www.sciencemag.org/cgi/content/full/science.aaf2416/DC1

Supplementary Materials for

Ecological selectivity of the emerging mass extinction in the oceans

Jonathan L. Payne,* Andrew M. Bush, Noel A. Heim, Matthew L. Knope, Douglas J. McCauley

*Corresponding author. Email: jlpayne@stanford.edu

Published 14 September 2016 on Science First Release DOI: 10.1126/science.aaf2416

This PDF file includes:

Materials and Methods Supplementary Text Figs. S1 to S10 Table S1 References

Materials and Methods Taxonomic Level

To more accurately and transparently compare patterns of modern biodiversity threat to extinction events in the fossil record, we analyzed all patterns at the genus level. Extrapolation of genus-level losses in the fossil record to species-level losses is not tenable because inferred species losses are sensitive to assumptions regarding the statistical distribution of species into genera (31) and the extent to which species losses are random versus taxonomically clustered (32). Taxonomic Coverage We developed a list of valid genera and their stratigraphic ranges using Sepkoski’s (33) compendium of fossil animal genera and the Treatise on Invertebrate Paleontology (34-39). We opted to use these sources rather than the Paleobiology Database because more than 20% of the genera in our analysis lack occurrences in the Paleobiology Database and so would have to be excluded from the analysis if based on this data source. Following standard taxonomic practice in paleontology (40-42), we elevated subgenera to the rank of genera, thus avoiding problems of taxonomic uncertainty at sub-genus taxonomic levels. We checked taxonomic names from literature sources against more recent taxonomic opinions compiled in the Paleobiology Database (http://paleobiodb.org). We gave preference to the Paleobiology Database in instances where there was a difference in rank or opinion. See Heim et al. (43) for a full description of taxonomic treatment and sources.

We restricted our analysis of extinction selectivity to marine members of phylum Mollusca and subphylum Vertebrata of phylum Chordata (excluding birds) because they have the best data coverage in both the IUCN Red List (44) and the Heim et al. (43) body size database. Across extant and extinct genera, mollusc data comprise classes Bivalvia, Cephalopoda, Gastropoda, Polyplacophora, Tergomya, Paragastropoda, Rostroconchia, Scaphopoda, and Tentaculita. Vertebrate data comprise the classes Actinopterygii, Chondrichtyes, Mammalia, Reptilia, Osteichthyes, Conodonta, and Placodermi (Fig. S1). No other phyla have more than 10 assessed genera and body size data due to the near absence of IUCN assessments for marine arthropods, brachiopods, and echinoderms. We further restricted our analysis to those genera known from the fossil record (see Stratigraphic Range Information below) in order to avoid identifying differences between Anthropocene extinctions and paleontological counterparts that arise from differences in taxonomic and ecological coverage of the data sets. The restricted analysis spans 2497 extant and extinct genera, of which 1243 are extant (Fig. S1). For our primary analysis of extinction threat selectivity in the modern oceans, we used all extant genera with fossil records and made the optimistic assumption that genera lacking IUCN assessments are not threatened. Of the extant genera, 264 contain species with IUCN assessments (other than ‘data deficient’; Fig. S1). We demonstrate via sensitivity analyses (Figs. S3-S5) that our findings are not materially affected by inclusion or exclusion of genera with or without IUCN assessments and with or without fossil records.

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Modern Threat Assessments We used the IUCN Red List (v. 2014.2) to designate the threat level for each

marine animal included in these comparisons. The IUCN uses a six-level hierarchy to characterize species threat (from more to less threat): “extinct”, “critically endangered”, “endangered”, “vulnerable”, “near threatened”, and “least concern”. The IUCN makes these assignments at the species level. We reassigned threat levels at the genus level in two ways: 1) by adopting the threat level of the most-threatened species within each genus and 2) by adopting the threat level of the least-threatened species within each genus. We use the former data treatment in our primary analysis, but demonstrate in supplementary analyses that using the latter approach does not qualitatively alter our conclusions. Genera were then classified in a binary system as ‘threatened’ or ‘not threatened’ to replicate the binary outcome of previous extinction events in which genera either survived or went extinct. For our primary analysis, we considered all genera classified as ‘near threatened’ or worse as threatened and only genera classified as ‘least concern’ as ‘not threatened.’ We demonstrate through sensitivity analyses that the precise choice of the cutoff between ‘threatened’ and ‘not threatened’ genera does not meaningfully alter the results. In our dataset, 250 out of 310 extant vertebrate genera (80.6%) with fossil records have IUCN-assessed species, whereas only 14 out of 933 extant mollusc genera (1.5%) have IUCN-assessed species. Following previous studies (45, 46), we have treated our data both with a conservative approach, in which we assume that assessed taxa are representative of those without assessments (or assessed as ‘data deficient’), and with a more optimistic scenario in which all genera without assessed species are assumed not to be at risk of extinction. As discussed in the text, these two contrasting approaches yield similar patterns of extinction selectivity despite substantial differences in projected extinction intensity for the molluscs (due to the large number of genera without assessments).

Body Size Data

We used the comprehensive database of Heim et al. (43) to assign body size, expressed in terms of maximum length, to each genus. We compiled additional size data for genera not covered in this database following the same methods. These data are available in the supporting online materials.

Ecology Data

We used the database of Knope et al. (47), following the coding scheme of Bush et al. (48), to code each genus for three traits representing foundational elements of ecological function: feeding mode (predator versus non-predator), tiering level, here referred to as ‘habitat zone’ (living on or in the sediment versus living in the water column), and motility level (motile in the adult form versus sessile in the adult form). We collapsed the six-part ecological assignments for each trait in the Knope et al. (47) database into the binary divisions listed above in order to establish sufficient statistical power to conduct regression analyses for all geological intervals. For feeding mode, we distinguished predators from non-predators. In the Knope data set, this corresponds to mode 5 versus modes 1-4 and 6. For habitat zone, we distinguished pelagic from benthic (mode 1 versus modes 2-6). For motility, we distinguished motile (fully motile, sensu ref. 48) from non-motile (non-motile plus facultatively motile, sensu ref. 48) adult forms

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(modes 1 and 2 versus 3-6). For genera not included in the Knope et al. (47) database, we used the primary literature to code ecological traits following the same methods.

Data Analysis

We calculated extinction intensity as the percentage of genera known from a given time interval (geological stage) that did not survive into the next stage. Other metrics are available for occurrence-based paleontological data (49), but percentages permit comparisons with data on modern extinction threat and do not require any assumption regarding the time interval over which taxonomic losses may occur. We calculated extinction selectivity as the coefficient of association between the predictor variable and survival status (survived versus extinct) in a multiple logistic regression model. To address both uncertainty of parameter values within models as well as uncertainty regarding the appropriate model for the data, we calculated regression coefficients for predictors using AICc-based multi-model averaging (50) using the AICcmodavg package (51) in R (52). In this approach, the coefficient for each predictor is calculated as the weighted average among all possible subsets from the intercept-only model to the full regression model including all predictors with the weight of each model reflecting is AICc weight. The coefficient values calculated via this all-subsets regression approach generally have less bias than the coefficient values associated with the single best model and take into account uncertainty both within individual modes and among models considered (50).

Comparison to Previous Studies of Body Size and Extinction in the Fossil Record

The lack of a consistent, positive association between body size and extinction probability in our dataset, prior to the modern, is largely consistent with previous analyses of the marine fossil record. Previous studies are substantially more limited in taxonomic and temporal coverage, largely focusing on the end-Cretaceous mass extinction. Most previous analyses have also failed to identify a significant association between body size and extinction probability during mass extinctions in bivalves and gastropods (27, 53-56). The association between body size and extinction probability in bivalves during background intervals appears to be heterogeneous among subclades (57). Body size was positively associated with extinction probability in teleost fishes during the end-Cretaceous mass extinction (58), but the strength of association was approximately one-fifth of that observed in the modern oceans (0.33 for the end-Cretaceous teleosts (7) versus 1.53 for living Actinopterygii). (We adjusted the coefficient from reference (9) by multiplying by ln(10) to adjust from the natural logarithm scale of reference (9) to the log10 scale of this study. We then divided the coefficient by two to adjust for the use of area as the size measure in reference (9) to the use of length in this study, because area is approximately the square of length.) Although fishes also decreased in size during the 30 Myr following the Late Devonian extinction, the mean size actually increased between the Frasnian (383-372 Mya) and Famennian (372-359 Mya) stages (59) – the event considered here. Thus, findings presented here appear to reflect a general lack of association between large body size and extinction probability in the marine fossil record. Moreover, the strength of the association in the modern ocean is much larger than the one well-documented case in the marine fossil record.

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Fig. S1 Taxonomic composition of the study dataset used for analyses of extinction selectivity. Number of genera given in parentheses. Red shading indicates molluscan classes, blue shading indicates vertebrate classes.

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Fig. S2 Proportion of genera categorized as threatened as a function of taxonomic grouping and IUCN threat level cut-off. For vertebrates and molluscs, the open and closed circular symbols are not visible because they plot beneath the corresponding square symbols. EX – extinct; CR – critically endangered; EN – endangered; VU – vulnerable; NT – near threatened.

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Fig. S3 Coefficients from multiple logistic regression analysis of extinction threat predicted by ecological covariates as a function of data treatment. The consistency of coefficients among data treatments demonstrates that associations between predictors and extinction risk do not depend on whether the genus is coded based on the least-threatened member species (low) or most-threatened member species (high) or whether the analysis includes only genera with IUCN-coded species (iucn) or assumes all non-coded genera are at low risk (all). The N/A values for minimal threat level in motility simply reflect the fact that all threatened genera based on the lower estimate are motile. Consequently, the odds ratio is undefined with respect to this parameter under this data treatment. Error bars represent 95% confidence intervals on estimated coefficients.

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Fig. S4 Coefficients from multiple logistic regression analysis of extinction risk based on threat level used to distinguish threatened versus non-threatened genera. The consistency of coefficient values among data treatments illustrates that the results do not depend upon the cutoff used to distinguish threatened from non-threatened genera. The results presented here assume the upper level of extinction risk for all genera and that uncoded genera are at low risk of extinction. Other data treatments yield similar results. The N/A values for motility in treatments considering only endangered and/or critically endangered genera as threatened reflects the fact that all threatened genera based on this threshold are motile. Consequently, the odds ratio is undefined with respect to this parameter under this data treatment. Error bars represent 95% confidence intervals on estimated coefficients.

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Fig. S5 Regression coefficients from multiple logistic regression analysis of extinction risk based on the inclusion or exclusion of genera without a fossil record as well as genera with or without IUCN assessments. This analysis assumes genera lacking IUCN-assessed species (or containing only data deficient species) are at low risk of extinction and that extinction risk for the genus is determined by the most-threatened species within the genus, but other data treatments yield qualitatively similar results. Error bars represent 95% confidence intervals on estimated coefficients.

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Fig. S6 Association between extinction risk and body size for taxa with at least five genera at risk and five not at risk for extinction, assuming taxa IUCN-assessed as near threatened or worse are at risk of extinction. Logistic regression coefficients illustrate a taxonomically pervasive association between body size and extinction risk. Error bars represent 95% confidence intervals on estimated coefficients.

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Fig. S7 Boxplots illustrating the size distributions of genera at risk of extinction versus those not at risk, illustrating the strong size bias of extinction risk at nearly all taxonomic levels. Results of a logistic regression of extinction risk as a function of log10-transformed size are presented in Figure 3. Dark black lines represent the medians. Boxes encompass the 25th through 75th percentiles of the data. Whiskers extend one and a half times the interquartile range or to the extremes of the data if the latter is closer to the relevant quartile. The bottom right panel illustrates the proportion of genera at risk (upper estimate) as a function of the mean length in the taxon, showing that extinction risk is correlated with mean size of the taxon. Blue – molluscs; red – vertebrates; black – molluscs and vertebrates; square – multiple phyla; circle – phylum; triangle – class.

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Fig. S8 Cenozoic pattern of extinction selectivity with respect to body size. Results are comparable for all molluscs (a) and for non-cephalopod molluscs (b), demonstrating that the overall inverse association between size and extinction probability is not the product of simply mixing larger-bodied taxonomic groups, such as cephalopods, with other molluscs. Error bars represent 95% confidence intervals on estimated coefficients.

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Fig. S9 Scatterplot illustrating the coefficients from single logistic regressions of extinction probability as a function of body size by class for both fossil and recent vertebrates and molluscs. These results illustrate the difference between extinction threat in the modern oceans (red symbols) and extinction patterns in the fossil record (black symbols). Statistically significant associations are illustrated with filled symbols. Open symbols indicate associations that are not statistically significant. Error bars have been omitted for clarity. Analytical protocol for the modern genera as in Figures 2 & 3.

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Fig. S10 Coefficients from logistic regression models for each ecological trait across geological time after excluding all vertebrate and mollusc genera smaller than 2 cm in maximum length. These results demonstrate that the tendency for smaller-bodied genera to go extinct in the fossil record is not a simple function of the generally poor sampling of the smallest specimens. Poor sampling typically affects specimens smaller than 1 cm in maximum length (59). We have used a threshold of 2 cm to be conservative. Some stages are excluded from this analysis because fewer than five genera of length greater than 2 cm went extinct during the interval. Error bars represent 95% confidence intervals on estimated coefficients. The error bar for habitat zone at 66 Mya (K/Pg mass extinction) has been truncated to preserve clarity and a common vertical axis on all panels.

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Table S1. Percent of genera at risk of extinction by category, based on combined mollusc and vertebrate data. NT – near threatened; VU – vulnerable; EN – endangered; CR – critically endangered; EX – extinct. The low estimate is calculated by applying the conservation status of the least threatened species within the genus. The high estimate is calculated by applying the conservation status of the most threatened species in the genus. Genera lacking IUCN-assessed species were assumed not to be threatened in the calculations for all genera and genera with a fossil record.

All genera All genera

Genera with fossil record only

Genera with fossil record only

Fossil record & IUCN assessment

Fossil record & IUCN assessment

Cutoff Low estimate

High estimate

Low estimate

High estimate

Low estimate

High estimate

NT 3.7 6.6 5.1 8.5 24.2 40.4

VU 2.2 5.6 3.1 7.4 14.7 35.1

EN 1 2.9 1.3 3.7 6.4 17.4

CR 0.3 0.7 0.5 1 2.3 4.5

EX 0.1 0.1 0.2 0.2 0.8 0.8

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