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.

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.

Recovery and analysis of ancient beetle DNA from subfossil packrat middens using high-throughput sequencing.

The study of ancient DNA is revolutionizing our understanding of paleo-ecology and the evolutionary history of species. Insects are essential components in many ecosystems and constitute the most diverse group of animals. Yet they are largely neglected in ancient DNA studies. We report the results of the first targeted investigation of insect ancient DNA to positively identify subfossil insects to species, which includes the recovery of endogenous content from samples as old as ~ 34,355 ybp. Potential inhibitors currently limiting widespread research on insect ancient DNA are discussed, including the lack of closely related genomic reference sequences (decreased mapping efficiency) and the need for more extensive collaborations with insect taxonomists. The advantages of insect-based studies are also highlighted, especially in the context of understanding past climate change. In this regard, insect remains from ancient packrat middens are a rich and largely uninvestigated resource for exploring paleo-ecology and species dynamics over time.

Climate Dipoles as Continental Drivers of Plant and Animal Populations.

Ecological processes, such as migration and phenology, are strongly influenced by climate variability. Studying these processes often relies on associating observations of animals and plants with climate indices, such as the El Niño-Southern Oscillation (ENSO). A common characteristic of climate indices is the simultaneous emergence of opposite extremes of temperature and precipitation across continental scales, known as climate dipoles. The role of climate dipoles in shaping ecological and evolutionary processes has been largely overlooked. We review emerging evidence that climate dipoles can entrain species dynamics and offer a framework for identifying ecological dipoles using broad-scale biological data. Given future changes in climatic and atmospheric processes, climate and ecological dipoles are likely to shift in their intensity, distribution, and timing.

Life history traits predict colonization and extinction lags of desert plant species since the Last Glacial Maximum.

Variation in life-history strategies can affect metapopulation dynamics and consequently the composition and diversity of communities. However, data sets that allow for the full range of species turnover from colonization to extinction over relevant time periods are limited. The late Quaternary record provides unique opportunities to explore the traits that may have influenced interspecific variation in responses to past climate warming, in particular the rate at which species colonized newly suitable habitat or went locally extinct from degrading habitat. We controlled for differences in species climate niches in order to predict expected colonization and extinction sequences recorded in packrat middens from 15 localities in the Mohave, Sonoran, and Chihuahuan deserts of North America. After accounting for temperature niche differences, we tested the hypotheses that dispersal syndrome (none, wind, vertebrate), growth form (herb, shrub, tree) and seed mass mediated variation in postglacial colonization lags among species, whereas clonality (clonal, non-clonal), growth form, and seed mass affected extinction lags. Growth form and dispersal syndrome interactively affected colonization lags, where herbaceous species lacking long-distance dispersal mechanisms exhibited lags that exceeded those of woody, wind or vertebrate-dispersed species by an average of 2,000-5,000 yr. Growth form and seed mass interactively affected extinction lags, with very small-seeded shrubs persisting for 4,000-8,000 yr longer than other functional groups. Taller, vertebrate-dispersed plants have been shown in other studies to disperse farther than shorter plants without specialized dispersal mechanisms. We found that variation along this axis of dispersal syndromes resulted in dramatic differences in colonization rates in response to past climate change. Very small seeded shrubs may have a unique combination of long vegetative and seed bank lifetimes that may allow them to persist for long periods despite declines in habitat condition. This study indicates that readily measurable traits may help predict which species will be more or less sensitive to future climate change, and inform interventions that can stabilize and promote at-risk populations.

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.

Iterative near-term ecological forecasting: Needs, opportunities, and challenges.

Two foundational questions about sustainability are "How are ecosystems and the services they provide going to change in the future?" and "How do human decisions affect these trajectories?" Answering these questions requires an ability to forecast ecological processes. Unfortunately, most ecological forecasts focus on centennial-scale climate responses, therefore neither meeting the needs of near-term (daily to decadal) environmental decision-making nor allowing comparison of specific, quantitative predictions to new observational data, one of the strongest tests of scientific theory. Near-term forecasts provide the opportunity to iteratively cycle between performing analyses and updating predictions in light of new evidence. This iterative process of gaining feedback, building experience, and correcting models and methods is critical for improving forecasts. Iterative, near-term forecasting will accelerate ecological research, make it more relevant to society, and inform sustainable decision-making under high uncertainty and adaptive management. Here, we identify the immediate scientific and societal needs, opportunities, and challenges for iterative near-term ecological forecasting. Over the past decade, data volume, variety, and accessibility have greatly increased, but challenges remain in interoperability, latency, and uncertainty quantification. Similarly, ecologists have made considerable advances in applying computational, informatic, and statistical methods, but opportunities exist for improving forecast-specific theory, methods, and cyberinfrastructure. Effective forecasting will also require changes in scientific training, culture, and institutions. The need to start forecasting is now; the time for making ecology more predictive is here, and learning by doing is the fastest route to drive the science forward.

A dynamic leaf gas-exchange strategy is conserved in woody plants under changing ambient CO2 : evidence from carbon isotope discrimination in paleo and CO2 enrichment studies.

Rising atmospheric [CO2 ], ca , is expected to affect stomatal regulation of leaf gas-exchange of woody plants, thus influencing energy fluxes as well as carbon (C), water, and nutrient cycling of forests. Researchers have proposed various strategies for stomatal regulation of leaf gas-exchange that include maintaining a constant leaf internal [CO2 ], ci , a constant drawdown in CO2 (ca  - ci ), and a constant ci /ca . These strategies can result in drastically different consequences for leaf gas-exchange. The accuracy of Earth systems models depends in part on assumptions about generalizable patterns in leaf gas-exchange responses to varying ca . The concept of optimal stomatal behavior, exemplified by woody plants shifting along a continuum of these strategies, provides a unifying framework for understanding leaf gas-exchange responses to ca . To assess leaf gas-exchange regulation strategies, we analyzed patterns in ci inferred from studies reporting C stable isotope ratios (δ(13) C) or photosynthetic discrimination (∆) in woody angiosperms and gymnosperms that grew across a range of ca spanning at least 100 ppm. Our results suggest that much of the ca -induced changes in ci /ca occurred across ca spanning 200 to 400 ppm. These patterns imply that ca  - ci will eventually approach a constant level at high ca because assimilation rates will reach a maximum and stomatal conductance of each species should be constrained to some minimum level. These analyses are not consistent with canalization toward any single strategy, particularly maintaining a constant ci . Rather, the results are consistent with the existence of a broadly conserved pattern of stomatal optimization in woody angiosperms and gymnosperms. This results in trees being profligate water users at low ca , when additional water loss is small for each unit of C gain, and increasingly water-conservative at high ca , when photosystems are saturated and water loss is large for each unit C gain.

Climatic dipoles drive two principal modes of North American boreal bird irruption.

Pine Siskins exemplify normally boreal seed-eating birds that can be sparse or absent across entire regions of North America in one year and then appear in large numbers the next. These dramatic avian "irruptions" are thought to stem from intermittent but broadly synchronous seed production (masting) in one year and meager seed crops in the next. A prevalent hypothesis is that widespread masting in the boreal forest at high latitudes is driven primarily by favorable climate during the two to three consecutive years required to initiate and mature seed crops in most conifers. Seed production is expensive for trees and is much reduced in the years following masting, driving boreal birds to search elsewhere for food and overwintering habitat. Despite this plausible logic, prior efforts to discover climate-irruption relationships have been inconclusive. Here, analysis of more than 2 million Pine Siskin observations from Project FeederWatch, a citizen science program, reveals two principal irruption modes (North-South and West-East), both of which are correlated with climate variability. The North-South irruption mode is, in part, influenced by winter harshness, but the predominant climate drivers of both modes manifest in the warm season as continental-scale pairs of oppositely signed precipitation and temperature anomalies (i.e., dipoles). The climate dipoles juxtapose favorable and unfavorable conditions for seed production and wintering habitat, motivating a push-pull paradigm to explain irruptions of Pine Siskins and possibly other boreal bird populations in North America.

Local extinction and unintentional rewilding of bighorn sheep (Ovis canadensis) on a desert island.

Bighorn sheep (Ovis canadensis) were not known to live on Tiburón Island, the largest island in the Gulf of California and Mexico, prior to the surprisingly successful introduction of 20 individuals as a conservation measure in 1975. Today, a stable island population of ∼500 sheep supports limited big game hunting and restocking of depleted areas on the Mexican mainland. We discovered fossil dung morphologically similar to that of bighorn sheep in a dung mat deposit from Mojet Cave, in the mountains of Tiburón Island. To determine the origin of this cave deposit we compared pellet shape to fecal pellets of other large mammals, and extracted DNA to sequence mitochondrial DNA fragments at the 12S ribosomal RNA and control regions. The fossil dung was 14C-dated to 1476-1632 calendar years before present and was confirmed as bighorn sheep by morphological and ancient DNA (aDNA) analysis. 12S sequences closely or exactly matched known bighorn sheep sequences; control region sequences exactly matched a haplotype described in desert bighorn sheep populations in southwest Arizona and southern California and showed subtle differentiation from the extant Tiburón population. Native desert bighorn sheep previously colonized this land-bridge island, most likely during the Pleistocene, when lower sea levels connected Tiburón to the mainland. They were extirpated sometime in the last ∼1500 years, probably due to inherent dynamics of isolated populations, prolonged drought, and (or) human overkill. The reintroduced population is vulnerable to similar extinction risks. The discovery presented here refutes conventional wisdom that bighorn sheep are not native to Tiburón Island, and establishes its recent introduction as an example of unintentional rewilding, defined here as the introduction of a species without knowledge that it was once native and has since gone locally extinct.

Woodland dynamics at the northern range periphery: a challenge for protected area management in a changing world.

Managers of protected natural areas increasingly are confronted with novel ecological conditions and conflicting objectives to preserve the past while fostering resilience for an uncertain future. This dilemma may be pronounced at range peripheries where rates of change are accelerated and ongoing invasions often are perceived as threats to local ecosystems. We provide an example from City of Rocks National Reserve (CIRO) in southern Idaho, positioned at the northern range periphery of pinyon-juniper (P-J) woodland. Reserve managers are concerned about P-J woodland encroachment into adjacent sagebrush steppe, but the rates and biophysical variability of encroachment are not well documented and management options are not well understood. We quantified the rate and extent of woodland change between 1950 and 2009 based on a random sample of aerial photo interpretation plots distributed across biophysical gradients. Our study revealed that woodland cover remained at approximately 20% of the study area over the 59-year period. In the absence of disturbance, P-J woodlands exhibited the highest rate of increase among vegetation types at 0.37% yr(-1). Overall, late-successional P-J stands increased in area by over 100% through the process of densification (infilling). However, wildfires during the period resulted in a net decrease of woody evergreen vegetation, particularly among early and mid-successional P-J stands. Elevated wildfire risk associated with expanding novel annual grasslands and drought is likely to continue to be a fundamental driver of change in CIRO woodlands. Because P-J woodlands contribute to regional biodiversity and may contract at trailing edges with global warming, CIRO may become important to P-J woodland conservation in the future. Our study provides a widely applicable toolset for assessing woodland ecotone dynamics that can help managers reconcile the competing demands to maintain historical fidelity and contribute meaningfully to the U.S. protected area network in a future with novel, no-analog ecosystems.

Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile.

Nearly half the earth's surface is occupied by dryland ecosystems, regions susceptible to reduced states of biological productivity caused by climate fluctuations. Of these regions, arid zones located at the interface between vegetated semiarid regions and biologically unproductive hyperarid zones are considered most vulnerable. The objective of this study was to conduct a deep diversity analysis of bacterial communities in unvegetated arid soils of the Atacama Desert, to characterize community structure and infer the functional potential of these communities based on observed phylogenetic associations. A 454-pyrotag analysis was conducted of three unvegetated arid sites located at the hyperarid-arid margin. The analysis revealed communities with unique bacterial diversity marked by high abundances of novel Actinobacteria and Chloroflexi and low levels of Acidobacteria and Proteobacteria, phyla that are dominant in many biomes. A 16S rRNA gene library of one site revealed the presence of clones with phylogenetic associations to chemoautotrophic taxa able to obtain energy through oxidation of nitrite, carbon monoxide, iron, or sulfur. Thus, soils at the hyperarid margin were found to harbor a wealth of novel bacteria and to support potentially viable communities with phylogenetic associations to non-phototrophic primary producers and bacteria capable of biogeochemical cycling.

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.

The unusual nature of recent snowpack declines in the North American cordillera.

In western North America, snowpack has declined in recent decades, and further losses are projected through the 21st century. Here, we evaluate the uniqueness of recent declines using snowpack reconstructions from 66 tree-ring chronologies in key runoff-generating areas of the Colorado, Columbia, and Missouri River drainages. Over the past millennium, late 20th century snowpack reductions are almost unprecedented in magnitude across the northern Rocky Mountains and in their north-south synchrony across the cordillera. Both the snowpack declines and their synchrony result from unparalleled springtime warming that is due to positive reinforcement of the anthropogenic warming by decadal variability. The increasing role of warming on large-scale snowpack variability and trends foreshadows fundamental impacts on streamflow and water supplies across the western United States.

Facilitation drives 65 years of vegetation change in the Sonoran Desert.

Ecological processes of low-productivity ecosystems have long been considered to be driven by abiotic controls with biotic interactions playing an insignificant role. However, existing studies present conflicting evidence concerning the roles of these factors, in part due to the short temporal extent of most data sets and inability to test indirect effects of environmental variables modulated by biotic interactions. Using structural equation modeling to analyze 65 years of perennial vegetation change in the Sonoran Desert, we found that precipitation had a stronger positive effect on recruitment beneath existing canopies than in open microsites due to reduced evaporation rates. Variation in perennial canopy cover had additional facilitative effects on juvenile recruitment, which was indirectly driven by effects of density and precipitation on cover. Mortality was strongly influenced by competition as indicated by negative density-dependence, whereas precipitation had no effect. The combined direct, indirect, and interactive facilitative effects of precipitation and cover on recruitment were substantial, as was the effect of competition on mortality, providing strong evidence for dual control of community dynamics by climate and biotic interactions. Through an empirically derived simulation model, we also found that the positive feedback of density on cover produces unique temporal abundance patterns, buffering changes in abundance from high frequency variation in precipitation, amplifying effects of low frequency variation, and decoupling community abundance from precipitation patterns at high abundance. Such dynamics should be generally applicable to low-productivity systems in which facilitation is important and can only be understood within the context of long-term variation in climatic patterns. This predictive model can be applied to better manage low-productivity ecosystems, in which variation in biogeochemical processes and trophic dynamics may be driven by positive density-dependent feedbacks that influence temporal abundance and productivity patterns.

Ecology and the ratchet of events: climate variability, niche dimensions, and species distributions.

Climate change in the coming centuries will be characterized by interannual, decadal, and multidecadal fluctuations superimposed on anthropogenic trends. Predicting ecological and biogeographic responses to these changes constitutes an immense challenge for ecologists. Perspectives from climatic and ecological history indicate that responses will be laden with contingencies, resulting from episodic climatic events interacting with demographic and colonization events. This effect is compounded by the dependency of environmental sensitivity upon life-stage for many species. Climate variables often used in empirical niche models may become decoupled from the proximal variables that directly influence individuals and populations. Greater predictive capacity, and more-fundamental ecological and biogeographic understanding, will come from integration of correlational niche modeling with mechanistic niche modeling, dynamic ecological modeling, targeted experiments, and systematic observations of past and present patterns and dynamics.

Bacterial community structure in the hyperarid core of the Atacama Desert, Chile.

Soils from the hyperarid Atacama Desert of northern Chile were sampled along an east-west elevational transect (23.75 to 24.70 degrees S) through the driest sector to compare the relative structure of bacterial communities. Analysis of denaturing gradient gel electrophoresis (DGGE) profiles from each of the samples revealed that microbial communities from the extreme hyperarid core of the desert clustered separately from all of the remaining communities. Bands sequenced from DGGE profiles of two samples taken at a 22-month interval from this core region revealed the presence of similar populations dominated by bacteria from the Gemmatimonadetes and Planctomycetes phyla.

Role of multidecadal climate variability in a range extension of pinyon pine.

Evidence from woodrat middens and tree rings at Dutch John Mountain (DJM) in northeastern Utah reveal spatiotemporal patterns of pinyon pine (Pinus edulis Engelm.) colonization and expansion in the past millennium. The DJM population, a northern outpost of pinyon, was established by long-distance dispersal (approximately 40 km). Growth of this isolate was markedly episodic and tracked multidecadal variability in precipitation. Initial colonization occurred by AD 1246, but expansion was forestalled by catastrophic drought (1250-1288), which we speculate produced extensive mortality of Utah Juniper (Juniperus osteosperma (Torr.) Little), the dominant tree at DJM for the previous approximately 8700 years. Pinyon then quickly replaced juniper across DJM during a few wet decades (1330-1339 and 1368-1377). Such alternating decadal-scale droughts and pluvial events play a key role in structuring plant communities at the landscape to regional level. These decadal-length precipitation anomalies tend to be regionally coherent and can synchronize physical and biological processes across large areas. Vegetation forecast models must incorporate these temporal and geographic aspects of climate variability to accurately predict the effects of future climate change.

Pacific and Atlantic Ocean influences on multidecadal drought frequency in the United States.

More than half (52%) of the spatial and temporal variance in multidecadal drought frequency over the conterminous United States is attributable to the Pacific Decadal Oscillation (PDO) and the Atlantic Multidecadal Oscillation (AMO). An additional 22% of the variance in drought frequency is related to a complex spatial pattern of positive and negative trends in drought occurrence possibly related to increasing Northern Hemisphere temperatures or some other unidirectional climate trend. Recent droughts with broad impacts over the conterminous U.S. (1996, 1999-2002) were associated with North Atlantic warming (positive AMO) and northeastern and tropical Pacific cooling (negative PDO). Much of the long-term predictability of drought frequency may reside in the multidecadal behavior of the North Atlantic Ocean. Should the current positive AMO (warm North Atlantic) conditions persist into the upcoming decade, we suggest two possible drought scenarios that resemble the continental-scale patterns of the 1930s (positive PDO) and 1950s (negative PDO) drought.