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Applying a Bayesian weighted surveillance approach to detect chronic wasting disease in white‐tailed deer

Surveillance is critical for early detection of emerging and re‐emerging infectious diseases. Weighted surveillance leverages heterogeneity in infection risk to increase sampling efficiency. Here, we apply a Bayesian approach to estimate weights for 16 surveillance classes of white‐tailed deer in Wisconsin, USA, relative to hunter‐harvested yearling males. We used these weights to conduct a surveillance programme for detecting chronic wasting disease (CWD) in white‐tailed deer at Shenandoah National Park (SHEN) in Virginia, USA. Generally, for surveillance, risk of infection increased with age and was greater in males. Clinical suspect deer had the highest risk, with weight estimates of 33.33 and 9.09 for community‐reported and hunter‐reported suspect deer, respectively. Fawns had the lowest risk with an estimated weight of 0.001. We used surveillance weights for Wisconsin deer to determine sampling effort required to detect a CWD‐positive case in SHEN if prevalence in yearling males ≥0.025. The sampling required to detect CWD was 37–91 adult deer, depending on the adult male:female ratio in the surveillance stream. We collected rectal biopsies from 49 female and 21 male adult deer, and 10 additional samples from vehicle‐killed deer. CWD was not detected and we concluded with 95% probability that prevalence in the reference population (yearling males) was between 0.0% and 3.6%. Synthesis and applications . Our approach allows managers to estimate relative surveillance weights for different host classes and quantify limits of disease detection in real time when only a sample of animals from a population can be tested, resulting in considerable cost savings for agencies performing wildlife disease detection surveillance. Additionally, it provides a rigorous means of estimating prevalence limits when a disease/pathogen is not detected in a sample set. It is therefore applicable to other wildlife, domestic animal and human disease systems, which can be characterized by surveillance classes with heterogeneous probability of infection. This methodology is also extendable to other disciplines such as invasive species, environmental toxicology, and generally, any ecological question seeking to efficiently use scarce financial and human resources to maximize the detection probability of a rare event.

Journal of Applied Ecology

Wildfire reveals transient changes to individual traits and population responses of a native bumble bee ( Bombus vosnesenskii )

1. Fire-induced changes in the abundance and distribution of organisms, especially plants, can alter resource landscapes for mobile consumers driving bottom-up effects on their population sizes, morphologies, and reproductive potential. We expect these impacts to be most striking for obligate visitors of plants, like bees and other pollinators, but these impacts can be difficult to interpret due to the limited information provided by forager counts in the absence of survival or fitness proxies. 2. Increased bumble bee worker abundance is often coincident with the pulses of flowers that follow recent fire. However, it is unknown if observed postfire activity is due to underlying population growth or a stable pool of colonies recruiting more foragers to abundant resource patches. This distinction is necessary for determining the net impact of disturbance on bumble bees: are there population-wide responses or do just a few colonies reap the rewards? 3. We estimated colony abundance before and after fire in burned and unburned areas using a genetic mark-recapture framework. We paired colony abundance estimates with measures of body size, counts of queens, and estimates of foraging and dispersal to assess changes in worker size, reproductive output, and landscape-scale movements. 4. Higher floral abundance following fire not only increased forager abundance, but also the number of colonies from which those foragers came. Importantly, despite a larger population size we also observed increased mean worker size. Two years following fire, queen abundance was higher in both burned and unburned sites, potentially due to the dispersal of queens from burned into unburned areas. The effects of fire were transient; within two growing seasons, worker abundance was substantially reduced across the entire sampling area and body sizes were similar between burned and unburned sites. 5. Our results reveal how disturbance can temporarily release populations from resource limitation, boosting the genetic diversity, body size, and reproductive output of populations. Given that the effects of fire on bumble bees acted indirectly through pulsed resource availability, it is likely our results are generalizable to other situations, such as habitat restorations, where resource density is enhanced within the landscape.

California

Establishment of two invasive crustaceans (Copepoda: Harpacticoida) on the nearshore sands of Lake Michigan

Benthic copepods (Copepoda: Harpacticoida) in the nearshore sediments of southern Lake Michigan appear to be dominated by two new invasive species. We report the first occurrence in North America of Schizopera borutzkyi Montschenko, a native to the Danube River delta, and Heteropsyllus nr. nunni, likely a new species that is morphologically similar to the marine species Heteropsyllus nunni and represents the first occurrence of this genus in freshwater. Schizopera borutzkyi is a euryhaline species occurring in shallow sands in its native habitat and in deeper sands (6-15 m) in southern Lake Michigan. Based on the absence of these species from previous studies, we suggest that they are recent introductions. Heteropsyllus nr. nunni dominated (55-100%) the harpacticoid abundance to depths of 9 m, but S. borutzkyi comprised 75% of the harpacticoid abundance at 15 m. Native harpacticoids were always greatly outnumbered by invasive harpacticoids in our samples, which suggests that the natives are being replaced rapidly or that the invasive species are finding unused resources. The ecological implications of these introductions are not known, but these invasions may represent continued 'invasional meltdown' in Lake Michigan.

Canadian Journal of Fisheries and Aquatic Sciences

Investing in citizen science can improve natural resource management and environmental protection

Citizen science has made substantive contributions to science for hundreds of years. More recently, it has contributed to many articles in peer-reviewed scientific journals and has influenced natural resource management and environmental protection decisions and policies across the nation. Over the last 10 years, citizen science—participation by the public in a scientific project—has seen explosive growth in the United States, particularly in ecology, the environmental sciences, and related fields of inquiry. In this report, we explore the current use of citizen science in natural resource and environmental science and decision making in the United States and describe the investments organizations might make to benefit from citizen science.

Issues in Ecology

Stress gradients interact with disturbance to reveal alternative states in salt marsh: Multivariate resilience at the landscape scale

Stress gradients influence many ecosystem processes and properties, including ecosystem recovery from and resistance to disturbance. While recent analytical approaches have advanced multivariate metrics of ecosystem resilience that allow quantification of conceptual resilience models and identification of thresholds of state change, these approaches are not often translated to landscape scales. Using natural and restored salt marshes in Louisiana, USA, we quantified plant community recovery and resistance metrics along flooding stress gradients. n ‐dimensional hypervolumes of plant community biomass and structure were simulated using field data collected from disturbance‐recovery experiments. The relationships between multivariate resilience metrics and flooding stress gradients were then mapped at community‐ and landscape‐relevant scales by scaling with airborne‐derived data across the region. Greater pre‐disturbance abiotic stress decreased live belowground, but not aboveground, biomass, and ultimately led to lower post‐disturbance total recovery, recovery rates, and resistance of plant communities. Vegetated plots flooded >52% of the time transitioned to an alternative, unvegetated state after disturbance. Mapping revealed differences in spatial patterns of resilience‐ highlighting low, interior marsh edges as especially vulnerable to the combination of chronic flooding stress and acute disturbance. At the landscape scale, approximately half of the area (48%) is vulnerable to state change after pulse disturbances. Synthesis . Ultimately, we quantify the ball‐and‐cup conceptual model for a salt marsh ecosystem and its alternative state, mudflat. We find that increasing abiotic stress due to climate change diminishes ecosystem resilience, but the interaction with common episodic disturbances is necessary to reveal transitions to alternative states and quantify state change thresholds. Quantifying and mapping resilience and where alternative states may exist in this fashion improves ecologists’ ability to investigate the mechanisms of stress gradient control on emergent ecosystem properties, while providing spatially explicit resources for managing ecosystems according to their projected resilience.

Louisiana

Differing modes of biotic connectivity within freshwater ecosystem mosaics

We describe a collection of aquatic and wetland habitats in an inland landscape, and their occurrence within a terrestrial matrix, as a “freshwater ecosystem mosaic” (FEM). Aquatic and wetland habitats in any FEM can vary widely, from permanently ponded lakes, to ephemerally ponded wetlands, to groundwater‐fed springs, to flowing rivers and streams. The terrestrial matrix can also vary, including in its influence on flows of energy, materials, and organisms among ecosystems. Biota occurring in a specific region are adapted to the unique opportunities and challenges presented by spatial and temporal patterns of habitat types inherent to each FEM. To persist in any given landscape, most species move to recolonize habitats and maintain mixtures of genetic materials. Species also connect habitats through time if they possess needed morphological, physiological, or behavioral traits to persist in a habitat through periods of unfavorable environmental conditions. By examining key spatial and temporal patterns underlying FEMs, and species‐specific adaptations to these patterns, a better understanding of the structural and functional connectivity of a landscape can be obtained. Fully including aquatic, wetland, and terrestrial habitats in FEMs facilitates adoption of the next generation of individual‐based models that integrate the principles of population, community, and ecosystem ecology.

Journal of the American Water Resources Associatio

Tree mortality response to drought-density interactions suggests opportunities to enhance drought resistance

The future of dry forests around the world is uncertain given predictions that rising temperatures and enhanced aridity will increase drought-induced tree mortality. Using forest management and ecological restoration to reduce density and competition for water offers one of the few pathways that forests managers can potentially minimize drought-induced tree mortality. Competition for water during drought leads to elevated tree mortality in dense stands, although the influence of density on heat-induced stress, and the durations of hot or dry conditions that most impact mortality, remain unclear. Understanding how competition interacts with hot-drought stress is essential to recognize how, where, and how much reducing density can help sustain dry forests in a rapidly changing world. Here, we integrated repeat measurements of 28,881 ponderosa pine trees across the western US (2000-2017) with soil moisture estimates from a water balance model to examine how annual mortality responds to competition, temperature and soil moisture conditions. Tree mortality responded most strongly to basal area, and was elevated in places with high mean temperatures, unusually hot 7-year high temperature anomalies, and unusually dry 8-year low soil moisture anomalies. Mortality was also lower in places that experienced unusually wet 3-year soil moisture anomalies between measurements. Importantly, we found that basal area interacts with temperature and soil moisture, exacerbating mortality during times of stress imposed by high temperature or low moisture. Synthesis and Applications: Our results imply that a 50% reduction in forest basal area could reduce drought-driven tree mortality by 20-80%. The largest impacts of density reduction are seen in areas with high current basal area and places that experience high temperatures and/or severe multiyear droughts. These interactions between competition and drought are critical to understand past and future patterns of tree mortality in the context of climate change, and provide information for resource managers seeking to enhance dry forest drought resistance.

Journal of Applied Ecology.

Shorebird stopover habitat decisions in a changing landscape

To examine how habitat use by sandpipers ( Calidris spp.; Baird's sandpipers, dunlin, least sandpipers, pectoral sandpipers, semipalmated sandpipers, stilt sandpipers, and white-rumped sandpipers) varies across a broad suite of environmental conditions, we conducted surveys at wetlands throughout the spring migratory period in 2013 and 2014 in 2 important stopover regions: the Rainwater Basin (RWB) in Nebraska, USA, and the Prairie Pothole Region (PPR) in South Dakota, USA. Because providing adequate energetic resources for migratory birds is a high priority for wetland management, we also measured invertebrate abundance at managed wetlands in the RWB to determine how food abundance influences the occupancy and abundance of sandpipers on wetlands throughout the migratory period. To quantify habitat use, we surveyed wetlands every 7–10 days in both regions and visually estimated wetland attributes. Our results indicate that invertebrate abundance predicted occupancy, but not abundance, of sandpipers at wetlands in the RWB. The wetland vegetation characteristics that predict sandpiper occupancy are similar in both regions, but wetlands in the PPR support a higher abundance of sandpipers than wetlands in the RWB. Our results suggest that sandpipers make stopover decisions that balance local and regional wetland conditions. Managers should maintain the cues (i.e., mudflat) and ecological conditions beyond invertebrate abundance that predict sandpiper habitat use to successfully provide resources for sandpipers during migratory stopover if that is a goal of wetland management. © 2017 The Wildlife Society.

Nebraska, South Dakota

The transition from resistance to acceptance: Managing a marine invasive species in a changing world

Marine invasive species can transform coastal ecosystems, yet mitigating their effects can be difficult, and even impractical. Often, marine invasive species are managed at poorly matched spatial scales, and at the same time, rates of spread and establishment are increasing under climate change and can outpace resources available for population suppression. These circumstances challenge traditional conservation goals of maintaining a historic environmental state, especially for a species like the European green crab ( Carcinus maenas ), a formidable invader with few examples of successful long-term removal programs. A management paradigm where decision alternatives include resisting or accepting a new ecological trajectory may be needed. We apply mathematical concepts from decision theory to develop a quantitative framework for navigating management decisions in this new resist-accept paradigm. We develop a model of European green crab growth, removal and colonization, and we find optimal levels of removal effort that minimize both ecological change and removal cost. We establish a benchmark of colonization pressure at which green crab density becomes decoupled from a decision maker's actions, such that population control can no longer shape the invasion trajectory. For informing the decision boundary between resistance and acceptance, our results highlight that a decision maker's understanding of how removal cost scales with removal effort is more important than understanding the density-impact relationship. We show that assuming stationary system dynamics can result in sub-optimal levels of species removal effort, highlighting the importance of developing anticipatory management strategies by accounting for non-stationary dynamics. Policy implications . For marine invasive species that can disperse across long distances and recolonize rapidly after removal, the focus of conservation policy should shift away from understanding how to resist change to understanding when to stop resisting change. Navigating this decision problem involves trade-offs among competing objectives, highlighting the need for structured approaches to elicit objective weights that reflect the values of the decision maker. For natural resource managers facing possible ecosystem transformation, this decision framework can enable proactive and strategic decisions made under uncertainty in a changing world.

Journal of Applied Ecology

Terrestrial–aquatic linkages in spring-fed and snowmelt-dominated streams

The importance of trophic linkages between aquatic and terrestrial ecosystems is predicted to vary as a function of subsidy quantity and quality relative to in situ resources. To test this prediction, I used multi-year diet data from Bonneville cutthroat trout Oncorhynchus clarki Utah in spring-fed and snowmelt-driven streams in the high desert of western North America. I documented that trout in spring-fed streams consumed more (number and weight) aquatic than terrestrial invertebrates, while trout in snowmelt-driven streams consumed a similar number of both prey types but consumed more terrestrial than aquatic invertebrates by weight. Trout in spring-fed streams consumed more aquatic invertebrates than trout in snowmelt streams and trout consumed more terrestrial invertebrates in snowmelt than in spring-fed streams. Up to 93% of trout production in spring-fed streams and 60% in snowmelt streams was fueled by aquatic invertebrates, while the remainder of trout production in each stream type was from terrestrial production. I found that the biomass and occurrence of consumed terrestrial invertebrates were not related to our measures of in situ resource quality or quantity in either stream type. These empirical data highlight the importance of autotrophic-derived production to trout in xeric regions.

Idaho

Behavioural plasticity modulates temperature-related constraints on foraging time for a montane mammal

Contemporary climate change is altering temperature profiles across the globe. Increasing temperatures can reduce the amount of time during which conditions are suitable for animals to engage in essential activities, such as securing food. Behavioural plasticity, the ability to alter behaviour in response to the environment, may provide animals with a tool to adjust to changes in the availability of suitable thermal conditions. The extent to which individuals can alter fitness‐enhancing behaviours, such as food collection, to proximately buffer variation in temperature, however, remains unclear. Even less well understood are the potential performance advantages of flexible strategies among endotherms. We examined the degree to which individuals altered rates of food collection in response to temperature, and two potential benefits, using the American pika ( Ochotona princeps ), a temperature‐sensitive, food‐hoarding mammal, as a model. From July–September 2013–2015, we used motion‐activated cameras and in situ temperature loggers to examine pika food‐caching activity for 72 individuals across 10 sites in the central Rocky Mountains, USA. We quantified % nitrogen by cache volume as a metric of cache quality, and the number of events during which pikas were active in temperatures ≥25°C as a measure of potential thermoregulatory stress. We found a strong negative effect of temperature on the rate at which pikas cached food. Individual responses to temperature varied substantially in both the level of food‐collecting activity and in the degree to which individuals shifted activity with warming temperature. After accounting for available foraging time, individuals that exhibited greater plasticity collected a comparable amount of nitrogen, while simultaneously experiencing fewer occasions in which temperatures eclipsed estimated thermal tolerances. By varying food‐collection norms of reaction, individuals were able to plastically respond to temperature‐driven reductions in foraging time. Through this increased flexibility, individuals amassed food caches of comparable quality, while minimizing exposure to potentially stressful thermal conditions. Our results suggest that, given sufficient resource quality and availability, plasticity in foraging activity may help temperature‐limited endotherms adjust to climate‐related constraints on foraging time.

Wyoming

Lightning fires in North Dakota grasslands and in pine-savanna lands of South Dakota and Montana

Lightning strike fires which occurred between 1940 and 1981 were studied in mixed-grass prairie grasslands and in pine-savanna lands in the Northern Great Plains region. A majority (73%) of ignitions occurred during July and August, while a lesser number was recorded in April, May, June, and September. The April-September period is also the average time of the freeze-free period and approximates the average distribution period for thunderstorm activity in this region. The area burned by each of 293 lightning fires (most of which were suppressed) ranged from 0.004-1158.3 ha ( X̄ = 10.8 ha). The frequency of lightning fires in mixed-grass prairie grasslands averaged 6.0/yr per 10,000 km 2 in eastern North Dakota, 22.4/yr per 10,000 km 2 in southcentral North Dakota, 24.7/yr per 10,000 km 2 in western North Dakota, and 91.7/yr per 10,000 km 2 in pine-savanna lands in northwestern South Dakota and southeastern Montana. The ecological role of lightning-set fires is discussed relative to the development of resource research and management plans and to the interpretation of historical records of natural fire occurrence in the Northern Great Plains region.

Journal of Range Management

Competitive interactions between walleye (Sander vitreus) and smallmouth bass (Micropterus dolomieu) under various controlled conditions

The range of smallmouth bass (Micropterus dolomieu) is expanding northward, creating new interactions with native predators, including walleye (Sander vitreus). We used a series of experiments to investigate competition between walleye (WAE) and smallmouth bass (SMB) at different life stages and light conditions, identified behaviors that allowed one fish to outcompete another, and evaluated whether prey switching mitigated competitive interactions. Juvenile and adult SMB appeared to outcompete WAE when fed during the daytime; neither species dominated when fed near dusk. Attack rates and capture efficiencies of both species were similar with an intra- or interspecific competitor, but SMB often exploited prey before the competitor had a chance to feed (exploitative competition) or displayed agonistic behaviors toward a potential competitor (interference competition). Prey selectivity of WAE or SMB did not differ when by themselves or with a potential competitor. These results indicate that SMB could outcompete WAE under limiting prey conditions due to the aggressive nature of SMB, but resources may be partitioned at least along a temporal scale. ?? 2011 Taylor & Francis.

Journal of Freshwater Ecology

The early bird gets the shrimp: Confronting assumptions of isotopic equilibrium and homogeneity in a wild bird population

1. Because stable isotope distributions in organic material vary systematically across energy gradients that exist in ecosystems, community and population structures, and in individual physiological systems, isotope values in animal tissues have helped address a broad range of questions in animal ecology. It follows that every tissue sample provides an isotopic profile that can be used to study dietary or movement histories of individual animals. Interpretations of these profiles depend on the assumption that metabolic pools are isotopically well mixed and in equilibrium with dietary resources prior to tissue synthesis, and they extend to the population level by assuming isotope profiles are identically distributed for animals using the same proximal dietary resource. As these assumptions are never fully met, studying structure in the variance of tissue isotope values from wild populations is informative. 2. We studied variation in δ 13 C, δ 15 N, δ 2 H and δ 18 O data for feathers from a population of eared grebes (Podiceps nigricollis) that migrate to Great Salt Lake each fall to moult feathers. During this time, they cannot fly and feed almost exclusively on superabundant brine shrimp (Artemia franciscana). The ecological simplicity of this situation minimized the usual spatial and trophic complexities often present in natural studies of feather isotope values. 3. Ranges and variances of isotope values for the feathers were larger than those from previously published studies that report feather isotopic variance, but they were bimodally distributed in all isotope dimensions. Isotope values for proximal dietary resources and local surface water show that some of the feathers we assumed to have been grown locally must have been grown before birds reached isotopic equilibrium with local diet or immediately prior to arrival at Great Salt Lake. 4. Our study provides novel insights about resource use strategies in eared grebes during migration. More generally, it demonstrates the utility of studying variance structures and questioning assumptions implicit in the interpretation of stable isotope data from wild animals.

Utah

Low-complexity floodplain inundation model performs well for ecological and management applications in a large river ecosystem

Flooding is a dominant physical process that drives the form and function of river-floodplain ecosystems. Efficiently characterizing flooding dynamics can be challenging, especially over geographically broad areas or at spatial and temporal scales relevant for ecosystem management activities. Here, we empirically evaluated a low-complexity geospatial model of floodplain inundation in six study segments of the Upper Mississippi River System (UMRS) by pairing spatially extensive, temporally limited and spatially limited, temporally extensive sampling designs. We found little evidence of systematic bias in model performance although discrepancies between model predictions and empirical data did occur locally. Assessments of model predictions revealed low segment-wide discrepancies of wetted extent under contrasting flow conditions and agreement for inundation event detection and duration. Model performance for predicting event frequency and duration was similar among sites expected to exhibit contrasting patterns of hydrologic connectivity with the main channel. Our results suggest that low-complexity models can efficiently characterize a critical physical process across geographically broad, complex river-floodplain ecosystems. Such tools have the potential for advancing scientific understanding of landscape-scale ecological patterns and for prioritizing management actions in large, complex river-floodplain ecosystems like the UMRS.

Illinois, Iowa, Minnesota, Missouri, Wisconsin

[Book review] Waterfowl ecology and management: Selected readings

This book is a compilation of papers from the extensive and varied published literature on the ecology and management of waterfowl. The 125 technical papers reprinted in this book are arranged in eight major sections and are from 21 journals, government reports, several books, and proceedings of symposia and annual conferences. The most frequent sources of papers are The Journal of Wildlife Management, The Auk, Transactions North American Wildlife and Natural Resources Conference, and Wildfowl. These readings span the period from 1937 through 1981. A majority of the technical papers was published during the sixties and seventies, reflecting the expansion of waterfowl research during that period. The front cover and the introductory page of each section are illustrated with black-and-white drawings of North American waterfowl by D. R. Barrick.

The Auk

Age, growth, and reproductive biology of three catostomids from the Apalachicola River, Florida

Riverine catostomids can show a wide range of interspecific variation in life-history characteristics. Understanding these differences is an important consideration in evaluating the sensitivity of these fishes to disturbance and in formulating effective conservation strategies, particularly when dealing with an assemblage consisting of multiple species within a watershed. We collected Apalachicola redhorse Moxostoma n. sp. cf. poecilurum ( n = 125), spotted sucker Minytrema melanops ( n = 94), and quillback Carpiodes cyprinus ( n = 94) to determine age, growth, and reproductive biology of spawning catostomids in the Apalachicola River, Florida, during 2007. Quillback was the smallest in total length at age; longest-lived; most fecund; and produced the smallest eggs. Apalachicola redhorse was the largest in body size; had an intermediate life span; and produced the fewest yet largest eggs. Spotted sucker was more similar to Apalachicola redhorse in most characteristics. Growth during ages 1-3 in all three species seemed to be negatively related to the proportion of observations of extreme flow, both high (Q 90 ) and low (Q 10 ), per year and a positive response in growth rate to high flows (>Q 75 but < Q 90 ). However, Apalachicola redhorse and spotted sucker growth was more sensitive to flow conditions than that of quillback. Our results suggest the life histories and ecological response of Apalachicola River catostomids to flow regulation are important components for developing strategies that incorporate the needs of these fishery resources into an ecosystem-based management approach.

Florida

How will predicted land-use change affect waterfowl spring stopover ecology? Inferences from an individual-based model

Habitat loss, habitat fragmentation, overexploitation and climate change pose familiar and new challenges to conserving natural populations throughout the world. One approach conservation planners may use to evaluate the effects of these challenges on wildlife populations is scenario planning. We developed an individual-based model to evaluate the effects of future land use and land cover changes on spring-migrating dabbling ducks in North America. We assessed the effects of three Intergovernmental Panel on Climate Change emission scenarios (A1B, A2 and B1) on dabbling duck stopover duration, movement distances and mortality. We specifically focused on migration stopover duration because previous research has demonstrated that individuals arriving earlier on the nesting grounds exhibit increased reproductive fitness. Compared to present conditions, all three scenarios increased stopover duration and movement distances of agent ducks. Although all three scenarios presented migrating ducks with increased amounts of wetland habitat, scenarios also contained substantially less cropland, which decreased overall carrying capacity of the study area. Synthesis and applications . Land-use change may increase waterfowl spring migration stopover duration in the midcontinent region of North America due to reduced landscape energetic carrying capacity. Climate change will alter spatial patterns of crop distributions with corn and rice production areas shifting to different regions. Thus, conservation planners will have to address population-level energetic implications of shifting agricultural food resources and increased uncertainty in yearly precipitation patterns within the next 50 years.

Journal of Applied Ecology