Navigating uncertainty in maximum body size in marine metazoans.

Body size is a fundamental biological trait shaping ecological interactions, evolutionary processes, and our understanding of the structure and dynamics of marine communities on a global scale. Accurately defining a species' body size, despite the ease of measurement, poses significant challenges due to varied methodologies, tool usage, and subjectivity among researchers, resulting in multiple, often discrepant size estimates. These discrepancies, stemming from diverse measurement approaches and inherent variability, could substantially impact the reliability and precision of ecological and evolutionary studies reliant on body size data across extensive species datasets. This study examines the variation in reported maximum body sizes across 69,570 individual measurements of maximum size, ranging from <0.2 µm to >45 m, for 27,271 species of marine metazoans. The research aims to investigate how reported maximum size variations within species relate to organism size, taxonomy, habitat, and the presence of skeletal structures. The investigation particularly focuses on understanding why discrepancies in maximum size estimates arise and their potential implications for broader ecological and evolutionary studies relying on body size data. Variation in reported maximum sizes is zero for 38% of species, and low for most species, although it exceeds two orders of magnitude for some species. The likelihood of zero variation in maximum size decreased with more measurements and increased in larger species, though this varied across phyla and habitats. Pelagic organisms consistently had low maximum size range values, while small species with unspecified habitats had the highest variation. Variations in maximum size within a species were notably smaller than interspecific variation at higher taxonomic levels. Significant variation in maximum size estimates exists within marine species, and partially explained by organism size, taxonomic group, and habitat. Variation in maximum size could be reduced by standardized measurement protocols and improved meta-data. Despite the variation, egregious errors in published maximum size measurements are rare, and their impact on comparative macroecological and macroevolutionary research is likely minimal.

Reduced strength and increased variability of extinction selectivity during mass extinctions.

Two of the traits most often observed to correlate with extinction risk in marine animals are geographical range and body size. However, the relative effects of these two traits on extinction risk have not been investigated systematically for either background times or during mass extinctions. To close this knowledge gap, we measure and compare extinction selectivity of geographical range and body size of genera within five classes of benthic marine animals across the Phanerozoic using capture-mark-recapture models. During background intervals, narrow geographical range is strongly associated with greater extinction probability, whereas smaller body size is more weakly associated with greater extinction probability. During mass extinctions, the association between geographical range and extinction probability is reduced in every class and fully eliminated in some, whereas the association between body size and extinction probability varies in strength and direction across classes. While geographical range is universally the stronger predictor of survival during background intervals, variation among classes during mass extinction suggests a fundamental shift in extinction processes during these global catastrophes.

A global ecological signal of extinction risk in terrestrial vertebrates.

To determine the distribution and causes of extinction threat across functional groups of terrestrial vertebrates, we assembled an ecological trait data set for 18,016 species of terrestrial vertebrates and utilized phylogenetic comparative methods to test which categories of habitat association, mode of locomotion, and feeding mode best predicted extinction risk. We also examined the individual categories of the International Union for Conservation of Nature Red List extinction drivers (e.g., agriculture and logging) threatening each species and determined the greatest threats for each of the four terrestrial vertebrate groups. We then quantified the sum of extinction drivers threatening each species to provide a multistressor perspective on threat. Cave dwelling amphibians (p < 0.01), arboreal quadrupedal mammals (all of which are primates) (p < 0.01), aerial and scavenging birds (p < 0.01), and pedal (i.e., walking) squamates (p < 0.01) were all disproportionately threatened with extinction in comparison with the other assessed ecological traits. Across all threatened vertebrate species in the study, the most common risk factors were agriculture, threatening 4491 species, followed by logging, threatening 3187 species, and then invasive species and disease, threatening 2053 species. Species at higher risk of extinction were simultaneously at risk from a greater number of threat types. If left unabated, the disproportionate loss of species with certain functional traits and increasing anthropogenic pressures are likely to disrupt ecosystem functions globally. A shift in focus from species- to trait-centric conservation practices will allow for protection of at-risk functional diversity from regional to global scales.

Una Señal Ecológica Mundial del Riesgo de Extinción de los Vertebrados Terrestres Resumen Construimos un conjunto de datos de atributos ecológicos de 18,016 especies de vertebrados terrestres y utilizamos métodos de comparación filogenética para analizar cuáles categorías de asociación de hábitat, modo de locomoción y modo de alimentación predicen de mejor manera el riesgo de extinción. Lo anterior lo hicimos para determinar la distribución y las causas de las amenazas de extinción a lo largo de los grupos funcionales de vertebrados terrestres. También examinamos las categorías individuales de los factores de extinción (p. ej.: agricultura, tala de árboles) de la Lista Roja de la Unión Internacional para la Conservación de la Naturaleza que amenazan a cada especie y determinamos las principales amenazas para cada uno de los cuatro grupos de vertebrados terrestres. Después cuantificamos la suma de los factores de extinción que amenazan a cada especie para proporcionar una perspectiva de estresores múltiples sobre la amenaza. Los anfibios cavernícolas (p < 0.01), mamíferos arbóreos cuadrúpedos (todos son primates) (p < 0.01), aves aéreas y carroñeras (p < 0.01) y los escamados caminantes (p < 0.01) tuvieron una amenaza de extinción desproporcionada en comparación con los otros atributos ecológicos analizados. En todas las especies de vertebrados que estudiamos, los factores de riesgo más comunes fueron la agricultura, que amenaza a 4,491 especies, y la deforestación, que amenaza a 3,187 especies; le siguen las especies invasoras y las enfermedades, que juntas amenazan a 2,053 especies. Las especies con el mayor riesgo de extinción también se encontraban simultáneamente en riesgo por un mayor número de tipos de amenazas. Si esto se mantiene constante, la pérdida desproporcionada de especies con ciertos atributos funcionales y la creciente presión antropogénica probablemente alteren las funciones ecosistémicas a nivel mundial. Un cambio en el enfoque de las prácticas de conservación, de estar centradas en la especie a estar centradas en los atributos, permitirá la protección de la diversidad funcional en riesgo desde la escala regional hasta la global.

Mass extinctions alter extinction and origination dynamics with respect to body size.

Whether mass extinctions and their associated recoveries represent an intensification of background extinction and origination dynamics versus a separate macroevolutionary regime remains a central debate in evolutionary biology. The previous focus has been on extinction, but origination dynamics may be equally or more important for long-term evolutionary outcomes. The evolution of animal body size is an ideal process to test for differences in macroevolutionary regimes, as body size is easily determined, comparable across distantly related taxa and scales with organismal traits. Here, we test for shifts in selectivity between background intervals and the 'Big Five' mass extinction events using capture-mark-recapture models. Our body-size data cover 10 203 fossil marine animal genera spanning 10 Linnaean classes with occurrences ranging from Early Ordovician to Late Pleistocene (485-1 Ma). Most classes exhibit differences in both origination and extinction selectivity between background intervals and mass extinctions, with the direction of selectivity varying among classes and overall exhibiting stronger selectivity during origination after mass extinction than extinction during the mass extinction. Thus, not only do mass extinction events shift the marine biosphere into a new macroevolutionary regime, the dynamics of recovery from mass extinction also appear to play an underappreciated role in shaping the biosphere in their aftermath.

The evolution of complex life and the stabilization of the Earth system.

The half-billion-year history of animal evolution is characterized by decreasing rates of background extinction. Earth's increasing habitability for animals could result from several processes: (i) a decrease in the intensity of interactions among species that lead to extinctions; (ii) a decrease in the prevalence or intensity of geological triggers such as flood basalt eruptions and bolide impacts; (iii) a decrease in the sensitivity of animals to environmental disturbance; or (iv) an increase in the strength of stabilizing feedbacks within the climate system and biogeochemical cycles. There is no evidence that the prevalence or intensity of interactions among species or geological extinction triggers have decreased over time. There is, however, evidence from palaeontology, geochemistry and comparative physiology that animals have become more resilient to an environmental change and that the evolution of complex life has, on the whole, strengthened stabilizing feedbacks in the climate system. The differential success of certain phyla and classes appears to result, at least in part, from the anatomical solutions to the evolution of macroscopic size that were arrived at largely during Ediacaran and Cambrian time. Larger-bodied animals, enabled by increased anatomical complexity, were increasingly able to mix the marine sediment and water columns, thus promoting stability in biogeochemical cycles. In addition, body plans that also facilitated ecological differentiation have tended to be associated with lower rates of extinction. In this sense, Cambrian solutions to Cambrian problems have had a lasting impact on the trajectory of complex life and, in turn, fundamental properties of the Earth system.

Ecologically diverse clades dominate the oceans via extinction resistance.

Ecological differentiation is correlated with taxonomic diversity in many clades, and ecological divergence is often assumed to be a cause and/or consequence of high speciation rate. However, an analysis of 30,074 genera of living marine animals and 19,992 genera of fossil marine animals indicates that greater ecological differentiation in the modern oceans is actually associated with lower rates of origination over evolutionary time. Ecologically differentiated clades became taxonomically diverse over time because they were better buffered against extinction, particularly during mass extinctions, which primarily affected genus-rich, ecologically homogeneous clades. The relationship between ecological differentiation and taxonomic richness was weak early in the evolution of animals but has strengthened over geological time as successive extinction events reshaped the marine fauna.

Hierarchical complexity and the size limits of life.

Over the past 3.8 billion years, the maximum size of life has increased by approximately 18 orders of magnitude. Much of this increase is associated with two major evolutionary innovations: the evolution of eukaryotes from prokaryotic cells approximately 1.9 billion years ago (Ga), and multicellular life diversifying from unicellular ancestors approximately 0.6 Ga. However, the quantitative relationship between organismal size and structural complexity remains poorly documented. We assessed this relationship using a comprehensive dataset that includes organismal size and level of biological complexity for 11 172 extant genera. We find that the distributions of sizes within complexity levels are unimodal, whereas the aggregate distribution is multimodal. Moreover, both the mean size and the range of size occupied increases with each additional level of complexity. Increases in size range are non-symmetric: the maximum organismal size increases more than the minimum. The majority of the observed increase in organismal size over the history of life on the Earth is accounted for by two discrete jumps in complexity rather than evolutionary trends within levels of complexity. Our results provide quantitative support for an evolutionary expansion away from a minimal size constraint and suggest a fundamental rescaling of the constraints on minimal and maximal size as biological complexity increases.

Extinction intensity, selectivity and their combined macroevolutionary influence in the fossil record.

The macroevolutionary effects of extinction derive from both intensity of taxonomic losses and selectivity of losses with respect to ecology, physiology and/or higher taxonomy. Increasingly, palaeontologists are using logistic regression to quantify extinction selectivity because the selectivity metric is independent of extinction intensity and multiple predictor variables can be assessed simultaneously. We illustrate the use of logistic regression with an analysis of physiological buffering capacity and extinction risk in the Phanerozoic marine fossil record. We propose the geometric mean of extinction intensity and selectivity as a metric for the influence of extinction events. The end-Permian mass extinction had the largest influence on the physiological composition of the fauna owing to its combination of high intensity and strong selectivity. In addition to providing a quantitative measure of influence to compare among past events, this approach provides an avenue for quantifying the risk posed by the emerging biodiversity crisis that goes beyond a simple projection of taxonomic losses.

Ecological selectivity of the emerging mass extinction in the oceans.

To better predict the ecological and evolutionary effects of the emerging biodiversity crisis in the modern oceans, we compared the association between extinction threat and ecological traits in modern marine animals to associations observed during past extinction events using a database of 2497 marine vertebrate and mollusc genera. We find that extinction threat in the modern oceans is strongly associated with large body size, whereas past extinction events were either nonselective or preferentially removed smaller-bodied taxa. Pelagic animals were victimized more than benthic animals during previous mass extinctions but are not preferentially threatened in the modern ocean. The differential importance of large-bodied animals to ecosystem function portends greater future ecological disruption than that caused by similar levels of taxonomic loss in past mass extinction events.

Animal evolution. Cope's rule in the evolution of marine animals.

Cope's rule proposes that animal lineages evolve toward larger body size over time. To test this hypothesis across all marine animals, we compiled a data set of body sizes for 17,208 genera of marine animals spanning the past 542 million years. Mean biovolume across genera has increased by a factor of 150 since the Cambrian, whereas minimum biovolume has decreased by less than a factor of 10, and maximum biovolume has increased by more than a factor of 100,000. Neutral drift from a small initial value cannot explain this pattern. Instead, most of the size increase reflects differential diversification across classes, indicating that the pattern does not reflect a simple scaling-up of widespread and persistent selection for larger size within populations.

Metabolic dominance of bivalves predates brachiopod diversity decline by more than 150 million years.

Brachiopods and bivalves feed in similar ways and have occupied the same environments through geological time, but brachiopods were far more diverse and abundant in the Palaeozoic whereas bivalves dominate the post-Palaeozoic, suggesting a transition in ecological dominance 250 Ma. However, diversity and abundance data alone may not adequately describe key changes in ecosystem function, such as metabolic activity. Here, we use newly compiled body size data for 6066 genera of bivalves and brachiopods to calculate metabolic rates and revisit this question from the perspective of energy use, finding that bivalves already accounted for a larger share of metabolic activity in Palaeozoic oceans. We also find that the metabolic activity of bivalves has increased by more than two orders of magnitude over this interval, whereas brachiopod metabolic activity has declined by more than 50%. Consequently, the increase in bivalve energy metabolism must have occurred via the acquisition of new food resources rather than through the displacement of brachiopods. The canonical view of a mid-Phanerozoic transition from brachiopod to bivalve dominance results from a focus on taxonomic diversity and numerical abundance as measures of ecological importance. From a metabolic perspective, the oceans have always belonged to the clams.

Climate change and the selective signature of the Late Ordovician mass extinction.

Selectivity patterns provide insights into the causes of ancient extinction events. The Late Ordovician mass extinction was related to Gondwanan glaciation; however, it is still unclear whether elevated extinction rates were attributable to record failure, habitat loss, or climatic cooling. We examined Middle Ordovician-Early Silurian North American fossil occurrences within a spatiotemporally explicit stratigraphic framework that allowed us to quantify rock record effects on a per-taxon basis and assay the interplay of macrostratigraphic and macroecological variables in determining extinction risk. Genera that had large proportions of their observed geographic ranges affected by stratigraphic truncation or environmental shifts at the end of the Katian stage were particularly hard hit. The duration of the subsequent sampling gaps had little effect on extinction risk, suggesting that this extinction pulse cannot be entirely attributed to rock record failure; rather, it was caused, in part, by habitat loss. Extinction risk at this time was also strongly influenced by the maximum paleolatitude at which a genus had previously been sampled, a macroecological trait linked to thermal tolerance. A model trained on the relationship between 16 explanatory variables and extinction patterns during the early Katian interval substantially underestimates the extinction of exclusively tropical taxa during the late Katian interval. These results indicate that glacioeustatic sea-level fall and tropical ocean cooling played important roles in the first pulse of the Late Ordovician mass extinction in Laurentia.

Regional environmental breadth predicts geographic range and longevity in fossil marine genera.

BACKGROUND: Geographic range is a good indicator of extinction susceptibility in fossil marine species and higher taxa. The widely-recognized positive correlation between geographic range and taxonomic duration is typically attributed to either accumulating geographic range with age or an extinction buffering effect, whereby cosmopolitan taxa persist longer because they are reintroduced by dispersal from remote source populations after local extinction. The former hypothesis predicts that all taxa within a region should have equal probabilities of extinction regardless of global distributions while the latter predicts that cosmopolitan genera will have greater survivorship within a region than endemics within the same region. Here we test the assumption that all taxa within a region have equal likelihoods of extinction. METHODOLOGY/PRINCIPAL FINDINGS: We use North American and European occurrences of marine genera from the Paleobiology Database and the areal extent of marine sedimentary cover in North America to show that endemic and cosmopolitan fossil marine genera have significantly different range-duration relationships and that broad geographic range and longevity are both predicted by regional environmental breadth. Specifically, genera that occur outside of the focal region are significantly longer lived and have larger geographic ranges and environmental breadths within the focal region than do their endemic counterparts, even after controlling for differences in sampling intensity. Analyses of the number of paleoenvironmental zones occupied by endemic and cosmopolitan genera suggest that the number of paleoenvironmental zones occupied is a key factor of geographic range that promotes genus survivorship. CONCLUSIONS/SIGNIFICANCE: Wide environmental tolerances within a single region predict both broad geographic range and increased longevity in marine genera over evolutionary time. This result provides a specific driving mechanism for the spatial and temporal distributions of marine genera at regional and global scales and is consistent with the niche-breadth hypothesis operating on macroevolutionary timescales.