We evaluated the impacts of the recent drought on regional-scale mortality of piñon pine (Pinus edulis), which is sensitive to climate variation and dominates piñon-juniper woodlands, one of the most extensive vegetation types in the western North America (10-12). Specifically, we evaluated the impacts of the recent drought on regional-scale mortality in the context of the potential impacts of global-change-type drought, and (i) demonstrated that the recent drought is not as dry as the previous drought but is warmer in numerous respects, thereby providing a case study for global-change-type drought; (ii) quantified site-specific conditions in soil water content and local vegetation response (percentage of tree mortality, and a remotely sensed vegetation index related to photosynthetic activity and associated greenness, Normalized Difference Vegetation Index, NDVI) to precipitation and temperature dynamics; and (iii) estimated and verified regional-scale stress and mortality responses in vegetation to drought by using weekly NDVI data back to 1989 and supplemental aerial surveys and field inventories.

We obtained monthly climate data for all meteorological stations in Arizona, New Mexico, Colorado, and Utah that were listed with the Western Regional Climate Center (www.wrcc.dri.edu; Western U.S. Climate Historical Summaries, September 1, 2004-Decmber 14, 2004) and determined annual values for total precipitation, mean minimum temperature, and mean maximum temperature. We then identified 22 of those stations associated with piñon-juniper woodlands based on two criteria. First, stations were within 1,000 m of the piñon-juniper vegetation type where P. edulis was either the dominant or codominant plant species, as defined by the United States Geological Survey Gap Analysis Program (GAP) distribution map of dominant vegetation (scale of 1:100,000; www.gap.uidaho.edu). The GAP map is derived from satellite imagery combined with existing data, air and field study, and expert knowledge. Our second criterion was that the record of monthly precipitation and temperature for the drought intervals of interest, defined below, was relatively complete: ≤2 months missing for any year of interest, except for two stations (Moab and El Vado) that were missing up to 4 months of data for one of the years. We compared the recent drought with that of the 1950s by focusing on the four driest consecutive years for each: 2000-2003 and 1953-1956, respectively. We tested for differences in total precipitation, mean minimum temperature, and mean maximum temperature between the two drought intervals by using t tests paired by station; we applied sequential Bonferroni adjustment to determine tablewide significance for the three t tests (13). We categorized anomalously dry or warm years as in the extreme 10 percentiles.

We evaluated synoptic vegetation changes by using the NDVI (1 km² = 1 pixel), calculated by using near-IR and visible reflectance values collected by the advanced very highresolution radiometer located on several National Oceanic and Atmospheric Administration satellite platforms (14). NDVI has been widely used to estimate landscape patterns of primary production (14) and is correlated with foliar water content and water potential for P. edulis needles over a wide range of conditions, including recently deceased trees (15). Weekly values of NDVI from 1989 to 2003 were extracted by using the GAP-delineated piñon-juniper distribution of the four states. Before extraction, the NDVI data were corrected by using biweekly maximum value compositing to remove most cloud contamination and were corrected to reduce effects of atmospheric haze and ozone. These data were also detrended to account for artificial value drift by examining temporal signatures from invariant targets (16). The detrending provides a conservatively large adjustment that could mask some of the NDVI dynamics, and hence we present NDVI dynamics as a range bounded by nondetrended and detrended estimates. For each year, mean regional NDVI was calculated from the corrected images for late May through June (Julian weeks 22-26), a period when understory greenness was observed to have minimal effect, allowing overstory effects of die-off to be most apparent.

We used measurements from an intensively studied site located within the region, Mesita del Buey near Los Alamos, NM (17, 18), to document changes in (i) precipitation, temperature, and soil water content before and during the recent drought, and (ii) the associated responses in site NDVI and tree mortality. Soil water content was measured by using neutron attenuation at a 20-cm depth at 11 locations spaced at ≈10-m intervals; measurements were calibrated for local soils and generally obtained once or more per month. Mortality at Mesita del Buey was estimated through field surveys in 2002 and 2003 and was compared against baseline data. Weekly NDVI values for the Mesita del Buey site were estimated for a 3-×-3-pixel window (after comparing results with window sizes ranging from 1 × 1 to 9 × 9 pixels) to jointly mitigate spatial registration issues and land cover heterogeneity effects. For each year mean NDVI values for Mesita del Buey were calculated for late May through June (weeks 22-26) for intervals representing baseline (1989-1999) and drought after extensive die-off (2002-2003).

To confirm that regional NDVI changes within the GAP-delineated area were associated with tree mortality, we obtained data from aerial surveys conducted by the U.S. Department of Agriculture Forest Service and distributed by the Forest Health Technology Enterprise Team (19), which covered ≈60% of the piñon-juniper woodland distribution in the four states during 2002 and 2003. The surveys were flown 300-400 m above ground, and areas of noticeable stand-level mortality from drought and associated bark beetle infestation were sketch-mapped at the 1:100,000 scale. We also estimated P. edulis mortality for nonseedling trees (≥1-m height) at a verification site in each of the four states, based on either documented changes in inventories that were conducted before mortality event (Arizona, Colorado, New Mexico) or for which recent mortality was inferred (Utah); verification sites varied from 4 to 49 in number of plot or belt transects and 0.2-4.9 hectares for total area surveyed. The New Mexico site spanned the more intensively studied Mesita del Buey site and included wider coverage.

The recent drought spanning southwestern North America was anomalously dry, similar to the subcontinental drought of the 1950s, but contrasted with that drought in having anomalously high temperatures for the entire region (Fig. 1A) and for locations only within the distributional range of P. edulis (Fig. 1B). Within the distributional range of P. edulis, total precipitation during the 4-year interval for the recent drought (2000-2003) was slightly greater than that for the 1950s drought (Fig. 1B; P < 0.05). Yet the recent drought was warmer than the 1950s drought with respect to maximum annual temperature (Fig. 1C; P < 0.05) and particularly with respect to minimum annual temperature (Fig. 1D; P < 0.001) and average summer maximum temperature (June and July; P < 0.001). At the intensively studied site within the region located in northern New Mexico (Mesita del Buey), mean minimum and mean maximum temperatures were warmer during than before the recent drought (Fig. 2A), a period of reduced annual precipitation spanning 2000-2003 (Fig. 2B). The timing and amount of the reductions in precipitation in conjunction with simultaneous warmer temperatures resulted in 10 consecutive months (October 1999-August 2000) of dry soil water conditions (<15% volumetric water content, associated with a soil water potential of less than -2.5 MPa; ref. 18), which was later followed by an additional 15 consecutive months of dry soil water conditions (August 2001-October 2002; Fig. 2C). Bark beetle (Ips confusus) infestation and change in foliar water and spectral conditions were observed subsequently during 2002 and 2003 (15). Resulting P. edulis mortality at Mesita del Buey exceeded 90% (Fig. 2D). The tree mortality at this site is reflected in a >20% decrease in NDVI, highlighted by the reduced NDVI values for 2002 and 2003 that persisted once the P. edulis mortality began (Fig. 2 E and F). Premortality effects of the drought are evident in the depressed values of site NDVI for 2000, a very dry year, and then are partially offset by increased NDVI in 2001, because of a relatively wet 2000-2001 winter and associated herbaceous response. The site-specific changes in NDVI are roughly parallel with regional-scale changes in NDVI (Fig. 2G), which also dropped off substantially in 2002 and to a lesser extent in 2003. The site-specific mortality at Mesita del Buey proceeded into 2003, despite a pulse of soil moisture during the 2002-2003 winter (Fig. 2F), with NDVI remaining depressed through 2003. Conversely, at the regional scale where mortality was less complete, the winter 2002-2003 pulse of soil moisture appears to have resulted in an increased herbaceous response that partially masks the effect of the tree die-off (Fig. 2G). Nonetheless, even using the conservatively detrended estimate, NDVI-depressed values at the regional scale remain substantial. Indeed, reductions in NDVI of similar magnitude to those linked directly to tree mortality at Mesita del Buey covered much of the P. edulis distribution, indicating the spatial extent and variation of drought-induced mortality (Fig. 3A). Regional aerial surveys conducted by the U.S. Forest Service for a subset of the area within the study region confirm that there was widespread mortality for >12,000 km² (Fig. 3B), as reflected in our estimates of NDVI changes. Additional field plot inventories provide further confirmation of widespread P. edulis mortality, with mortality from the drought and associated infestations of the bark beetle I. confusus at the four verification areas ranging from 40% to 80% (Fig. 3B).

Fig. 1. Southwestern North American climate. (A and B) Annual mean precipitation (mm) and average of maximum and minimum temperatures (°C) for all stations in the four-state region (A) and only stations in or near piñon-juniper woodlands within (more ...)

Fig. 2. Drought-induced mortality at Mesita del Buey, northern New Mexico. Shown for predrought and drought periods are: minimum (blue) and maximum (red) temperature (°C) (A), precipitation (mm) (B), volumetric soil water content at 20 cm (%) (C), P. (more ...)

Fig. 3. Regional drought-induced vegetation changes. (A) Change map for NDVI for the region encompassing P. edulis distribution within Arizona, New Mexico, Colorado, and Utah, based on deviation from 2002-2003 relative to the predrought mean (1989-1999) during (more ...)

Our results are notable in documenting rapid, regional-scale mortality of a dominant tree species in response to subcontinental drought accompanied by anomalously high temperatures. Although the proximal cause of mortality for most of the trees was apparently infestation by bark beetles, such outbreaks are tightly tied to drought-induced water stress (5, 20). The soil water content in the months preceding tree mortality was sufficiently low to have produced high plant water stress and cessation of transpiration and photosynthesis in P. edulis (18). Importantly, there was high mortality of as much as 90% or more at studied high elevation sites, such as Mesita del Buey, Mesa Verde in Colorado, and near Flagstaff, AZ, which are near the upper limit of P. edulis distribution and where precipitation and water availability are generally greater than at many other locations where this species occurs. In contrast, mortality in response to the 1950s drought in the same landscape as Mesita del Buey in northern New Mexico was documented predominantly on drier, mostly lower elevation sites, based on the presence or absence of standing or downed dead piñon wood (21). Most of the patchy mortality in the 1950s was associated with trees >100 years old, whereas nearly complete tree mortality across many size and age classes was observed in response to the recent drought (ref. 22 and data for Figs. 2D and 3B). Collectively, these observations suggest that the mortality response to the recent drought was greater in magnitude and extent than the mortality response to the 1950s drought. The warmer temperatures associated with the recent drought would have increased the energy load and water stress demands on the trees and may account for the apparently greater resulting mortality. The effects of water and temperature stress during the recent drought could have been further exacerbated by (i) anomalously high precipitation in the southwestern North America from about 1978-1995 that allowed rapid tree growth and increased stand densities, resulting in potentially greater intraspecific competition for drought-limited water and greater susceptibility to drought, beetle infestation, and associated pathogens (22) and/or (ii) amplifying effects of warmer temperatures and longer growing seasons on beetle growth rates and population dynamics (23). Nonetheless, previous studies of drought-induced die-off have highlighted the underlying importance of water stress in triggering die-off (5, 20).

The rapid, extensive regional changes in vegetation cover through tree die-off that we have quantified for southwestern North America have a number of important, interrelated ecological implications (12, 24), including potentially large changes in carbon stores and dynamics, of concern for carbon-related polices and management (9). Other interrelated implications include large changes in near-ground solar radiation (25), runoff and erosion (5), genetic structure of the dominant tree species on the landscape (26), and land surface microclimate feedbacks to the atmosphere (27). Additionally, future production of piñon nuts, an important food source for several species of birds and small mammals and for local people (28), is expected to be greatly reduced over an extensive area. Persistence of the recent drought could lead to further mortality of P. edulis and other plant species within its distribution. Notably, a dominant herbaceous species within piñon-juniper woodlands, Boutelua gracilis, underwent a >50% reduction in live basal cover between 1999 and 2003 near the Mesita del Buey site. Even codominant, woody species of Juniperus monosperma, which are much more drought tolerant than P. edulis (18), are undergoing mortality in response to the drought, ranging from 2% to 26% at our four field verification sites.

The cessation of drought conditions may be insufficient for reestablishment of P. edulis and associated plant species, as documented for landscape response of Pinus ponderosa after the 1950s drought (5). Such rapid shifts in vegetation may represent abrupt, rapid, and persistent shifts in not only ecotones, but also in dominant vegetation cover and associated ecosystem process (5, 7-8). At a minimum, the spatially extensive die-off will need to be considered in regional environmental assessments and management decisions over the next several decades, the shortest interval required for a P. edulis-dominated overstory structure to reestablish. More generally, an improved predictive capability to forecast ecological responses to climate at regional scales is needed to effectively deal with the consequences of large-scale, long-term climate forcings (2, 8). Our results highlight how drought-induced die-off can span across the range of a vegetation type and challenges the current paradigm for climate-induced vegetation dynamics, which focuses largely on changes at the margins of a species' range and the ecotone boundaries within that range (1, 5, 6). Additionally, if temperatures continue to warm, vegetation die-off in response to future drought may be further amplified (5, 8, 9, 12). This recent drought episode in southwestern North America may be a harbinger of future global-change-type drought throughout much of North America and elsewhere, in which increased temperature in concert with multidecadal drought patterns associated with oceanic sea surface oscillations can drive extensive and rapid changes in vegetation and associated land surface properties.

We thank participants of the Drought Workshop in Flagstaff in 2003 and J. T. Overpeck, J. L. Betancourt, T. W. Swetnam, K. Larsen, F. J. Barnes, J. Salazar, J. L. Martinez, T. G. Schofield, and C. B. Zou for comments and/or technical support. D.D.B., P.M.R., and C.W.M. were supported by Los Alamos National Laboratory Directed Research. K.P.P. was supported by National Aeronautics and Space Administration Land Cover Land Use Change Grant NAG5-11337. C.D.A. was supported by the Global Change Program of the U.S. Geological Survey's Biological Resources Discipline. R.G.B. was supported by the U.S. Forest Service Rocky Mountain Research Station and the Los Alamos National Laboratory Biological Resources Management Program. O.B.M. was supported by National Institute of Environmental Health Sciences Grant P30ES012072. Support for regional collaboration was also provided by the National Science Foundation through the Drought-Induced Regional Ecosystem Response Network (National Science Foundation Grant DEB-0443526 to N.S.C.) and the Sustainability of Semi-Arid Hydrology and Riparian Areas Science and Technology Center (through National Science Foundation Cooperative Agreement EAR-9876800).