The first peoples of the Atacama Desert lived among the trees: A 11,600- to 11,200-year-old grove and congregation site.

In deserts, water has been singled out as the most important factor for choosing where to settle, but trees were likely an important part of the landscape for hunter-gatherers beyond merely constituting an economic resource. Yet, this critical aspect has not been considered archaeologically. Here, we present the results of mapping and radiocarbon dating of a truly unique archaeological record. Over 150 preserved stumps around five Late Pleistocene/Early Holocene archaeological campsites (12,800 to 11,200 cal BP) show that trees were key features in the creation of everyday habitats for the first inhabitants of the Atacama Desert. At two of these sites, QM12 and QM35, the spatial and chronological correlation between trees and hearths reveals that people located their homes under the tree canopy. At residential site QM35, artifact distribution coincides with a grove dated to ~11,600 to 11,200 cal BP. A third residential area (QM32) occurred along the grove margins ~12,000 to 11,200 cal BP. Based on the distinct cultural material of these two camps, we propose that two different groups intermittently shared this rich wetland-grove environment. The tree taxa suggest a preference for the native Schinus molle, a tree scarcely present on the landscape today, over the endemic, nitrogen-fixing Strombocarpa tamarugo, both for toolmaking and firewood and even though the S. tamarugo was locally more abundant. Together with the spatial and chronological coincidence of campsites, hearths, and trees, we propose that people spared the most abundant and resilient species to create their homes, in turn promoting fertility oases amid the Atacama's hyperaridity.

Phylogenetically diverse wild plant species use common biochemical strategies to thrive in the Atacama Desert.

The best ideotypes are under mounting pressure due to increased aridity. Understanding the conserved molecular mechanisms that evolve in wild plants adapted to harsh environments is crucial in developing new strategies for agriculture. Yet our knowledge of such mechanisms in wild species is scant. We performed metabolic pathway reconstruction using transcriptome information from 32 Atacama and phylogenetically related species that do not live in Atacama (sister species). We analyzed reaction enrichment to understand the commonalities and differences of Atacama plants. To gain insights into the mechanisms that ensure survival, we compared expressed gene isoform numbers and gene expression patterns between the annotated biochemical reactions from 32 Atacama and sister species. We found biochemical convergences characterized by reactions enriched in at least 50% of the Atacama species, pointing to potential advantages against drought and nitrogen starvation, for instance. These findings suggest that the adaptation in the Atacama Desert may result in part from shared genetic legacies governing the expression of key metabolic pathways to face harsh conditions. Enriched reactions corresponded to ubiquitous compounds common to extreme and agronomic species and were congruent with our previous metabolomic analyses. Convergent adaptive traits offer promising candidates for improving abiotic stress resilience in crop species.

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

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

Ecological and metabolic implications of the nurse effect of Maihueniopsis camachoi in the Atacama Desert.

Plant-plant positive interactions are key drivers of community structure. Yet, the underlying molecular mechanisms of facilitation processes remain unexplored. We investigated the 'nursing' effect of Maihueniopsis camachoi, a cactus that thrives in the Atacama Desert between c. 2800 and 3800 m above sea level. We hypothesised that an important protective factor is thermal amelioration of less cold-tolerant species with a corresponding impact on molecular phenotypes. To test this hypothesis, we compared plant cover and temperatures within the cactus foliage with open areas and modelled the effect of temperatures on plant distribution. We combined eco-metabolomics and machine learning to test the molecular consequences of this association. Multiple species benefited from the interaction with M. camachoi. A conspicuous example was the extended distribution of Atriplex imbricata to colder elevations in association with M. camachoi (400 m higher as compared to plants in open areas). Metabolomics identified 93 biochemical markers predicting the interaction status of A. imbricata with 79% accuracy, independently of year. These findings place M. camachoi as a key species in Atacama plant communities, driving local biodiversity with an impact on molecular phenotypes of nursed species. Our results support the stress-gradient hypothesis and provide pioneer insights into the metabolic consequences of facilitation.

Predictive metabolomics of multiple Atacama plant species unveils a core set of generic metabolites for extreme climate resilience.

Current crop yield of the best ideotypes is stagnating and threatened by climate change. In this scenario, understanding wild plant adaptations in extreme ecosystems offers an opportunity to learn about new mechanisms for resilience. Previous studies have shown species specificity for metabolites involved in plant adaptation to harsh environments. Here, we combined multispecies ecological metabolomics and machine learning-based generalized linear model predictions to link the metabolome to the plant environment in a set of 24 species belonging to 14 families growing along an altitudinal gradient in the Atacama Desert. Thirty-nine common compounds predicted the plant environment with 79% accuracy, thus establishing the plant metabolome as an excellent integrative predictor of environmental fluctuations. These metabolites were independent of the species and validated both statistically and biologically using an independent dataset from a different sampling year. Thereafter, using multiblock predictive regressions, metabolites were linked to climatic and edaphic stressors such as freezing temperature, water deficit and high solar irradiance. These findings indicate that plants from different evolutionary trajectories use a generic metabolic toolkit to face extreme environments. These core metabolites, also present in agronomic species, provide a unique metabolic goldmine for improving crop performances under abiotic pressure.

Plant ecological genomics at the limits of life in the Atacama Desert.

The Atacama Desert in Chile-hyperarid and with high-ultraviolet irradiance levels-is one of the harshest environments on Earth. Yet, dozens of species grow there, including Atacama-endemic plants. Herein, we establish the Talabre-Lejía transect (TLT) in the Atacama as an unparalleled natural laboratory to study plant adaptation to extreme environmental conditions. We characterized climate, soil, plant, and soil-microbe diversity at 22 sites (every 100 m of altitude) along the TLT over a 10-y period. We quantified drought, nutrient deficiencies, large diurnal temperature oscillations, and pH gradients that define three distinct vegetational belts along the altitudinal cline. We deep-sequenced transcriptomes of 32 dominant plant species spanning the major plant clades, and assessed soil microbes by metabarcoding sequencing. The top-expressed genes in the 32 Atacama species are enriched in stress responses, metabolism, and energy production. Moreover, their root-associated soils are enriched in growth-promoting bacteria, including nitrogen fixers. To identify genes associated with plant adaptation to harsh environments, we compared 32 Atacama species with the 32 closest sequenced species, comprising 70 taxa and 1,686,950 proteins. To perform phylogenomic reconstruction, we concatenated 15,972 ortholog groups into a supermatrix of 8,599,764 amino acids. Using two codon-based methods, we identified 265 candidate positively selected genes (PSGs) in the Atacama plants, 64% of which are located in Pfam domains, supporting their functional relevance. For 59/184 PSGs with an Arabidopsis ortholog, we uncovered functional evidence linking them to plant resilience. As some Atacama plants are closely related to staple crops, these candidate PSGs are a "genetic goldmine" to engineer crop resilience to face climate change.

High- and low-latitude forcings drive Atacama Desert rainfall variations over the past 16,000 years.

Late Quaternary precipitation dynamics in the central Andes have been linked to both high- and low-latitude atmospheric teleconnections. We use present-day relationships between fecal pellet diameters from ashy chinchilla rats (Abrocoma cinerea) and mean annual rainfall to reconstruct the timing and magnitude of pluvials (wet episodes) spanning the past 16,000 years in the Atacama Desert based on 81 14C-dated A. cinerea paleomiddens. A transient climate simulation shows that pluvials identified at 15.9 to 14.8, 13.0 to 8.6, and 8.1 to 7.6 ka B.P. can be linked to North Atlantic (high-latitude) forcing (e.g., Heinrich Stadial 1, Younger Dryas, and Bond cold events). Holocene pluvials at 5.0 to 4.6, 3.2 to 2.1, and 1.4 to 0.7 ka B.P. are not simulated, implying low-latitude internal variability forcing (i.e., ENSO regime shifts). These results help constrain future central Andean hydroclimatic variability and hold promise for reconstructing past climates from rodent middens in desert ecosystems worldwide.

Crossing a critical threshold: Accelerated and widespread land use changes drive recent carbon and nitrogen dynamics in Vichuquén Lake (35°S) in central Chile.

Global afforestation/deforestation processes (e.g., Amazon deforestation and Europe afforestation) create new anthropogenic controls on carbon cycling and nutrient supply that have not been fully assessed. Here, we use a watershed-lake dynamics approach to investigate how human-induced land cover changes have altered nutrient transference during the last 700 years in a mediterranean coastal area (Vichuquén Lake). We compare our multiproxy reconstruction with historical documentation and use satellite images to reconstruct land use/cover changes for the last 45 years. Historical landscape changes, including those during the indigenous settlements, Spanish conquest, and the Chilean Republic up to mid-20th century did not significantly alter sediment and nutrient fluxes to the lake. In contrast, the largest changes in the lake-watershed system occurred in the mid-20th century and particularly after the 1980s-90s and were characterized by a large increase in total nitrogen and organic carbon fluxes as well as negative shifts in sediment δ15N and δ13C values. This shift was coeval with the largest land cover transformation in the Vichuquén watershed, as native forests nearly disappeared while anthropogenic tree plantations expanded up to 60% of the surface area.

'White gold' guano fertilizer drove agricultural intensification in the Atacama Desert from AD 1000.

The archaeological record shows that large pre-Inca agricultural systems supported settlements for centuries around the ravines and oases of northern Chile's hyperarid Atacama Desert. This raises questions about how such productivity was achieved and sustained, and its social implications. Using isotopic data of well-preserved ancient plant remains from Atacama sites, we show a dramatic increase in crop nitrogen isotope values (δ15N) from around AD 1000. Maize was most affected, with δ15N values as high as +30‰, and human bone collagen following a similar trend; moreover, their carbon isotope values (δ13C) indicate a considerable increase in the consumption of maize at the same time. We attribute the shift to extremely high δ15N values-the highest in the world for archaeological plants-to the use of seabird guano to fertilize crops. Guano-'white gold' as it came to be called-thus sustained agricultural intensification, supporting a substantial population in an otherwise extreme environment.

A combined approach to establishing the timing and magnitude of anthropogenic nutrient alteration in a mediterranean coastal lake- watershed system.

Human activities have profoundly altered the global nutrient cycle through Land Use and Cover Changes (LUCCs) since the industrial revolution and especially during the Great Acceleration (1950 CE). Yet, the impact of such activities on terrestrial and aquatic ecosystems above their ecological baselines are not well known, especially when considering the response of these systems to the intensity of LUCCs on nutrient cycles. Here, we used a multiproxy approach (sedimentological, geochemical and isotopic analyses, historical records, climate data, and satellite images) to evaluate the role that LUCCs have on Nitrogen (N) cycling in a coastal mediterranean watershed system of central Chile over the last two centuries. Despite long-term anthropogenic use (agriculture, cattle grazing) in the Matanzas watershed- lake system, these LUCC appear to have had little impact on nutrient and organic matter transfer since the Spanish Colonial period. In contrast, the largest changes in N dynamics occurred in the mid-1970s, driven by the replacement of native forests and grasslands by government-subsidized tree plantations of introduced Monterey pine (Pinus radiata) and eucalyptus (Eucalyptus globulus). These LUCC had major impacts on the transfer of organic matter (which increased by 9.4%) and nutrients (as revealed by an increase in total N) to Laguna Matanzas. Our study shows that the presence of anthropogenic land use/cover changes do not necessarily alter nutrient supply and N availability per se but rather it is the magnitude and intensity of such changes that produce major impact on these processes in these mediterranean watersheds.

Multiscale climate change impacts on plant diversity in the Atacama Desert.

Comprehending ecological dynamics requires not only knowledge of modern communities but also detailed reconstructions of ecosystem history. Ancient DNA (aDNA) metabarcoding allows biodiversity responses to major climatic change to be explored at different spatial and temporal scales. We extracted aDNA preserved in fossil rodent middens to reconstruct late Quaternary vegetation dynamics in the hyperarid Atacama Desert. By comparing our paleo-informed millennial record with contemporary observations of interannual variations in diversity, we show local plant communities behave differentially at different timescales. In the interannual (years to decades) time frame, only annual herbaceous expand and contract their distributional ranges (emerging from persistent seed banks) in response to precipitation, whereas perennials distribution appears to be extraordinarily resilient. In contrast, at longer timescales (thousands of years) many perennial species were displaced up to 1,000 m downslope during pluvial events. Given ongoing and future natural and anthropogenically induced climate change, our results not only provide baselines for vegetation in the Atacama Desert, but also help to inform how these and other high mountain plant communities may respond to fluctuations of climate in the future.

Plant pathogen responses to Late Pleistocene and Holocene climate change in the central Atacama Desert, Chile.

Future climate change has the potential to alter the distribution and prevalence of plant pathogens, which may have significant implications for both agricultural crops and natural plant communities. However, there are few long-term datasets against which modelled predictions of pathogen responses to climate change can be tested. Here, we use 18S metabarcoding of 28 rodent middens (solidified deposits of rodent coprolites and nesting material) from the Central Atacama, spanning the last ca. 49 ka, to provide the first long-term late Quaternary record of change in plant pathogen communities in response to changing climate. Plant pathogen richness was significantly greater in middens deposited during the Central Andean Pluvial Event (CAPE); a period of increased precipitation between 17.5-8.5 ka. Moreover, the occurrence frequency of Pucciniaceae (rust fungi) was significantly greater during the CAPE, and the highest relative abundances for five additional potentially pathogenic taxa also occurred during this period. The results demonstrate the promising potential for ancient DNA analysis of late Quaternary samples to reveal insights into how plant pathogens responded to past climatic and environmental change, which could help predict how pathogens may responded to future change.

Past and future global transformation of terrestrial ecosystems under climate change.

Impacts of global climate change on terrestrial ecosystems are imperfectly constrained by ecosystem models and direct observations. Pervasive ecosystem transformations occurred in response to warming and associated climatic changes during the last glacial-to-interglacial transition, which was comparable in magnitude to warming projected for the next century under high-emission scenarios. We reviewed 594 published paleoecological records to examine compositional and structural changes in terrestrial vegetation since the last glacial period and to project the magnitudes of ecosystem transformations under alternative future emission scenarios. Our results indicate that terrestrial ecosystems are highly sensitive to temperature change and suggest that, without major reductions in greenhouse gas emissions to the atmosphere, terrestrial ecosystems worldwide are at risk of major transformation, with accompanying disruption of ecosystem services and impacts on biodiversity.

Structure and co-occurrence patterns in microbial communities under acute environmental stress reveal ecological factors fostering resilience.

Understanding the factors that modulate bacterial community assembly in natural soils is a longstanding challenge in microbial community ecology. In this work, we compared two microbial co-occurrence networks representing bacterial soil communities from two different sections of a pH, temperature and humidity gradient occurring along a western slope of the Andes in the Atacama Desert. In doing so, a topological graph alignment of co-occurrence networks was used to determine the impact of a shift in environmental variables on OTUs taxonomic composition and their relationships. We observed that a fraction of association patterns identified in the co-occurrence networks are persistent despite large environmental variation. This apparent resilience seems to be due to: (1) a proportion of OTUs that persist across the gradient and maintain similar association patterns within the community and (2) bacterial community ecological rearrangements, where an important fraction of the OTUs come to fill the ecological roles of other OTUs in the other network. Actually, potential functional features suggest a fundamental role of persistent OTUs along the soil gradient involving nitrogen fixation. Our results allow identifying factors that induce changes in microbial assemblage configuration, altering specific bacterial soil functions and interactions within the microbial communities in natural environments.

The pre-Columbian introduction and dispersal of Algarrobo (Prosopis, Section Algarobia) in the Atacama Desert of northern Chile.

Archaeological and palaeoecological studies throughout the Americas have documented widespread landscape and environmental transformation during the pre-Columbian era. The highly dynamic Formative (or Neolithic) period in northern Chile (ca. 3700-1550 yr BP) brought about the local establishment of agriculture, introduction of new crops (maize, quinoa, manioc, beans, etc.) along with a major population increase, new emergent villages and technological innovations. Even trees such as the Algarrobos (Prosopis section Algarobia) may have been part of this transformation. Here, we provide evidence that these species were not native to the Atacama Desert of Chile (18-27°S), appearing only in the late Holocene and most likely due to human actions. We assembled a database composed of 41 taxon specific AMS radiocarbon dates from archaeobotanical and palaeoecological records (rodent middens, leaf litter deposits), as well an extensive bibliographical review comprising archaeobotanical, paleoecological, phylogenetic and taxonomic data to evaluate the chronology of introduction and dispersal of these trees. Although Algarrobos could have appeared as early as 4200 yr BP in northernmost Chile, they only became common throughout the Atacama over a thousand years later, during and after the Formative period. Cultural and natural factors likely contributed to its spread and consolidation as a major silvicultural resource.

Coupled Socio-Environmental Changes Triggered Indigenous Aymara Depopulation of the Semiarid Andes of Tarapacá-Chile during the Late 19th-20th Centuries.

Socio-economic and environmental changes are well known causes of demographic collapse of agrarian cultures. The collapse of human societies is a complex phenomenon where historical and cultural dimensions play a key role, and they may interact with the environmental context. However, the importance of the interaction between socio-economic and climatic factors in explaining possible breakdowns in Native American societies has been poorly explored. The aim of this study is to test the role of socio-economic causes and rainfall variability in the collapse suffered by the Aymara people of the semiarid Andean region of Tarapacá during the period 1820-1970. Our motivation is to demonstrate that simple population dynamic models can be helpful in understanding the causes and relative importance of population changes in Andean agro-pastoral societies in responses to socio-environmental variability. Simple logistic models that combine the effects of external socio-economic causes and past rainfall variability (inferred from Gross Domestic Product [GDP] and tree-rings, respectively) were quite accurate in predicting the sustained population decline of the Aymara people. Our results suggest that the depopulation in the semiarid Tarapacá province was caused by the interaction among external socio-economic pressures given by the economic growth of the lowlands and demands for labor coupled with a persistent decline in rainfall. This study constitutes an example of how applied ecological knowledge, in particular the application of the logistic equation and theories pertaining to nonlinear population dynamics and exogenous perturbations, can be used to better understand major demographic changes in human societies.

Nitrogen cycling in an extreme hyperarid environment inferred from δ(15)N analyses of plants, soils and herbivore diet.

Climate controls on the nitrogen cycle are suggested by the negative correlation between precipitation and δ(15)N values across different ecosystems. For arid ecosystems this is unclear, as water limitation among other factors can confound this relationship. We measured herbivore feces, foliar and soil δ(15)N and δ(13)C values and chemically characterized soils (pH and elemental composition) along an elevational/climatic gradient in the Atacama Desert, northern Chile. Although very positive δ(15)N values span the entire gradient, soil δ(15)N values show a positive correlation with aridity as expected. In contrast, foliar δ(15)N values and herbivore feces show a hump-shaped relationship with elevation, suggesting that plants are using a different N source, possibly of biotic origin. Thus at the extreme limits of plant life, biotic interactions may be just as important as abiotic processes, such as climate in explaining ecosystem δ(15)N values.

Emergence of social complexity among coastal hunter-gatherers in the Atacama Desert of northern Chile.

The emergence of complex cultural practices in simple hunter-gatherer groups poses interesting questions on what drives social complexity and what causes the emergence and disappearance of cultural innovations. Here we analyze the conditions that underlie the emergence of artificial mummification in the Chinchorro culture in the coastal Atacama Desert in northern Chile and southern Peru. We provide empirical and theoretical evidence that artificial mummification appeared during a period of increased coastal freshwater availability and marine productivity, which caused an increase in human population size and accelerated the emergence of cultural innovations, as predicted by recent models of cultural and technological evolution. Under a scenario of increasing population size and extreme aridity (with little or no decomposition of corpses) a simple demographic model shows that dead individuals may have become a significant part of the landscape, creating the conditions for the manipulation of the dead that led to the emergence of complex mortuary practices.

Accumulation of impact markers in desert wetlands and implications for the Younger Dryas impact hypothesis.

The Younger Dryas impact hypothesis contends that an extraterrestrial object exploded over North America at 12.9 ka, initiating the Younger Dryas cold event, the extinction of many North American megafauna, and the demise of the Clovis archeological culture. Although the exact nature and location of the proposed impact or explosion remain unclear, alleged evidence for the fallout comes from multiple sites across North America and a site in Belgium. At 6 of the 10 original sites (excluding the Carolina Bays), elevated concentrations of various "impact markers" were found in association with black mats that date to the onset of the Younger Dryas. Black mats are common features in paleowetland deposits and typically represent shallow marsh environments. In this study, we investigated black mats ranging in age from approximately 6 to more than 40 ka in the southwestern United States and the Atacama Desert of northern Chile. At 10 of 13 sites, we found elevated concentrations of iridium in bulk and magnetic sediments, magnetic spherules, and/or titanomagnetite grains within or at the base of black mats, regardless of their age or location, suggesting that elevated concentrations of these markers arise from processes common to wetland systems, and not a catastrophic extraterrestrial impact event.

Perennial stream discharge in the hyperarid Atacama Desert of northern Chile during the latest Pleistocene.

A large fraction of the vital groundwater in the Atacama Desert of northern Chile is likely composed of "fossil" or "ancient" reserves that receive little or no recharge in today's hyperarid climate. Here, we present evidence for latest Pleistocene perennial streamflow in canyons from the hyperarid core of the Atacama Desert in northern Chile. Fluvial terraces in the Pampa del Tamarugal (PdT) basin (21 degrees S) contain widespread fossil wood, in situ roots, and well preserved leaf litter deposits indicative of perennial surface flow currently absent in these channels. Nineteen radiocarbon dates on these deposits from four separate drainages within this endorheic basin indicate ages from 16,380 to 13,740 cal yr BP, synchronous with paleolake Tauca on the Bolivian Altiplano and other regional evidence for wetter conditions during the latest Pleistocene. Groundwater-fed riparian ecosystems and associated fluvial deposits abound today in the absence of direct rainfall in northern Atacama canyons with perennial discharge. Our relict riparian ecosystems from the PdT basin are indicative of conditions similar to these northern canyons. Given that discharge was higher than present during this time, we propose that these deposits represent the most important groundwater recharge events of the last 18,000 years. A lesser recharge event occurred during the Holocene, when phreatophytic trees also grew in these drainages between 1,070 and 700 cal yr BP, during the Medieval Climatic Anomaly. Taken together, our evidence lends further support for gradient changes in the equatorial Pacific as a major driver of hydrologic change in the Atacama on both centennial and millennial time scales.