Figure 2

Correlated summary of abiotic and biotic changes in the Southwest German and Yorkshire Basins over the Early Toarcian Oceanic Anoxic Event. Vertebrate data from the current study; geochemical data from the sources noted below. PC1 (Stenopterygius quadriscissus) represents the reduction of six morphological measurements, as discussed in “Methods”. Small ichthyosaur taxa (<4 m adult body length) are indicated by asterisks in the legend. δ13C and total organic carbon (TOC) curves from Röhl et al. (Reference Röhl, Schmid-Röhl, Oschmann, Frimmel and Schwark2001), aryl isoprenoid curve from Schwark and Frimmel (Reference Schwark and Frimmel2004), δ18O, Mg/Ca ratios and strontium isotope curves from Bailey et al. (Reference Bailey, Rosenthal, McArthur, Schootbrugge and Thirwall2003), and osmium isotope profile from Cohen et al. (Reference Cohen, Coe, Harding and Schwark2004).

The Southwest German Basin is the only locality producing abundant ichthyosaur material from the period spanning the T-OAE: a single specimen from southern France potentially referable to Temnodontosaurus has been described from the tenuicostatum Zone (Fischer et al. Reference Fischer, Guiomar and Godefroit2011), but no ichthyosaur remains of this age are reported from other European epicontinental basins or the Cleveland Basin (UK) (Benton and Spencer Reference Benton and Spencer1995; Caine and Benton Reference Caine and Benton2011). No diagnostic Toarcian ichthyosaur remains have been reported outside of Europe. This shortage of comparative material limits the potential geographical scope of the study.

Intraspecific body size evolution

Stenopterygius quadriscissus is one of the smallest and most abundant ichthyosaur species from the Posidonia Shale, with adult body lengths of 2.0–3.5 m (Maisch Reference Maisch2008). The stratigraphic distribution of this species, from the tenuicostatum–bifrons Zones spans the T-OAE. We used the criteria established by previous authors to assign specimens to species (Maisch Reference Maisch2008; Maxwell Reference Maxwell2012). Individuals with mandibular lengths of over 400 mm are considered to be sexually mature (adult), a criterion established based on the size of the smallest known female with embryos preserved in the body cavity (McGowan Reference McGowan1979).

Using specimens in existing museum collections (SMNS, SMF, GPIT, MHH; Supplementary Table 1), we obtained six linear measurements for each adult specimen for which stratigraphic information was available (length of the premaxilla, mandible, humerus, radius, femur, ischiopubis; n=26). These measurements were log-transformed and then reduced to a single multivariate metric of size for each individual using principal components analysis (PC1, hereafter referred to as the size score; PC1=85% of observed variance, all variables have weak positive loadings with the postcranial measurements having higher loadings than the cranial measurements). We plotted the size scores relative to stratigraphic horizon to determine the pattern of size distribution through time (Fig. 2). Ichthyosaurs continue to increase in body size after sexual maturity, so every stratigraphic bin should contain specimens ranging in size from the maturity cutoff to the largest individual sampled. In practice, all time bins were biased in favor of larger adults (Supplementary Figure 1). This bias against small individuals makes mean body size an unreliable metric, so we opted to use maximum size for our analysis.

To test for change in maximum size over the T-OAE, we assessed the probability that the time bin with the most sampled individuals (εII3: n=10 adults) would contain such a small maximum size score (z=0.11) given the distribution of size scores in the falciferum Zone. We pooled the observed specimen size scores and selected random samples of n=10 with replacement over 10 000 replicates. If the largest size score in a random sample was smaller than 0.12 (i.e., consistent with εII3), the replicate received a score of 0. If the largest size score in the sample exceeded this cut-off, the replicate received a score of 1. The average score of all replicates determined the probability of selecting a sample of ten individuals where the largest individual had a z-score of 0.11 by chance. In addition, we ranked all size scores and performed a Mann-Whitney test to examine distributional differences in ranked size scores between Stenopterygius quadriscissus adults from the tenuicostatum (n=14) and falciferum (n=12) zones.

Interspecific community body size structure

Stratigraphic data for Suevoleviathan (n=4), Temnodontosaurus (n=20), Eurhinosaurus (n=17), and Stenopterygius (n=64) specimens were obtained from the literature (Maisch Reference Maisch1998a,Reference Maischb); stratigraphic data for Hauffiopteryx (n=7) and specimens of Eurhinosaurus not mentioned in Maisch (Reference Maisch1998b) were obtained through personal observation. Classification of genera based on body size was obtained using the rankings outlined in McGowan and Motani (Reference McGowan and Motani2003): small-medium (adults <4 m long) versus large (adults ≥4 m long), with the exception of St. uniter which we classified as small-medium as no adults in our sample exceeded 3.75 m total length and most were between 3.0–3.5 m.

Results

Intraspecific trends in body size

A trend of increasing body size in Stenopterygius quadriscissus may occur throughout the tenuicostatum Zone (Fig. 2), with the smallest pregnant female from stratum εI2 being much smaller than the smallest pregnant female from later intervals (Fig. 3). However, due to small sample sizes in the Protogrammoceras paltum Subzone significance cannot be assessed. A significant increase in body size occurred between the late semicelatum Subzone and the latest semicelatum Subzone/earliest Harpoceras exaratum Subzone (εII3 and εII4; P=0.0016). Maximum size remains constant for the duration of the falciferum Zone (εII4–εII10), and no adult specimens referable to S. quadriscissus are known from the bifrons Zone. The results of the Mann-Whitney test support the results of the maximum size analysis: the mean size rank of specimens from the tenuicostatum Zone=8.4, and that of specimens from the falciferum Zone=19.5 (U=156, n(tenuicostatum)=14, n(falciferum)=12, P<0.001).

Figure 3

The smallest (SMNS 52036; 208 cm in length), mid-range (SMNS 50963; 285 cm) and largest (MHH 1981/33; 310 cm) pregnant Stenopterygius quadriscissus specimens in the sample, illustrating the range of body sizes of sexually mature females of this species. Temnodontosaurus (SMNS 15950; 770 cm length) is figured for comparison.

Interspecific patterns

Sampling is poor in the early tenuicostatum Zone (paltum – earliest semicelatum subzones: εI1-4), with only two specimens both referred to S. quadriscissus. The number of recovered specimens improves dramatically in the late semicelatum Subzone (εII1-3), coinciding with increased preservation potential based on fish abundance, but ichthyosaur diversity remains low—almost three quarters of the ichthyosaurs from this interval are S. quadriscissus (Fig. 2); S. triscissus and Hauffiopteryx are present at low abundance. Large ichthyosaurs (adult lengths of >4 m) are very rare, represented only by a partial forelimb referred to Temnodontosaurus (Maisch Reference Maisch1998b). In later time intervals, overall diversity increases, species abundance becomes more even, and in particular the relative abundance of S. quadriscissus decreases: by εII6 (late exaratum–early Harpoceras elegans Subzone), S. quadriscissus represents <20% of all specimens recovered. This decline coincides with an increase in the number and relative abundance of large genera in εII4-6 (early-middle exaratum–early elegans subzones). Consistent with this trend is the first occurrence of S. uniter, the largest Toarcian representative of the genus Stenopterygius, in εII6 (late exaratum–early elegans Subzone). εII5 (middle exaratum Subzone) represents a special case, where small taxa (adult body lengths of <4 m) are extremely rare. Whether this reflects an unbiased biological signal is unclear.

The large ichthyosaur genera Suevoleviathan, Temnodontosaurus, and Eurhinosaurus have been preferentially acquired and prepared by museums, since they are more rare than Stenopterygius and make impressive exhibition pieces. Thus, the relative proportion of these genera in some horizons may be inflated, but their apparent absence in the Fleins (εII3), the most intensively sampled horizon in the sequence (Keller Reference Keller1985), cannot be attributed to collecting bias. Based on the relatively quiet benthic environment of the Posidonia Shale sea (Röhl et al. Reference Röhl, Schmid-Röhl, Oschmann, Frimmel and Schwark2001), as well as the presence of invertebrates in the Fleins as large as the large ichthyosaurs (i.e., Seirocrinus colonies: Hauff [Reference Hauff1921]) preservational biases such as size-sorting are also unlikely. Eurhinosaurus longirostris first appears in εII4 (latest semicelatum – early exaratum Subzone), but other large taxa (T. trigonodon, Su. disinteger) are not present before εII5 (mid-exaratum Subzone). Large ichthyosaurs as a group remain present and proportionately abundant for the duration of the falciferum Zone (Fig. 2). All large genera belong to lineages that originated in the Late Triassic (see Fischer et al. Reference Fischer, Appleby, Naish, Liston, Riding, Brindley and Godefroit2013), and thus their appearance in the falciferum Zone represents multiple invasions rather than diversification of a single lineage.

Discussion

We recognize two general phases in ichthyosaur body size change in the early Toarcian of the Southwest German Basin, bridged by a short transitional period (εII4). During the late tenuicostatum Zone (εII3), corresponding to the onset of environmental deterioration, diversity was low and small taxa (Stenopterygius, Hauffiopteryx) dominated the ichthyosaur assemblage. S. quadriscissus was particularly abundant in εII3, and was at its smallest body size with adult total lengths between 2.1 and 2.9 m (Maisch Reference Maisch2008). The invertebrate extinction horizon falls between εII3 and εII4 in the Southwest German Basin (Hauff Reference Hauff1921). At this time, δ13Ccarb and δ13Corg values significantly decrease, and coeval increase of sea water temperatures (as seen in an abrupt shift toward lower values of the δ18O and higher values of the Mg/Ca ratios), as well as the onset of the large excursion in the 187Os/188Os ratio, suggesting increased terrestrial weathering (Fig. 2; Bailey et al. Reference Bailey, Rosenthal, McArthur, Schootbrugge and Thirwall2003; Suan et al. Reference Suan, Mattioli, Pittet, Lécuyer, Suchéras-Marx, Duarte, Philippe, Reggiani and Martineau2010). Among ichthyosaurs, the biotic event was followed by a decline in the abundance of S. quadriscissus relative to Hauffiopteryx, and taxonomic diversity began to increase with the appearance of Eurhinosaurus. A significant body size increase occurred in S. quadriscissus, with specimens commonly ≥3 m total length (Maisch Reference Maisch2008).

In the late exaratum–early elegans subzones, Toarcian ichthyosaur diversity reached its acme and the maximum size of S. quadriscissus stabilized, 230–500 Kyr prior to the end of oil shale deposition at the top of the elegans Subzone (Röhl et al. Reference Röhl, Schmid-Röhl, Oschmann, Frimmel and Schwark2001). This corresponds to the end of the postulated survival phase (Harries and Little Reference Harries and Little1999). Many invertebrate taxa did not begin to increase in body size prior to this time (Morten and Twitchett Reference Morten and Twitchett2009), suggesting that ecosystem recovery at lower trophic levels lagged behind higher ones. Food webs are understood to recover from disruption in a stepwise manner, with large vertebrate predators appearing last (Chen and Benton Reference Chen and Benton2012 and references therein; see Scheyer et al. Reference Scheyer, Romano, Jenks and Bucher2014 for a different interpretation). Our results indicate that apex predators (e.g., Temnodontosaurus) may be able to colonize disturbed ecosystems faster than species diversity can recover at lower trophic levels, possibly because of generalist dietary preferences and a high biomass of a few resilient prey species (Böttcher Reference Böttcher1989).

Extinction events have a well-documented effect on the taxonomic composition, species diversity and abundance in both marine and terrestrial ecosystems (Hallam and Wignall Reference Hallam and Wignall1997). Within species, body size is typically reduced, and a non-diverse assemblage of smaller species dominate the fauna in the aftermath of an extinction event (“post-event syndrome”, with the inter- and intraspecific reductions in body size frequently referred to as the “Lilliput effect”: Urbanek, Reference Urbanek1993; e.g. Urbanek Reference Urbanek1993; Hallam Reference Hallam1998; Twitchett Reference Twitchett2007; Morten and Twitchett Reference Morten and Twitchett2009; Borths and Ausich Reference Borths and Ausich2011; Huttenlocker Reference Huttenlocker2014). The evolutionary response of vertebrates to decreasing environmental quality is poorly documented, with only a few studies providing empirical support for a decrease in body size associated with extinction event survivors (e.g., increase in size of shark denticles in the Early Triassic following an end-Permian minimum [Mutter and Neuman Reference Mutter and Neuman2009]; proportional loss of large terrestrial taxa in the aftermath of the Permian and end-Cretaceous extinctions [Bakker Reference Bakker1977; Fara Reference Fara2000; Twitchett Reference Twitchett2007; Sahney and Benton Reference Sahney and Benton2008; Metcalfe et al. Reference Metcalfe, Twitchett and Price-Lloyd2011; Huttenlocker Reference Huttenlocker2014]; changes in growth strategy and decrease in adult size in Triassic synapsids relative to their Permian congeners [Huttenlocker and Botha-Brink Reference Huttenlocker and Botha-Brink2013]).

Toarcian falciferum Zone invertebrate faunas demonstrate characteristics typical of post-event syndrome (e.g., Harries and Little Reference Harries and Little1999; Caswell et al. Reference Caswell, Coe and Cohen2009; Morten and Twitchett Reference Morten and Twitchett2009; Fraguas and Young Reference Fraguas and Young2011; Caswell and Coe Reference Caswell and Coe2013). In contrast, it appears that the ichthyosaur assemblage does not, showing the opposite pattern to the one predicted: few, predominantly small species occur at the onset of environmental deterioration preceding the invertebrate extinction horizon, and increased generic diversity, intra- and interspecific body size characterize the period immediately following the extinction interval. It should be noted that carbon cycle perturbations and an elevated extinction rate among ammonites have also been reported at the Pliensbachian/Toarcian boundary (Dera et al. Reference Dera, Neige, Dommergues, Fara, Laffont and Pellenard2010; Littler et al. 2010), so the tenuicostatum Zone ichthyosaurs may not be characteristic of a stable environment. A poor Pliensbachian vertebrate record makes this difficult to assess.

Potential underlying causes of the ichthyosaur body size increase in the early falciferum Zone can only be speculated upon; one possibility involves a shift in the relative abundance of prey species. Coleoid cephalopods are very rare in basins influenced by deoxygenation over most of the falciferum Zone (Hauff Reference Hauff1921; Caswell and Coe Reference Caswell and Coe2014), but fish remains are abundant (Fig. 2). Gastric contents suggest that coleoid cephalopods were the preferred prey of Stenopterygius adults (Keller Reference Keller1976), whereas larger ichthyosaur genera such as Temnodontosaurus appear to have consumed a wider range of prey types (Böttcher Reference Böttcher1989). If large body size was positively selected in Stenopterygius during a shift away from a coleoid-dominated diet, this may explain body size increase over the T-OAE. The increased abundance of fish may also explain the higher diversity of large, presumably generalist genera, if indeed the number of preserved fishes reflects overall abundance. A second possibility for increased body size in Stenopterygius quadriscissus over the T-OAE involves rising seawater temperatures (Bailey et al. Reference Bailey, Rosenthal, McArthur, Schootbrugge and Thirwall2003; Rosales et al. Reference Rosales, Quesada and Robles2004; Gómez et al. Reference Gómez, Goy and Canales2008). Isotopic evidence suggests that some ichthyosaurs maintained a body temperature warmer than the ambient environment (Bernard et al. Reference Bernard, Lécuyer, Vincent, Amiot, Bardet, Buffetaut, Cuny, Fourel, Martineau, Mazin and Prieur2010). Warmer temperatures might result in more energy being expended on growth rather than thermoregulation, resulting in the intraspecific size increase.

The end-Triassic mass extinction is also characterized by a negative CIE, climatic warming, and increased continental weathering (Ruhl et al. Reference Ruhl, Bonis, Reichert, Sinninghe Damsté and Kürschner2011), and is often cited as an evolutionary bottleneck that severely restricted morphological disparity in ichthyosaurs (Thorne et al. Reference Thorne, Ruta and Benton2011). Ichthyosaurs from the pre-planorbis beds of the Blue Lias (UK) deposited during the 120 Kyr interval following the initial end-Triassic negative CIE and extinction interval and approximately corresponding to the main negative CIE (“pre-recovery period”: Ruhl et al. [Reference Ruhl, Deenen, Abels, Bonis, Krijgsman and Kürschner2010]) are relatively small and non-diverse, consisting of Ichthyosaurus communis and Leptonectes tenuirostris (McGowan, Reference McGowan1974a; McGowan, Reference McGowan1989). No size data is available for the former; the latter is reported to have a maximum body length of no more than three meters (McGowan, Reference McGowan1989). The more abundant ichthyosaur remains from the late Hettangian indicate that by this point, multiple species of Ichthyosaurus were present, the large genus Temnodontosaurus had appeared, and maximum length of Leptonectes tenuirostris had increased to four meters (McGowan, Reference McGowan1974a; McGowan, Reference McGowan1974b, Reference McGowan1989). However, maximum diversity was not reached prior to the Sinemurian (McGowan and Motani, Reference McGowan and Motani2003). The slower recovery may be attributed to the much greater ecological disruption attributed to the Triassic/Jurassic boundary event relative to the T-OAE (Hallam and Wignall, Reference Hallam and Wignall1997) and ichthyosaur diversity over this interval appears to follow the post-event pattern predicted by Urbanek (Reference Urbanek1993).

Size selectivity over mass extinction events is a common theme in both the theoretical and empirical literature, but most work on this topic discusses invertebrates, due to larger available sample sizes and better stratigraphic data. We show that during a minor extinction event initiated by increasing atmospheric pCO2 and global warming, marine reptiles are remarkably resilient, showing faster recovery times in terms of both body size and diversity than their prey. Rapid invasion, rather than extinction and radiation, dominate the pattern observed compared with the invertebrate taxa. Body size increases are observed both within and between ichthyosaur species. Greater mobility allowing the exploitation of ephemeral resources and opportunistic feeding behavior may be responsible for minimizing the impact of the regional environmental degradation on these large vertebrates. However, increasing severity of ecological disturbance may limit the effectiveness of these strategies.

Acknowledgments

Thanks to R. Schoch and J. Müller for discussion and logistical support, and P. Havlik (Geologisch-Paläontologisches Institut und Museum, Universität Tübingen), R. Brocke (Senckenberg Forschungsinstitut und Naturmuseum Frankfurt) and R. Hauff (Urwelt Museum Hauff) for collections access. Thanks to B. Caswell and P. Harries for providing critical comments on an earlier version of the manuscript, and to N. Fröbisch, J. Massare and an anonymous reviewer. This project was funded through Natural Sciences and Engineering Research Council of Canada postdoctoral fellowship to E.E. Maxwell and Alexander von Humboldt postdoctoral fellowships to E.E. Maxwell and P. Vincent.

Supplementary Material

Supplemental Material deposited at Dryad: doi:10.5061/dryad.pm4v7

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Figure 0

Figure 1 Map showing the extent of Posidonia Shale exposure (black shading) in the Southwest German Basin. The most productive fossil vertebrate localities are situated in and around the village of Holzmaden (modified from Röhl et al. 2001).

Figure 1

Figure 2 Correlated summary of abiotic and biotic changes in the Southwest German and Yorkshire Basins over the Early Toarcian Oceanic Anoxic Event. Vertebrate data from the current study; geochemical data from the sources noted below. PC1 (Stenopterygius quadriscissus) represents the reduction of six morphological measurements, as discussed in “Methods”. Small ichthyosaur taxa (<4 m adult body length) are indicated by asterisks in the legend. δ13C and total organic carbon (TOC) curves from Röhl et al. (2001), aryl isoprenoid curve from Schwark and Frimmel (2004), δ18O, Mg/Ca ratios and strontium isotope curves from Bailey et al. (2003), and osmium isotope profile from Cohen et al. (2004).

Figure 2

Figure 3 The smallest (SMNS 52036; 208 cm in length), mid-range (SMNS 50963; 285 cm) and largest (MHH 1981/33; 310 cm) pregnant Stenopterygius quadriscissus specimens in the sample, illustrating the range of body sizes of sexually mature females of this species. Temnodontosaurus (SMNS 15950; 770 cm length) is figured for comparison.