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.

Phanerozoic co-evolution of O2-CO2 and ocean habitability.

This perspective reviews how atmospheric compositions, animals and marine algae evolved together to determine global ocean habitability during the past 500 million years.

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.

Reduction in animal abundance and oxygen availability during and after the end-Triassic mass extinction.

The end-Triassic biodiversity crisis was one of the most severe mass extinctions in the history of animal life. However, the extent to which the loss of taxonomic diversity was coupled with a reduction in organismal abundance remains to be quantified. Further, the temporal relationship between organismal abundance and local marine redox conditions is lacking in carbonate sections. To address these questions, we measured skeletal grain abundance in shallow-marine limestones by point counting 293 thin sections from four stratigraphic sections across the Triassic/Jurassic boundary in the Lombardy Basin and Apennine Platform of western Tethys. Skeletal abundance decreased abruptly across the Triassic/Jurassic boundary in all stratigraphic sections. The abundance of skeletal organisms remained low throughout the lower-middle Hettangian strata and began to rebound during the late Hettangian and early Sinemurian. A two-way ANOVA indicates that sample age (p < .01, η2  = 0.30) explains more of the variation in skeletal abundance than the depositional environment or paleobathymetry (p < .01, η2  = 0.15). Measured I/Ca ratios, a proxy for local shallow-marine redox conditions, show this same pattern with the lowest I/Ca ratios occurring in the early Hettangian. The close correspondence between oceanic water column oxygen levels and skeletal abundance indicates a connection between redox conditions and benthic organismal abundance across the Triassic/Jurassic boundary. These findings indicate that the end-Triassic mass extinction reduced not only the biodiversity but also the carrying capacity for skeletal organisms in early Hettangian ecosystems, adding to evidence that mass extinction of species generally leads to mass rarity among survivors.

Breathless through Time: Oxygen and Animals across Earth's History.

AbstractOxygen levels in the atmosphere and ocean have changed dramatically over Earth history, with major impacts on marine life. Because the early part of Earth's history lacked both atmospheric oxygen and animals, a persistent co-evolutionary narrative has developed linking oxygen change with changes in animal diversity. Although it was long believed that oxygen rose to essentially modern levels around the Cambrian period, a more muted increase is now believed likely. Thus, if oxygen increase facilitated the Cambrian explosion, it did so by crossing critical ecological thresholds at low O2. Atmospheric oxygen likely remained at low or moderate levels through the early Paleozoic era, and this likely contributed to high metazoan extinction rates until oxygen finally rose to modern levels in the later Paleozoic. After this point, ocean deoxygenation (and marine mass extinctions) is increasingly linked to large igneous province eruptions-massive volcanic carbon inputs to the Earth system that caused global warming, ocean acidification, and oxygen loss. Although the timescales of these ancient events limit their utility as exact analogs for modern anthropogenic global change, the clear message from the geologic record is that large and rapid CO2 injections into the Earth system consistently cause the same deadly trio of stressors that are observed today. The next frontier in understanding the impact of oxygen changes (or, more broadly, temperature-dependent hypoxia) in deep time requires approaches from ecophysiology that will help conservation biologists better calibrate the response of the biosphere at large taxonomic, spatial, and temporal scales.

Impact of warming on aquatic body sizes explained by metabolic scaling from microbes to macrofauna.

Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O2) changes based on thermal and geometric constraints on organismal O2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the "temperature-size rule" [TSR]). First, the interspecific mean and variability of the TSR is predicted from species' temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern-its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O2 demand declines while its benefit to O2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs.

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.

Ecological Filtering and Exaptation in the Evolution of Marine Snakes.

AbstractConvergent evolution is often attributed to adaptation of form to function, but it can also result from ecological filtering, exaptation, or nonaptation. Testing among these possibilities is critical to understanding how and why morphological similarities emerge independently in multiple lineages. To address this challenge, we combined multiple preexisting phylogenetic methods to jointly estimate the habitats and morphologies of lineages within a phylogeny. We applied this approach to the invasions of snakes into the marine realm. We utilized a data set for 1,243 extant snake species consisting of newly compiled biome occupancy information and preexisting data on reproductive strategy, body mass, and environmental temperature and elevation. We find evidence for marine clades arising from a variety of aquatic and terrestrial habitats. Furthermore, there is strong evidence of ecological filtering for nonmarine ancestors that were already viviparous, had slightly larger-than-average body sizes, and lived in environments with higher-than-average temperatures and lower-than-average elevations. In aggregate, similarities among independent lineages of marine snakes result from a combination of exaptation and strong ecological filtering. Strong barriers to entry of new habitats appear to be more important than common adaptations following invasions for producing similarities among independent lineages invading a shared, novel habitat.

Lepidoptera demonstrate the relevance of Murray's Law to circulatory systems with tidal flow.

BACKGROUND: Murray's Law, which describes the branching architecture of bifurcating tubes, predicts the morphology of vessels in many amniotes and plants. Here, we use insects to explore the universality of Murray's Law and to evaluate its predictive power for the wing venation of Lepidoptera, one of the most diverse insect orders. Lepidoptera are particularly relevant to the universality of Murray's Law because their wing veins have tidal, or oscillatory, flow of air and hemolymph. We examined over one thousand wings representing 667 species of Lepidoptera. RESULTS: We found that veins with a diameter above approximately 50 microns conform to Murray's Law, with veins below 50 microns in diameter becoming less and less likely to conform to Murray's Law as they narrow. The minute veins that are most likely to deviate from Murray's Law are also the most likely to have atrophied, which prevents efficient fluid transport regardless of branching architecture. However, the veins of many taxa continue to branch distally to the areas where they atrophied, and these too conform to Murray's Law at larger diameters (e.g., Sesiidae). CONCLUSIONS: This finding suggests that conformity to Murray's Law in larger taxa may reflect requirements for structural support as much as fluid transport, or may indicate that selective pressures for fluid transport are stronger during the pupal stage-during wing development prior to vein atrophy-than the adult stage. Our results increase the taxonomic scope of Murray's Law and provide greater clarity about the relevance of body size.

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.

Physiological constraints on body size distributions in Crocodyliformes.

At least 26 species of crocodylian populate the globe today, but this richness represents a minute fraction of the diversity and disparity of Crocodyliformes. Fossil forms are far more varied, spanning from erect, fully terrestrial species to flippered, fully marine species. To quantify the influence of a marine habitat on the directionality, rate, and variance of evolution of body size in Crocodyliformes and thereby identify underlying selective pressures, we compiled a database of body sizes for 264 fossil and modern species of crocodyliform covering terrestrial, semi-aquatic, and marine habitats. We find increases in body size coupled with increases in strength of selection and decreases in variance following invasions of marine habitats but not of semiaquatic habitats. A model combining constraints from thermoregulation and lung capacity provides a physiological explanation for the larger minimum and average sizes of marine species. It appears that constraints on maximum size are shared across Crocodyliformes, perhaps through factors such as the allometric scaling of feeding rate versus basal metabolism with body size. These findings suggest that broad-scale patterns of body size evolution and the shapes of body size distributions within higher taxa are often determined more by physiological constraints than by ecological interactions or environmental fluctuations.

A Cretaceous peak in family-level insect diversity estimated with mark-recapture methodology.

The history of insects' taxonomic diversity is poorly understood. The two most common methods for estimating taxonomic diversity in deep time yield conflicting results: the 'range through' method suggests a steady, nearly monotonic increase in family-level diversity, whereas 'shareholder quorum subsampling' suggests a highly volatile taxonomic history with family-level mass extinctions occurring repeatedly, even at the midpoints of geological periods. The only feature shared by these two diversity curves is a steep increase in standing diversity during the Early Cretaceous. This apparent diversification event occurs primarily during the Aptian, the pre-Cenozoic interval with the most described insect occurrences, raising the possibility that this feature of the diversity curves reflects preservation and sampling biases rather than insect evolution and extinction. Here, the capture-mark-recapture (CMR) approach is used to estimate insects' family-level diversity. This method accounts for the incompleteness of the insect fossil record as well as uneven sampling among time intervals. The CMR diversity curve shows extinctions at the Permian/Triassic and Cretaceous/Palaeogene boundaries but does not contain any mass extinctions within geological periods. This curve also includes a steep increase in diversity during the Aptian, which appears not to be an artefact of sampling or preservation bias because this increase still appears when time bins are standardized by the number of occurrences they contain rather than by the amount of time that they span. The Early Cretaceous increase in family-level diversity predates the rise of angiosperms by many millions of years and can be better attributed to the diversification of parasitic and especially parasitoid insect lineages.

Greater vulnerability to warming of marine versus terrestrial ectotherms.

Understanding which species and ecosystems will be most severely affected by warming as climate change advances is important for guiding conservation and management. Both marine and terrestrial fauna have been affected by warming1,2 but an explicit comparison of physiological sensitivity between the marine and terrestrial realms has been lacking. Assessing how close populations live to their upper thermal limits has been challenging, in part because extreme temperatures frequently drive demographic responses3,4 and yet fauna can use local thermal refugia to avoid extremes5-7. Here we show that marine ectotherms experience hourly body temperatures that are closer to their upper thermal limits than do terrestrial ectotherms across all latitudes-but that this is the case only if terrestrial species can access thermal refugia. Although not a direct prediction of population decline, this thermal safety margin provides an index of the physiological stress caused by warming. On land, the smallest thermal safety margins were found for species at mid-latitudes where the hottest hourly body temperatures occurred; by contrast, the marine species with the smallest thermal safety margins were found near the equator. We also found that local extirpations related to warming have been twice as common in the ocean as on land, which is consistent with the smaller thermal safety margins at sea. Our results suggest that different processes will exacerbate thermal vulnerability across these two realms. Higher sensitivities to warming and faster rates of colonization in the marine realm suggest that extirpations will be more frequent and species turnover faster in the ocean. By contrast, terrestrial species appear to be more vulnerable to loss of access to thermal refugia, which would make habitat fragmentation and changes in land use critical drivers of species loss on land.

Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction.

Rapid climate change at the end of the Permian Period (~252 million years ago) is the hypothesized trigger for the largest mass extinction in Earth's history. We present model simulations of the Permian/Triassic climate transition that reproduce the ocean warming and oxygen (O2) loss indicated by the geologic record. The effect of these changes on animal survival is evaluated using the Metabolic Index (Φ), a measure of scope for aerobic activity governed by organismal traits sampled in diverse modern species. Modeled loss of aerobic habitat predicts lower extinction intensity in the tropics, a pattern confirmed with a spatially explicit analysis of the marine fossil record. The combined physiological stresses of ocean warming and O2 loss can account for more than half the magnitude of the "Great Dying."

Body size downgrading of mammals over the late Quaternary.

Since the late Pleistocene, large-bodied mammals have been extirpated from much of Earth. Although all habitable continents once harbored giant mammals, the few remaining species are largely confined to Africa. This decline is coincident with the global expansion of hominins over the late Quaternary. Here, we quantify mammalian extinction selectivity, continental body size distributions, and taxonomic diversity over five time periods spanning the past 125,000 years and stretching approximately 200 years into the future. We demonstrate that size-selective extinction was already under way in the oldest interval and occurred on all continents, within all trophic modes, and across all time intervals. Moreover, the degree of selectivity was unprecedented in 65 million years of mammalian evolution. The distinctive selectivity signature implicates hominin activity as a primary driver of taxonomic losses and ecosystem homogenization. Because megafauna have a disproportionate influence on ecosystem structure and function, past and present body size downgrading is reshaping Earth's biosphere.

Energetic tradeoffs control the size distribution of aquatic mammals.

Four extant lineages of mammals have invaded and diversified in the water: Sirenia, Cetacea, Pinnipedia, and Lutrinae. Most of these aquatic clades are larger bodied, on average, than their closest land-dwelling relatives, but the extent to which potential ecological, biomechanical, and physiological controls contributed to this pattern remains untested quantitatively. Here, we use previously published data on the body masses of 3,859 living and 2,999 fossil mammal species to examine the evolutionary trajectories of body size in aquatic mammals through both comparative phylogenetic analysis and examination of the fossil record. Both methods indicate that the evolution of an aquatic lifestyle is driving three of the four extant aquatic mammal clades toward a size attractor at ∼500 kg. The existence of this body size attractor and the relatively rapid selection toward, and limited deviation from, this attractor rule out most hypothesized drivers of size increase. These three independent body size increases and a shared aquatic optimum size are consistent with control by differences in the scaling of energetic intake and cost functions with body size between the terrestrial and aquatic realms. Under this energetic model, thermoregulatory costs constrain minimum size, whereas limitations on feeding efficiency constrain maximum size. The optimum size occurs at an intermediate value where thermoregulatory costs are low but feeding efficiency remains high. Rather than being released from size pressures, water-dwelling mammals are driven and confined to larger body sizes by the strict energetic demands of the aquatic medium.

Phanerozoic pO2 and the early evolution of terrestrial animals.

Concurrent gaps in the Late Devonian/Mississippian fossil records of insects and tetrapods (i.e. Romer's Gap) have been attributed to physiological suppression by low atmospheric pO2 Here, updated stable isotope inputs inform a reconstruction of Phanerozoic oxygen levels that contradicts the low oxygen hypothesis (and contradicts the purported role of oxygen in the evolution of gigantic insects during the late Palaeozoic), but reconciles isotope-based calculations with other proxies, like charcoal. Furthermore, statistical analysis demonstrates that the gap between the first Devonian insect and earliest diverse insect assemblages of the Pennsylvanian (Bashkirian Stage) requires no special explanation if insects were neither diverse nor abundant prior to the evolution of wings. Rather than tracking physiological constraint, the fossil record may accurately record the transformative evolutionary impact of insect flight.

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.