A 485-million-year history of Earth's surface temperature.

A long-term record of global mean surface temperature (GMST) provides critical insight into the dynamical limits of Earth's climate and the complex feedbacks between temperature and the broader Earth system. Here, we present PhanDA, a reconstruction of GMST over the past 485 million years, generated by statistically integrating proxy data with climate model simulations. PhanDA exhibits a large range of GMST, spanning 11° to 36°C. Partitioning the reconstruction into climate states indicates that more time was spent in warmer rather than colder climates and reveals consistent latitudinal temperature gradients within each state. There is a strong correlation between atmospheric carbon dioxide (CO2) concentrations and GMST, identifying CO2 as the dominant control on variations in Phanerozoic global climate and suggesting an apparent Earth system sensitivity of ~8°C.

Isotopic clumping in wood as a proxy for photorespiration in trees.

Photorespiration can limit gross primary productivity in terrestrial plants. The rate of photorespiration relative to carbon fixation increases with temperature and decreases with atmospheric [CO2]. However, the extent to which this rate varies in the environment is unclear. Here, we introduce a proxy for relative photorespiration rate based on the clumped isotopic composition of methoxyl groups (R-O-CH3) in wood. Most methoxyl C-H bonds are formed either during photorespiration or the Calvin cycle and thus their isotopic composition may be sensitive to the mixing ratio of these pathways. In water-replete growing conditions, we find that the abundance of the clumped isotopologue 13CH2D correlates with temperature (18-28 °C) and atmospheric [CO2] (280-1000 ppm), consistent with a common dependence on relative photorespiration rate. When applied to a global dataset of wood, we observe global trends of isotopic clumping with climate and water availability. Clumped isotopic compositions are similar across environments with temperatures below ~18 °C. Above ~18 °C, clumped isotopic compositions in water-limited and water-replete trees increasingly diverge. We propose that trees from hotter climates photorespire substantially more than trees from cooler climates. How increased photorespiration is managed depends on water availability: water-replete trees export more photorespiratory metabolites to lignin whereas water-limited trees either export fewer overall or direct more to other sinks that mitigate water stress. These disparate trends indicate contrasting responses of photorespiration rate (and thus gross primary productivity) to a future high-[CO2] world. This work enables reconstructing photorespiration rates in the geologic past using fossil wood.

The PhanSST global database of Phanerozoic sea surface temperature proxy data.

Paleotemperature proxy data form the cornerstone of paleoclimate research and are integral to understanding the evolution of the Earth system across the Phanerozoic Eon. Here, we present PhanSST, a database containing over 150,000 data points from five proxy systems that can be used to estimate past sea surface temperature. The geochemical data have a near-global spatial distribution and temporally span most of the Phanerozoic. Each proxy value is associated with consistent and queryable metadata fields, including information about the location, age, and taxonomy of the organism from which the data derive. To promote transparency and reproducibility, we include all available published data, regardless of interpreted preservation state or vital effects. However, we also provide expert-assigned diagenetic assessments, ecological and environmental flags, and other proxy-specific fields, which facilitate informed and responsible reuse of the database. The data are quality control checked and the foraminiferal taxonomy has been updated. PhanSST will serve as a valuable resource to the paleoclimate community and has myriad applications, including evolutionary, geochemical, diagenetic, and proxy calibration studies.

Diversification in the Rosales is influenced by dispersal, geographic range size, and pre-existing species richness.

PREMISE: Biodiversity results from origination and extinction, justifying interest in identifying traits that influence this balance. Traits implicated in the success or failure of lineages include dispersal, colonization ability, and geographic range size. We investigated the impact of dispersal and range size on contemporary diversity in the Rosales. METHODS: We used the multiple-state speciation and extinction (MuSSE) method to explore the effects on genus-level diversification of two genus-level traits (geographic range size and within-genus proclivity to speciate) and two species traits (seed dispersal and growth habit) and the multiple hidden-state speciation and extinction (MuHiSSE) method for species-level associations. Finally, we conducted a PGLS (phylogenetic least-squares) analysis to distinguish between speciation within genera versus origination of new genera. RESULTS: At the species level, animal dispersal enhances diversification rate in both woody and herbaceous lineages, while woody lineages without animal dispersal have higher extinction rates than speciation rates. At the genus level, herbaceous taxa have positive diversification rates regardless of other character states. Diversification rate variation is also explained by two interactions: (1) a three-way interaction between large geographic range, animal-mediated dispersal, and high within-genus species richness, whereby genera possessing all three traits have high diversification rates, and (2) a four-way interaction by which the three-way interaction is stronger in woody genera than in herbaceous genera. CONCLUSIONS: Colonization ability may underlie the relationship between dispersal type and range size and may influence past diversification rates by decreasing extinction rates during late Cenozoic climate volatility. Thus, colonization ability could be used to predict future extinction risk to aid conservation.

Fossil papilionoids of the Bowdichia clade (Leguminosae) from the Paleogene of North America.

PREMISE: Understanding the evolutionary history of flowering plants has been enriched by the integration of molecular phylogenies and evidence from the fossil record. Fossil fruits and leaves from the late Paleocene and Eocene of Wyoming and Eocene of Kentucky and Tennessee are described as extinct genera in the tropical American Bowdichia clade of the legume subfamily Papilionoideae. Recent phylogenetic study and taxonomic revision of the Bowdichia clade have facilitated understanding of relationships of the fossil taxa and their evolutionary implications and paleoenvironmental significance. METHODS: The fossils were studied using standard methods of specimen preparation and light microscopy and compared to fruits and leaves from extant legume taxa using herbarium collections. Phylogenetic relationships of the fossil taxa were assessed using morphology and DNA sequence data. RESULTS: Two new fossil genera are described and their phylogenetic relationships are established. Paleobowdichia lamarensis is placed as sister to the extant genus Bowdichia and Tobya claibornensis is placed with the extant genera Guianodendron and Staminodianthus. CONCLUSIONS: These fossils demonstrate that the tropical American Bowdichia clade was present in North America during a period when tropical or subtropical conditions prevailed in the northern Rocky Mountains during the late Paleocene and the Mississippi Embayment during the middle Eocene. These fossils also document that the Bowdichia clade had diversified by the late Paleocene when the fossil record of the family is relatively sparse. This result suggests that future work on early fossil legumes should focus on tropical and subtropical climatic zones, wherever they may occur latitudinally.

Extinction at the end-Cretaceous and the origin of modern Neotropical rainforests.

The end-Cretaceous event was catastrophic for terrestrial communities worldwide, yet its long-lasting effect on tropical forests remains largely unknown. We quantified plant extinction and ecological change in tropical forests resulting from the end-Cretaceous event using fossil pollen (>50,000 occurrences) and leaves (>6000 specimens) from localities in Colombia. Late Cretaceous (Maastrichtian) rainforests were characterized by an open canopy and diverse plant-insect interactions. Plant diversity declined by 45% at the Cretaceous-Paleogene boundary and did not recover for ~6 million years. Paleocene forests resembled modern Neotropical rainforests, with a closed canopy and multistratal structure dominated by angiosperms. The end-Cretaceous event triggered a long interval of low plant diversity in the Neotropics and the evolutionary assembly of today's most diverse terrestrial ecosystem.

An image dataset of cleared, x-rayed, and fossil leaves vetted to plant family for human and machine learning.

Leaves are the most abundant and visible plant organ, both in the modern world and the fossil record. Identifying foliage to the correct plant family based on leaf architecture is a fundamental botanical skill that is also critical for isolated fossil leaves, which often, especially in the Cenozoic, represent extinct genera and species from extant families. Resources focused on leaf identification are remarkably scarce; however, the situation has improved due to the recent proliferation of digitized herbarium material, live-plant identification applications, and online collections of cleared and fossil leaf images. Nevertheless, the need remains for a specialized image dataset for comparative leaf architecture. We address this gap by assembling an open-access database of 30,252 images of vouchered leaf specimens vetted to family level, primarily of angiosperms, including 26,176 images of cleared and x-rayed leaves representing 354 families and 4,076 of fossil leaves from 48 families. The images maintain original resolution, have user-friendly filenames, and are vetted using APG and modern paleobotanical standards. The cleared and x-rayed leaves include the Jack A. Wolfe and Leo J. Hickey contributions to the National Cleared Leaf Collection and a collection of high-resolution scanned x-ray negatives, housed in the Division of Paleobotany, Department of Paleobiology, Smithsonian National Museum of Natural History, Washington D.C.; and the Daniel I. Axelrod Cleared Leaf Collection, housed at the University of California Museum of Paleontology, Berkeley. The fossil images include a sampling of Late Cretaceous to Eocene paleobotanical sites from the Western Hemisphere held at numerous institutions, especially from Florissant Fossil Beds National Monument (late Eocene, Colorado), as well as several other localities from the Late Cretaceous to Eocene of the Western USA and the early Paleogene of Colombia and southern Argentina. The dataset facilitates new research and education opportunities in paleobotany, comparative leaf architecture, systematics, and machine learning.

StomataCounter: a neural network for automatic stomata identification and counting.

Stomata regulate important physiological processes in plants and are often phenotyped by researchers in diverse fields of plant biology. Currently, there are no user-friendly, fully automated methods to perform the task of identifying and counting stomata, and stomata density is generally estimated by manually counting stomata. We introduce StomataCounter, an automated stomata counting system using a deep convolutional neural network to identify stomata in a variety of different microscopic images. We use a human-in-the-loop approach to train and refine a neural network on a taxonomically diverse collection of microscopic images. Our network achieves 98.1% identification accuracy on Ginkgo scanning electron microscropy micrographs, and 94.2% transfer accuracy when tested on untrained species. To facilitate adoption of the method, we provide the method in a publicly available website at http://www.stomata.science/.

Fossil Atmospheres: a case study of citizen science in question-driven palaeontological research.

Palaeontologists increasingly use large datasets of observations collected from museum specimens to address broad-scale questions about evolution and ecology on geological timescales. One such question is whether information from fossil organisms can be used as a robust proxy for atmospheric carbon dioxide through time. Here, we present the citizen science branch of 'Fossil Atmospheres', a project designed to refine stomatal index of Ginkgo leaves as a palaeo-CO2 proxy by involving citizen scientists in data collection through the Zooniverse website. Citizen science helped to overcome a barrier presented by the time taken to count cells in Ginkgo samples; however, a new set of challenges arose as a result. A beta-testing phase with Zooniverse volunteers provided an opportunity to improve instructions to ensure high fidelity data. Exploration of citizen scientists' estimates shows that volunteer counts of stomata are accurate with respect to counts made by the project's lead scientist. However, counts of epidermal cells have a wide range, and mean values tend to underestimate expert counts. We demonstrate a variety of approaches to reducing the inaccuracy in the calculated stomatal index that this variation causes. Zooniverse serves as an ideal tool for collection of palaeontological data where the distribution of fossils would be impossible, but where specimens can be easily imaged. Such an approach facilitates the collection of a large palaeontological dataset, as well as providing an opportunity for citizens to engage with climate research.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Binary-state speciation and extinction method is conditionally robust to realistic violations of its assumptions.

BACKGROUND: Phylogenetic comparative methods allow us to test evolutionary hypotheses without the benefit of an extensive fossil record. These methods, however, make simplifying assumptions, among them that clades are always increasing or stable in diversity, an assumption we know to be false. This study simulates hypothetical clades to test whether the Binary State Speciation and Extinction (BiSSE) method can be used to correctly detect relative differences in diversification rate between ancestral and derived character states even as net diversification rates are declining overall. We simulate clades with declining but positive diversification rates, as well those in which speciation rates decline below extinction rates so that they are losing richness for part of their history. We run these analyses both with simulated symmetric and asymmetric speciation rates to test whether BiSSE can be used to detect them correctly. RESULTS: For simulations with a neutral character, the fit for a BiSSE model with a neutral character is better than alternative models so long as net diversification rates remain positive. Once net diversification rates become negative, the BiSSE model with the greatest likelihood often has a non-neutral character, even though there is no such character in the simulation. BiSSE's usefulness in detecting real asymmetry in speciation rates improves with clade age, even well after net diversification rates have become negative. CONCLUSIONS: BiSSE is most useful in analyzing clades of intermediate age, before they have reached peak diversity and gone into decline. After this point, users of BiSSE risk incorrectly inferring differential evolutionary rates when none exist. Fortunately, most studies using BiSSE and similar models focus on rapid, recent diversifications, and are less likely to encounter the biases BiSSE models are subject to for older clades. For extant groups that were once more diverse than now, however, caution should be taken in inferring past diversification patterns without fossil data.

Consequences of elevated temperature and pCO2 on insect folivory at the ecosystem level: perspectives from the fossil record.

Paleoecological studies document the net effects of atmospheric and climate change in a natural laboratory over timescales not accessible to laboratory or ecological studies. Insect feeding damage is visible on well-preserved fossil leaves, and changes in leaf damage through time can be compared to environmental changes. We measured percent leaf area damaged on four fossil leaf assemblages from the Bighorn Basin, Wyoming, that range in age from 56.1 to 52.65 million years (Ma). We also include similar published data from three US sites 49.4 to ~45 Ma in our analyses. Regional climate was subtropical or warmer throughout this period, and the second oldest assemblage (56 Ma) was deposited during the Paleocene-Eocene Thermal Maximum (PETM), a geologically abrupt global warming event caused by massive release of carbon into the atmosphere. Total and leaf-chewing damage are highest during the PETM, whether considering percent area damaged on the bulk flora, the average of individual host plants, or a single plant host that occurs at multiple sites. Another fossil assemblage in our study, the 52.65 Ma Fifteenmile Creek paleoflora, also lived during a period of globally high temperature and pCO 2, but does not have elevated herbivory. Comparison of these two sites, as well as regression analyses conducted on the entire dataset, demonstrates that, over long timescales, temperature and pCO 2 are uncorrelated with total insect consumption at the ecosystem level. Rather, the most important factor affecting herbivory is the relative abundance of plants with nitrogen-fixing symbionts. Legumes dominate the PETM site; their prevalence would have decreased nitrogen limitation across the ecosystem, buffering generalist herbivore populations against decreased leaf nutritional quality that commonly occurs at high pCO 2. We hypothesize that nitrogen concentration regulates the opposing effects of elevated temperature and CO 2 on insect abundance and thereby total insect consumption, which has important implications for agricultural practices in today's world of steadily increasing pCO 2.

Computer vision cracks the leaf code.

Understanding the extremely variable, complex shape and venation characters of angiosperm leaves is one of the most challenging problems in botany. Machine learning offers opportunities to analyze large numbers of specimens, to discover novel leaf features of angiosperm clades that may have phylogenetic significance, and to use those characters to classify unknowns. Previous computer vision approaches have primarily focused on leaf identification at the species level. It remains an open question whether learning and classification are possible among major evolutionary groups such as families and orders, which usually contain hundreds to thousands of species each and exhibit many times the foliar variation of individual species. Here, we tested whether a computer vision algorithm could use a database of 7,597 leaf images from 2,001 genera to learn features of botanical families and orders, then classify novel images. The images are of cleared leaves, specimens that are chemically bleached, then stained to reveal venation. Machine learning was used to learn a codebook of visual elements representing leaf shape and venation patterns. The resulting automated system learned to classify images into families and orders with a success rate many times greater than chance. Of direct botanical interest, the responses of diagnostic features can be visualized on leaf images as heat maps, which are likely to prompt recognition and evolutionary interpretation of a wealth of novel morphological characters. With assistance from computer vision, leaves are poised to make numerous new contributions to systematic and paleobotanical studies.

Holocene shifts in the assembly of plant and animal communities implicate human impacts.

Understanding how ecological communities are organized and how they change through time is critical to predicting the effects of climate change. Recent work documenting the co-occurrence structure of modern communities found that most significant species pairs co-occur less frequently than would be expected by chance. However, little is known about how co-occurrence structure changes through time. Here we evaluate changes in plant and animal community organization over geological time by quantifying the co-occurrence structure of 359,896 unique taxon pairs in 80 assemblages spanning the past 300 million years. Co-occurrences of most taxon pairs were statistically random, but a significant fraction were spatially aggregated or segregated. Aggregated pairs dominated from the Carboniferous period (307 million years ago) to the early Holocene epoch (11,700 years before present), when there was a pronounced shift to more segregated pairs, a trend that continues in modern assemblages. The shift began during the Holocene and coincided with increasing human population size and the spread of agriculture in North America. Before the shift, an average of 64% of significant pairs were aggregated; after the shift, the average dropped to 37%. The organization of modern and late Holocene plant and animal assemblages differs fundamentally from that of assemblages over the past 300 million years that predate the large-scale impacts of humans. Our results suggest that the rules governing the assembly of communities have recently been changed by human activity.

Reading the leaves: A comparison of leaf rank and automated areole measurement for quantifying aspects of leaf venation.

The reticulate venation that is characteristic of a dicot leaf has excited interest from systematists for more than a century, and from physiological and developmental botanists for decades. The tools of digital image acquisition and computer image analysis, however, are only now approaching the sophistication needed to quantify aspects of the venation network found in real leaves quickly, easily, accurately, and reliably enough to produce biologically meaningful data. In this paper, we examine 120 leaves distributed across vascular plants (representing 118 genera and 80 families) using two approaches: a semiquantitative scoring system called "leaf ranking," devised by the late Leo Hickey, and an automated image-analysis protocol. In the process of comparing these approaches, we review some methodological issues that arise in trying to quantify a vein network, and discuss the strengths and weaknesses of automatic data collection and human pattern recognition. We conclude that subjective leaf rank provides a relatively consistent, semiquantitative measure of areole size among other variables; that modal areole size is generally consistent across large sections of a leaf lamina; and that both approaches-semiquantitative, subjective scoring; and fully quantitative, automated measurement-have appropriate places in the study of leaf venation.

Biomechanical and leaf-climate relationships: a comparison of ferns and seed plants.

PREMISE OF THE STUDY: Relationships of leaf size and shape (physiognomy) with climate have been well characterized for woody non-monocotyledonous angiosperms (dicots), allowing the development of models for estimating paleoclimate from fossil leaves. More recently, petiole width of seed plants has been shown to scale closely with leaf mass. By measuring petiole width and leaf area in fossils, leaf mass per area (MA) can be estimated and an approximate leaf life span inferred. However, little is known about these relationships in ferns, a clade with a deep fossil record and with the potential to greatly expand the applicability of these proxies. METHODS: We measured the petiole width, MA, and leaf physiognomic characters of 179 fern species from 188 locations across six continents. We applied biomechanical models and assessed the relationship between leaf physiognomy and climate using correlational approaches. KEY RESULTS: The scaling relationship between area-normalized petiole width and MA differs between fern fronds and pinnae. The scaling relationship is best modeled as an end-loaded cantilevered beam, which is different from the best-fit biomechanical model for seed plants. Fern leaf physiognomy is not influenced by climatic conditions. CONCLUSIONS: The cantilever beam model can be applied to fossil ferns. The lack of sensitivity of leaf physiognomy to climate in ferns argues against their use to reconstruct paleoclimate. Differences in climate sensitivity and biomechanical relationships between ferns and seed plants may be driven by differences in their hydraulic conductivity and/or their differing evolutionary histories of vein architecture and leaf morphology.

Plant response to a global greenhouse event 56 million years ago.

PREMISE OF THE STUDY: The fossil record provides information about the long-term response of plants to CO2-induced climate change. The Paleocene-Eocene Thermal Maximum (PETM), a 200000-yr-long period of rapid carbon release and warming that occurred ∼56 million years ago, is analogous to future anthropogenic global warming. METHODS: We collected plant macrofossils in the Bighorn Basin, Wyoming, United States, from a period spanning the PETM and studied changes in floristic composition. We also compiled and summarized published records of floristic change during the PETM. KEY RESULTS: There was radical floristic change in the Bighorn Basin during the PETM reflecting local or regional extirpation of mesophytic plants, notably conifers, and colonization of the area by thermophilic and dry-tolerant species, especially Fabaceae. This floristic change largely reversed itself as the PETM ended, though some immigrant species persisted and some Paleocene species never returned. Less detailed records from other parts of the world show regional variation in floristic response, but are mostly consistent with the Bighorn Basin trends. CONCLUSIONS: Despite geologically rapid extirpation, colonization, and recolonization, we detected little extinction during the PETM, suggesting the rate of climate change did not exceed the dispersal capacity of terrestrial plants. Extrapolating the response of plants from the PETM to future anthropogenic climate change likely underestimates risk because rates of climate change during the PETM may have been an order of magnitude slower than current rates of change and because the abundant, widespread species common as fossils are likely resistant to extinction.

Evolution of the earliest horses driven by climate change in the Paleocene-Eocene Thermal Maximum.

Body size plays a critical role in mammalian ecology and physiology. Previous research has shown that many mammals became smaller during the Paleocene-Eocene Thermal Maximum (PETM), but the timing and magnitude of that change relative to climate change have been unclear. A high-resolution record of continental climate and equid body size change shows a directional size decrease of ~30% over the first ~130,000 years of the PETM, followed by a ~76% increase in the recovery phase of the PETM. These size changes are negatively correlated with temperature inferred from oxygen isotopes in mammal teeth and were probably driven by shifts in temperature and possibly high atmospheric CO(2) concentrations. These findings could be important for understanding mammalian evolutionary responses to future global warming.