Dietary options and behavior suggested by plant biomarker evidence in an early human habitat

The availability of plants and freshwater shapes the diets and social behavior of chimpanzees, our closest living relative. However, limited evidence about the spatial relationships shared between ancestral human (hominin) remains, edible resources, refuge, and freshwater leaves the influence of local resources on our species’ evolution open to debate. Exceptionally well-preserved organic geochemical fossils—biomarkers—preserved in a soil horizon resolve different plant communities at meter scales across a contiguous 25,000 m² archaeological land surface at Olduvai Gorge from about 2 Ma. Biomarkers reveal hominins had access to aquatic plants and protective woods in a patchwork landscape, which included a spring-fed wetland near a woodland that both were surrounded by open grassland. Numerous cut-marked animal bones are located within the wooded area, and within meters of wetland vegetation delineated by biomarkers for ferns and sedges. Taken together, plant biomarkers, clustered bone debris, and hominin remains define a clear spatial pattern that places animal butchery amid the refuge of an isolated forest patch and near freshwater with diverse edible resources.Spatial patterns in archaeological remains provide a glimpse into the lives of our ancestors (1–5). Although many early hominin environments are interpreted as grassy or open woodlands (6–8), fossil bones and plant remains are rarely preserved together in the same settings. As a result, associated landscape reconstructions commonly lack coexisting fossil evidence for hominins and local-scale habitat (microhabitat) that defined the distribution of plant foods, refuge, and water (7). This problem is exacerbated by the discontinuous nature and low time resolution often available across ancient soil (paleosol) horizons, including hominin archaeological localities. One notable exception is well-time-correlated 1.8-million-y-old paleosol horizons exposed at Olduvai Gorge. Associated horizons contain exceptionally preserved plant biomarkers along with many artifacts and fossilized bones. Plant biomarkers, which previously revealed temporal patterns in vegetation and water (8), are well preserved in the paleosol horizon and document plant-type spatial distributions that provide an ecosystem context (9, 10) for resources that likely affected the diets and behavior of hominin inhabitants.Plant biomarkers are delivered by litter to soils and can distinguish plant functional type differences in standing biomass over scales of 1–1,000 m² (11). Trees, grasses, and other terrestrial plants produce leaf waxes that include long-chain n-alkanes such as hentriacontane (nC₃₁), whereas aquatic plants and phytoplankton produce midchain homologs (e.g., nC₂₃) (12, 13). The ratio of shorter- versus long-chain n-alkane abundances distinguish relative organic matter inputs from aquatic versus terrestrial plants to sediments (13):P_aq = (nC₂₃ + nC₂₅)/(nC₂₃ + nC₂₅ + nC₂₉ + nC₃₁).Sedges and ferns are prolific in many tropical ecosystems (14). These plants both have variable and therefore nondiagnostic n-alkane profiles. However, sedges produce distinctive phenolic compounds [e.g., 5-n-tricosylresorcinol (ⁿR₂₃)] and ferns produce distinctive midchain diols [e.g., 1,13-dotriacontanediol (C₃₂-diol)] (SI Discussion).Lignin monomers provide evidence for woody and nonwoody plants. This refractory biopolymer occurs in both leaves and wood, serves as a structural tissue, and accounts for up to half of the total organic carbon in modern vegetation (11). Lignin is composed of three phenolic monomer types that show distinctive distributions in woody and herbaceous plant tissues. Woody tissues from dicotyledonous trees and shrubs contain syringyl (S) and vanillyl (V) phenols (12), whereas cinnamyl (C) phenols are exclusively found in herbaceous tissues (12). The relative abundance of C versus V phenols (C/V) is widely used to distinguish between woody and herbaceous inputs to sedimentary and soil organic matter (15).Plant biomarker ¹³C/¹²C ratios (expressed as δ¹³C values) are sensitive indicators of community composition, ecosystem structure, and climate conditions (8). Most woody plants and forbs in eastern Africa use C₃ photosynthesis (6), whereas arid-adapted grasses use C₄ photosynthesis (8, 14). These two pathways discriminate differently against ¹³C during photosynthesis, resulting in characteristic δ¹³C values for leaf waxes derived from C₃ (about –36.0‰) and C₄ (–21.0‰) plants (16). Carbon isotopic abundances of phenolic monomers of lignin amplify the C₃–C₄ difference and range between ca. –34.0‰ (C₃) and –14.0‰ (C₄) in tropical ecosystems (15). Terrestrial C₃ plant δ¹³C values decrease with increased exposure to water, respired CO₂, and shade (8), with lowest values observed in moist regions with dense canopy (17). Although concentration and δ¹³C values of atmospheric CO₂ can affect C₃ plant δ¹³C values (17), this influence is not relevant to our work here, which focuses on a single time window (SI Discussion). The large differences in leaf-wax δ¹³C values between closed C₃ forest to open C₄ grassland are consistent with soil organic carbon isotope gradients across canopy-shaded ground surfaces (6) and serve as a quantitative proxy for woody cover (f_woody) in savannas (8).As is observed for nonhuman primates, hominin dietary choices were likely shaped by ecosystem characteristics over habitat scales of 1–1,000 m² (3–5). To evaluate plant distributions at this small spatial scale (9), we excavated 71 paleosol samples from close-correlated trenches across a ∼25,000-m² area that included FLK Zinjanthropus Level 22 (FLK Zinj) at Olduvai Gorge (Fig. 1). Recent excavations (18–21) at multiple trenches at four sites (FLK^NN, FLK^N, FLK, and FLK^S, Fig. 1D) exposed a traceable thin (5–50 cm), waxy green to olive-brown clay horizon developed by pedogenic alterations of playa lake margin alluvium (22). Weak stratification and irregular redox stains suggest initial soil development occurred during playa lake regression (18, 22), around 1.848 Ma (ref. 23 and SI Discussion). To date, craniodental remains from at least three hominin individuals (18–20), including preadolescent early Homo and Paranthropus boisei, were recovered from FLK Zinj. Fossils and artifacts embedded in the paleosol horizon often protrude into an overlying airfall tuff (18, 19), which suggests fossil remains were catastrophically buried in situ under volcanic ash. Rapid burial likely fostered the exceptional preservation of both macrofossils (10) and plant biomarkers across the FLK Zinj land surface.Open in a separate windowFig. 1.Location and map of FLK Zinj paleosol excavations. (A and B) Location of FLK Zinj as referenced to reconstructed depositional environments at Olduvai Gorge during the early Pleistocene (18, 22) and the modern gorge walls. The perennial lake contained shallow saline–alkaline waters that frequently flooded the surrounding playa margin (i.e., floodplain) flats. (C) Outline of FLK Zinj paleosol excavation sites used for our spatial biomarker reconstructions. (D) Concentric (5 m) gridded distribution map of FLK Zinj paleosol excavations relative to previous archaeological trenches (18–21). Major aggregate complexes (FLK^NN, FLK^N, FLK, and FLK^S) are color-coded to show excavation-site associations.Plant biomarker signatures reveal distinct types of vegetation juxtaposed across the FLK Zinj land surface (Figs. 2–4 and Fig. S1). In the northwest, FLK^NN trenches show high nC₂₃ δ¹³C values (Fig. 2B) as well as high C/V and P_aq values (Figs. 3 and ​and4A).4A). They indicate floating or submerged aquatic plants (macrophytes) in standing freshwater (13), a finding that is consistent with nearby low-temperature freshwater carbonates (tufa), interpreted to be deposited from spring waters (22). Adjacent FLK^N trenches have lower P_aq values (Fig. 4A) with occurrences of fern-derived C₃₂-diol and sedge-derived ⁿR₂₃ (Fig. 2 C and D). These biomarker distributions indicate an abrupt (around 10 m) transition from aquatic to wetland vegetation. Less than 100 m away (Fig. 1C), low nC₃₁ δ¹³C values (Fig. 2A) and low C/V and very low P_aq values (Figs. 3 and ​and4A)4A) collectively indicate dense woody cover (Fig. 4B). In the farthest southeastern (FLK^S) trenches, high C/V values and high δ¹³C values for C lignin phenols (Fig. 3) indicate open C₄ grassland.Open in a separate windowFig. 2.Spatial distributions and δ¹³C values for plant biomarkers across FLK Zinj. Measured and modeled δ¹³C values (large and smaller circles, respectively) are shown for (A) nC₃₁ from terrestrial plants, (B) nC₂₃ from (semi)aquatic plants, (C) C₃₂-diol from ferns, and (D) ⁿR₂₃ from sedges (see refs. 12 and 13 and SI Discussion). Modeled values [inverse distance-weighted (9)] account for spatial autocorrelation (15-m radius) in standing biomass (35) over scales of soil organic matter accumulation (11). Black dots represent paleosols with insufficient plant biomarker concentrations for isotopic analysis.Open in a separate windowFig. 3.Molecular and isotopic signatures for lignin phenols across FLK Zinj. Bivariate plots are shown for diagnostic lignin compositional parameters (see refs. 12 and 15 and Fig. 1C). Symbols are colored according to respective δ¹³C values for the C lignin phenol, p-coumaric acid. FLK symbols are uncolored due to insufficient p-coumaric acid concentrations for isotopic analysis. Representative lignin compositional parameters (12, 15) are shown for monocotyledonous herbaceous tissues (G), dicotyledonous herbaceous tissues (H), cryptogams (N), and dicotyledonous woody tissues (W).Open in a separate windowFig. 4.Spatial relationships shared between local plant resources and hominin remains. Measured and modeled values (large and smaller circles, respectively) are shown for (A) P_aq (13) and (B) f_woody (8). Modeled values [inverse distance-weighted (9)] account for spatial autocorrelation (15-m radius) in standing biomass (35) over scales of soil organic matter accumulation (11). (C) Kernel density map of cut-marked bones (18–21) across the FLK Zinj land surface (Fig. S4). High estimator values indicate hotspots of hominin butchery (Fig. S5). A shaded rectangle captures the area (ca. 0.68 probability mass) with highest cut-marked bone densities and is shown in A and B for reference.Open in a separate windowFig. S1.Total ion chromatograms for saturated hydrocarbons in representative paleosols at (A) FLK^NN, (B) FLK^N, (C) FLK, and (D) FLK^S. C₂₃, tricosane; C₂₅, pentacosane; C₂₉ nonacosane; C₃₁, hentriacontane.Biomarkers define a heterogeneous landscape at Olduvai and suggest an influence of local resources on hominin diets and behavior. It is recognized (2, 24–26) that early Homo species and P. boisei had similar physiological characteristics. These similarities in physical attributes suggest behavioral differences were what allowed for overlapping ranges and local coexistence (sympatry) of both hominins. For instance, differences in seasonal subsistence strategies or different behavior during periods of drought and limited food could have reduced local hominin competition and fostered diversification via niche specialization (27–29).Physical and isotopic properties of fossil teeth indicate P. boisei was more water-dependent [low enamel δ¹⁸O values (24)] and consumed larger quantities of abrasive, ¹³C-enriched foodstuffs [flat-worn surfaces (25) and high enamel δ¹³C values (26)] than coexisting early Homo species. Although ¹³C-enriched enamel is commonly attributed to consumption of C₄ grasses or meat from grazers (14), this was not likely, because P. boisei craniodental features are inconsistent with contemporary gramnivores (24, 25) or extensive uncooked flesh mastication (26). Numerous scholars have proposed the nutritious underground storage organs (USOs) of C₄ sedges were a staple of hominin diets (14, 24, 26, 27). Consistent with this suggestion, occurrences of ⁿR₂₃ attest to the presence of sedges at FLK^NN and FLK^N (Fig. 2D). However, the low δ¹³C values measured for ⁿR₂₃ at these same sites (Fig. 2D and Fig. S2) indicate C₃ photosynthesis (12, 16), a trait common in modern sedges that grow in alkaline wetlands and lakes (30) (Fig. S3). Thus, biomarker signatures support the presence of C₃ sedges in the wetland area of FLK Zinj.Open in a separate windowFig. S2.Total ion chromatogram [TIC (A)] and selected ion chromatograms for derivatized 5-n-alkylresorcinols [m/z 268 (●)] and midchain diols [m/z 369 (○)] from a representative paleosol at FLK^N. Also shown are δ¹³C values for homologous (B) 5-n-alkylresorcinols and (C) midchain diols. C₃₂-diol, dotriacontanediol; ⁿR₂₃, tricosylresorcinol.Open in a separate windowFig. S3.Summary phyogenetic consensus tree of Cyperaceae (sedges) based on nucleotide (rcbL and ETS1f) sequence data (50–54, 95, 96). Important taxonomic distinctions discussed in SI Discussion, Fern Alkyldiols are shown explicitly. Triangle-enclosed digits represent the number of additional branches at different levels of taxonomic classification. CEFA, Cypereae Eleocharideae Fuireneae Abildgaardieae; CSD, Cariceae Scirpeae Dulichieae.Alternative foodstuffs with abrasive, ¹³C-enriched biomass include seedless vascular plants (cryptogams), such as ferns and lycophytes [e.g., quillworts (27, 30)]. Ferns are widely distributed throughout eastern Africa in moist and shaded microhabitats (31) and are often found near dependable sources of drinking water (32). Today, ferns serve as a dietary resource for humans and nonhuman primates alike (27), and fiddlehead consumption is consistent with the inferred digestive physiology [salivary proteins (33)] and the microwear on molars (34) of P. boisei in eastern Africa (25, 26). Ferns were present at FLK^N, based on measurements of C₃₂-diol (Fig. 2D). Further, the high δ¹³C values measured for these compounds are consistent with significant fern consumption by P. boisei at Olduvai Gorge.Ferns and grasses were not the only plant foods present during the time window documented by FLK Zinj. Further, the exclusive reliance on a couple of dietary resources was improbable for P. boisei, because its fossils occur in diverse localities (24–26). Aquatic plants are an additional candidate substrate, as evidenced by high P_aq values at FLK^NN and FLK^N (Fig. 4A). Floating and submerged plants proliferate in wetlands throughout eastern Africa today (13, 14), and many produce nutritious leaves and rootstock all year long (27, 28). Although C₄ photosynthesis is rare among modern macrophytes (30), they can assimilate bicarbonate under alkaline conditions, which results in C₄-like isotope signatures in their biomass (30). Their leaf waxes, such as nC₂₃ (13), are both present and carry ¹³C-enriched signatures at FLK^NN and FLK^N (Fig. 2B). It is also likely that aquatic macrophytes sustained invertebrates and fish with comparably ¹³C-enriched biomass, as they do in modern systems (14), and we suggest aquatic animal foods could have been important in P. boisei diets (27, 28).Biomarkers across the FLK Zinj soil horizon resolve clear patterns in the distribution of plants and water and suggest critical resources that shaped hominin existence at Olduvai Gorge. The behavioral implications of local conditions require understanding of regional climate and biogeography (3–5, 7), because hominin species likely had home ranges much larger than the extent of excavated sites at FLK Zinj. Lake sediments at Olduvai Gorge include numerous stacked tuffs with precise radiometric age constraints (23). These tephrostratigraphic correlations (21) tie the FLK Zinj landscape horizon to published records of plant biomarkers in lake sediments that record climate cycles and catchment-scale variations in ecology. Correlative lake sediment data indicate the wet and wooded microhabitats of FLK Zinj sat within a catchment dominated by arid C₄ grassland (8). Under similarly arid conditions today, only a small fraction of landscape area (ca. 0.05) occurs within 5 km of either forest or standing freshwater (35). Given a paucity of shaded refuge and potable water in the catchment, the concentration of hominin butchery debris (18–21) exclusively within the forest microhabitat and adjacent to a freshwater wetland (Fig. 4) is notable. We suggest the spatial patterns defined by both macro- and molecular fossils reflect hominins engaged in social transport of resources (1–5), such as bringing animal carcasses and freshwater-sourced foods from surrounding grassy or wetland habitats to a wooded patch that provided both physical protection and access to water.     

Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group

Since Darwin, biologists have been struck by the extraordinary diversity of teleost fishes, particularly in contrast to their closest “living fossil” holostean relatives. Hypothesized drivers of teleost success include innovations in jaw mechanics, reproductive biology and, particularly at present, genomic architecture, yet all scenarios presuppose enhanced phenotypic diversification in teleosts. We test this key assumption by quantifying evolutionary rate and capacity for innovation in size and shape for the first 160 million y (Permian–Early Cretaceous) of evolution in neopterygian fishes (the more extensive clade containing teleosts and holosteans). We find that early teleosts do not show enhanced phenotypic evolution relative to holosteans. Instead, holostean rates and innovation often match or can even exceed those of stem-, crown-, and total-group teleosts, belying the living fossil reputation of their extant representatives. In addition, we find some evidence for heterogeneity within the teleost lineage. Although stem teleosts excel at discovering new body shapes, early crown-group taxa commonly display higher rates of shape evolution. However, the latter reflects low rates of shape evolution in stem teleosts relative to all other neopterygian taxa, rather than an exceptional feature of early crown teleosts. These results complement those emerging from studies of both extant teleosts as a whole and their sublineages, which generally fail to detect an association between genome duplication and significant shifts in rates of lineage diversification.Numbering ∼29,000 species, teleost fishes account for half of modern vertebrate richness. In contrast, their holostean sister group, consisting of gars and the bowfin, represents a mere eight species restricted to the freshwaters of eastern North America (1). This stark contrast between teleosts and Darwin''s original “living fossils” (2) provides the basis for assertions of teleost evolutionary superiority that are central to textbook scenarios (3, 4). Classic explanations for teleost success include key innovations in feeding (3, 5) (e.g., protrusible jaws and pharyngeal jaws) and reproduction (6, 7). More recent work implicates the duplicate genomes of teleosts (8–10) as the driver of their prolific phenotypic diversification (8, 11–13), concordant with the more general hypothesis that increased morphological complexity and innovation is an expected consequence of genome duplication (14, 15).Most arguments for enhanced phenotypic evolution in teleosts have been asserted rather than demonstrated (8, 11, 12, 15, 16; but see ref. 17), and draw heavily on the snapshot of taxonomic and phenotypic imbalance apparent between living holosteans and teleosts. The fossil record challenges this neontological narrative by revealing the remarkable taxonomic richness and morphological diversity of extinct holosteans (Fig. 1) (18, 19) and highlights geological intervals when holostean taxonomic richness exceeded that of teleosts (20). This paleontological view has an extensive pedigree. Darwin (2) invoked a long interval of cryptic teleost evolution preceding the late Mesozoic diversification of the modern radiation, a view subsequently supported by the implicit (18) or explicit (19) association of Triassic–Jurassic species previously recognized as “holostean ganoids” with the base of teleost phylogeny. This perspective became enshrined in mid-20th century treatments of actinopterygian evolution, which recognized an early-mid Mesozoic phase dominated by holosteans sensu lato and a later interval, extending to the modern day, dominated by teleosts (4, 20, 21). Contemporary paleontological accounts echo the classic interpretation of modest teleost origins (22–24), despite a systematic framework that substantially revises the classifications upon which older scenarios were based (22–25). Identification of explosive lineage diversification in nested teleost subclades like otophysans and percomorphs, rather than across the group as a whole, provides some circumstantial neontological support for this narrative (26).Open in a separate windowFig. 1.Phenotypic variation in early crown neopterygians. (A) Total-group holosteans. (B) Stem-group teleosts. (C) Crown-group teleosts. Taxa illustrated to scale.In contrast to quantified taxonomic patterns (20, 23, 24, 27), phenotypic evolution in early neopterygians has only been discussed in qualitative terms. The implicit paleontological model of morphological conservatism among early teleosts contrasts with the observation that clades aligned with the teleost stem lineage include some of the most divergent early neopterygians in terms of both size and shape (Fig. 1) (see, for example, refs. 28 and 29). These discrepancies point to considerable ambiguity in initial patterns of phenotypic diversification that lead to a striking contrast in the vertebrate tree of life, and underpins one of the most successful radiations of backboned animals.Here we tackle this uncertainty by quantifying rates of phenotypic evolution and capacity for evolutionary innovation for the first 160 million y of the crown neopterygian radiation. This late Permian (Wuchiapingian, ca. 260 Ma) to Cretaceous (Albian, ca. 100 Ma) sampling interval permits incorporation of diverse fossil holosteans and stem teleosts alongside early diverging crown teleost taxa (Figs. 1 and ​and2A2A and Figs. S1 and ​andS2),S2), resulting in a dataset of 483 nominal species-level lineages roughly divided between the holostean and teleost total groups (Fig. 2B and Fig. S2). Although genera are widely used as the currency in paleobiological studies of fossil fishes (30; but see ref. 31), we sampled at the species level to circumvent problems associated with representing geological age and morphology for multiple congeneric lineages. We gathered size [both log-transformed standard length (SL) and centroid size (CS); results from both are highly comparable (Figs. S3 and ​andS4);S4); SL results are reported in the main text] and shape data (the first three morphospace axes arising from a geometric morphometric analysis) (Fig. 2A and Figs. S1) from species where possible. To place these data within a phylogenetic context, we assembled a supertree based on published hypotheses of relationships. We assigned branch durations to a collection of trees under two scenarios for the timescale of neopterygian diversification based on molecular clock and paleontological estimates. Together, these scenarios bracket a range of plausible evolutionary timelines for this radiation (Fig. 2B). We used the samples of trees in conjunction with our morphological datasets to test for contrasts in rates of, and capacity for, phenotypic change between different partitions of the neopterygian Tree of Life (crown-, total-, and stem-group teleosts, total-group holosteans, and neopterygians minus crown-group teleosts), and the sensitivity of these conclusions to uncertainty in both relationships and evolutionary timescale. Critically, these include comparisons of phenotypic evolution in early crown-group teleosts—those species that are known with certainty to possess duplicate genomes—with rates in taxa characterized largely (neopterygians minus crown teleosts) or exclusively (holosteans) by unduplicated genomes. By restricting our scope to early diverging crown teleost lineages, we avoid potentially confounding signals from highly nested radiations that substantially postdate both genome duplication and the origin of crown teleosts (26, 32). This approach provides a test of widely held assumptions about the nature of morphological evolution in teleosts and their holostean sister lineage.Open in a separate windowFig. 2.(A) Morphospace of Permian–Early Cretaceous crown Neopterygii. (B) One supertree subjected to our paleontological (Upper) and molecular (Lower) timescaling procedures to illustrate contrasts in the range of evolutionary timescales considered. Colors of points (A) and branches (B) indicate membership in major partitions of neopterygian phylogeny. Topologies are given in Datasets S4 and S5. See Dataset S6 for source trees.Open in a separate windowFig. S1.Morphospace of 398 Permian–Early Cretaceous Neopterygii. Three major axes of shape variation are presented. Silhouettes and accompanying arrows illustrate the main anatomical correlates of these principal axes, as described in Open in a separate windowFig. S2.Morphospace of 398 Permian–Early Cretaceous Neopterygii, illustrating the major clades of (A) teleosts and (B) holosteans.Open in a separate windowFig. S3.Comparisons of size rates between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, (C) crown teleosts and stem teleosts, (D) crown teleosts and holosteans, and (E) stem teleosts and holosteans. Comparisons were made using the full-size SL dataset, a CS dataset, and a smaller SL dataset pruned to exactly match the taxon sampling of the CS dataset. Identical taxon sampling leads the CS and pruned SL datasets to yield near identical results. Although the larger SL dataset results often differ slightly, the overall conclusion from each pairwise comparison (i.e., which outcome is the most likely in an overall majority of trees) is identical in all but one comparison (E, under molecular timescales).Open in a separate windowFig. S4.Comparisons of size innovation between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, (C) crown teleosts and stem teleosts, (D) crown teleosts and holosteans, and (E) stem teleosts and holosteans. Comparisons were made using the full-size SL dataset, a CS dataset, and a smaller SL dataset pruned to exactly match the taxon sampling of the CS dataset. Comparisons of size innovation are presented for K value distributions of the three datasets resemble each other closely.     

Groundwater sapping as the cause of irreversible desertification of Hunshandake Sandy Lands,Inner Mongolia,northern China

In the middle-to-late Holocene, Earth’s monsoonal regions experienced catastrophic precipitation decreases that produced green to desert state shifts. Resulting hydrologic regime change negatively impacted water availability and Neolithic cultures. Whereas mid-Holocene drying is commonly attributed to slow insolation reduction and subsequent nonlinear vegetation–atmosphere feedbacks that produce threshold conditions, evidence of trigger events initiating state switching has remained elusive. Here we document a threshold event ca. 4,200 years ago in the Hunshandake Sandy Lands of Inner Mongolia, northern China, associated with groundwater capture by the Xilamulun River. This process initiated a sudden and irreversible region-wide hydrologic event that exacerbated the desertification of the Hunshandake, resulting in post-Humid Period mass migration of northern China’s Neolithic cultures. The Hunshandake remains arid and is unlikely, even with massive rehabilitation efforts, to revert back to green conditions.Earth’s climate is subject to abrupt, severe, and widespread change, with nonlinear vegetation–atmosphere feedbacks that produced extensive and catastrophic ecosystem shifts and subsequent cultural disruption and dispersion during the Holocene (1–7). In the early and middle Holocene, northern China’s eastern deserts, including much of the currently sparsely vegetated and semistabilized Hunshandake (Figs. 1 and ​and2),2), were covered by forests (8), reflecting significantly wetter climate associated with intensification of monsoon precipitation by up to 50% (6).Open in a separate windowFig. 1.Geographical location of the Hunshandake Sandy Lands (A) and its area (encircled by red line in B). The black rectangle in B marks the location of the enlarged maps C and D on the Right, and the green rectangle shows the location of Fig. 2. Map C shows the localities of water samples, and map D shows the localities of sections with stratigraphy presented in Fig. 3. The sand–paleosol section P (Fig. 3) is on the southern margin, and the site Bayanchagan marks the coring site of ref. 8. Rivers with headwaters in the Hunshandake likely formed by groundwater sapping are marked in blue. Drainages to the southwest and west are currently undergoing groundwater sapping, with substantial spring-driven flow found at the current river base level.Open in a separate windowFig. 2.(Left) Holocene lakes and channels in the Hunshandake and lake extent at selected epochs. Upper, middle, and lower lakes are indicated by points A, B, and C, respectively. Xilamulun River (point D) drains to the east. Groundwater-sapping headcuts at the upper reaches of incised canyons (point E) suggest a mid-Holocene interval of easterly surface flow, followed by groundwater drainage beginning at the ca. 4.2 ka event. Northern and central channels at point E are currently abandoned, and groundwater sapping has migrated to the southerly of the three channels shown. (Right) Cross-sections of the predrainage shift, northerly drainage into Dali Lake (Localities shown on the Left), showing the increase in widths of channels downstream (Vertical exaggeration ∼30:1).Monsoonal weakening, in response to middle-to-late Holocene insolation decrease, reduced precipitation, leading to a green/sandy shift and desertification across Inner Mongolia between ca. 5,000 and 3,000 y (years) ago (6). However, variations in the timing of this transition (9, 10) suggest local/regional thresholds or possibly environmental tipping by stochastic fluctuations. The impacts of this wet-to-dry shift in the Hunshandake, expressed as variations in surface and subsurface hydrology coincident with the termination of the formation of thick and spatially extensive paleosols, and the impacts of a ca. 4.2 ka (1 ka = 1,000 years) mid-Holocene desiccation of the Hunshandake on the development of early Chinese culture remain poorly understood and controversial (6, 11). Here we report for the first time to our knowledge on variability in a large early-to-middle Holocene freshwater lake system in China’s Hunshandake Sandy Lands and associated vegetation change, which demonstrates a model of abrupt green/desert switching. We document a possible hydrologic trigger event for this switching and discuss associated vegetation and hydrologic disruptions that significantly impacted human activities in the region.     

Amphitheater-headed canyons formed by megaflooding at Malad Gorge,Idaho

Many bedrock canyons on Earth and Mars were eroded by upstream propagating headwalls, and a prominent goal in geomorphology and planetary science is to determine formation processes from canyon morphology. A diagnostic link between process and form remains highly controversial, however, and field investigations that isolate controls on canyon morphology are needed. Here we investigate the origin of Malad Gorge, Idaho, a canyon system cut into basalt with three remarkably distinct heads: two with amphitheater headwalls and the third housing the active Wood River and ending in a 7% grade knickzone. Scoured rims of the headwalls, relict plunge pools, sediment-transport constraints, and cosmogenic (³He) exposure ages indicate formation of the amphitheater-headed canyons by large-scale flooding ∼46 ka, coeval with formation of Box Canyon 18 km to the south as well as the eruption of McKinney Butte Basalt, suggesting widespread canyon formation following lava-flow diversion of the paleo-Wood River. Exposure ages within the knickzone-headed canyon indicate progressive upstream younging of strath terraces and a knickzone propagation rate of 2.5 cm/y over at least the past 33 ka. Results point to a potential diagnostic link between vertical amphitheater headwalls in basalt and rapid erosion during megaflooding due to the onset of block toppling, rather than previous interpretations of seepage erosion, with implications for quantifying the early hydrosphere of Mars.Landscapes adjust to perturbations in tectonics and base level through upstream propagation of steepened river reaches, or knickzones, thereby communicating environmental signals throughout a drainage basin (e.g., ref. 1). Nowhere are knickzones more important and apparent than in landscapes where canyon heads actively cut into plateaus, such as tributaries of the Grand Canyon, United States, and the basaltic plains of Mars (e.g., refs. 2–4). Here the stark topographic contrast between low-relief uplands and deeply incised canyons sharply delineates canyon rims and planform morphology. Canyon heads can have varied shapes from amphitheaters with vertical headwalls to more pointed planform shapes with lower gradients, and a prominent goal in geomorphology and planetary science is to link canyon morphology to formation processes (e.g., refs. 4–8), with implications for understanding the history of water on Mars.Amphitheater-headed canyons on Mars are most likely cut into layered basalt (9, 10), and canyon-formation interpretations have ranged widely from slow seepage erosion to catastrophic megafloods (4–6, 11, 12). Few studies have been conducted on the formation of amphitheater-headed canyons in basalt on Earth, however, and instead, terrestrial canyons in other substrates are often used as Martian analogs. For example, groundwater sapping is a key process in forming amphitheater-headed canyons in unconsolidated sand (e.g., refs. 8, 13, 14), but its importance is controversial in rock (5, 12, 15). Amphitheater-headed canyons are also common to plateaus with strong-over-weak sedimentary rocks (3, 16); however, here the tendency for undercutting is so strong that canyon-head morphology may bear little information about erosional processes, whether driven by groundwater or overland flow (e.g., refs. 3, 5, 17). Canyons in some basaltic landscapes lack strong-over-weak stratigraphy, contain large boulders that require transport, and show potential for headwall retreat by block toppling (18–21), all of which make extension of process–form relationships in sand and sedimentary rocks to basalt and Mars uncertain.To test the hypothesis of a link between canyon formation and canyon morphology in basalt, we need field measurements that can constrain formation processes for canyons with distinct morphologies, but carved into the same rock type. Here we report on the origin of Malad Gorge, a canyon complex eroded into columnar basalt with markedly different shaped canyon heads. Results point to a potential diagnostic link between canyon-head morphology and formative process by megaflood erosion in basalt.Malad Gorge is a tributary to the Snake River Canyon, Idaho, within the Snake River Plain, a broad depression filled by volcanic flows that erupted between ∼15 Ma and ∼2 ka (22, 23). The gorge sits at the northern extent of Hagerman Valley, a particularly wide (∼7 km) part of the Snake River Canyon (Fig. 1). Malad Gorge is eroded into the Gooding Butte Basalt [⁴⁰Ar/³⁹Ar eruption age: 373 ± 12 ka (25)] which is composed of stacked lava beds, each several meters thick with similar well-defined columns bounded by cooling joints and no apparent differences in strength between beds. The Wood (or Malad) River, a major drainage system from the Sawtooth Range to the north, drains through Malad Gorge before joining the Snake River. The Wood River is thought to have been diverted from an ancestral, now pillow lava-filled canyon into Malad Gorge by McKinney Butte basalt flows (24) [⁴⁰Ar/³⁹Ar eruption age: 52 ± 24 ka (25) (Fig. 1).Open in a separate windowFig. 1.Shaded relief map of the study region (50-m contour interval) showing basalt flows (23), their exposure age sample locations, and the path of the ancestral Wood River following Malde (24) (US Geological Survey).Malad Gorge contains three distinct canyon heads herein referred to as Woody’s Cove, Stubby Canyon, and Pointed Canyon (Fig. 2A). Woody’s Cove and Stubby have amphitheater heads with ∼50-m-high vertical headwalls (Fig. 2C), and talus accumulation at headwall bases indicates long-lived inactive fluvial transport (Fig. 3 A and B). Woody’s Cove, the shortest of the three canyons, lacks major spring flows and has minor, intermittent overland flow partially fed by irrigation runoff that spills over the canyon rim. Stubby has no modern-day overland flow entering the canyon, and springs emanate from a pool near its headwall (Fig. 3B). In contrast, Pointed Canyon is distinctly more acute in planform morphology, contains a 7% grade knickzone composed of multiple steps rather than a vertical headwall (Figs. 2C and ​and3C),3C), and extends the farthest upstream.Open in a separate windowFig. 2.Malad Gorge topography (10-m contour interval) and aerial orthophotography (US Geological Survey). (A) Overview map and (B) close-up for Stubby and Pointed canyons showing mapped bedrock scours (white arrows), exposure age sample locations (red circles) with age results, location of the uppermost active knickpoint (black circle), abandoned bedrock channels (blue dashed lines), and grain-size analysis sites (blue squares). The blue star shows the reconstructed location of the headwall of Pointed Canyon at 46 ka (see Discussion and Fig. 5). (C) Longitudinal profile along Stubby and Pointed canyons from their confluence (shown as white lines in B) with local slope, S, averaged over regions demarked by dashed lines (Fig. 4A shows close-up of profile in Stubby Canyon).Open in a separate windowFig. 3.Photographs of (A) headwall of Woody’s Cove (person for scale, circled), (B) ∼50-m-high headwall of Stubby Canyon, (C) downstream-most waterfall at Pointed Canyon knickzone (12-m-high waterfall with overcrossing highway for scale), (D) fluted and polished notch at the rim of Stubby Canyon (notch relief is 10 m), (E) upstream-most waterfall at Pointed Canyon knickzone (within the southern anabranch of Fig. S2), and (F) upstream-most abandoned channel in Fig. 2B and Fig. S2 (channel relief is ∼10 m). White coloring on the headwalls in A and B is likely residue from irrigation runoff.Early work attributed the amphitheater-headed canyons in this region—Malad Gorge, Box Canyon, located 18 km south of Malad Gorge (Fig. 1), and Blue Lakes Canyon located 42 km to the SE—to formation by seepage erosion because of no modern overland flow and the occurrence of some of the largest springs in the United States in this region (7). Because spring flows (e.g., ∼10 m³/s in Box Canyon; US Geological Survey gauge 13095500) are far deficient to move the boulders that line the canyon floors, Stearns (7) reasoned that the boulders must chemically erode in place. This explanation is improbable, however, given the young age of the Quaternary basalt (25), spring water saturated in dissolved solids (19), and no evidence of rapid chemical weathering (e.g., talus blocks are angular and have little to no weathering rinds). Instead of groundwater sapping, Box Canyon was likely carved by a large-scale flood event that occurred ∼45 ka based on ³He cosmogenic exposure age dating of the scoured rim of the canyon headwall (19, 26). In addition, Blue Lakes Canyon was formed during the Bonneville Flood [∼18–22 ka (27, 28)], one of the world’s largest outburst floods that occurred as a result of catastrophic draining of glacial lake Bonneville (21). In both cases, canyon formation was inferred to have occurred through upstream headwall propagation by waterfall erosion.Herein we aim to test whether the amphitheater-headed canyons at Malad Gorge also owe their origin to catastrophic flooding, whether Pointed Canyon has a different origin, and whether canyon morphology is diagnostic of formation process. To this end we present field observations, sediment-size measurements, hydraulic modeling, and cosmogenic exposure ages of water-scoured rock surfaces and basalt-flow surfaces (Methods and Tables S1 and S2).     

Insect nicotinic receptor interactions in vivo with neonicotinoid,organophosphorus, and methylcarbamate insecticides and a synergist

The nicotinic acetylcholine (ACh) receptor (nAChR) is the principal insecticide target. Nearly half of the insecticides by number and world market value are neonicotinoids acting as nAChR agonists or organophosphorus (OP) and methylcarbamate (MC) acetylcholinesterase (AChE) inhibitors. There was no previous evidence for in vivo interactions of the nAChR agonists and AChE inhibitors. The nitromethyleneimidazole (NMI) analog of imidacloprid, a highly potent neonicotinoid, was used here as a radioligand, uniquely allowing for direct measurements of house fly (Musca domestica) head nAChR in vivo interactions with various nicotinic agents. Nine neonicotinoids inhibited house fly brain nAChR [³H]NMI binding in vivo, corresponding to their in vitro potency and the poisoning signs or toxicity they produced in intrathoracically treated house flies. Interestingly, nine topically applied OP or MC insecticides or analogs also gave similar results relative to in vivo nAChR binding inhibition and toxicity, but now also correlating with in vivo brain AChE inhibition, indicating that ACh is the ultimate OP- or MC-induced nAChR active agent. These findings on [³H]NMI binding in house fly brain membranes validate the nAChR in vivo target for the neonicotinoids, OPs and MCs. As an exception, the remarkably potent OP neonicotinoid synergist, O-propyl O-(2-propynyl) phenylphosphonate, inhibited nAChR in vivo without the corresponding AChE inhibition, possibly via a reactive ketene metabolite reacting with a critical nucleophile in the cytochrome P450 active site and the nAChR NMI binding site.The nicotinic nervous system has two principal sites of insecticide action, the nicotinic receptor (nAChR) activated by acetylcholine (ACh) and neonicotinoid agonists (1–6), and acetylcholinesterase (AChE) inhibited by organophosphorus (OP) and methylcarbamate (MC) compounds to generate and maintain localized toxic ACh levels (Fig. 1) (7). The nAChR and AChE targets have been identified in insects by multiple techniques but not by direct assays of the ACh binding site in the brain of poisoned insects. Here we use the outstanding insecticidal potency of the nitromethyleneimidazole (NMI) analog of imidacloprid (IMI) (8) as a radioligand (9), designated [³H]NMI, to directly measure the house fly (Musca domestica) nAChR not only in vitro but also in vivo, allowing us to validate by a previously undescribed method the neonicotinoid direct and OP/MC indirect nAChR targets (Fig. 2). This approach also helped solve the intriguing mechanism by which an O-(2-propynyl) phosphorus compound strongly synergizes neonicotinoid insecticidal activity (10) by dual inhibition of cytochrome P450 (CYP) (11–13) and the nAChR agonist site (described herein). Insecticide disruption at the insect nAChR can now be readily studied in vitro and in vivo with a single radioligand allowing better understanding of the action of several principal insecticide chemotypes (Fig. 3).Open in a separate windowFig. 1.The insect nicotinic receptor is the direct or indirect target for neonicotinoids, organophosphorus compounds and methylcarbamates, which make up about 45% of the insecticides by number and world market value (2, 7).Open in a separate windowFig. 2.In this study, Musca nicotinic receptor in vivo interactions with major insecticide chemotypes are revealed by a [³H]NMI radioligand reporter assay. *Position of tritium label.Open in a separate windowFig. 3.Two neonicotinoid nicotinic agonists and two anticholinesterase insecticides.     

Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution

As one of the earliest-known mammaliaforms, Haramiyavia clemmenseni from the Rhaetic (Late Triassic) of East Greenland has held an important place in understanding the timing of the earliest radiation of the group. Reanalysis of the type specimen using high-resolution computed tomography (CT) has revealed new details, such as the presence of the dentary condyle of the mammalian jaw hinge and the postdentary trough for mandibular attachment of the middle ear—a transitional condition of the predecessors to crown Mammalia. Our tests of competing phylogenetic hypotheses with these new data show that Late Triassic haramiyids are a separate clade from multituberculate mammals and are excluded from the Mammalia. Consequently, hypotheses of a Late Triassic diversification of the Mammalia that depend on multituberculate affinities of haramiyidans are rejected. Scanning electron microscopy study of tooth-wear facets and kinematic functional simulation of occlusion with virtual 3D models from CT scans confirm that Haramiyavia had a major orthal occlusion with the tallest lingual cusp of the lower molars occluding into the lingual embrasure of the upper molars, followed by a short palinal movement along the cusp rows alternating between upper and lower molars. This movement differs from the minimal orthal but extensive palinal occlusal movement of multituberculate mammals, which previously were regarded as relatives of haramiyidans. The disparity of tooth morphology and the diversity of dental functions of haramiyids and their contemporary mammaliaforms suggest that dietary diversification is a major factor in the earliest mammaliaform evolution.Haramiyidans are among the first mammaliaforms to appear during the Late Triassic in the evolutionary transition from premammalian cynodonts. Their fossils have a cosmopolitan distribution during the Late Triassic to the Jurassic (1–8), tentatively with the youngest record in the Late Cretaceous of India (9). Most of these occurrences are of isolated teeth. For this reason, Haramiyavia clemmenseni (1) holds a special place in mammaliaform phylogeny: It is the best-preserved Late Triassic haramiyid with intact molars, nearly complete mandibles, and also postcranial skeletal elements (Figs. 1 and ​and22 and SI Appendix, Figs. S1–S4) (1). By its stratigraphic provenance from the Tait Bjerg Beds of the Fleming Fjord Formation, East Greenland (Norian-Rhaetic Age) (7), Haramiyavia is also the oldest known haramiyid (5, 7). Haramiyids, morganucodonts, and kuehneotheriids are the three earliest mammaliaform groups that are distinctive from each other in dental morphology and masticatory functions (10–12).Open in a separate windowFig. 1.(A and B) Composite reconstruction of Haramiyavia clemmenseni right mandible in lateral (A) and medial (B) views. Dark red: original bone with intact periosteal surface; brown: broken surface of preserved bone or remnant of bone; light blue: morphologies preserved in mold outlines or clear impression. (C) Morganucodon mandible in medial view.Open in a separate windowFig. 2.Molar features of Haramiyavia. (A) Right M1–M3 in occlusal view (medio-lateral orientation by the zygomatic root and the palate). (B) Occlusal facets of upper molars. (C) Lingual view of M1–M3. (D) Root structures of upper molars (M1 and M2 show three partially divided anterior roots connected by dentine and two posterior roots connected by dentine; M3 has two anterior and two posterior roots connected respectively by dentine). These roots have separate root canals. (E) Buccal view of M1–M3. All roots are bent posteriorly, suggesting that crowns shifted mesially, relative to the roots, during the tooth eruption, also known as mesial drift of teeth (arrowhead), typical of successive eruption of multirooted postcanines. (F) SEM photograph of lower m3 in a posterior occlusal view. (G) Approximate extent of wear facets by orthal occlusion (a1 cusp in embrasure of upper molars) (blue) and palinal movement of b2–b4 cusps sliding across the median furrow of upper molars (green). (H) Lingual view of m3. There are no wear facets on lingual side of cusps a1–a4. (I) Buccal view of m3 showing wear facets on the buccal sides of cusps b1–b4 and on apices.Haramiyids are characterized by their complex molars with longitudinal rows of multiple cusps. The cusp rows occlude alternately between the upper and lower molars. Primarily because of similarities in molar morphology, haramiyids are considered to be related to poorly known theroteinids of the Late Triassic (5, 13) and eleutherodontids of the Middle to Late Jurassic (14–17). Collectively haramiyids and eleutherodontids are referred to as “haramiyidans” (10, 14, 15, 18, 19). Recent discoveries of diverse eleutherodontids or eleutherodontid-related forms with skeletons from the Tiaojishan Formation (Middle to Late Jurassic) of China (18–20) have greatly augmented the fossil record of haramiyidans, ranking them among the most diverse mammaliaform clades of the Late Triassic and Jurassic.Historically, it has been a contentious issue whether haramiyidans (later expanded to include theroteinids and eleutherodontids) are closely related to the more derived multituberculates from the Middle Jurassic to Eocene (13) or represent a stem clade of mammaliaforms excluded from crown mammals (21, 22). The conflicting placement of haramiyidans was attributable in part to the uncertainties in interpreting the isolated teeth of most Late Triassic haramiyids (21, 22). More recent phylogenetic disagreements have resulted from different interpretations of mandibular characters in Haramiyavia (17–20, 23–25), which has not been fully described (figure 2 in ref. 1).Here we present a detailed study of the mandibles and teeth of Haramiyavia from the exhaustive documentation during initial fossil preparation (Fig. 1 and SI Appendix, Figs. S1–S4), from scanning electron microscopy (SEM) images, and from computed tomography (CT) scans and 3D image analyses of the two fossil slabs with mandibles (MCZ7/95A and B), plus a referred specimen of upper molars in a maxilla (MCZ10/G95) (Figs. 2 and ​and3,3, SI Appendix, Figs. S5–S8 and Tables S2 and S3, and Movie S1). These new data are informative for testing alternative mammaliaform phylogenies (Fig. 4 and SI Appendix) and are useful for reconstructing evolutionary patterns of feeding function in the earliest mammaliaforms.Open in a separate windowFig. 3.Molar occlusion of haramiyids. (A) In Haramiyavia the upper and lower molars form an en echelon pattern, a series of parallel and step-like occlusal surfaces in lingual and buccal views (based on 3D scaled models from CT scans of MCZ7/G95 and MCZ10/G95). (B–E) In Haramiyavia are shown the occlusal paths of cusps a1–a4 of the lingual row (B), cusps b2–b4 of the buccal row (shown with the lingual half of the tooth cut away) (C), and tooth orientation and the cut-away plane (D). During the orthal occlusion phase, the tallest lingual cusp a1 occludes into the embrasure of the preceding and the opposing upper molars (B and E), and the tallest buccal cusp b2 occludes into the upper furrow and behind the A1–B1 saddle of the upper molar (C). During the palinal occlusion phase, cusps b1–b4 of the buccal row slide posteriorly in the upper furrow, and in the upper row cusps B5–B1 slide in the lower furrow (lower molars with blue and green shading, superpositioned by flipped upper molar in clear outlines) (E). (F) Extent of wear on molars during the orthal phase (blue) and the palinal movement (green) produced by OFA simulation (Movie S1). (G–I) In Thomasia, reconstruction of upper and lower molar series on the basis of wear surfaces and tooth crown morphology (revised from refs. 2, 3, and 10). (G) The en echelon occlusal surfaces in lingual view. (H) Orthal occlusion (blue) is followed by palinal occlusal movement (green). (I) Occlusal wear facets of molars. Facets worn by orthal occlusion are shown in blue, and facets worn by palinal occlusion are shown in gray hatching. Cusp and facet designations are after refs 3 and 6.Open in a separate windowFig. 4.Hypotheses concerning the phylogenetic relationship of Haramiyavia and timing estimates of the basal diversification of crown mammals. (A) Haramiyavia is a close relative of multituberculates, both nested in the crown Mammalia. This hypothesis (haramiyidan node position 1) was based on a misinterpretation of a previous illustration of a fragment of the mandible (17, 18). (B) Haramiyavia is a stem mammaliaform, as determined by incorporating the features preserved on both mandibles into phylogenetic estimates (haramiyidan node position 2). (C) Placement of Haramiyavia and other haramiyidans among mammaliaforms according to this study. Many mandibular features were treated as unknown by studies favoring a Late Triassic diversification of mammals (18, 23). A more complete sampling of informative features revealed by this study now has overturned the previous placement. Clades: crown Mammalia (node a); Mammaliaformes (node b); haramiyidans (node 1 or 2, alternative positions); Eleutherodontida (node c). The rescored datasets and analyses are presented in SI Appendix.     

Late Miocene episodic lakes in the arid Tarim Basin,western China

The Tibetan Plateau uplift and Cenozoic global cooling are thought to induce enhanced aridification in the Asian interior. Although the onset of Asian desertification is proposed to have started in the earliest Miocene, prevailing desert environment in the Tarim Basin, currently providing much of the Asian eolian dust sources, is only a geologically recent phenomenon. Here we report episodic occurrences of lacustrine environments during the Late Miocene and investigate how the episodic lakes vanished in the basin. Our oxygen isotopic (δ¹⁸O) record demonstrates that before the prevailing desert environment, episodic changes frequently alternating between lacustrine and fluvial-eolian environments can be linked to orbital variations. Wetter lacustrine phases generally corresponded to periods of high eccentricity and possibly high obliquity, and vice versa, suggesting a temperature control on the regional moisture level on orbital timescales. Boron isotopic (δ¹¹B) and δ¹⁸O records, together with other geochemical indicators, consistently show that the episodic lakes finally dried up at ∼4.9 million years ago (Ma), permanently and irreversibly. Although the episodic occurrences of lakes appear to be linked to orbitally induced global climatic changes, the plateau (Tibetan, Pamir, and Tianshan) uplift was primarily responsible for the final vanishing of the episodic lakes in the Tarim Basin, occurring at a relatively warm, stable climate period.Once part of the Neo-Tethys Sea, indicated by the Paleogene littoral-neritic deposits with intercalated marine strata (1), the Tarim Basin in western China (Fig. 1) has experienced dramatic environmental and depositional changes during the Cenozoic. The eventual separation of the basin from the remnant sea probably occurred during the middle to late Eocene (1, 2), and since then, terrestrial sedimentation and environment have prevailed. Today, the basin has relatively flat topography with elevation ranging between 800 and 1,300 m above sea level (asl), surrounded by high mountain ranges with average elevation exceeding 4,000 m. Hyperarid climate prevails with mean annual precipitation <50 mm and evaporation ∼3,000 mm. Active sand dunes occupy 80% of the basin, forming the Taklimakan Desert, the largest desert in China and the second largest in the world (3). Thick desert deposits in the basin also provide a major source for dust storms occurring in East Asia (4).Open in a separate windowFig. 1.Digital elevation model of the Tarim Basin and surrounding mountain ranges. The studied 1,050-m sediment core is retrieved from Lop Nor (1), at a relatively low elevation (∼800 m asl) in the eastern basin. Also indicated are locations of previous studied sections, near Sanju (2), Kuqa (3), and Korla (4) in the basin.The Tibetan Plateau uplift, long-term global cooling, and the associated retreat of the remnant sea during the Cenozoic, through their complex interplay, may have all contributed to the enhanced aridification in the Asian interior and eventually the desert formation (2, 5–11). Although the onset of Asian desertification is proposed to have started in the earliest Miocene (12, 13), prevailing desert environment in the Tarim Basin, currently providing much of the Asian eolian dust sources (4), is only a geologically recent phenomenon (9). Previous lithological and pollen studies (9, 14, 15) suggest that the currently prevailing desert environment started probably at ∼5 Ma. However, what kind of environmental conditions prevailed before that and how the dramatic changes occurred largely remain elusive.To better decipher the aridification history, we used a 1,050-m-long, continuous sediment core retrieved from Lop Nor (39°46''0''''N, 88°23''19''''E) in the eastern basin (Fig. S1). The core site has a relatively low elevation (∼800 m asl) (Fig. 1) and thus effectively records basin environment. Previous study sites came from elevated basin margins (9, 14). The core mainly consists of lacustrine sediments with associated fluvial-eolian sands (Fig. 2). The core chronology was established previously based on paleomagnetic polarity (15). The total 706 remanence measurements on the continuous sediment profile allow straightforward correlation with the CK95 geomagnetic polarity timescale (16) and identification of 14 normal (N1–N14) and 13 reversal (R1–R13) polarity zones over the last 7.1 Ma (Fig. S1). The CK95 timescale is largely consistent (within a few ky) with that inferred from marine archives (17) over the last 5.23 Ma, and before 5.23 Ma a practical measure of chronological uncertainty was estimated to be within ∼100 ky (18), assuring that the terrestrial records can be directly compared with marine records and orbital changes at the timescale of >100 ky. The derived chronology yields an average sedimentation rate of ∼200 m/Ma at lower sections (>1.77 Ma), allowing high-resolution studies of the desertification history at the critical interval.Open in a separate windowFig. 2.Records of δ¹¹B, δ¹⁸O, TOC, and CaCO₃ changes in the Lop Nor profile. Representative photos show lithological changes mainly from lacustrine bluish gray argillaceous limestone to fluvial-eolian brown/red clayey silt, as shown in the lithological column with visual colors indicated (15). High levels and large fluctuations of proxy values occurred only before ∼4.9 Ma, and since then, those remain low and within a small range, largely similar to modern conditions. The transition from episodic occurrences of lacustrine phases to prevailing desert environments thus appears to be permanent and irreversible.Boron and oxygen isotopes from carbonates are important environmental indicators (19–25) and used here to infer the environmental evolution in the Tarim Basin. We also present total organic carbon (TOC), calcium carbonate (CaCO₃), ostracod, and grain size records to substantiate the isotopic evidence (SI Materials and Methods). Our δ¹¹B profile shows substantial, stepwise changes over the last ∼7.1 Ma (Fig. 2). Carbonate δ¹¹B values were −5.0 ± 1.6‰ (n = 3) before 6.0 Ma, increased rapidly to ∼11‰ at 4.9–6.0 Ma, and then stayed at roughly the same level (10.7 ± 2.2‰, n = 25) for the remaining 4.9 Ma. Higher-resolution δ¹⁸O, TOC, and CaCO₃ profiles generally confirm the pattern observed in the low-resolution δ¹¹B one (Fig. 2). The δ¹⁸O values remained low, ranging from −10‰ to −4‰ over the last 4.9 Ma. However, δ¹⁸O values frequently oscillated between −10‰ and 5‰ before that. Similarly, the TOC profile shows consistently low organic carbon content (0–0.2%) after 4.9 Ma and large fluctuations (0–1.0%) before then. The CaCO₃ profile also indicates consistently low values (0–25%) after 4.9 Ma and large fluctuations (0–50%) earlier (Fig. 2).The multiple proxy records strongly suggest that critical environmental changes must have occurred at ∼4.9 Ma. δ¹¹B values of carbonates from marine sources differ substantially from those of nonmarine carbonates (19–21). δ¹¹B values after 4.9 Ma are close to those from marine carbonates, but values before 6 Ma fall into the range of lacustrine carbonates (22). Positive δ¹⁸O values before 4.9 Ma also indicate lacustrine environments at that time. Carbonates from modern lakes in arid and semiarid regions of northwestern China show similar positive δ¹⁸O values (23), due to strong evaporation processes. High TOC and CaCO₃ contents (Fig. 2) further support that lacustrine environments existed in the basin before ∼4.9 Ma. δ¹⁸O values after 4.9 Ma are comparable to those in Cenozoic soil carbonates (24) and ancient marine carbonates in the Tarim Basin (25). However, the accompanying carbonate δ¹³C values throughout the record, ranging from −4‰ to 1‰ (Dataset S1), are significantly higher than those from Cenozoic soil carbonates reported (26), essentially ruling out the possibility of soil carbonate source. Using modern prevailing desert environment in the basin as an analog, the combined δ¹¹B and δ¹⁸O evidence thus suggests that the sediment deposits in the basin after 4.9 Ma must be eolian-fluvial in origin and their sources, at least carbonate grains, came from weathered ancient marine carbonates in nearby regions.Sedimentological and stratigraphic patterns in other exposed sections from different parts of the basin (9, 14) share great similarity with the Lop Nor core profile (Fig. S1). Episodic lacustrine mudstones and/or siltstones during the Late Miocene were present in all sections and were replaced by fluvial-eolian deposits later. Studies of ostracod assemblages (27) also suggest a shallow paleolake with brackish water environments in the northern basin during the Late Miocene. Changes in the depositional environment from our Lop Nor profile alone could be plausibly explained by a shift in basin center due to tectonic compressions, as evidenced from the slightly uplifted central basin (Fig. 1). However, similar temporal changes occurring basin-wide at ∼4.9 Ma argue against it. Instead, our results, together with previous studies (5, 14, 15, 27), suggest that paleolakes were widely present in the low lands of the basin during the Late Miocene, much different from currently prevailing desert environments with a few scattered small lakes. The existing evidence, although still limited (Fig. 1), would point to the occurrence of a possible megalake in the Tarim Basin during the Late Miocene.Three high-resolution records, δ¹⁸O, TOC, and CaCO₃, further suggest that lacustrine environments before ∼4.9 Ma were not permanent (Fig. 2). These large fluctuations indicate frequent switches between lacustrine and fluvial-eolian environments in the basin. High proxy values, δ¹⁸O in particular, appear to indicate lacustrine environments, whereas low values, similar to ones after 4.9 Ma, correspond to fluvial-eolian deposits. This is consistent with lithological features at this interval, showing argillaceous limestone intercalated with clayey layers (15), the occurrence of ostracod assemblages (Fig. 3) from lacustrine sediments, grain size changes (Fig. S2), and detrital carbonate grains identified in photomicrographs of fluvial-eolian deposits (Fig. S3).Open in a separate windowFig. 3.δ¹⁸O fluctuations linked to eccentricity and obliquity orbital variations at 4.5–7.1 Ma. Lacustrine phases (high δ¹⁸O) generally correspond to periods of high eccentricity and obliquity. Fluvial-eolian environment (low δ¹⁸O, highlighted with gray bars), developed more around 6.5, 6.1, 5.7, and 5.2 Ma, at a ∼400-ky eccentricity beat. The red bar indicates the last occurrence of lacustrine environment at ∼4.9 Ma. Occurrences of ostracod assemblages with total number >100 are also indicated.To further investigate such episodic changes, we performed spectral analysis on the δ¹⁸O record over the interval 4.5–7.1 Ma. Strong spectral power at orbital frequencies were identified, with periods of ∼400 ky throughout the interval, ∼41 ky particularly at 6–6.5 Ma, and ∼100 ky at 5–6 Ma and 6.5–7.1 Ma (Fig. S4). Precessional ∼20-ky power might also have existed but was relatively weak and discontinuous. Lacustrine phase as indicated by high δ¹⁸O values and ostracod assemblages generally occurred at periods of high eccentricity and obliquity (28) (Fig. 3). At 6–6.5 Ma, δ¹⁸O shows clear correspondence to orbital obliquity variation (Fig. 3A). Additionally, the number of low δ¹⁸O values (fluvial-eolian environment) occurred more around 6.5, 6.1, 5.6, and 5.2 Ma, at a ∼400-ky beat following orbital eccentricity variation (Fig. 3B). The cluster of high δ¹⁸O values (>0‰) at 4.9–5.0 Ma signals the last occurrence of lacustrine environments in the basin. Our orbital association thus allows us to precisely determine the timing of desert formation at ∼4.9 Ma, ∼400 ky (an eccentricity cycle) later than the age inferred from basin margins (9, 14) and yet all occurring at eccentricity minima (Fig. 3B). As high eccentricity and obliquity generally correspond to warm conditions at orbital timescales, lacustrine (wet) phase could be associated with warm periods, consistent with the notion that cooler conditions would reduce moisture in the atmosphere and enhance continental drying (10, 11). We recognize that the chronological uncertainty from the geomagnetic polarity timescale before 5.23 Ma, within ∼100 ky (18), could confound our association of wet phase with high obliquity, although it is unlikely affected at the 400-ky eccentricity beat. However, the opposite association, wet phase with low obliquity, and the combination with high eccentricity, would require a different, yet unknown mechanism that is inconsistent with the orbital theory of Pleistocene ice ages.Superimposed on the orbitally episodic changes, the δ¹⁸O record also shows a long-term trend of deteriorating lacustrine conditions at 4.9–7.1 Ma. As δ¹⁸O values indicate two depositional environments, lacustrine and fluvial-eolian, the range of δ¹⁸O changes (between −10‰ and 5‰) does not vary much over this period (Fig. 3). Rather, the duration of high δ¹⁸O vs. low values would reflect the long-term trend. The mean δ¹⁸O values over 40-ky and 400-ky intervals both show a decreasing trend, with dominant lacustrine phase before 6.1 Ma, more developed fluvial-eolian environment at 5.7–6.1 Ma, a return to slightly better lacustrine environment at 5.3–5.7 Ma, and lacustrine phase permanently vanished around 4.9 Ma (Fig. 4).Open in a separate windowFig. 4.Long-term δ¹⁸O changes compared with global climatic conditions and regional tectonic activities. Global benthic δ¹⁸O (29) and northwestern Pacific SST (30) records show minimal long-term changes at 4–7 Ma, whereas occurrences of detrital apatite fission track ages (35) in northern western Kunlun peaked, and the Tarim episodic lakes gradually vanished. The dark thick lines are their 400-ky running means, and the light green line on δ¹⁸O represents the 40-ky running mean.The gradual disappearance of the Tarim episodic lakes could be potentially explained by the two driving forces, plateau uplift (the Tibetan Plateau, Pamir Plateau, and Tianshan) and long-term global cooling. However, the long-term global climate was relatively warm and stable during this period (Fig. 4). The global benthic δ¹⁸O record (29) shows that much of the Miocene cooling occurred between 15 and 11 Ma, and the cooling between 8 and 5 Ma was minimal. Supporting this view, sea surface temperature records from the northwestern Pacific (30) show that almost no cooling occurred between 6 and 4 Ma (perhaps further to 3 Ma) (Fig. 4). Particularly, the mean global climate (29, 30) was even warmer at 4.1–4.5 Ma than at 5.7–6.1 Ma, whereas lacustrine phase permanently disappeared after ∼4.9 Ma (Fig. 4), indicating decoupling of the lake evolution from global climate. Therefore, long-term global cooling might have played a subordinate role in the lake disappearance.Instead, the growth of surrounding mountain ranges (Tibetan, Pamir, and Tianshan) may have blocked moisture from the west and south, changed air circulations, and eventually led to the permanent lake disappearance within the basin. Today, the Tarim Basin receives limited moisture from westerlies (31) through the Pamir and Tianshan Ranges (and perhaps from the Indian Ocean in summertime as well). Although the Indo–Eurasian convergence since the Late Eocene resulted in high elevations of the Tibetan Plateau and, to a lesser degree, surrounding mountains including Pamir and Tianshan by the mid-Miocene time (8), tectonic activities in broad areas around the Tarim Basin appear to be rejuvenated since the Late Miocene. Tectonic deformations during the Late Miocene–Early Pliocene inferred from growth strata, sedimentary facies changes, and low-temperature thermochronologic studies occurred in Tianshan to the north of the Tarim Basin, in the Kunlun Mountains to its south and the Pamir to its west (32–35). Syntectonic growth strata from the foreland basins of the Kunlun and Tianshan Ranges (32) show that strong crust shortening and potential mountain uplift initiated ∼6.5–5 Ma and lasted to the Early Pleistocene (Fig. S5), similarly reported in northern Pamir (33). Cenozoic sequences in the Pamir–Tianshan convergence zone, changing from an arid continental plain to an intermountain basin by ∼5 Ma, support surface uplift of the west margin of the Tarim Basin (34). Occurrence of detrital apatite fission track ages from West Kunlun Ranges (35) also peaked at ∼4.5 Ma (Fig. 4). Thus, the reactivated uplift of Pamir and West Kunlun Ranges and northward movement of Pamir during the Late Miocene–Pliocene would progressively block moisture into the basin and enhance regional aridity to a certain threshold to terminate lacustrine environments even during warm periods with favorable orbital configuration. Although inconsistencies indeed exist in linking regional climatic and environmental changes to tectonic events (8), the final vanishing of the Tarim episodic lakes is better explained by tectonic factors.Therefore, our multiple-proxy results consistently show that the Taklimakan sand sea began to form at ∼4.9 Ma and that the transition into prevailing desert environment was permanent and irreversible. The episodic occurrences of lacustrine environments at favorable climatic conditions (warm periods) during the Late Miocene suggest that uplifted mountain ranges then were not high enough to effectively block moisture from being transported into the basin. The transition from episodic lacustrine environments to prevailing desert deposits was gradual, from 7.1 Ma (or earlier beyond our record) to 4.9 Ma, for which we suggest that although long-term global cooling enhanced the overall aridification in the Asian interior during the Late Cenozoic (10, 11), plateau uplift played a more important role in finally drying up the episodic lakes within a relatively warm, stable climate period, thus decoupling regional climate temporally from a global trend. Our high-resolution records thus demonstrate that regional climate in the Tarim Basin reached a critical state in the Late Miocene, with the dual effects from global climate conditions and regional tectonic settings then. With global climate remaining relatively stable and warm entering the Pliocene, by ∼3–4 Ma (Fig. 4), drying up of episodic lakes at ∼4.9 Ma could thus be largely attributed to rejuvenated tectonic activities.     

Drought,agricultural adaptation,and sociopolitical collapse in the Maya Lowlands

Paleoclimate records indicate a series of severe droughts was associated with societal collapse of the Classic Maya during the Terminal Classic period (∼800–950 C.E.). Evidence for drought largely derives from the drier, less populated northern Maya Lowlands but does not explain more pronounced and earlier societal disruption in the relatively humid southern Maya Lowlands. Here we apply hydrogen and carbon isotope compositions of plant wax lipids in two lake sediment cores to assess changes in water availability and land use in both the northern and southern Maya lowlands. We show that relatively more intense drying occurred in the southern lowlands than in the northern lowlands during the Terminal Classic period, consistent with earlier and more persistent societal decline in the south. Our results also indicate a period of substantial drying in the southern Maya Lowlands from ∼200 C.E. to 500 C.E., during the Terminal Preclassic and Early Classic periods. Plant wax carbon isotope records indicate a decline in C₄ plants in both lake catchments during the Early Classic period, interpreted to reflect a shift from extensive agriculture to intensive, water-conservative maize cultivation that was motivated by a drying climate. Our results imply that agricultural adaptations developed in response to earlier droughts were initially successful, but failed under the more severe droughts of the Terminal Classic period.The decline of the lowland Classic Maya during the Terminal Classic period (800–900/1000 C.E.) is a preeminent example of societal collapse (1), but its causes have been vigorously debated (2–5). Paleoclimate inferences from lake sediment and cave deposits (6–11) indicate that the Terminal Classic was marked by a series of major droughts, suggesting that climate change destabilized lowland Maya society. Most evidence for drought during the Terminal Classic comes from the northern Maya Lowlands (Fig. 1) (6–8, 10), where societal disruption was less severe than in the southern Maya Lowlands (12, 13). There are fewer paleoclimate records from the southern Maya Lowlands, and they are equivocal with respect to the relative magnitude of drought impacts during the Terminal Classic (9, 11, 14). Further, the supposition that hydrological impacts were a primary cause for societal change is often challenged by archaeologists, who stress spatial variability in societal disruption across the region and the complexity of human responses to environmental change (2, 3, 12). The available paleoclimate data, however, do not constrain possible spatial variability in drought impacts (6–11). Arguments for drought as a principal cause for societal collapse have also not considered the potential resilience of the ancient Maya during earlier intervals of climate change (15).Open in a separate windowFig. 1.Map of the Maya Lowlands indicating the distribution of annual precipitation (64) and the location of paleoclimate archives discussed in the text. The locations of modern lake sediment and soil samples (Fig. 2) are indicated by diamonds.For this study, we analyzed coupled proxy records of climate change and ancient land use derived from stable hydrogen and carbon isotope analyses of higher-plant leaf wax lipids (long-chain n-alkanoic acids) in sediment cores from Lakes Chichancanab and Salpeten, in the northern and southern Maya Lowlands, respectively (Fig. 1). Hydrogen isotope compositions of n-alkanoic acids (δD_wax) are primarily influenced by the isotopic composition of precipitation and isotopic fractionation associated with evapotranspiration (16). In the modern Maya Lowlands, δD_wax is well correlated with precipitation amount and varies by 60‰ across an annual precipitation gradient of 2,500 mm (Fig. 2). This modern variability in δD_wax is strongly influenced by soil water evaporation (17), and it is possible that changes in potential evapotranspiration could also impact paleo records. Accordingly, we interpret δD_wax values as qualitative records of water availability influenced by both precipitation amount and potential evapotranspiration. These two effects are complementary, since less rainfall and increased evapotranspiration would lead to both increased δD_wax values and reduced water resources, and vice versa.Open in a separate windowFig. 2.Scatter plot showing the negative relationship between annual precipitation and δD_wax-corr measured in modern lake sediment and soil samples (Fig. 1). Results from Lake Chichancanab (CH) and Salpeten (SP) are indicated. The black line indicates a linear regression fit to these data, with regression statistics reported at the bottom of the plot. Large squares indicate mean values for each sampling region, with error bars indicating SEM in both δD_wax-corr and annual precipitation. The black error bar indicates the 1σ error for δD_wax-corr values (SI Text). Original δD_wax data from ref. 17. VSMOW, Vienna Standard Mean Ocean Water.Plant wax carbon isotope signatures (δ¹³C_wax) in sediments from low-elevation tropical environments, including the Maya lowlands, are primarily controlled by the relative abundance of C₃ and C₄ plants (18–20). Ancient Maya land use was the dominant influence on the relative abundance of C₃ and C₄ plants during the late Holocene, because Maya farmers cleared C₃ plant-dominated forests and promoted C₄ grasses, in particular, maize (21–24). Thus, we apply δ¹³C_wax records as an indicator of the relative abundance of C₄ and C₃ plants that reflects past land use change (SI Text). Physiological differences between plant groups also result in differing δD_wax values between C₃ trees and shrubs and C₄ grasses (16), and we use δ¹³C_wax records to correct for the influence of vegetation change on δD_wax values (25) (δD_wax-corr, SI Text and Fig. S1).Plant waxes have been shown to have long residence times in soils in the Maya Lowlands (26). Therefore, age−depth models for our plant wax isotope records are based on compound-specific radiocarbon ages (Fig. 3), which align our δD_wax records temporally with nearby hydroclimate records derived from other methodologies (26) (SI Text and Fig. S2). The mean 95% confidence range for the compound-specific age−depth models is 230 y at Lake Chichancanab and 250 y at Lake Salpeten. Given these age uncertainties, we focus our interpretation on centennial-scale variability (26). The temporal resolution of our plant wax isotope records is lower than speleothem-derived climate records (8, 9), but combining plant wax records from multiple sites allows comparisons of climate change and land use in the northern and southern Maya Lowlands, which would otherwise not be possible. In addition, plant wax isotope records extend to the Early Preclassic/Late Archaic period (1500–2000 B.C.E.), providing a longer perspective on climate change in the Maya Lowlands than most other regional records (6, 8–11).Open in a separate windowFig. 3.Plant wax (green; left) and terrigenous macrofossil (red; right) age−depth models for (A) Lake Chichancanab and (B) Lake Salpeten. The age probability density of individual radiocarbon analyses is shown. The black lines indicate the best age model based on the weighted mean of 1,000 age model iterations (62). Colored envelopes indicate 95% confidence intervals. Cal, calendar.     

From the Cover: Evidence for superconductivity in Li-decorated monolayer graphene

Monolayer graphene exhibits many spectacular electronic properties, with superconductivity being arguably the most notable exception. It was theoretically proposed that superconductivity might be induced by enhancing the electron–phonon coupling through the decoration of graphene with an alkali adatom superlattice [Profeta G, Calandra M, Mauri F (2012) Nat Phys 8(2):131–134]. Although experiments have shown an adatom-induced enhancement of the electron–phonon coupling, superconductivity has never been observed. Using angle-resolved photoemission spectroscopy (ARPES), we show that lithium deposited on graphene at low temperature strongly modifies the phonon density of states, leading to an enhancement of the electron–phonon coupling of up to λ ? 0.58. On part of the graphene-derived π^?-band Fermi surface, we then observe the opening of a Δ ? 0.9-meV temperature-dependent pairing gap. This result suggests for the first time, to our knowledge, that Li-decorated monolayer graphene is indeed superconducting, with T_c ? 5.9 K.Although not observed in pure bulk graphite, superconductivity occurs in certain graphite intercalated compounds (GICs), with T_c values of up to 11.5 K in the case of CaC₆ (1, 2). The origin of superconductivity in these materials has been identified in the enhancement of electron–phonon coupling induced by the intercalant layers (3, 4). The observation of a superconducting gap on the graphitic π^?-bands in bulk CaC₆ (5) suggests that realizing superconductivity in monolayer graphene might be a real possibility. This prospect has, indeed, attracted intense theoretical and experimental efforts (6–12). In particular, recent density functional theory calculations have suggested that, analogous to the case of intercalated bulk graphite, superconductivity can be induced in monolayer graphene through the adsorption of certain alkali metals (8).Although the Li-based GIC—bulk LiC₆—is not known to be superconducting, Li-decorated graphene emerges as a particularly interesting case with a predicted superconducting T_c of up to 8.1 K (8). The proposed mechanism for this enhancement of T_c is the removal of the confining potential of the graphite C₆ layers, which changes both the occupancy of the Li 2s band (or the ionization of the Li) and its position with respect to the graphene layer. These modifications lead to an increase of the electron–phonon coupling constant from λ = 0.33 to λ = 0.61, in going from bulk to monolayer LiC₆. It has been argued that the LiC₆ monolayer should exhibit the largest values of both λ and T_c among all alkali–metal–C₆ superlattices (8). Nevertheless, although there is thorough experimental evidence for adatom-enhanced electron–phonon coupling in graphene (7, 11, 13), superconductivity has not yet been observed in decorated monolayer graphene.Angle-resolved photoemission spectroscopy (ARPES) measurements of the electronic dispersion of pristine and Li-decorated graphene at 8 K, characterized by the distinctive Dirac cones at the corners of the hexagonal Brillouin zone (Fig. 1E), are shown in Fig. 1 A and B. Li adatoms electron-dope the graphene sheet by charge transfer doping, leading to a shift of the Dirac point to higher binding energies. As evidenced by the evolution of the graphene sheet carrier density in Fig. 1F, this trend begins to saturate after several minutes of Li deposition. Concomitantly, we observe the emergence of a new spectral weight (Fig. 1E) at the Brillouin zone center (the comparison of the Γ-point ARPES dispersion for pristine and 10-min Li-decorated graphene is shown in Fig. 1 C and D). The origin of this spectral weight is probably the Li-2s band expected for this system (8) superimposed with the folded graphene bands caused by a Li superstructure, which were observed in Li and Ca bulk GIC systems (5, 14). This spectral weight, which disappears above  ～ 50 K and is not recovered on subsequent cooling, is associated with the strong enhancement of electron–phonon coupling (discussed later, see Fig. 3 and SI Appendix).Open in a separate windowFig. 1.Charge transfer doping of graphene by lithium adatoms. Dirac-cone dispersion measured by ARPES at 8 K (A) on pristine graphene and (B) after 3 min of Li evaporation along the K-point momentum cut indicated by the white line in the Fermi surface plot in E. The Dirac cone–Fermi surface was measured at this specific K point and then replicated at the other K points by symmetry (note that high-symmetry points are here defined for the Brillouin zone of pristine graphene and not of 3×3R30° reconstructed Li-graphene, which is, instead, the notation in ref. 8). The point at which the spectroscopic gap is studied is indicated by the shaded white circle. The Dirac point, (A) already located below E_F on pristine graphene because of the charge transfer from the SiC substrate, further shifts to higher energies with (B) Li evaporation. The presence of a single well-defined Dirac cone indicates a macroscopically uniform Li-induced doping. (C) Although no bands are present at the Γ-point on pristine graphene, spectral weight is detected on 10-min Li-decorated graphene in D and E. As illustrated in the 8 K sheet carrier density plot vs. Li deposition time in F, which accounts for the filling of the π??? Fermi surface, the spectral weight at Γ is observed for charge densities n_2D ? 9 × 10¹³ cm^-2 (but completely disappears if the sample temperature is raised above  ～ 50 K and is not recovered on subsequent cooling) (SI Appendix).Open in a separate windowFig. 3.Analysis of electron–phonon coupling in Li-decorated graphene. (A) Dirac dispersion from 3-min Li-decorated graphene along the k-space cut indicated in the Fermi surface plot in E that exhibits kink anomalies caused by electron–phonon coupling (white line indicates MDC dispersion). (B–D) MDC dispersion and bare bands obtained from the self-consistent Kramers–Kronig bare-band fitting (KKBF) routine (20, 21) for several Li coverages (Methods and SI Appendix); the real part of the self-energy Σ′ is shown in Right (orange indicates Σ′ from the KKBF routine analysis, and black indicates Σ′ corresponding to the Eliashberg function presented below). (F–H) Eliashberg function α²F(ω) from the integral inversion of Σ′(ω) (22) and electron–phonon coupling constant λ = 2∫dω?α²F(ω)/ω (Methods and SI Appendix); in H, the theoretical results from ref. 8 for a LiC₆ monolayer are also shown (gray shading). (I) Experimentally determined contribution to the total electron–phonon coupling (black circles) from phonon modes in the energy ranges 100–250 meV (blue shading and white circles) and 0–100 meV (orange shading); the coupling of low-energy modes strongly increases with Li coverage.Next, we use high-resolution, low-temperature ARPES to search for the opening of a temperature-dependent pairing gap along the π^?-band Fermi surface as a direct spectroscopic signature of the realization of a superconducting state in monolayer LiC₆. To increase our experimental sensitivity, as illustrated in Fig. 2A, using the approach introduced for FeAs (17) and cuprate (18) superconductors, we perform an analysis of ARPES energy distribution curves (EDCs) integrated in dk along a 1D momentum–space cut perpendicular to the Fermi surface. This method also provides the added benefit that the integrated EDCs can be modeled in terms of a simple Dynes gap function (19) multiplied by a linear background and the Fermi–Dirac distribution, all convolved with a Gaussian resolution function (Methods and Eq. 4). As shown in Fig. 2A and especially, Fig. 2B, for data from the k-space location indicated by the white circles in Figs. 1E and ​and3E,3E, a temperature dependence characteristic of the opening of a pairing gap can be observed near E_F. The leading-edge midpoints of the Li-graphene spectra move away from E_F (Fig. 2B) in cooling from 15 to 3.5 K, which is at variance with the case of Au spectra crossing precisely at E_F according to the Fermi–Dirac distribution (Fig. 2D). Fitting these data with Eq. 4 returns a gap value of Δ = 0.9 ± 0.2 meV at 3.5 K (with Γ ? 0.09 meV). [Note that the parameter Γ in the Dynes fitting function is not treated as a free-fitting parameter, because the broadening of the coherence peaks and filling in of the gap are dominated by the experimental energy resolution. However, setting this parameter to small realistic values (Γ ～ 0.1Δ) improves the fit at the center of the gap (i.e., at E = 0 in the symmetrized data) without affecting the value of the gap itself.] Given its small value compared with the experimental resolution, the gap opening is best visualized in the symmetrized data in Fig. 2C, which minimize the effects of the Fermi function. Finally, we note that the gap appears to be anisotropic and is either absent or below our detection limit along the K ? M direction (SI Appendix, Fig. S4).Open in a separate windowFig. 2.Spectroscopic observation of a pairing gap in Li-decorated graphene. (A) Dirac dispersion from 10-min Li-decorated graphene measured at 15 and 3.5 K at the k-space location indicated by the white circles in Figs. 1E and ​and3E;3E; the temperature dependence is here evaluated for EDCs integrated in the 0.1-Å^-1 momentum region about k_F shown by the white box in Lower, with (Upper) the only changes occurring near E_F. (D) Although Au spectra cross at E_f as described by the Fermi–Dirac distribution, (B) the crossing points of the Li-graphene spectra are shifted away from E_F (cyan dashed line) because of the pull back of the leading edge at 3.5 K. A fit to the Dynes gap equation (Methods) yields a gap of Δ ? 0.9 meV at 3.5 K (and 0 meV at 15 K). The superconducting gap opening is best visualized in the symmetrized data in C [i.e., by taking I(ω) + I(?ω), which minimizes the effects of the Fermi function, even in the case of finite energy and momentum resolutions (15, 16); blue and red symbols in C represent the smoothed data, whereas the light shading gives the rmsds of the raw data]. The qualitatively similar behavior observed on polycrystalline niobium—and returning a superconducting gap Δ ? 1.4 meV—is shown in E and F.The detection of a temperature-dependent anisotropic gap at the Fermi level with a leading-edge profile described by the Dynes function—with its asymmetry about E_F and associated transfer of spectral weight to just below the gap edge—is suggestive of a superconducting pairing gap. The phenomenology would, in fact, be very different in the case of a Coulomb gap, which is typically observed in disordered semiconductors (23–25) because of the combination of disorder with long-range Coulomb interactions. A Coulomb gap would lead to a rigid shift of the spectra leading edge (isotropic in momentum) and result in a vanishing of the momentum-integrated density of states at E_F. Similarly, the observed gap is unlikely to have a charge density wave origin, because the observed gap is tied to the Fermi energy as opposed to a particular high-symmetry wavevector (the latter might occur at the M points, when graphene is doped all of the way to the Van Hove singularity, resulting in a highly nested hexagonal Fermi surface; or the K points, in the case of a 3 ×3 R 30° reconstruction, leading to a Dirac point gap). Finally, we note that these measurements do not allow us to speculate on the precise symmetry of the gap along a single Dirac cone–Fermi surface or the relative phases of the gap on the six disconnected Fermi pockets. As such, our results do not rule out any of the recent proposals for a possible unconventional superconducting order parameter in graphene (9, 26, 27).To further explore the nature of the gap observed on Li-decorated graphene (and also show our ability to resolve a gap of the order of 1 meV), in Fig. 2 E and F, we show as a benchmark comparison the analogous results from a bulk polycrystalline niobium sample—a known conventional superconductor with T_c ? 9.2?K. The Dynes fit of the integrated EDCs Fermi edge in Fig. 2E determines the gap to be Δ = 1.4 ± 0.2 meV (with Γ ? 0.14 meV), in excellent agreement with reported values (28). Although the leading-edge shift (Fig. 2E) and the dip in the symmetrized spectra (Fig. 2F) are more pronounced than for Li-graphene owing to the larger gap, the behavior is qualitatively very similar. This similarity provides additional support to the superconducting origin of the temperature-dependent gap observed in Li-decorated graphene.If the spectroscopic gap observed in Li-graphene is, indeed, a superconducting gap, the responsible mechanism may likely be electron–phonon coupling, which was predicted by the theory for monolayer Li-graphene (8) and also, seen experimentally for the bulk GIC CaC₆ (5). In direct support of this scenario, we present a detailed analysis of the graphene π^?-bands in Fig. 3, showing that the Li-induced enhancement of the electron–phonon coupling is, indeed, sufficient to stabilize a low-temperature superconducting state. Graphene doped with alkali adatoms always shows a strong kink in the π^?-band dispersion at a binding energy of about 160 meV (11). For the Li-graphene studied here, the same effect is seen in the momentum distribution curve (MDC) dispersions and the corresponding real part of the self-energy Σ′ in Fig. 3 B–D. This structure stems from the coupling to carbon in-plane (C_xy) phonons (4, 8). Despite the apparent strength of this kink, the interaction with these phonon modes contributes little to the overall coupling parameter because of their high energy (note that ω is a weighting factor in the integral calculation of λ) (Methods). As illustrated by the white circles in Fig. 3I, the contribution to λ from these high-energy (100–200 meV) modes is determined to be 0.14 ± 0.05, and it remains approximately constant for all Li coverages studied here. This value is, however, too small to stabilize a superconducting state in this system (8, 11).With increasing Li coverage and the appearance of the spectral weight at Γ, significant modifications to the low-energy part of the dispersion ( ? 100 meV) become apparent (Fig. 3 B–D). With 10 min of Li deposition (Fig. 3D), an additional kink is visible at a binding energy of ∼30 meV along with the associated peak in the real part of the self-energy Σ′. The extracted (Methods) Eliashberg functions and energy-resolved λ(ω) in Fig. 3 F–H show that, at high Li coverage, phonon modes at energies below 60 meV are coupling strongly to the graphene electronic excitations. The phonon modes in this energy range are of Li in-plane (Li_xy) and C out-of-plane (C_z) character (4, 8). This assignment is in agreement with predictions (8) as shown by the direct comparison between theory and experiment in Fig. 3H. [As for the theoretical and experimental Eliashberg functions α²F(k, ω) in Fig. 3H, the agreement may, at first glance, appear not as good as the one for λ(ω). We note, however, that, in this regard, the relevant information is in the macroscopic energy distribution of the α²F(k, ω) weight rather than in its detailed structure.] As for the total electron–phonon coupling λ for each coverage (black circles in Fig. 3I), our values measured on the π^?-band Fermi surface at an intermediate location between Γ ? K and K ? M directions (Fig. 3E) provide an effective estimate for the momentum-averaged coupling strength. [The electron–phonon coupling parameter increases monotonically along the π^?-band Fermi surface in going from the Γ ? K to the K ? M direction as observed in both decorated graphene (11) and intercalated graphite (29). Empirically, the value measured at the intermediate Fermi crossing corresponds to the momentum-averaged coupling strength along the π^?-band Fermi surface.] Remarkably, the value λ = 0.58 ± 0.05 observed at the highest Li coverage (Fig. 3I) is comparable with λ = 0.61 predicted for monolayer LiC₆ (8) as well as λ ? 0.58 observed for bulk CaC₆ (29)—it is, thus, large enough for inducing superconductivity in Li-decorated graphene. It is also significantly larger than the momentum-averaged results previously reported for both Li and Ca depositions on monolayer graphene [λ ? 0.22 and λ ? 0.28, respectively (11)]. We note that achieving such a large λ-value is critically dependent on the presence of the spectral weight observed at Γ when Li is deposited on graphene at low temperatures, presumably forming an ordered structure on the surface and not intercalating. As shown in SI Appendix, we find λ = 0.13 ± 0.05 after the same sample is annealed at 60 K for several minutes, destroying the Li order and associated Γ-spectral weight.Taken together, our ARPES study of Li-decorated monolayer graphene provides evidence for the presence of a temperature-dependent pairing gap on part of the graphene-derived π^? Fermi surface. The detailed evolution of the density of states at the gap edge as well as the phenomenology analogous to the one of known superconductors, such as Nb—as well as CaC₆ and NbSe₂, which also show a similarly anisotropic gap around the K point (30–34)—indicate that the pairing gap observed at 3.5 K in graphene is most likely associated with superconductivity. Based on the Bardeen–Cooper–Schrieffer gap equation, Δ = 3.5?k_b?T_c, we estimate a superconducting transition temperature T_c ? 5.9 K, remarkably close to the value of 8.1 K found in density functional theory calculations (8). This work constitutes the first, to our knowledge, experimental realization of superconductivity in graphene—the most prominent electronic phenomenon still missing among the remarkable properties of this single layer of carbon atoms.     

Universal features in the photoemission spectroscopy of high-temperature superconductors

The energy gap for electronic excitations is one of the most important characteristics of the superconducting state, as it directly reflects the pairing of electrons. In the copper–oxide high-temperature superconductors (HTSCs), a strongly anisotropic energy gap, which vanishes along high-symmetry directions, is a clear manifestation of the d-wave symmetry of the pairing. There is, however, a dramatic change in the form of the gap anisotropy with reduced carrier concentration (underdoping). Although the vanishing of the gap along the diagonal to the square Cu–O bond directions is robust, the doping dependence of the large gap along the Cu–O directions suggests that its origin might be different from pairing. It is thus tempting to associate the large gap with a second-order parameter distinct from superconductivity. We use angle-resolved photoemission spectroscopy to show that the two-gap behavior and the destruction of well-defined electronic excitations are not universal features of HTSCs, and depend sensitively on how the underdoped materials are prepared. Depending on cation substitution, underdoped samples either show two-gap behavior or not. In contrast, many other characteristics of HTSCs, such as the dome-like dependence of on doping, long-lived excitations along the diagonals to the Cu–O bonds, and an energy gap at the Brillouin zone boundary that decreases monotonically with doping while persisting above (the pseudogap), are present in all samples, irrespective of whether they exhibit two-gap behavior or not. Our results imply that universal aspects of high- superconductivity are relatively insensitive to differences in the electronic states along the Cu–O bond directions.Elucidating the mechanism of high-temperature superconductivity in the copper–oxide materials remains one of the most challenging open problems in physics. It has attracted the attention of scientists working in fields as diverse as materials science, condensed matter physics, cold atoms, and string theory. To clearly define the problem of high-temperature superconductors (HTSCs), it is essential to establish which of the plethora of observed features are universal, namely, qualitatively unaffected by material-specific details.An important early result concerns the universality of the symmetry of the order parameter for superconductivity. The order parameter was found to change sign under a 90° rotation (1, 2), which implies that the energy gap must vanish along the diagonal to the Cu–O bonds, i.e., the Brillouin zone diagonal. This sign change is consistent with early spectroscopic studies of near-optimally-doped samples (those with the highest in a given family), where a energy gap (3, 4) was observed (ϕ being the angle from the Cu–O bond direction), the simplest functional form consistent with d-wave pairing. More recently, there is considerable evidence (5–8) that, with underdoping, the anisotropy of the energy gap deviates markedly from the simple form. Although the gap node at is observed at all dopings, the gap near the antinode (near and 90°) is significantly larger than that expected from the simplest d-wave form. Further, the large gap continues to persist in underdoped (UD) materials as the normal-state pseudogap (9–11) above . This suggests that the small (near-nodal) and large (antinodal) gaps are of completely different origin, the former related to superconductivity and the latter to some other competing order parameter.This two-gap picture has attracted much attention (8), raising the possibility that multiple energy scales are involved in the HTSC problem. There is mounting evidence for additional broken symmetries (12–14) in UD cuprates, once superconductivity is weakened upon approaching the Mott insulating state. The central issue is the role of these additional order parameters in impacting the universal properties of high- superconductivity.In this paper we use angle-resolved photoemission (ARPES) to examine the universality of the two-gap scenario in HTSCs by addressing the following questions. To what extent are the observed deviations from a simple d-wave energy gap independent of material details? How does the observed gap anisotropy correlate, as a function of doping, with other spectroscopic features such as the size of the antinodal gap, and the spectral weights of the nodal and antinodal quasiparticle excitations?We systematically examine the electronic spectra of various families of cation-substituted Bi₂Sr₂CaCu₂O_8+δ single crystals as a function of carrier concentration to elucidate which properties are universal and which are not. We present ARPES data on four families of float-zone-grown Bi₂Sr₂CaCu₂O_8+δ single crystals, where was adjusted by both oxygen content and cation doping. As-grown samples, labeled Bi2212, have an optimal of 91 K. These crystals were UD to by varying the oxygen content. Ca-rich crystals (grown from material with a starting composition Bi_2.1Sr_1.4Ca_1.5Cu₂O_8+δ) with an optimal of 82 K are labeled Ca. Two Dy-doped families grown with starting compositions Bi_2.1Sr_1.9Ca_{1 − x}Dy_xCu₂O_8+δ with x = 0.1 and 0.3 are labeled Dy1 and Dy2, respectively. A full list of the samples used and their determined from magnetization measurements are shown in SI Text, where we also show high-resolution X-ray data that give evidence for the excellent structural quality of our samples.Our main result is that the Dy1 and Dy2 samples show clear evidence of a two-gap behavior in the UD regime , with loss of coherent quasiparticles in the antinodal region of k space where the gap deviates from a simple d-wave form. In marked contrast, the UD Bi2212 samples and the Ca samples show a simple d-wave gap in the superconducting state and sharp quasiparticles over the entire Fermi surface in a similar range of the UD regime. We conclude by discussing the implications of the nonuniversality of the two-gap behavior for the phenomenon of high superconductivity.We begin our comparison of the various families of samples by focusing in Fig. 1 on the superconducting state antinodal spectra as a function of underdoping. The antinode is the Fermi momentum k_F on the Brillouin zone boundary, where the energy gap is a maximum and, as we shall see, the differences between the various samples are the most striking. We show data at optimal doping, corresponding to the highest in each family, in Fig. 1A. Increasing Dy leads to a small suppression of the optimal compared with Bi2212, together with an increase in the antinodal gap and a significant reduction of the quasiparticle weight. This trend continues down to moderate underdoping, as seen in Fig. 1B, where we show UD Bi2212 and Dy2 samples with very similar . For more severely UD samples, with , spectral changes in the Dy-substituted samples are far more dramatic. In Fig. 1C, we see that quasiparticle peaks in the Dy samples are no longer visible, even well below , consistent with earlier work on Y-doped Bi2212 and also Bi2201 and La_1.85Sr_0.15CuO₄ (5, 15–18). In contrast, Bi2212 and Ca-doped samples with comparable continue to exhibit quasiparticle peaks. In this respect the latter two are similar to epitaxially grown thin-film samples that exhibit quasiparticle peaks all of the way down to the lowest (19).Open in a separate windowFig. 1.Superconducting state antinodal ARPES spectra. We use the label “Bi2212” for samples without cation doping, “Dy1” for 10% Dy, “Dy2” for 30% Dy, and “Ca” for Ca-doped samples. The temperature is indicated along with . OP denotes optimal doped, UD underdoped, and OD overdoped samples. (A) Antinodal spectra for OP samples of three different families: Bi2212 (blue), Dy1 (green), and Dy2 (red), showing an increase in gap and a decrease in quasiparticle weight with increasing Dy content. (B) Antinodal spectra for UD samples with similar (≃66 K) for Bi2212 (blue) and Dy2 (red). As in A, there is a larger gap and smaller coherent weight in the Dy-substituted sample. (C) Same as in B, but for four UD samples with near 55 K for Bi2212 (dark blue), Ca (light blue), Dy1 (green), and Dy2 (red). The Bi2212 and Ca spectra are very similar to each other and quite different from those of the Dy1 and Dy2 materials. (D) Doping evolution of the antinodal spectra of four Dy1 samples from OP to UD . (E) Doping evolution of the antinodal spectra of four Dy2 samples from OP to UD . We see in D and E the sudden loss of quasiparticle weight for below 60 K. (F) Doping evolution of the antinodal spectra of three Bi2212 samples and three Ca samples, showing well-defined quasiparticle peaks in all cases.A significant feature of the highly UD Dy samples in Fig. 1C is that, in addition to the strong suppression of the quasiparticle peak, there is severe loss of low-energy spectral weight. To clearly highlight this, we show the doping evolution of antinodal spectra for the Dy1 (Fig. 1D) and Dy2 (Fig. 1E) samples. These observations are in striking contrast with the Bi2212 and Ca-doped data in Fig. 1F, where we do see a systematic reduction of the quasiparticle peak with underdoping, but not a complete wipeout of the low-energy spectral weight. To the extent that the superconducting state peak–dip–hump line shape (20, 21) originates from one broad normal-state spectral peak, the changes in spectra of the Dy materials are not simply due to a loss of coherence, but more likely a loss of the entire spectral weight near the chemical potential.The doping evolution of the k-dependent gap is illustrated in Figs. 2 and​and 3. 3. In Fig. 2 we contrast the optimally doped Dy1 (T_c = 86 K) sample (Fig. 2 A and B) with a severely UD Dy1 (T_c = 38 K) sample (Fig. 2 C and D ), the spectra being particle–hole-symmetrized to better illustrate the gap. The OP 86 K sample shows a well-defined quasiparticle peak over the entire Fermi surface (Fig. 2A) with a simple d-wave gap of the form (blue curve in Fig. 2B). For the UD 38 K sample, we see in Fig. 2C well-defined quasiparticles near the node (red spectra), but not near the antinode (blue spectra). The near-nodal gaps (red triangles in Fig. 2D) are obtained from the energy of quasiparticle peaks and continue to follow a d-wave gap (blue curve in Fig. 2D). However, once the quasiparticle peak is lost closer to the antinode, one has to use some other definition of the gap scale. We identify a break in the slope of the spectrum, by locating the energy scale at which it deviates from the black straight lines (Fig. 2C), which leads to the gap estimates (blue squares) in Fig. 2D.Open in a separate windowFig. 2.Superconducting state spectra and energy gap for OD and highly UD Dy1 samples. (A) Symmetrized spectra at k_F, from the antinode (Upper) to the node (Lower) for an OP 86 K Dy1 sample. (B) Gap as a function of Fermi surface angle (0° is the antinode and 45° the node). The blue curve is a d-wave fit to the data. (C) Same as A for an UD 38 K Dy1 sample. Curves, near the node, with discernible quasiparticle peaks are shown in red; those near the antinode are shown in blue. (D) Gap along the Fermi surface from data of C.Open in a separate windowFig. 3.Energy gap anisotropies of various samples. (A) OD 79 K Ca (where ); (B) UD 54 K Ca; (C) OP 81 K Dy2; and (D) UD 59 K Dy2. The two near-optimal samples in A and C both show a simple d-wave gap. This behavior persists in the UD Ca sample of B, but the UD Dy2 sample of D has a two-gap behavior despite having a similar to the UD Ca sample.Despite the larger error bar associated with gap scale extraction in the absence of quasiparticles, it is nevertheless clear (Fig. 2D) that the UD 38 K Dy1 sample has an energy gap that deviates markedly from the simple d-wave form. This observation is called two-gap in the UD regime, in contrast with a single gap near optimality (Fig. 2B). It is easy to observe from Fig. 2 that the Fermi surface angle at which the energy gap starts to deviate from the form matches the one at which the spectral peak gets washed out. This is very similar to the two-gap behavior demonstrated in refs. 5, 15–18. From this, one might conclude that two-gap behavior is directly correlated with a loss of well-defined quasiparticle excitations in the antinodal region. However, we point to recent ARPES data on Y-doped Bi2212 (6, 7), where two-gap behavior has been observed despite the presence of small antinodal quasiparticle peaks.We next show that the two-gap behavior is not a universal feature of all UD samples. To make this point, we compare in Fig. 3 the gap anisotropies of the Ca-doped samples (Fig. 3 A and B) with the Dy2 samples (Fig. 3 C and D) with essentially identical , where both families have the same optimal . The near-optimal samples, OD 79 K Ca (Fig. 3A) and OP 81 K Dy2 (Fig. 3C) samples, both have a simple d-wave anisotropy (although different maximum gap values at the antinode). However, upon underdoping to similar values, the two have markedly different gap anisotropies. The UD 59 K Dy2 sample (Fig. 3D) shows two-gap behavior, and an absence of quasiparticles near the antinode (similar to the discussion in connection with Fig. 2 above). However, the UD 54 K Ca sample (Fig. 3B) continues to exhibit sharp spectral peaks and a single-gap, despite a very similar as the UD 59 K Dy2.Having established the qualitative differences in the gap anisotropies for various samples as a function of underdoping, we next summarize in Fig. 4 the doping evolution of various spectroscopic features. Instead of estimating the carrier concentration in our samples using an empirical equation (22) (that may or may not be valid for various cation substitutions), we prefer to use the measured to label the doping. In Fig. 4A we show the doping evolution of the antinodal energy gap, which is consistent with the known increase in the gap with underdoping.Open in a separate windowFig. 4.Antinodal gaps and quasiparticle weights. (A) Antinodal energy gap as a function of doping for various samples is seen to grow monotonically with underdoping. Here, and in B and C, the doping is characterized by the measured quantity , with UD samples shown to the left of and OD samples to the right. All results are at temperatures well below . (B) Coherent spectral weight for antinodal quasiparticles as a function of doping. Dy-doped samples exhibit a rapid suppression of this weight to zero for UD , whereas the Ca-doped samples show robust antinodal peaks even for . (C) Coherent spectral weight for nodal quasiparticles as a function of doping, which is seen to be much more robust than the antinodal one.The coherent spectral weight Z for antinodal quasiparticles is plotted in Fig. 4B (for details on the procedure used to estimate this weight, from a ratio of spectral areas, see SI Text). The Dy1 and Dy2 samples both show a sudden and complete loss of Z with underdoping (23), which coincides with the appearance of two-gap behavior. In marked contrast with the Dy samples, the Bi2212 and Ca samples that exhibit a single d-wave gap show a gradual drop in the antinodal Z. On the other hand, we find that the nodal excitations are much less sensitive to how the sample is UD compared with the antinodal ones. Similar sharp nodal excitations have been observed in Dy-doped Bi2212 samples in ref. 7 as well. The nodal quasiparticle weight Z in Fig. 4C decreases smoothly with underdoping for all families of samples, as expected for a doped Mott insulator (24).The two-gap behavior and the attendant loss of quasiparticle weight near the antinode imply a nodal–antinodal dichotomy, aspects of which have been recognized in k space (25–27) and in real space (28–30). Two possible, not mutually exclusive, causes of this behavior are disorder and competing orders.It is known that antinodal states are much more susceptible to impurity scattering, whereas near-nodal excitations are protected (31). However, it is not a priori clear why certain cation substitutions (Dy) should lead to more electronic disorder than others (Ca). As shown by our X-ray studies in SI Text, there is no difference in the structural disorder in Dy and Ca samples. One possibility is that Dy has a local moment, but there is no direct experimental evidence for this.The two-gap behavior in UD materials, with a large antinodal gap that persists above , is suggestive of an order parameter, distinct from d-wave superconductivity, which sets in at the pseudogap temperature . There are several experiments (12–14) that find evidence for a broken symmetry at . However, it is not understood how the observed small, and often subtle, order parameter(s) could lead to large antinodal gaps of , with a loss of spectral weight over a much larger energy range (Fig. 1 D and E).We now discuss the pertinence of competing order parameters based on our measurements. First, in our ARPES data, we have not found any direct evidence for density wave ordering (say, from zone folding). Second, our X-ray data did not provide any signature for additional diffraction peaks expected for long-range density wave ordering. However, none of these null results provide definitive evidence for the absence of a density wave ordering, particularly if it were short range. In contrast, in previously published work (5, 15–18), two-gap behavior has been conjectured to be a direct consequence of phase competition between d-wave superconductivity and some type of density wave ordering. As we have demonstrated, two-gap behavior in and of itself is a sample-specific issue and hence, even if we assume a linkage between competing order and two-gap behavior, it cannot be central to the question of superconductivity in HTSC systems.Whatever the mechanism leading to qualitatively different gap anisotropies for the UD Dy and Ca samples, it only produces relatively small, quantitative changes in key aspects of these materials, such as the dependence of on doping, the presence of sharp nodal quasiparticles, and the pseudogap. We thus conclude that antinodal states do not make a substantial contribution to the universal features of HTSCs. Clearly, two gaps are not necessary for high-temperature superconductivity.     

Conjugated polymers based on metalla-aromatic building blocks

Conjugated polymers usually require strategies to expand the range of wavelengths absorbed and increase solubility. Developing effective strategies to enhance both properties remains challenging. Herein, we report syntheses of conjugated polymers based on a family of metalla-aromatic building blocks via a polymerization method involving consecutive carbyne shuttling processes. The involvement of metal d orbitals in aromatic systems efficiently reduces band gaps and enriches the electron transition pathways of the chromogenic repeat unit. These enable metalla-aromatic conjugated polymers to exhibit broad and strong ultraviolet–visible (UV–Vis) absorption bands. Bulky ligands on the metal suppress π–π stacking of polymer chains and thus increase solubility. These conjugated polymers show robust stability toward light, heat, water, and air. Kinetic studies using NMR experiments and UV–Vis spectroscopy, coupled with the isolation of well-defined model oligomers, revealed the polymerization mechanism.

Conjugated polymers are macromolecules usually featuring a backbone chain with alternating double and single bonds (1–3). These characteristics allow the overlapping p-orbitals to form a system with highly delocalized π-electrons, thereby giving rise to intriguing chemical and physical properties (4–6). They have exhibited many applications in organic light-emitting diodes, organic thin film transistors, organic photovoltaic cells, chemical sensors, bioimaging and therapies, photocatalysis, and other technologies (7–10). To facilitate the use of solar energy, tremendous efforts have been devoted in recent decades to developing previously unidentified conjugated polymers exhibiting broad and strong absorption bands (11–13). The common strategies for increasing absorption involve extending π-conjugation by incorporating conjugated cyclic moieties, especially fused rings; modulating the strength of intramolecular charge transfer between donor and acceptor units (D–A effect); increasing the coplanarity of π conjugation through weak intramolecular interactions (e.g., hydrogen bonds); and introducing heteroatoms or heavy atoms into the repeat units of conjugated polymers (11–16). Additionally, appropriate solubility is a prerequisite for processing and using polymers and is usually achieved with the aid of long alkyl or alkoxy side chains (12, 17).Aromatic rings are among the most important building blocks for conjugated polymers. In addition to aromatic hydrocarbons, a variety of aromatic heterocycles composed of main-group elements have been used as fundamental components. These heteroatom-containing conjugated polymers show unique optical and electronic properties (4–10). However, while metalla-aromatic systems bearing a transition metal have been known since 1979 due to the pioneering work by Thorn and Hoffmann (18), none of them have been used as building blocks for conjugated polymers. The HOMO–LUMO gaps (E_g) of metalla-aromatics are generally narrower (Fig. 1) than those of their organic counterparts (19–22). We reasoned that this feature should broaden the absorption window if polymers stemming from metalla-aromatics are achievable.Open in a separate windowFig. 1.Comparison of traditional organic skeletons with metalla-aromatic building blocks (the computed energies are in eV). (A) HOMO–LUMO gaps of classic aromatic skeletons. (B) Carbolong frameworks as potential building blocks for novel conjugated polymers with broad absorption bands and improved solubility.In recent years, we have reported a series of readily accessible metal-bridged bicyclic/polycyclic aromatics, namely carbolong complexes, which are stable in air and moisture (23–25). The addition of osmium carbynes (in carbolong complexes) and alkynes gave rise to an intriguing family of d_π–p_π conjugated systems, which function as excellent electron transport layer materials in organic solar cells (26, 27). These observations raised the following question: Can this efficient addition reaction be used to access metalla-aromatic conjugated polymers? It is noteworthy that incorporation of metalla-aromatic units into conjugated polymers is hitherto unknown. In this contribution, we disclose a polymerization reaction involving M≡C analogs of C≡C bonds, which involves a unique carbyne shuttling strategy (Fig. 2A). This led to examples of metalla-aromatic conjugated polymers (polycarbolongs) featuring metal carbyne units in the main chain. On the other hand, the development of polymerization reactions plays a crucial role in involving certain building blocks in conjugated polymers (28–32). These efficient, specific, and feasible polymerizations could open an avenue for the synthesis of conjugated polymers.Open in a separate windowFig. 2.Design of polymers and synthesis of monomers. (A) Schematic illustration of the polymerization strategy. (B) Preparation of carbolong monomers. Insert: X-ray molecular structure for the cations of complex 3. Ellipsoids are shown at the 50% probability level; phenyl groups in PPh₃ are omitted for clarity.     

Rapid seafloor changes associated with the degradation of Arctic submarine permafrost

Repeated high-resolution bathymetric surveys of the shelf edge of the Canadian Beaufort Sea during 2- to 9-y-long survey intervals reveal rapid morphological changes. New steep-sided depressions up to 28 m in depth developed, and lateral retreat along scarp faces occurred at multiple sites. These morphological changes appeared between 120-m and 150-m water depth, near the maximum limit of the submerged glacial-age permafrost, and are attributed to permafrost thawing where ascending groundwater is concentrated along the relict permafrost boundary. The groundwater is produced by the regional thawing of the permafrost base due to the shift in the geothermal gradient as a result of the interglacial transgression of the shelf. In contrast, where groundwater discharge is reduced, sediments freeze at the ambient sea bottom temperature of ∼−1.4 °C. The consequent expansion of freezing sediment creates ice-cored topographic highs or pingos, which are particularly abundant adjacent to the discharge area.

The effects of on-going terrestrial permafrost degradation (1–3) have been appraised by comparison of sequential images of Arctic landscapes that show geomorphic changes attributed primarily to thermokarst activity induced by recent atmospheric warming and ongoing natural periglacial processes (4–8). While the existence of extensive relict submarine permafrost on the continental shelves in the Arctic has been known for years (9, 10), the dynamics of submarine permafrost growth and decay and consequent modifications of seafloor morphology are largely unexplored.Throughout the Pleistocene, much of the vast continental shelf areas of the Arctic Ocean experienced marine transgressions and regressions associated with ∼125-m global sea level changes (11). Extensive terrestrial permafrost formed during sea-level low stands when the mean annual air temperatures of the exposed shelves were less than −15 °C (11, 12). Exploration wells drilled on the continental shelf in the Canadian Beaufort Sea show that relict terrestrial permafrost occurs in places to depths >600 m below seafloor (mbsf) and forms a seaward-thinning wedge beneath the outer shelf (10, 13, 14) (Fig. 1 A and B). The hydrography of the Canadian Beaufort Sea slows the degradation of the relict permafrost because a cold-water layer with temperatures usually near -1.4 °C blankets the seafloor from midshelf depths down to ∼200-m water depth (mwd) (15, 16) (Fig. 1B). As the freezing point temperature of interstitial waters is also controlled by salinity and sediment grain size, partially frozen sediments occur in a zone delimited by the ∼−2 °C and 0 °C isotherms (17, 18) (Fig. 1B).Open in a separate windowFig. 1.Map and cross-section showing the relationship between shelf edge morphology and the subsurface thermal structure along the shelf edge in the Canadian Beaufort Sea. (A) Shows the location of the study area with respect to estimates of submarine permafrost density (see key) and thickness, modified after 14. Thin contours indicate permafrost thickness in meters. Thicker contour is 120-m isobath marking the shelf edge. Area of repeat mapping coverage shown in Fig. 2 is indicated with a red box. (B) Shows a schematic cross-section with contours of selected subsurface isotherms modified after 15 along line x-x’ in A. The dotted blue line illustrates a thermal minimum (T-min) running through the relict permafrost isotherm and Beaufort Sea waters (16). Green shading indicates relict permafrost. Turquoise arrows show inferred flow of water from permafrost thawing along the base of the relict permafrost to the seafloor. The brown area indicates the zone where relict Pleistocene permafrost is predicted to have thawed with consequent movement of liberated groundwater, associated latent heat transfer and thaw consolidation causing surface settlement. Dashed brown lines define the subbottom limits for methane hydrate stability zone (MHSZ) which starts at ∼240 m below the sea surface and extends into the subsurface depending on the pressure and temperature gradient. The red box indicates the area shown in more detail in C with the same color scheme. The area of denuded seafloor in C is flanked by PLFs (dark-blue fill). Red arrows indicate the direction of heat transfer along the seaward edge of relict permafrost wedge.Distinctive surface morphologies characterize terrestrial permafrost areas. Conical hills (3 to 100 m in diameter) called pingos are common in the Arctic (19, 20). Pingos are formed due to freezing of groundwater. They characteristically contain lenses of nearly pure ground ice that cause heaving of the ground surface. Positive relief features with similar dimensions, referred to as pingo-like features (PLFs), are scattered across the Canadian Beaufort shelf (21, 22). On land, permafrost thawing, where there is ground ice in excess of the sediment pore space, can induce sediment consolidation (23), and surface subsidence results in widespread thermokarst landforms. Among the more dramatic occurrences are retrogressive thaw slumps (4–8, 24). These form where ice-rich permafrost experiences surface thaw causing thaw settlement and release of liquified sediment flows. Because of the loss of volume associated with thawing of massive ground ice, thaw slumps can quickly denude permafrost landscapes.During the first systematic multibeam mapping surveys in 2010 covering part of the shelf edge and slope in the Canadian Beaufort Sea, a band of unusually rough seafloor morphology between ∼120 and ∼200 mwds (25) was discovered along a ∼95-km-long stretch of the shelf. Subsequently, three additional multibeam surveys covering small characteristic areas (Fig. 2A) were conducted to understand the processes responsible for the observed morphologies. Here, we document the unique morphologies and seafloor change in this area and explore how the seafloor features may be related to subsea permafrost degradation and formation.Open in a separate windowFig. 2.(A) Shows bathymetry of a small section of the shelf edge indicated in Fig. 1A, with a color scale going from white (128 m) to blue (200 m) and contours at 120, 140, 170, and 200 mbsf. Outlines of areas resurveyed in 2013 (blue), 2017 (turquoise), and 2019 (green) are superimposed on the 2019 and regional 2010 survey. Colored symbols indicate locations of cores with porewater data using same key as Fig. 5B. The red star indicates the location of a temperature tripod deployed in the period 2015 to 2016. The location of ROV dive tracks (blue paths) are indicated. (B) Covers the same area as A with polygons identifying sites where changes were noted between surveys as follows: 2010 to 2013 (green), 2013 to 2017 (purple), 2017 to 2019 (black), and 2010 and 2019 (red). (C) Shows the same area, colored according to the difference in bathymetry between the 2019 survey and an idealized smooth surface extending between the top of the shelf edge scarp and the layered sediments occurring between the numerous PLFs. This is used to estimate the volume of material that eroded assuming the earlier Holocene seafloor corresponded with this idealized surface. Three zones of topography are labeled. Red boxes are locations of Figs. 3 and ​and5.5. (D) Shows Chirp profiles with the position of profiles shown in C and Fig. 5A. Light-green backdrop in X-X’ indicates possible void produced by retrogressive slide retreat used to calculated volume loss. Also indicated are TL, tilted layers; P, pingo-like-feature; and DR, diffuse reflector.     

North American tree migration paced by climate in the West,lagging in the East

Tree fecundity and recruitment have not yet been quantified at scales needed to anticipate biogeographic shifts in response to climate change. By separating their responses, this study shows coherence across species and communities, offering the strongest support to date that migration is in progress with regional limitations on rates. The southeastern continent emerges as a fecundity hotspot, but it is situated south of population centers where high seed production could contribute to poleward population spread. By contrast, seedling success is highest in the West and North, serving to partially offset limited seed production near poleward frontiers. The evidence of fecundity and recruitment control on tree migration can inform conservation planning for the expected long-term disequilibrium between climate and forest distribution.

Effective planning for the redistribution of habitats from climate change will depend on understanding demographic rates that control population spread at continental scales. Mobile species are moving, some migrating poleward (1, 2) and/or upward in elevation (3, 4). Species redistribution is also predicted for sessile, long-lived trees that provide the resource and structural foundation for global forest biodiversity (5–7), but their movement is harder to study. Contemporary range shifts are recognized primarily where contractions have followed extensive die-backs (8) or where local changes occur along compact climate gradients in steep terrain (9, 10). Whether migration capacity can pace habitat shifts of hundreds of kilometers on decade time scales depends on seed production and juvenile recruitment (Fig. 1A), which have not been fitted to data in ways that can be incorporated in models to anticipate biogeographic change (11–13). For example, do the regions of rapid warming coincide with locations where species can produce abundant seed (Fig. 1B)? If so, does seed production translate to juvenile recruitment? Here, we combine continent-wide fecundity estimates from the Masting Inference and Forecasting (MASTIF) network (13) with tree inventories to identify North American hotspots for recruitment and find that species are well-positioned to track warming in the West and North, but not in parts of the East.Open in a separate windowFig. 1.Transitions, hypothesized effects on spread, and sites. (A) Population spread from trees (BA) to new recruits is controlled by fecundity (seed mass per BA) followed by recruitment (recruits per seed mass). (B) The CTH that warming has stimulated fecundity ahead of the center of adult distributions, which reflect climate changes of recent decades. Arrows indicate how centroids from trees to fecundity to recruitment could be displaced poleward with warming climate. (C) The RSH that cold-sensitive fecundity is optimal where minimum temperatures are warmer than for adult trees and, thus, may slow northward migration. The two hypotheses are not mutually exclusive. B and C refer to the probability densities of the different life stages. (D) MASTIF sites are summarized in SI Appendix, Table S2.2 by eco-regions: mixed forest (greens), montane (blues), grass/shrub/desert (browns), and taiga (blue-green).Suitable habitats for many species are projected to shift hundreds of kilometers in a matter of decades (14, 15). While climate effects on tree mortality are increasingly apparent (16–19), advances into new habitats are not (20–23). For example, natural populations of Pinus taeda may be sustained only if the Northeast can be occupied as habitats are lost in the South (Fig. 2). Current estimates of tree migration inferred from geographic comparisons of juvenile and adult trees have been inconclusive (2, 7, 21, 24, 25). Ambiguous results are to be expected if fecundity and juvenile success do not respond to change in the same ways (20, 26–29). Moreover, seedling abundances (7, 30) do not provide estimates of recruitment rates because seedlings may reside in seedling banks for decades, or they may turn over annually (31–33). Another method based on geographic shifts in population centers calculated from tree inventories (3, 34) does not separate the effects of mortality from recruitment, i.e., the balance of losses in some regions against gains in others. The example in Fig. 2 is consistent with an emerging consensus that suitable habitats are moving fast (2, 14, 15), even if population frontiers are not, highlighting the need for methods that can identify recruitment limitation on population spread. Management for forest products and conservation goals under transient conditions can benefit from an understanding of recruitment limitation that comes from seed supply, as opposed to seedling survival (35).Open in a separate windowFig. 2.Suitable habitats redistribute with decade-scale climate change for P. taeda (BA units m² /ha). (Suitability is not a prediction of abundance, but rather, it is defined for climate and habitat variables included in a model, to be modified by management and disturbance [e.g., fire]. By providing habitat suitability in units of BA, it can be related it to the observation scale for the data.) Predictive distributions for suitability under current (A) and change expected from mid-21^st-century climate scenario Representative Concentration Pathway 4.5 (B) showing habitat declines in the Southwest and East. Specific climate changes important for this example include net increases in aridity in the southeast (especially summer) and western frontier and warming to the North. Occupation of improving habitats depends on fecundity in northern parts of the range and how it is responding. Obtained with Generalized Joint Attribute Modeling (see Materials and Methods for more information).We hypothesized two ways in which fecundity and recruitment could slow or accelerate population spread. Contemporary forests were established under climates that prevailed decades to centuries ago. These climate changes combine with habitat variables to affect seeds, seedlings, and adults in different ways (36, 37). The “climate-tracking hypothesis” (CTH) proposes that, after decades of warming and changing moisture availability (Fig. 3 A and B), seed production for many species has shifted toward the northern frontiers of the range, thus primed for poleward spread. “Fecundity,” the transition from tree basal area (BA) to seed density on the landscape (Fig. 1A), is taken on a mass basis (kg/m² BA) as a more accurate index of reproductive effort than seed number (38, 39). “Recruitment,” the transition from seed density to recruit density (recruits per kg seed), may have also shifted poleward, amplifying the impact of poleward shifts in fecundity on the capacity for poleward spread (Fig. 1B). Under CTH, the centers for adult abundance, fecundity, and recruitment are ordered from south to north in Fig. 1B as might be expected if each life-history stage leads the previous stage in a poleward migration.Open in a separate windowFig. 3.Climate change and tracking. (A) Mean annual temperatures since 1990 have increased rapidly in the Southwest and much of the North. (Zero-change contour line is in red.) (B) Moisture deficit index (monthly potential evapotranspiration minus P summed over 12 mo) has increased in much of the West. (Climate sources are listed in SI Appendix.) (C) Fecundity (kg seed per BA summed over species) is high in the Southeast. (D) Recruits per kg seed (square-root transformed) is highest in the Northeast. (E and F) Geographic displacement of 81 species show transitions in Fig. 1A, as arrows from centroids for adult BA to fecundity (E) and from fecundity to recruitment (F). Blue arrows point north; red arrows point south. Consistent with the RSH (Fig. 1B), most species centered in the East and Northwest have fecundity centroids south of adult distributions (red arrows in E). Consistent with the CTH, species of the interior West have fecundity centroids northwest of adults (blue arrows). Recruitment is shifted north of fecundity for most species (blue arrows in F). SI Appendix, Fig. S2 shows that uncertainty in vectors is low.The “reproductive-sensitivity hypothesis” (RSH) proposes that recruitment may limit population growth in cold parts of the range (Fig. 1C), where fecundity and/or seedling survival is already low. Cold-sensitive reproduction in plants includes late frost that can disrupt flowering, pollination, and/or seed development, suggesting that poleward population frontiers tend to be seed-limited (40–44). While climate warming could reduce the negative impacts of low temperatures, especially at northern frontiers, these regions still experience the lowest temperatures. The view of cold-sensitive fecundity as a continuing rate-limiting step, i.e., that has not responded to warming in Fig. 1C, is intended to contrast with the case where warming has alleviated temperature limitation in Fig. 1B. Lags can result if cold-sensitive recruitment naturally limits growth at high-latitude/high-altitude population frontiers (Fig. 1C). In this case, reproductive sensitivity may delay the pace of migration to an extent that depends on fecundity, recruitment, or both at poleward frontiers. The arrows in Fig. 1C depict a case where optimal fecundity is equator-ward of optimal growth and recruitment. The precise location of recruitment relative to fecundity in Fig. 1C will depend on all of the direct and indirect effects of climate, including through seed and seedling predators and disturbances like fire. Fig. 1C depicts one of many hypothetical examples to show that climate variables might have opposing effects on fecundity and recruitment.Both CTH and RSH can apply to both temperature and moisture; the latter is here quantified as cumulative moisture deficit between potential evapotranspiration and precipitation, D=∑m=112(PETm−Pm) for month m, derived from the widely used Standardized Precipitation Evapotranspiration Index (45). Whereas latitude dominates temperature gradients and longitude is important for moisture in the East, gradients are complicated by steep terrain in the West, with temperature tending to decline and moisture increase with elevation.We quantified the transitions that control population spread, from adult trees (BA) to fecundity (seeds per BA) to recruitment (recruits per kg seed) (Fig. 1A–C). Fecundity observations are needed to establish the link between trees and recruits in the migration process. They must be available at the tree scale across the continent because seed production depends on tree species and size, local habitat, and climate for all of the dominant species and size classes (13, 46). These estimates are not sufficient in themselves, because migration depends on seed production per area, not per tree. The per-area estimates come from individual seed production and dispersal from trees on inventory plots that monitor all trees that occupy a fixed sample area. Fecundity estimates were obtained in the MASTIF project (13) from 211,000 (211K) individual trees and 2.5 million (2.5M) tree-years from 81 species. We used a model that accommodates individual tree size, species, and environment and the codependence between trees and over time (Fig. 1C). In other words, it allows valid inference on fecundity, the quasisynchronous, quasiperiodic seed production typical of many species (47). The fitted model was then used to generate a predictive distribution of fecundity for each of 7.6M trees on 170K forest inventory plots across the United States and Canada. Because trees are modeled together, we obtain fecundity estimates per plot and, thus, per area. BA (m² /ha) of adult trees and new recruits into the smallest diameter class allowed us to determine fecundity as kg seed per m² BA and recruitment per kg seed, i.e., each of the transitions in Fig. 1A.Recruitment rates, rather than juvenile abundances, come from the transitions from seedlings to sapling stages. The lag between seed production and recruitment does not allow for comparisons on an annual basis; again, residence times in a seedling bank can span decades. Instead, we focus on geographic variation in mean rates of fecundity and recruitment.We summarized the geographic distributions for each transition as 1) the mean transition rates across all species and 2) the geographic centroids (central tendency) for each species as weighted-average locations, where weights are the demographic transitions (BA to fecundity, fecundity to recruitment, and BA to recruitment). We analyzed central tendency, or centroids (e.g., refs. 3 and 34) because range limits cannot be accurately identified on the basis of small inventory plots (21). If fecundity is not limiting poleward spread (CTH of Fig. 1B), then fecundity centroids are expected to be displaced poleward from the adult population. If reproductive sensitivity dominates population spread (RSH of Fig. 1C), then fecundity and/or recruitment centroids will be displaced equator-ward from adult BA. The same comparisons between fecundity and recruitment determine the contribution of recruitment to spread.     

INAUGURAL ARTICLE by a Recently Elected Academy Member:Pelvic girdle and fin of Tiktaalik roseae

A major challenge in understanding the origin of terrestrial vertebrates has been knowledge of the pelvis and hind appendage of their closest fish relatives. The pelvic girdle and appendage of tetrapods is dramatically larger and more robust than that of fish and contains a number of structures that provide greater musculoskeletal support for posture and locomotion. The discovery of pelvic material of the finned elpistostegalian, Tiktaalik roseae, bridges some of these differences. Multiple isolated pelves have been recovered, each of which has been prepared in three dimensions. Likewise, a complete pelvis and partial pelvic fin have been recovered in association with the type specimen. The pelves of Tiktaalik are paired and have broad iliac processes, flat and elongate pubes, and acetabulae that form a deep socket rimmed by a robust lip of bone. The pelvis is greatly enlarged relative to other finned tetrapodomorphs. Despite the enlargement and robusticity of the pelvis of Tiktaalik, it retains primitive features such as the lack of both an attachment for the sacral rib and an ischium. The pelvic fin of Tiktaalik (NUFV 108) is represented by fin rays and three endochondral elements: other elements are not preserved. The mosaic of primitive and derived features in Tiktaalik reveals that the enhancement of the pelvic appendage of tetrapods and, indeed, a trend toward hind limb-based propulsion have antecedents in the fins of their closest relatives.At first glance, the origin of tetrapods (limbed vertebrates) from finned precursors seems an almost insurmountable transition between life in water and life on land. If the basis of comparison were living taxa alone, then the anatomical and behavioral differences among finned and limbed vertebrates could appear vast: for example, fin structure and function differ dramatically from those of limbs. Fossil evidence, in particular vertebrates from the middle and late part of the Devonian period (393–359 Mya), offers intermediate conditions that bridge this gap (1). The fossils that provide the most informative anatomical intermediates are from the tetrapodomorph lineage (also known as stem tetrapods) and have been recovered from a variety of nonmarine and marginal marine deposits from around the globe (2–4). The creatures closest to the node containing the most basal limbed vertebrates—elpistostegalids, such as Panderichthys, Tiktaalik, and Elpistostege—are most enlightening in understanding the primitive conditions from which tetrapods arose. Although most work has focused on revealing homologies and function of the pectoral appendage of these forms (4–7), relatively little is known of the pelvic appendage beyond limited material of Panderichthys (8). Consequently, analyses of the pelvic fin have been given only sporadic attention over the past decades (4, 8–11) largely because they are often poorly preserved or not preserved at all. In most cases, it is thought that this poor preservation of the pelvic appendage is due to its putative small size and fragility (10).Pelves, and in some cases pelvic appendages, of taxa that span the fin-to-limb transition are known from Gooloogongia (Rhizodontida) (12), Eusthenopteron (Osteolepida) (10, 13), Panderichthys (Elpistostegalia) (7, 8), and Acanthostega and Ichthyostega (Tetrapoda) (14–17). Comparisons of these forms reveal large differences between the pelvic appendages of finned tetrapodomorphs and tetrapods (Fig. 1). Most noticeable is that, in finned taxa, the entire pelvic appendage is significantly smaller than the pectoral. In particular, the pelvic girdle of finned tetrapodomorphs is diminutive relative to the pectoral: the pelvis represents a small fraction of the length of the body (the maximum length of pelvis-to-body length is 1:20 in Eusthenopteron per ref. 10). In addition, there are major differences in the morphology of the pelvic girdles of finned and limbed taxa. The girdles of Eusthenopteron and Gooloogongia have posteriorly facing acetabulae and lack sacral ribs and ischial bones, among other features (10, 12). Unfortunately, the pelvic girdle of Panderichthys is not preserved in sufficient detail to understand the distribution of these morphological features in elpistostegalids (8). However, the best comparisons available from these data strongly supported the hypothesis that the closest finned relatives of tetrapods were “front wheel drive animals,” possessing enlarged pectoral fins, robust pectoral girdles, and relatively small pelvic appendages that were incapable of providing extensive degrees of body support and propulsion.Open in a separate windowFig. 1.Right pelves of Gooloogongia (A), Eusthenopteron (B), and Acanthostega (C) in lateral view. Gooloogongia is preserved as a natural cast in one orientation. Figures were modified from refs. 10, 12, and 14. Cranial is to the right.Previously undescribed material of the stem tetrapod, Tiktaalik roseae, can inform these issues. The type specimen (NUFV108), recovered in 2004 and described in 2006 (5, 6), has since been revealed to contain a partial pelvic appendage, including the right side of the pelvic girdle and an incomplete pelvic fin consisting of endochondral bones and lepidotrichia (Figs. 2 and ​and3).3). This specimen allows direct comparison of the relative size of the pelvic girdle and appendage with the rest of the body because the type consists of a relatively articulated skeleton from head to pelvis. In addition, work at the same site in Nunavut Territory during 2006, 2008, and 2013 has revealed additional isolated pelves of four other individuals. Together, these specimens offer the possibility to test the front wheel drive hypothesis and provide insights into the sequence in the acquisition of tetrapod pelvic appendage structure and locomotor function.Open in a separate windowFig. 2.Type specimen (NUFV108): ventral surface of cranial block (figured in ref. 6) aligned in preserved position with ventral view of the block containing the pelvic fin. (Inset) Line diagram of lepidotrichia and preserved portions of endochondral bones of pelvic fin. f, fin; i, intermedium?; l, lepidotrichia; r, radials.Open in a separate windowFig. 3.Tiktaalik roseae, stereopairs of the right pelvis from NUFV108 in (A) ventral (cranial is to the Top), (B) dorsal (cranial is to the Bottom), (C) caudal (lateral is to the Right), and (D) cranial views (lateral is to the Left). A, acetabulum; i, ilium; p, pubis; r, ossified ridge; u, unfinished bone.     

Anomalous scaling law of strength and toughness of cellulose nanopaper

The quest for both strength and toughness is perpetual in advanced material design; unfortunately, these two mechanical properties are generally mutually exclusive. So far there exists only limited success of attaining both strength and toughness, which often needs material-specific, complicated, or expensive synthesis processes and thus can hardly be applicable to other materials. A general mechanism to address the conflict between strength and toughness still remains elusive. Here we report a first-of-its-kind study of the dependence of strength and toughness of cellulose nanopaper on the size of the constituent cellulose fibers. Surprisingly, we find that both the strength and toughness of cellulose nanopaper increase simultaneously (40 and 130 times, respectively) as the size of the constituent cellulose fibers decreases (from a mean diameter of 27 μm to 11 nm), revealing an anomalous but highly desirable scaling law of the mechanical properties of cellulose nanopaper: the smaller, the stronger and the tougher. Further fundamental mechanistic studies reveal that reduced intrinsic defect size and facile (re)formation of strong hydrogen bonding among cellulose molecular chains is the underlying key to this new scaling law of mechanical properties. These mechanistic findings are generally applicable to other material building blocks, and therefore open up abundant opportunities to use the fundamental bottom-up strategy to design a new class of functional materials that are both strong and tough.The need for engineering materials that are both strong and tough is ubiquitous. However, the design of strong and tough materials is often inevitably a compromise as these two properties generally contradict each other (1). Toughness requires a material’s ability of dissipating local high stress by enduring deformation. Consequently, hard materials tend to be brittle (less tough); lower-strength materials, which can deform more readily, tend to be tougher (2, 3). For example, the toughness of metals and alloys is usually inversely proportional to their strength (4). Acknowledging such a necessary compromise, one would expect that research on advanced material design would be focused on achieving an optimum combination of these two properties. Indeed much research effort is focused on pursuing higher strength, with rather limited corresponding regard for toughness (5–10). One example is the enthusiasm sparked by the discovery of carbon nanotubes (CNTs), which exhibit remarkably high strength. However, it still remains uncertain how such a strong material can be incorporated with bulk materials to benefit from its high strength without sacrificing toughness.There have been tremendous efforts recently to develop materials with higher strength using smaller material structures. For example, by decreasing the grain size of metals, dislocation motions (thus plasticity) are more restricted, leading to a higher strength (5–10). However, such treatments also minimize possible mechanisms (e.g., crack-tip blunting) to relieve local high stress, resulting in lower toughness. The atomic scale origins of high strength of a material, e.g., strong directional bonding and limited dislocation mobility, are also essentially the roots for brittleness of the material. In short, the well-recognized scaling law of “the smaller, the stronger” comes at a price of sacrificing toughness (Fig. 1).Open in a separate windowFig. 1.An anomalous but desirable scaling law of mechanical properties requires defeating the conventional conflict between strength and toughness.The prevailing toughening mechanisms can be categorized into two types: intrinsic and extrinsic. Intrinsic toughening operates ahead of a crack tip to suppress its propagation; it is primarily related to plasticity, and thus the primary source of fracture toughness in ductile materials. Recent progress involves introducing high-density nanotwin boundaries in metals to achieve high strength and toughness (11–15). Intrinsic toughening mechanisms are essentially ineffective with brittle materials, e.g., ceramics, which invariably must rely on extrinsic toughening (2). Extrinsic toughening acts mainly behind the crack tip to effectively reduce the crack-driving force by microstructural mechanisms, e.g., crack bridging and meandering and crack surface sliding (16–18). A counterintuitive but successful example is the development of bulk metallic glass (BMG)-based composites, in which a crystalline dendrite second phase is introduced into the BMG matrix to promote the formation of multiple shear bands, leading to a strong and also tough material (3, 9, 16, 19–21). Intrinsic and extrinsic toughening mechanisms are also found to be effective in natural materials (e.g., bones and nacres), which often involve the hierarchical structure and/or a “brick-and-mortar” hybrid microstructure of the material (22–26). Nature-inspired toughening mechanisms are also used to synthesize biomimetic structural materials. Nonetheless, so far, there exists only rather limited success in attaining both strength and toughness, which often involve material-specific, complicated (e.g., growing high density nanotwins), or expensive (e.g., BMG-dendrite composites) synthesis processes and thus are hardly applicable to other materials. A general and feasible mechanism to address the conflict between strength and toughness still remains elusive.Aiming to shed insight on the long-sought strategy addressing the conflict between strength and toughness, we rationally design cellulose-based nanopaper and investigate the dependence of their mechanical properties on constituent cellulose fiber size. Surprisingly, we find that both the strength and toughness of the nanopaper increase simultaneously (40 and 130 times, respectively) as the size of the constituent cellulose building blocks decreases (from a mean diameter of 27 µm to 11 nm). These stimulating results suggest the promising potential toward a new and highly desirable scaling law: the smaller, the stronger and the tougher (Fig. 1). Though the increasing strength as the diameter of cellulose fiber decreases can be attributed to reduced intrinsic defect size, and the dependence is well captured by a continuum fracture mechanics model, our atomistic simulations reveal that facile formation and reformation of strong hydrogen bonding among cellulose chains is the key to the simultaneously increasing toughness. These mechanistic findings that underpin the highly desirable scaling law of mechanical properties suggest a fundamental bottom-up material design strategy generally applicable to other material building blocks as well, and therefore open up abundant opportunities toward a novel class of engineering materials that are both strong and tough.Cellulose is the most abundant biopolymer on Earth and has long been used as the sustainable building block for conventional paper. Cellulose has appealing mechanical properties, with specific modulus [∼100 GPa/(g/cm³)] and specific strength [∼4 GPa/(g/cm³)] higher than most metals and composites, and many ceramics, making it as a promising building block for functional and structural materials (27). Wood fibers are the main natural source of cellulose and have an intrinsically hierarchical structure (Fig. 2). A 20- to ∼50-µm-thick native wood fiber comprises thousands of nanofibrillated cellulose (CNF) fibers (5–50 nm in diameter), each of which can be disintegrated into finer elementary fibrils consisting of cellulose molecular chains (27–36). Cellulose molecule is a linear chain of ringed glucose molecules, with a repeat unit (Fig. S1) comprising two anhydroglucose rings (C₆H₁₀O₅) linked through C–O–C covalent bond. Rich hydroxyl groups in cellulose molecule (six in each repeat unit) enable facile formation of hydrogen bonds, both intrachain and interchain (Fig. 2). Whereas the intrachain hydrogen bonding stabilizes the linkage and results in the linear configuration of the cellulose chain, interchain hydrogen bonding among neighboring cellulose molecules plays a pivotal role in the deformation and failure behaviors of cellulose-based materials.Open in a separate windowFig. 2.Hierarchical structure of wood fibers and the characteristic of cellulose fibrils. Note the rich interchain hydrogen bonds among neighboring cellulose molecular chains.Open in a separate windowFig. S1.Atomic structure of a cellulose chain repeat unit. Note the six hydroxyl groups (red circles) in each repeat unit.In this study, cellulose fibers of different mean diameters [27 μm (native fiber), 28 nm, and 11 nm, respectively] are isolated from wood cell walls using a top-down approach and characterized (SI Text and Figs. S2 and ​andS3).S3). Cellulose nanopaper is made of a highly entangled random network of CNF fibers (Fig. 3A; Materials and Methods). Regular paper made of 27-μm native cellulose fibers with the same mass per area as the nanopaper is also fabricated as the control. The mechanical properties of both the cellulose nanopaper and regular paper are measured according to ASTM Standard D638 (details in SI Text).Open in a separate windowFig. 3.An anomalous scaling law of strength and toughness of cellulose nanopaper. (A) Schematic of cellulose nanopaper, made of a random network of CNF fibers. (Inset) High-resolution transmission electron microscopy (HRTEM) image of an ∼11-nm CNF fiber. (B) Stress–strain curves of cellulose paper made of cellulose fibers of various mean diameters. As the cellulose fiber diameter decreases from micrometer scale to nanometer scale, both tensile strength and ductility of the cellulose paper increases significantly, leading to an anomalous scaling law (C): the smaller, the stronger and the tougher. (D) Reveals that the ultimate tensile strength scales inversely with the square root of cellulose fiber diameter.Open in a separate windowFig. S2.(A) Optical microscope image of native cellulose fiber with a mean diameter of 27 μm. (B) Size distribution histogram. (C) AFM image of cellulose fibers with mean diameters of 28 nm. (D) Size distribution histogram. (E) HRTEM crystalline lattice image of fiber with a mean diameter of 11 nm. (F) Size distribution histogram.Open in a separate windowFig. S3.(A) A picture of a transparent cellulose nanopaper (made of CNF fibers of a mean diameter of 11 nm) on the university logo (Left). A schematic of fibrous nanostructure of the nanopaper is also shown (Right). (B) Optical transmittance of transparent cellulose nanopaper in visible and near-infrared range. (C) AFM image of cellulose nanopaper made of CNF fibers of a mean diameter of 28 nm. (D) AFM image and height scan of cellulose nanopaper made of CNF fibers of a mean diameter of 11 nm, showing rms at 1 × 1-μm scan size is 1.5 nm.