What kills the virtually immortal palms of the Florida scrub?

PREMISE: Life span varies greatly across plants, with some species being capable of extreme longevity. Yet even long-lived individuals are susceptible to climatic events, fire, and other challenges. We examined rare mortality events and their causes in two long-lived palmettos over four decades. METHODS: We monitored the survival of the clonal Serenoa repens and non-clonal, Florida-endemic Sabal etonia from 1981 to 2022 in four habitats along an elevational gradient within the globally imperiled Florida scrub ecosystem. We considered several challenges to palmetto survival, including extreme fires, shading due to lack of fire, droughts, periods of high precipitation, and possible pathogens. RESULTS: Survival of palmettos was remarkably high, and mortality was infrequent (Serenoa: cumulative, 5.7%; annualized, 0%-0.68%; Sabal: cumulative, 3.5%; annualized, 0%-0.43%). Mortality was highest in higher-elevation habitats with greater soil drainage, and smaller palmettos were more likely to die. When subjected to extreme fire, Serenoa suffered greater mortality than Sabal. Mortality in long-unburned habitats with increased shading rivaled that which occurred with extreme fire. There was no evidence of mortality due to lethal bronzing palm disease. CONCLUSIONS: Both palmettos had exceptionally low mortality rates, which, coupled with earlier work showing slow rates of transition from seedling to adult and remarkable adult longevity, suggest notably low rates of population turnover. Observed mortality in long-unburned habitats suggests the importance of fire-management planning with prescription burning. Lengthy age to reproduction and/or dependency on clonal propagation limits migration or genetic adaptation to altered conditions caused by climate change.

Detection of acoustic events in lavender for measuring xylem vulnerability to embolism and cellular damage.

Acoustic emission analysis is promising to investigate the physiological events leading to drought-induced injury and mortality. However, their nature and source are not fully understood, making this technique difficult to use as a direct measure of the loss of xylem hydraulic conductance. Acoustic emissions were recorded during severe dehydration in lavender plants (Lavandula angustifolia) and compared with the dynamics of embolism development and cell damage. The timing and characteristics of acoustic signals from two independent recording systems were compared by principal component analysis (PCA). Changes in water potential, branch diameter, loss of hydraulic conductance, and cellular damage were also measured to quantify drought-induced damages. Two distinct phases of acoustic emissions were observed during dehydration: the first one associated with a rapid loss of diameter and a significant increase in loss of xylem conductance (90%), and the second with slower changes in diameter and a significant increase in cellular damage. Based on PCA, a developed algorithm discriminated hydraulic-related acoustic signals from other sources, proposing a reconstruction of hydraulic vulnerability curves. Cellular damage preceded by hydraulic failure seems to lead to a lack of recovery. The second acoustic phase would allow detection of plant mortality.

When do Janzen-Connell effects matter? A phylogenetic meta-analysis of conspecific negative distance and density dependence experiments.

The Janzen-Connell (J-C) hypothesis suggests that specialised natural enemies cause distance- or density-dependent mortality among host plants and is regarded as an important mechanism for species coexistence. However, there remains debate about whether this phenomenon is widespread and how variation is structured across taxa and life stages. We performed the largest meta-analysis of experimental studies conducted under natural settings to date. We found little evidence of distance-dependent or density-dependent mortality when grouping all types of manipulations. Our analysis also reveals very large variation in response among species, with 38.5% of species even showing positive responses to manipulations. However, we found a strong signal of distance-dependent mortality among seedlings but not seed experiments, which we attribute to (a) seedlings sharing susceptible tissues with adults (leaves, wood, roots), (b) seedling enemies having worse dispersal than seed enemies and (c) seedlings having fewer physical and chemical defences than seeds. Both density- and distance-dependent mortality showed large variation within genera and families, suggesting that J-C effects are not strongly phylogenetically conserved. There were no clear trends with latitude, rainfall or study duration. We conclude that J-C effects may not be as pervasive as widely thought. Understanding the variation in J-C effects provides opportunities for new discoveries that will refine our understanding of J-C effects and its role in species coexistence.

Episodic defoliation rapidly reduces starch but not soluble sugars in an invasive shrub, Tamarix spp.

PREMISE: Plants rely on pools of internal nonstructural carbohydrates (NSCs: soluble sugars plus starch) to support metabolism, growth, and regrowth of tissues damaged from disturbance such as foliage herbivory. However, impacts of foliage herbivory on the quantity and composition of NSC pools in long-lived woody plants are currently unclear. We implemented a controlled defoliation experiment on mature Tamarix spp.-a dominant riparian woody shrub/tree that has evolved with intense herbivory pressure-to test two interrelated hypotheses: (1) Repeated defoliation disproportionately impacts aboveground versus belowground NSC storage. (2) Defoliation disproportionately impacts starch versus soluble sugar storage. METHODS: Hypotheses were tested by transplanting six Tamarix seedlings into each of eight cylinder mesocosms (2 m diameter, 1 m in depth). After 2.5 years, plants in four of the eight mesocosms were mechanically defoliated repeatedly over a single growing season, and all plants were harvested in the following spring. RESULTS: Defoliation had no impact on either above- or belowground soluble sugar pools. However, starch in defoliated plants dropped to 55% and 26% in stems and roots, respectively, relative to control plants, resulting in an over 2-fold higher soluble sugar to starch ratio in defoliated plants. CONCLUSIONS: The results suggest that defoliation occurring over a single growing season does not impact immediate plant functions such as osmoregulation, but depleted starch could limit future fitness, particularly where defoliation occurs over multiple years. These results improve our understanding of how woody plants cope with episodic defoliation caused by foliage herbivory and other disturbances.

Mechanisms of severe dieback and mortality in a classically drought-tolerant shrubland species (Arctostaphylos glauca).

PREMISE: Mortality events involving drought and pathogens in natural plant systems are on the rise due to global climate change. In Santa Barbara, California, United States, big berry manzanita (Arctostaphylos glauca) has experienced canopy dieback related to a multi-year drought and infection from fungal pathogens in the Botryosphaeriaceae family. A greenhouse experiment was conducted using Neofusicoccum australe to test the specific influences of drought and fungal infection on A. glauca. METHODS: A full factorial design was used to compare four treatment groups (drought + inoculation; drought - inoculation; watering + inoculation; and control: watering - inoculation). Data were collected for 10 weeks on stress symptoms, changes in leaf fluorescence and photosynthesis, and mortality. RESULTS: Results indicated significant effects of watering and inoculation treatments on net photosynthesis, dark-adapted fluorescence, and disease symptom severity (P < 0.05), and a strong correlation was found between physiological decline and visible stress (P < 0.0001). Mortality differed between treatments, with all groups except for the control experiencing mortality (43% mortality in drought - inoculation, 83% in watering - inoculation, and 100% in drought + inoculation). A Kaplan-Meier survival analysis showed drought + inoculation to have the least estimated survivorship compared to all other treatment groups. CONCLUSIONS: In addition to a possible synergistic interaction between drought and fungal infection in disease onset and mortality rates in A. glauca, these results indicate that young, non-drought-stressed plants are susceptible to mortality from N. australe infection, with important implications for the future of wildland shrub communities.

Greater focus on water pools may improve our ability to understand and anticipate drought-induced mortality in plants.

Drought-induced tree mortality has major impacts on ecosystem carbon and water cycles, and is expected to increase in forests across the globe with climate change. A large body of research in the past decade has advanced our understanding of plant water and carbon relations under drought. However, despite intense research, we still lack generalizable, cross-scale indicators of mortality risk. In this Viewpoint, we propose that a more explicit consideration of water pools could improve our ability to monitor and anticipate mortality risk. Specifically, we focus on the relative water content (RWC), a classic metric in plant water relations, as a potential indicator of mortality risk that is physiologically relevant and integrates different aspects related to hydraulics, stomatal responses and carbon economy under drought. Measures of plant water content are likely to have a strong mechanistic link with mortality and to be integrative, threshold-prone and relatively easy to measure and monitor at large spatial scales, and may complement current mortality metrics based on water potential, loss of hydraulic conductivity and nonstructural carbohydrates. We discuss some of the potential advantages and limitations of these metrics to improve our capacity to monitor and predict drought-induced tree mortality.

Drought-induced shoot dieback starts with massive root xylem embolism and variable depletion of nonstructural carbohydrates in seedlings of two tree species.

Combining hydraulic- and carbon-related measurements helps to understand drought-induced plant mortality. Here, we investigated the role that plant respiration (R) plays in determining carbon budgets under drought. We measured the hydraulic conductivity of stems and roots, and gas exchange and nonstructural carbohydrate (NSC) concentrations of leaves, stems and roots of seedlings of two resprouting species exposed to drought or well-watered conditions: Ulmus minor (riparian tree) and Quercus ilex (dryland tree). With increasing water stress (occurring more rapidly in larger U. minor), declines in leaf, stem and root R were less pronounced than that in leaf net photosynthetic CO2 uptake (Pn ). Daytime whole-plant carbon gain was negative below -4 and -6 MPa midday xylem water potential in U. minor and Q. ilex, respectively. Relative to controls, seedlings exhibiting shoot dieback suffered c. 80% loss of hydraulic conductivity in both species, and reductions in NSC concentrations in U. minor. Higher drought-induced depletion of NSC reserves in U. minor was related to higher plant R, faster stomatal closure, and premature leaf-shedding. Differences in drought resistance relied on the ability to maintain hydraulic conductivity during drought, rather than tolerating conductivity loss. Root hydraulic failure elicited shoot dieback and precluded resprouting without root NSC reserves being apparently limiting for R.

Herbivory-induced mortality increases with radial growth in an invasive riparian phreatophyte.

BACKGROUND AND AIMS: Under equal conditions, plants that allocate a larger proportion of resources to growth must do so at the expense of investing fewer resources to storage. The critical balance between growth and storage leads to the hypothesis that in high-resource environments, plants that express high growth rates are more susceptible to episodic disturbance than plants that express lower growth rates. METHODS: This hypothesis was tested by measuring the radial growth, basal area increment (BAI) and carbon isotope ratios (δ(13)C) in tree-ring α-cellulose of 62 mature tamarisk trees (Tamarix spp.) occurring at three sites in the western USA (n = 31 live and 31 killed trees across all sites, respectively). All of the trees had been subjected to periods of complete foliage loss by episodic herbivory over three or more consecutive growing seasons by the tamarisk leaf beetle (Diorhabda carinulata), resulting in approx. 50 % mortality at each site. KEY RESULTS: Mean annual BAI (measured from annual ring widths) in the 10 years prior to the onset of herbivory was on average 45 % higher in killed trees compared with live trees (P < 0·0001). Killed trees that had higher growth rates also expressed higher (less negative) δ(13)C ratios compared with live trees. In fact, at one site near Moab, UT, the mean annual BAI was 100 % higher in killed trees despite having about a 0·5 ‰ higher δ(13)C relative to live trees (P = 0·0008). Patterns of δ(13)C suggest that the intrinsic water-use efficiency was higher in killed than surviving trees, possibly as a consequence of lower whole-canopy stomatal conductance relative to live trees. CONCLUSIONS: The results show that a likely trade-off occurs between radial growth and survival from foliage herbivory in Tamarix spp. that currently dominates riparian areas throughout the western USA and northern Mexico. Thus, herbivory by D. carinulata may reduce the overall net primary productivity of surviving Tamarix trees and may result in a reduction in genetic variability in this dominant invasive tree species if these allocation patterns are adaptive.

Topography and vegetation structure mediate drought impacts on the understory of the South American Atlantic Forest.

Droughts have increased in frequency, duration, and severity across most of the tropics but their effect on forest communities remain not fully understood. Here we assessed the effects of a severe El Niño-induced drought event on dominant and low abundance understory plant species and the consequent impacts on ecosystem functions in the South American Atlantic Forest. We established 20 permanent plots with contrasting vegetation structure and topography. In each plot, we measured the stem diameter at breast height (DBH) of every understory woody plant (i.e. 1 to 10 cm stem diameter) before and after a severe 4-year drought event to calculate relative growth and mortality rates after drought. Litter biomass, litter nutrient content and soil nutrients, as well as tree canopy cover, were also quantified. High stem density reduced survival to drought for both dominant and low abundance understory woody species. The growth rate of dominant and low abundance species was lower on steeper slopes during the drought. Dominant species were the main contributor of litter biomass production whereas low abundance species were important drivers of litter quality. Overall, our findings suggest that habitats with low tree density and larger trees on flat areas, such as in valleys, can act as refuges for understory plant species during drought periods. These habitats are resource-rich, providing nutrients and water during unfavorable drought periods and might improve forest resilience to climate change in the long term.

Grass bud responses to fire in a semiarid savanna system.

Increasingly, land managers have attempted to use extreme prescribed fire as a method to address woody plant encroachment in savanna ecosystems. The effect that these fires have on herbaceous vegetation is poorly understood. We experimentally examined immediate (<24 hr) bud response of two dominant graminoids, a C3 caespitose grass, Nassella leucotricha, and a C4 stoloniferous grass, Hilaria belangeri, following fires of varying energy (J/m2) in a semiarid savanna in the Edwards Plateau ecoregion of Texas. Treatments included high- and low-energy fires determined by contrasting fuel loading and a no burn (control) treatment. Belowground axillary buds were counted and their activities classified to determine immediate effects of fire energy on bud activity, dormancy, and mortality. High-energy burns resulted in immediate mortality of N. leucotricha and H. belangeri buds (p < .05). Active buds decreased following high-energy and low-energy burns for both species (p < .05). In contrast, bud activity, dormancy, and mortality remained constant in the control. In the high-energy treatment, 100% (n = 24) of N. leucotricha individuals resprouted while only 25% (n = 24) of H. belangeri individuals resprouted (p < .0001) 3 weeks following treatment application. Bud depths differed between species and may account for this divergence, with average bud depths for N. leucotricha 1.3 cm deeper than H. belangeri (p < .0001). Synthesis and applications: Our results suggest that fire energy directly affects bud activity and mortality through soil heating for these two species. It is imperative to understand how fire energy impacts the bud banks of grasses to better predict grass response to increased use of extreme prescribed fire in land management.

Understanding the drivers of extensive plant damage in boreal and Arctic ecosystems: Insights from field surveys in the aftermath of damage.

The exact cause of population dieback in nature is often challenging to identify retrospectively. Plant research in northern regions has in recent decades been largely focussed on the opposite trend, namely increasing populations and higher productivity. However, a recent unexpected decline in remotely-sensed estimates of terrestrial Arctic primary productivity suggests that warmer northern lands do not necessarily result in higher productivity. As large-scale plant dieback may become more frequent at high northern latitudes with increasing frequency of extreme events, understanding the drivers of plant dieback is especially urgent. Here, we report on recent extensive damage to dominant, short, perennial heath and tundra plant populations in boreal and Arctic Norway, and assess the potential drivers of this damage. In the High-Arctic archipelago of Svalbard, we recorded that 8-50% of Cassiope tetragona and Dryas octopetala shoots were dead, and that the ratios of dead shoots increased from 2014 to 2015. In boreal Norway, 38-63% of Calluna vulgaris shoots were dead, while Vaccinium myrtillus had damage to 91% of shoots in forested sites, but was healthy in non-forested sites. Analyses of numerous sources of environmental information clearly point towards a winter climate-related reason for damage to three of these four species. In Svalbard, the winters of 2011/12 and 2014/15 were documented to be unusually severe, i.e. insulation from ambient temperature fluctuation by snow was largely absent, and ground-ice enforced additional stress. In boreal Norway, the 2013/14 winter had a long period with very little snow combined with extremely low precipitation rates, something which resulted in frost drought of uncovered Calluna plants. However, extensive outbreaks of a leaf-defoliating geometrid moth were identified as the driver of Vaccinium mortality. These results suggest that weather and biotic extreme events potentially have strong impacts on the vegetation state of northern lands.

High mortality, fluctuation in numbers, and heavy subterranean insect herbivory in bush lupine, Lupinus arboreus.

Sporadic patchy die-off of bush lupine, Lupinus arboreus, has long been known. We describe in detail a series of these incidents on the central California coast, based upon observational and comparative evidence. Stands of thousands of plants die, while nearby mature plants live on. In some sites, repeated die-off followed by regeneration from the seed bank has led to the cover and density of this woody, perennial plant fluctuating widely over the 40 year period for which records exist. Root damage by caterpillars of the ghost moth or "swift" Hepialus californicus (Lepidoptera, Hepialidae) is a major cause of individual bush death and a probable cause of die-off of stands of lupine. Hidden from view underground, a few of these insects readily kill a juvenile or young mature plant by girdling and reaming-out roots. The mass mortality of L. arboreus that we observed involved heavy root damage by these caterpillars in evenaged stands of plants in their first (1.5-year-old) or second (2.5-year-old) flowering season. The injured plants set seed before dying. Older, larger bush lupines better withstood root damage. In plants aged 3 or more years, damage and mortality were correlated with the intensity of ghost moth caterpillars in the roots. At the highest intensity (mean = 37.5, maximum = 62 caterpillars/root), a stand of large, old L. arboreus suffered 41% mortality; 45% of root cambium (median value) was destroyed by feeding caterpillars. Mass death of mature L. arboreus was not correlated with folivory, and leaf damage ranged from nil to moderate in instances of die-off. The western tussock moth, Orgyia vetusta, accounted for the highest levels of folivory, but this insect was rare when die-offs occurred. The lowest lupine mortality rates in our study occurred where tussock caterpillar intensities were high and where plants were repeatedly defoliated by this insect. However, experimental defoliation by high, but realistic, intensities of tussock moth caterpillars resulted in some mortality of mature bushes, and the combined effects of leaf and root herbivory have yet to be assessed. In its natural range on the California coast, bush lupine has several additional species of insect herbivores that can be locally abundant and injurious to the plant, although none is associated with die-off. Subterranean natural enemies of ghost moth caterpillars may play a role in the patchy waxing and waning of this shrub. Locally, a new species of entomophagous nematode (Heterorhabditis sp.) cause high mortality in the soil, before ghost moth caterpillars have entered the root. This natural enemy may thus afford lupines protection from heavy underground herbivory.

Pattern and mortality in Colorado Desert plants.

We tested for intraspecific interference among Colorado Desert shrubs using an integrated analysis of spatial pattern and juvenile mortality. The data set included 7,000 woody perennials of 24 species in a mapped hectare of Joshua Tree National Monument, California. The site is dominated by Ambrosia dumosa (62.0% of the stems), with Larre tridentata a conspicuous secondary species (2.3% of the stems). Analyses of static pattern for common species showed: (1) aggregated adults and juveniles for Ambrosia dumosa, Erigonum fasciculatum, Mirabilis bigelovii, and Sphaeralcea ambigua, with more aggregation among juveniles than adults; (2) randomly distributed adults and juveniles for Krameria grayi, Opuntia rasmosissima, Simondsia chinensis, and Yucca schidigera. The summed volumes and distances between nearest conspecific neighbors were positively correlated for Ambrosia dumosa and Larrea tridentata, but not significantly correlated for eight remaining species with ≥100 individuals. Static pattern suggests only weak evidence for negative interactions in Ambrosia and Larrea, and little evidence for other species. Alternative mechanisms other than negative interaction that could give rise to these static patterns are discussed. Juvenile mortality was documented for four common species (Ambrosia dumosa, Eriogonum fasciculatum, Mirabilis bigelovii, and Sphaeralcea ambigua) that experienced substantial mortality. Analyses show: (1) the proportion of individuals that died was independent of the initial density of conspecifics; (2) distance to conspecific adults did not differ for juveniles that died versus those that survived; and (3) death was no more likely for juveniles that contacted other plants than for those that were isolated. The exception was a vine, Mirabilis bigelovii, whose juveniles survived better in contact with other plants. In sum, neither spatial pattern nor patterns of mortality showed clear evidence of negative intraspecific interference.

Biology and Pathogenicity of Pratylenchus neglectus on Alfalfa.

Pratylenchus neglectus reduced the growth of alfalfa cultivars in greenhouse and growth chamber studies. Inocula (1,000, 5,000 and 10,000 nematodes per plant) reduced shoot dry weights of Ranger by 16, 27, and 40%, of Lahontan by 16, 32, and 40%, and of Nevada Synthetic XX (Nev Syn XX) by 18, 26, and 37%, respectively, at 26 ñ 2 C. Pratylenchus neglectus at 1,000 nematodes per plant reduced Ranger shoot dry weights by 5, 12, 18, and 27%, at 15, 20, 25, and 30 C, respectively, whereas 5,000 nematodes per plant reduced shoot dry weights by 12, 17, 26, and 38%, respectively, at similar temperatures. Reductions in dry root weights were directly related to reductions in shoot growth. At 1,000 nematodes per plant, Ranger root dry weights were reduced by 3, 14, 40, and 40%, whereas 5,000 nematodes per plant reduced root dry weight by 25, 31, 59, and 63%, respectively, at similar temperatures. Similar results were observed on Lahontan and Nev Syn XX at the same inoculum levels and soil temperatures. Nematode reproductive indices (final nematode population per plant divided by initial nematode inoculum per plant) were higher at 1,000 nematodes per plant than at 5,000 nematodes per plant, were positively correlated with temperature, and were unaffected by cultivar.