Unique functional diversity during early Cenozoic mammal radiation of North America.

Mammals influence nearly all aspects of energy flow and habitat structure in modern terrestrial ecosystems. However, anthropogenic effects have probably altered mammalian community structure, raising the question of how past perturbations have done so. We used functional diversity (FD) to describe how the structure of North American mammal palaeocommunities changed over the past 66 Ma, an interval spanning the radiation following the K/Pg and several subsequent environmental disruptions including the Palaeocene-Eocene Thermal Maximum (PETM), the expansion of grassland, and the onset of Pleistocene glaciation. For 264 fossil communities, we examined three aspects of ecological function: functional evenness, functional richness and functional divergence. We found that shifts in FD were associated with major ecological and environmental transitions. All three measures of FD increased immediately following the extinction of the non-avian dinosaurs, suggesting that high degrees of ecological disturbance can lead to synchronous responses both locally and continentally. Otherwise, the components of FD were decoupled and responded differently to environmental changes over the last ~56 Myr.

New uses for ancient middens: bridging ecological and evolutionary perspectives.

Rodent middens provide a fine-scale spatiotemporal record of plant and animal communities over the late Quaternary. In the Americas, middens have offered insight into biotic responses to past environmental changes and historical factors influencing the distribution and diversity of species. However, few studies have used middens to investigate genetic or ecosystem level responses. Integrating midden studies with neoecology and experimental evolution can help address these gaps and test mechanisms underlying eco-evolutionary patterns across biological and spatiotemporal scales. Fully realizing the potential of middens to answer cross-cutting ecological and evolutionary questions and inform conservation goals in the Anthropocene will require a collaborative research community to exploit existing midden archives and mount new campaigns to leverage midden records globally.

Late Pleistocene megafauna extinction leads to missing pieces of ecological space in a North American mammal community.

The conservation status of large-bodied mammals is dire. Their decline has serious consequences because they have unique ecological roles not replicated by smaller-bodied animals. Here, we use the fossil record of the megafauna extinction at the terminal Pleistocene to explore the consequences of past biodiversity loss. We characterize the isotopic and body-size niche of a mammal community in Texas before and after the event to assess the influence on the ecology and ecological interactions of surviving species (>1 kg). Preextinction, a variety of C4 grazers, C3 browsers, and mixed feeders existed, similar to modern African savannas, with likely specialization among the two sabertooth species for juvenile grazers. Postextinction, body size and isotopic niche space were lost, and the δ13C and δ15N values of some survivors shifted. We see mesocarnivore release within the Felidae: the jaguar, now an apex carnivore, moved into the specialized isotopic niche previously occupied by extinct cats. Puma, previously absent, became common and lynx shifted toward consuming more C4-based resources. Lagomorphs were the only herbivores to shift toward C4 resources. Body size changes from the Pleistocene to Holocene were species-specific, with some animals (deer, hare) becoming significantly larger and others smaller (bison, rabbits) or exhibiting no change to climate shifts or biodiversity loss. Overall, the Holocene body-size-isotopic niche was drastically reduced and considerable ecological complexity lost. We conclude biodiversity loss led to reorganization of survivors and many "missing pieces" within our community; without intervention, the loss of Earth's remaining ecosystems that support megafauna will likely suffer the same fate.

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals.

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

The road to a larger brain.

Ecological opportunities in the early Cenozoic favored larger, not smarter, mammals.

Response to Comment on "The influence of juvenile dinosaurs on community structure and diversity".

The analysis of dinosaur ecology hinges on the appropriate reconstruction and analysis of dinosaur biodiversity. Benson et al. question the data used in our analysis and our subsequent interpretation of the results. We address these concerns and show that their reanalysis is flawed. Indeed, when occurrences are filtered to include only valid taxa, their revised dataset strengthens our earlier conclusions.

A Framework for Investigating Rules of Life by Establishing Zones of Influence.

The incredible complexity of biological processes across temporal and spatial scales hampers defining common underlying mechanisms driving the patterns of life. However, recent advances in sequencing, big data analysis, machine learning, and molecular dynamics simulation have renewed the hope and urgency of finding potential hidden rules of life. There currently exists no framework to develop such synoptic investigations. Some efforts aim to identify unifying rules of life across hierarchical levels of time, space, and biological organization, but not all phenomena occur across all the levels of these hierarchies. Instead of identifying the same parameters and rules across levels, we posit that each level of a temporal and spatial scale and each level of biological organization has unique parameters and rules that may or may not predict outcomes in neighboring levels. We define this neighborhood, or the set of levels, across which a rule functions as the zone of influence. Here, we introduce the zone of influence framework and explain using three examples: (a) randomness in biology, where we use a Poisson process to describe processes from protein dynamics to DNA mutations to gene expressions, (b) island biogeography, and (c) animal coloration. The zone of influence framework may enable researchers to identify which levels are worth investigating for a particular phenomenon and reframe the narrative of searching for a unifying rule of life to the investigation of how, when, and where various rules of life operate.

The influence of juvenile dinosaurs on community structure and diversity.

Despite dominating biodiversity in the Mesozoic, dinosaurs were not speciose. Oviparity constrained even gigantic dinosaurs to less than 15 kg at birth; growth through multiple morphologies led to the consumption of different resources at each stage. Such disparity between neonates and adults could have influenced the structure and diversity of dinosaur communities. Here, we quantified this effect for 43 communities across 136 million years and seven continents. We found that megatheropods (more than 1000 kg) such as tyrannosaurs had specific effects on dinosaur community structure. Although herbivores spanned the body size range, communities with megatheropods lacked carnivores weighing 100 to 1000 kg. We demonstrate that juvenile megatheropods likely filled the mesocarnivore niche, resulting in reduced overall taxonomic diversity. The consistency of this pattern suggests that ontogenetic niche shift was an important factor in generating dinosaur community structure and diversity.

Metabolic asymmetry and the global diversity of marine predators.

Species richness of marine mammals and birds is highest in cold, temperate seas-a conspicuous exception to the general latitudinal gradient of decreasing diversity from the tropics to the poles. We compiled a comprehensive dataset for 998 species of sharks, fish, reptiles, mammals, and birds to identify and quantify inverse latitudinal gradients in diversity, and derived a theory to explain these patterns. We found that richness, phylogenetic diversity, and abundance of marine predators diverge systematically with thermoregulatory strategy and water temperature, reflecting metabolic differences between endotherms and ectotherms that drive trophic and competitive interactions. Spatial patterns of foraging support theoretical predictions, with total prey consumption by mammals increasing by a factor of 80 from the equator to the poles after controlling for productivity.

Trophic rewilding as a climate change mitigation strategy?

The loss of megafauna at the terminal Pleistocene has been linked to a wide range of Earth-system-level changes, such as altered greenhouse gas budgets, fire regimes and biome-level vegetation changes. Given these influences and feedbacks, might part of the solution for mitigating anthropogenic climate change lie in the restoration of extant megafauna to ecosystems? Here, we explore the potential role of trophic rewilding on Earth's climate system. We first provide a novel synthesis of the various ways that megafauna interact with the major drivers of anthropogenic climate change, including greenhouse gas storage and emission, aerosols and albedo. We then explore the role of rewilding as a mitigation tool at two scales: (i) current and near-future opportunities for national or regional climate change mitigation portfolios, and (ii) more radical opportunities at the global scale. Finally, we identify major knowledge gaps that complicate the complete characterization of rewilding as a climate change mitigation strategy. Our perspective is urgent since we are losing the Earth's last remaining megafauna, and with it a potential option to address climate change.This article is part of the theme issue 'Trophic rewilding: consequences for ecosystems under global change'.

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.

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.

The changing role of mammal life histories in Late Quaternary extinction vulnerability on continents and islands.

Understanding extinction drivers in a human-dominated world is necessary to preserve biodiversity. We provide an overview of Quaternary extinctions and compare mammalian extinction events on continents and islands after human arrival in system-specific prehistoric and historic contexts. We highlight the role of body size and life-history traits in these extinctions. We find a significant size-bias except for extinctions on small islands in historic times. Using phylogenetic regression and classification trees, we find that while life-history traits are poor predictors of historic extinctions, those associated with difficulty in responding quickly to perturbations, such as small litter size, are good predictors of prehistoric extinctions. Our results are consistent with the idea that prehistoric and historic extinctions form a single continuing event with the same likely primary driver, humans, but the diversity of impacts and affected faunas is much greater in historic extinctions.

The fossil record of the sixth extinction.

Comparing the magnitude of the current biodiversity crisis with those in the fossil record is difficult without an understanding of differential preservation. Integrating data from palaeontological databases with information on IUCN status, ecology and life history characteristics of contemporary mammals, we demonstrate that only a small and biased fraction of threatened species (< 9%) have a fossil record, compared with 20% of non-threatened species. We find strong taphonomic biases related to body size and geographic range. Modern species with a fossil record tend to be large and widespread and were described in the 19(th) century. The expected magnitude of the current extinction based only on species with a fossil record is about half of that of one based on all modern species; values for genera are similar. The record of ancient extinctions may be similarly biased, with many species having originated and gone extinct without leaving a tangible record.

Megafauna and ecosystem function from the Pleistocene to the Anthropocene.

Large herbivores and carnivores (the megafauna) have been in a state of decline and extinction since the Late Pleistocene, both on land and more recently in the oceans. Much has been written on the timing and causes of these declines, but only recently has scientific attention focused on the consequences of these declines for ecosystem function. Here, we review progress in our understanding of how megafauna affect ecosystem physical and trophic structure, species composition, biogeochemistry, and climate, drawing on special features of PNAS and Ecography that have been published as a result of an international workshop on this topic held in Oxford in 2014. Insights emerging from this work have consequences for our understanding of changes in biosphere function since the Late Pleistocene and of the functioning of contemporary ecosystems, as well as offering a rationale and framework for scientifically informed restoration of megafaunal function where possible and appropriate.

Exploring the influence of ancient and historic megaherbivore extirpations on the global methane budget.

Globally, large-bodied wild mammals are in peril. Because "megamammals" have a disproportionate influence on vegetation, trophic interactions, and ecosystem function, declining populations are of considerable conservation concern. However, this is not new; trophic downgrading occurred in the past, including the African rinderpest epizootic of the 1890s, the massive Great Plains bison kill-off in the 1860s, and the terminal Pleistocene extinction of megafauna. Examining the consequences of these earlier events yields insights into contemporary ecosystem function. Here, we focus on changes in methane emissions, produced as a byproduct of enteric fermentation by herbivores. Although methane is ∼ 200 times less abundant than carbon dioxide in the atmosphere, the greater efficiency of methane in trapping radiation leads to a significant role in radiative forcing of climate. Using global datasets of late Quaternary mammals, domestic livestock, and human population from the United Nations as well as literature sources, we develop a series of allometric regressions relating mammal body mass to population density and CH4 production, which allows estimation of methane production by wild and domestic herbivores for each historic or ancient time period. We find the extirpation of megaherbivores reduced global enteric emissions between 2.2-69.6 Tg CH4 y(-1) during the various time periods, representing a decrease of 0.8-34.8% of the overall inputs to tropospheric input. Our analyses suggest that large-bodied mammals have a greater influence on methane emissions than previously appreciated and, further, that changes in the source pool from herbivores can influence global biogeochemical cycles and, potentially, climate.

The importance of considering animal body mass in IPCC greenhouse inventories and the underappreciated role of wild herbivores.

Methane is an important greenhouse gas, but characterizing production by source sector has proven difficult. Current estimates suggest herbivores produce ~20% (~76-189 Tg yr(-1) ) of methane globally, with wildlife contributions uncertain. We develop a simple and accurate method to estimate methane emissions and reevaluate production by wildlife. We find a strikingly robust relationship between body mass and methane output exceeding the scaling expected by differences in metabolic rate. Our allometric model gives a significantly better fit to empirical data than IPCC Tier 1 and 2 calculations. Our analysis suggests that (i) the allometric model provides an easier and more robust estimate of methane production than IPCC models currently in use; (ii) output from wildlife is much higher than previously considered; and (iii) because of the allometric scaling of methane output with body mass, national emissions could be reduced if countries favored more, smaller livestock, over fewer, larger ones.

Response to Comments on "Evidence for mesothermy in dinosaurs".

D'Emic and Myhrvold raise a number of statistical and methodological issues with our recent analysis of dinosaur growth and energetics. However, their critiques and suggested improvements lack biological and statistical justification.

Dinosaur physiology. Evidence for mesothermy in dinosaurs.

Were dinosaurs ectotherms or fast-metabolizing endotherms whose activities were unconstrained by temperature? To date, some of the strongest evidence for endothermy comes from the rapid growth rates derived from the analysis of fossil bones. However, these studies are constrained by a lack of comparative data and an appropriate energetic framework. Here we compile data on ontogenetic growth for extant and fossil vertebrates, including all major dinosaur clades. Using a metabolic scaling approach, we find that growth and metabolic rates follow theoretical predictions across clades, although some groups deviate. Moreover, when the effects of size and temperature are considered, dinosaur metabolic rates were intermediate to those of endotherms and ectotherms and closest to those of extant mesotherms. Our results suggest that the modern dichotomy of endothermic versus ectothermic is overly simplistic.

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing.

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.