WHY DOES DROUGHT KILL TREES? INTERACTIONS BETWEEN WATER, CARBON, AND FUNGAL SYMBIONTS

One of the global causes of forest die-off is climate-change induced drought. Drought kills trees by reducing water supply and non-structural carbohydrate (NSC) availability and by increasing susceptibility to negative biotic interactions. However, we lack an understanding of how water, NSC, and biotic agents interact. As a result, we still cannot accurately predict drought-induced mortality. The overarching goal of my dissertation is to increase our understanding of the interacting mechanisms leading to drought-induced mortality (DIM) and to identify physiological variables that accurately predict risk of DIM. Via greenhouse experiments with Pinus ponderosa (ponderosa pine) seedlings, I addressed three overarching research questions: (1) which physiological variables are good predictors of DIM?, (2) What is the role of NSC on plant water relations and DIM?, and (3) Do fungal symbionts affect plant water relations by altering host NSC during periods of carbon deficit? I first show that plant water content integrates the negative effects of reduced water supply and NSC availability under drought and it accurately predicts DIM risk. Further, plant water content shows a threshold at which DIM risk increases. I also provide evidence that plants use NSC to retain water in living tissues and maintain plant water content above critical mortality thresholds. Next, I show that plant water content is a good predictor of DIM risk across populations of ponderosa pine despite differences in morphology, physiology, and drought strategies. The integrative nature of plant water content is relevant because it can be detected remotely, which may allow large-scale assessments of mortality risk. Lastly, I show that fungal symbionts connecting multiple plant hosts can become parasitic and deplete NSC in some hosts. Such a depletion impairs plant water relations, which could increase host vulnerability to drought. My dissertation provides insight on physiological mechanisms leading to DIM and identifies simple physiological variables useful for monitoring DIM risk

Species climatic niche explains drought-induced die-off in a Mediterranean woody community

During the last decades, plant die-off has been reported worldwide as a result of increased frequency and intensity of extreme drought events. From a niche perspective, a species performance should decrease as the climatic conditions defining a drought event differ from those characterizing the species climatic niche (the average conditions experienced by the species). Species distribution models (SDMs) can potentially be used to test the link between species performance and their climatic niche by means of climatic suitability indexes. We studied the remaining green canopy of 18 woody species co-occurring in a Mediterranean shrubland from the central Iberian Peninsula that experienced a severe die-off following an extreme drought event. We found that the suitability of the climatic conditions estimated by SDMs strongly declined for all species during the extreme drought event. Species die-off was significantly explained by the decrease in climatic suitability during the event, estimated as the ratio between the historic and the extreme event climatic suitability. Species with high occupancy levels across the landscape exhibited higher die-off likely because (1) these species have short life-span and mortality would be compensated by later high recruitment or (2) populations of rare species may have experienced local adaptation to drier conditions. Our results indicate that extreme drought events can have a negative effect, even in shrubland communities living in arid environments. Also, we develop a new approach that connects population-level responses to species climatic niches through SDMs, and it can be applied to predict community responses to strong climatic variability, such as drought events

Climatic suitability derived from species distribution models captures community responses to an extreme drought episode

The differential responses of co-occurring species in rich communities to climate change-particularly to drought episodes-have been fairly unexplored. Species distribution models (SDMs) are used to assess changes in species suitability under environmental shifts, but whether they can portray population and community responses is largely undetermined, especially in relation to extreme events. Here we studied a shrubland community in SE Spain because this region constitutes an ecotone between the Mediterranean biome and subtropical arid areas, and it has recently suffered its driest hydrological year on record. We used four different modeling algorithms (Mahalanobis distance, GAM, BRT, and MAXENT) to estimate species' climatic suitability before (1950-2000) and during the extreme drought. For each SDM, we related species' climatic suitability with their remaining green canopy as a proxy for species resistance to drought. We consistently found a positive correlation between remaining green canopy and species' climatic suitability before the event. This relationship supports the hypothesis of a higher vulnerability of populations living closer to their species' limits of aridity tolerance. Contrastingly, climatic suitability during the drought did not correlate with remaining green canopy, likely because the exceptional episode led to almost zero suitability values. Overall, our approach highlights climatic niche modeling as a robust approach to standardizing and comparing the behavior of different co-occurring species facing strong climatic fluctuations. Although many processes contribute to resistance to climatic extremes, the results confirm the relevance of populations' position in the species' climatic niche for explaining sensitivity to climate change

Canopy spectral reflectance detects oak wilt at the landscape scale using phylogenetic discrimination

The oak wilt disease caused by the invasive fungal pathogen Bretziella fagacearum is one of the greatest threats to oak-dominated forests across the Eastern United States. Accurate detection and monitoring over large areas are necessary for management activities to effectively mitigate and prevent the spread of oak wilt. Canopy spectral reflectance contains both phylogenetic and physiological information across the visible near-infrared (VNIR) and short-wave infrared (SWIR) ranges that can be used to identify diseased red oaks. We develop partial least square discriminant analysis (PLS-DA) models using airborne hyperspectral reflectance to detect diseased canopies and assess the importance of VNIR, SWIR, phylogeny, and physiology for oak wilt detection. We achieve high accuracy through a three-step phylogenetic process in which we first distinguish oaks from other species (90% accuracy), then red oaks from white oaks (Quercus macrocarpa) (93% accuracy), and, lastly, infected from non-infected trees (80% accuracy). Including SWIR wavelengths increased model accuracy by ca. 20% relative to models based on VIS-NIR wavelengths alone; using a phylogenetic approach also increased model accuracy by ca. 20% over a single-step classification. SWIR wavelengths include spectral information important in differentiating red oaks from other species and in distinguishing diseased red oaks from healthy red oaks. We determined the most important wavelengths to identify oak species, red oaks, and diseased red oaks. We also demonstrated that several multispectral indices associated with physiological decline can detect differences between healthy and diseased trees. The wavelengths in these indices also tended to be among the most important wavelengths for disease detection within PLS-DA models, indicating a convergence of the methods. Indices were most significant for detecting oak wilt during late August, especially those associated with canopy photosynthetic activity and water status. Our study suggests that coupling phylogenetics, physiology, and canopy spectral reflectance provides an interdisciplinary and comprehensive approach that enables detection of forest diseases at large scales. These results have potential for direct application by forest managers for detection to initiate actions to mitigate the disease and prevent pathogen spread

Non-structural carbohydrate dynamics associated with drought-induced die-off in woody species of a shrubland community

The relationship between plant carbon economy and drought responses of co-occurring woody species can be assessed by comparing carbohydrate (C) dynamics following drought and rain periods, relating these dynamics to species' functional traits. We studied nine woody species coexisting in a continental Mediterranean shrubland that experienced severe drought effects followed by rain. During drought, NSC concentrations were overall lower in stems and roots of plants experiencing leaf loss, while SS decreases were smaller. Roots had higher NSC concentrations than stems. After the rain, NSC concentrations continued to decrease, while SS increased. Green foliage recovered after rain, particularly in plants previously experiencing higher leaf loss, independently of NSC concentrations during drought. Species with lower WD tended to have more SS during drought and lower SS increases after rain. In low-WD species, plants with severe leaf loss had lower NSC relative to undefoliated ones. No significant relationship was found between H or SLA and C content or dynamics. Our community-level study reveals that, while responses were species-specific, C stocks overall diminished in plants affected by prolonged drought and did not increase after a pulse of seasonal rain. Dynamics were faster for SS than NSC. We found limited depletion of SS, consistent with their role in basal metabolic, transport and signalling functions. In a scenario of increased drought under climate change, NSC stocks in woody plants are expected to decrease differentially in coexisting species, with potential implications for their adaptive abilities and community dynamics

Attempting Physical Contact with Geologic Time

Science and the arts have long been understood as two opposing systems of thought involving logic and emotion. However, both disciplines rely on similar thought processes to create something new. Thus, thinking of science and the arts as counterparts is not only false but also eliminates the potential for interaction and generation of powerful outreach tools which use both logic and emotion. Attempting Physical Contact with Geologic Time examines the cellular structure of plant stems as they transport water and how that structure is affected by drought stress, one of the main drivers of forest die-off worldwide. Under drought, plant stems experience high tension inside their vascular cells, also called tracheids, as a result of the polar bonding between water molecules and the demand of water by the dry atmosphere. This tension increases as water availability decreases. When this tension becomes too great, a plant cell can experience an embolism that disrupts water flow. After too many embolisms, the plant can no longer transport water. The art pieces in our project make these complex and microscopic processes visible and tangible in a new way. Viewers can literally walk around the work and examine it from multiple angles. The delicate physicality of this work evokes the strength and fragility of the natural systems upon which we depend. In one piece, holes burned through layers of the fabric represent the hollow cavities through which water is transported in a two-year-old pine seedling. The fabric panels are suspended in groups from the ceiling and an image of a cross-section of the seedling is projected from both sides of the piece. Slivers of light from the projection snake through the holes in the layers of fabric, echoing the meandering path of water up a plant stem. Another series stretches fabric taut over shaped panels that jut off the wall. By walking around the panels, viewers can see a vivid painting on the wall, almost hidden behind the surface of the white fabric. Embroidery on the taut silk evokes the structure of tracheid valves, but also is reminiscent of chromosomes and cellular reproduction. The measured, angular geometry of both the frames and the repeated embroidered valve motif is subverted by slight imperfections and irregularities in the stretched silk and the way it reflects color in unexpected ways. Two panels, human-height, are lifted at a precarious angle from the ground, suspended only by a weighted string. Walking behind those panels, which seem liable to fall at any moment, heightens the sense of tension, insecurity, and impermanence. This intrusion of chaos within ordered patterns reflects our imperfect methods of collecting and interpreting data. While taking a cross-section of a stem may provide information on growth patterns, it also kills the plant. The functioning of plant cells and seeds are points of departure for these works, but the pieces are also meant to raise questions about how our current methods of discovering new information alter the natural state of organisms, obscuring as much as they reveal

Species climatic niche explains drought-induced die-off in a Mediterranean woody community

During the last decades, plant die-off has been reported worldwide as a result of increased frequency and intensity of extreme drought events. From a niche perspective, a species performance should decrease as the climatic conditions defining a drought event differ from those characterizing the species climatic niche (the average conditions experienced by the species). Species distribution models (SDMs) can potentially be used to test the link between species performance and their climatic niche by means of climatic suitability indexes. We studied the remaining green canopy of 18 woody species co-occurring in a Mediterranean shrubland from the central Iberian Peninsula that experienced a severe die-off following an extreme drought event. We found that the suitability of the climatic conditions estimated by SDMs strongly declined for all species during the extreme drought event. Species die-off was significantly explained by the decrease in climatic suitability during the event, estimated as the ratio between the historic and the extreme event climatic suitability. Species with high occupancy levels across the landscape exhibited higher die-off likely because (1) these species have short life-span and mortality would be compensated by later high recruitment or (2) populations of rare species may have experienced local adaptation to drier conditions. Our results indicate that extreme drought events can have a negative effect, even in shrubland communities living in arid environments. Also, we develop a new approach that connects population-level responses to species climatic niches through SDMs, and it can be applied to predict community responses to strong climatic variability, such as drought events

Positive root pressure is critical for whole-plant desiccation recovery in two species of terrestrial resurrection ferns

Desiccation-tolerant (DT) organisms can lose nearly all their water without dying. Desiccation tolerance allows organisms to survive in a nearly completely dehydrated, dormant state. At the cellular level, sugars and proteins stabilize cellular components and protect them from oxidative damage. However, there are few studies of the dynamics and drivers of whole-plant recovery in vascular DT plants. In vascular DT plants, whole-plant desiccation recovery (resurrection) depends not only on cellular rehydration, but also on the recovery of organs with unequal access to water. In this study, in situ natural and artificial irrigation experiments revealed the dynamics of desiccation recovery in two DT fern species. Organ-specific irrigation experiments revealed that the entire plant resurrected when water was supplied to roots, but leaf hydration alone (foliar water uptake) was insufficient to rehydrate the stele and roots. In both species, pressure applied to petioles of excised desiccated fronds resurrected distal leaf tissue, while capillarity alone was insufficient to resurrect distal pinnules. Upon rehydration, sucrose levels in the rhizome and stele dropped dramatically as starch levels rose, consistent with the role of accumulated sucrose as a desiccation protectant. These findings provide insight into traits that facilitate desiccation recovery in dryland ferns associated with chaparral vegetation of southern California

Climatic suitability derived from species distribution models captures community responses to an extreme drought episode

The differential responses of co-occurring species in rich communities to climate change-particularly to drought episodes-have been fairly unexplored. Species distribution models (SDMs) are used to assess changes in species suitability under environmental shifts, but whether they can portray population and community responses is largely undetermined, especially in relation to extreme events. Here we studied a shrubland community in SE Spain because this region constitutes an ecotone between the Mediterranean biome and subtropical arid areas, and it has recently suffered its driest hydrological year on record. We used four different modeling algorithms (Mahalanobis distance, GAM, BRT, and MAXENT) to estimate species' climatic suitability before (1950-2000) and during the extreme drought. For each SDM, we related species' climatic suitability with their remaining green canopy as a proxy for species resistance to drought. We consistently found a positive correlation between remaining green canopy and species' climatic suitability before the event. This relationship supports the hypothesis of a higher vulnerability of populations living closer to their species' limits of aridity tolerance. Contrastingly, climatic suitability during the drought did not correlate with remaining green canopy, likely because the exceptional episode led to almost zero suitability values. Overall, our approach highlights climatic niche modeling as a robust approach to standardizing and comparing the behavior of different co-occurring species facing strong climatic fluctuations. Although many processes contribute to resistance to climatic extremes, the results confirm the relevance of populations' position in the species' climatic niche for explaining sensitivity to climate change

Canopy spectral reflectance detects oak wilt at the landscape scale using phylogenetic discrimination

The oak wilt disease caused by the invasive fungal pathogen Bretziella fagacearum is one of the greatest threats to oak-dominated forests across the Eastern United States. Accurate detection and monitoring over large areas are necessary for management activities to effectively mitigate and prevent the spread of oak wilt. Canopy spectral reflectance contains both phylogenetic and physiological information across the visible near-infrared (VNIR) and short-wave infrared (SWIR) ranges that can be used to identify diseased red oaks. We develop partial least square discriminant analysis (PLS-DA) models using airborne hyperspectral reflectance to detect diseased canopies and assess the importance of VNIR, SWIR, phylogeny, and physiology for oak wilt detection. We achieve high ac- curacy through a three-step phylogenetic process in which we first distinguish oaks from other species (90% accuracy), then red oaks from white oaks (Quercus macrocarpa) (93% accuracy), and, lastly, infected from non- infected trees (80% accuracy). Including SWIR wavelengths increased model accuracy by ca. 20% relative to models based on VIS-NIR wavelengths alone; using a phylogenetic approach also increased model accuracy by ca. 20% over a single-step classification. SWIR wavelengths include spectral information important in differentiating red oaks from other species and in distinguishing diseased red oaks from healthy red oaks. We determined the most important wavelengths to identify oak species, red oaks, and diseased red oaks. We also demonstrated that several multispectral indices associated with physiological decline can detect differences between healthy and diseased trees. The wavelengths in these indices also tended to be among the most important wavelengths for disease detection within PLS-DA models, indicating a convergence of the methods. Indices were most significant for detecting oak wilt during late August, especially those associated with canopy photosynthetic activity and water status. Our study suggests that coupling phylogenetics, physiology, and canopy spectral reflectance provides an interdisciplinary and comprehensive approach that enables detection of forest diseases at large scales. These results have potential for direct application by forest managers for detection to initiate actions to mitigate the disease and prevent pathogen spread