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The plant phenology monitoring design for the National Ecological Observatory Network

Phenology is an integrative science that comprises the study of recurring biological activities or events. In an era of rapidly changing climate, the relationship between the timing of those events and environmental cues such as temperature, snowmelt, water availability or day length are of particular interest. This article provides an overview of the plant phenology sampling which will be conducted by the U.S. National Ecological Observatory Network NEON, the resulting data, and the rationale behind the design. Trained technicians will conduct regular in situ observations of plant phenology at all terrestrial NEON sites for the 30-year life of the observatory. Standardized and coordinated data across the network of sites can be used to quantify the direction and magnitude of the relationships between phenology and environmental forcings, as well as the degree to which these relationships vary among sites, among species, among phenophases, and through time. Vegetation at NEON sites will also be monitored with tower-based cameras, satellite remote sensing and annual high-resolution airborne remote sensing. Ground-based measurements can be used to calibrate and improve satellite-derived phenometrics. NEON’s phenology monitoring design is complementary to existing phenology research efforts and citizen science initiatives throughout the world and will produce interoperable data. By collocating plant phenology observations with a suite of additional meteorological, biophysical and ecological measurements (e.g., climate, carbon flux, plant productivity, population dynamics of consumers) at 47 terrestrial sites, the NEON design will enable continentalscale inference about the status, trends, causes and ecological consequences of phenological change.

Ecosphere

Status, ecology, and management of the invasive plant, Miconia calvescens DC (Melastomataceae) in the Hawaiian islands

Miconia calvescens (Melastomataceae), native to montane forests of the neotropics, has now invaded wet forests of both the Society and Hawaiian Islands. This tree, which grows up to 15 m tall, is potentially the most invasive and damaging weed of rainforests of Pacific islands. In moist conditions, it grows rapidly, tolerates shade, and produces abundant seed that is effectively dispersed by birds and accumulates in a large, persistent soil seed-bank. Introduced to the Hawaiian Islands in 1961, M. calvescens appears to threaten much of the biological diversity in native forests receiving 1800–2000 mm or more annual precipitation. Currently, M. calvescens is found on 4 Hawaiian islands— Hawaii, Maui, Oahu, and Kauai. Widespread awareness of this invader began in the early 1990s. Although biological control is being pursued, conventional control techniques (mechanical and chemical) to contain and eradicate it locally are underway.

Hawaii

Demographic stochasticity in small remnant populations of the declining distylous plant Primula veris

We studied ecological consequences of distyly for the declining perennial plant Primula veris in the Swiss Jura. Distyly favours cross-fertilization and avoids inbreeding, but may lead to pollen limitation and reduced reproduction if morph frequencies deviate from 50 %. Disassortative mating is promoted by the reciprocal position of stigmas and anthers in the two morphs (pin and thrum) and by intramorph incompatibility and should result in equal frequencies of morphs at equilibrium. However, deviations could arise because of demographic stochasticity, the lower intra-morph incompatibility of the pin morph, and niche differentiation between morphs. Demographic stochasticity should result in symmetric deviations from an even morph frequency among populations and in increased deviations with decreasing population size. If crosses between pins occurred, these would only generate pins, and this could result in a pin-bias of morph frequencies in general and in small populations in particular. If the morphs have different niches, morph frequencies should be related to environmental factors, morphs might be spatially segregated, and morphological differences between morphs would be expected. We tested these hypotheses in the declining distylous P. veris. We studied morph frequencies in relation to environmental conditions and population size, spatial segregation in field populations, morphological differences between morphs, and growth responses to nutrient addition. Morph frequencies in 76 populations with 1 - 80000 flowering plants fluctuated symmetrically about 50 %. Deviations from 50 % were much larger in small populations, and sixof the smallest populations had lost one morph altogether. In contrast, morph frequencies were neither related to population size nor to 17 measures of environmental conditions. We found no spatial segregation or morphological differences in the field or in the common garden. The results suggest that demographic stochasticity caused deviations of the morph ratiofrom unity in small populations. Demographic stochasticity was probably caused by the random elimination of plants during the fragmentation of formerly large continuous populations. Biased morph frequencies may be one of the reasons for the strongly reduced reproduction in small populations of P. veris.

Basic and Applied Ecology

Climate dipoles as continental drivers of plant and animal populations

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

Trends in Ecology and Evolution

Seed dispersal by specialist versus generalist foragers: The plant's perspective

I examined the seed dispersal ecology of the stem parasitic plant, desert mistletoe (Phoradendron californicum, Viscaceae), with the objectives of (1) determining the relative effectiveness of specialist and generalist foragers for seed dispersal, (2) determining the extent to which desert mistletoe fruiting characteristics correspond to those predicted for plants attracting specialist versus generalist foragers, and (3) examining the potential consequences of the observed dispersal strategy for mistletoe reproduction. Three species of birds, phainopepla, Gila woodpecker, and northern mockingbird, fed on desert mistletoe at my study site. The specialist, phainopepla, was the most abundant and the most likely to perch in host species, where defecated seeds had a greater probability of lodging in a site suitable for establishment. Gila woodpeckers, although abundant, spent little time in host plants, thus dooming most of the seeds they consumed. Mockingbirds may disperse a small number of seeds, but were abundant enough to consume only a small portion of the available fruits. As expected for plants attracting specialist frugivores, mistletoes produced fruits throughout the 6-month season in which phainopeplas reside in the Sonoran desert. Contrary to expectation, numbers of fruits produced far exceeded the amount that could be consumed by the frugivores at my study site. Fruit crop size was positively related to absolute fruit removal, but not to proportional removal at the scale of the entire study site. However, crop size was positively related to proportional removal within the neighborhood of mistletoes occupying an individual host tree. Frugivores were attracted to infected hosts, host attractiveness increased, although proportional removal of fruit declined, with number of female mistletoes. The observed dispersal ecology of desert mistletoe suggests the likelihood of increasingly clumped distributions of mistletoe plants, as more and more seeds are deposited on previously infected hosts, and increased density of mistletoes attract ever more visits by birds. I observed no decline in vigor, in terms of fruit production, within the levels of infestation at my study site. The seed dispersal strategy of desert mistletoe thus includes aspects of that expected both for plants dependent on specialists and those dependent on generalists. Fruits are available through the entire season to maintain the specialist. Production far exceeds that expected, but serves to attract the specialist within a neighborhood of vigorously fruiting conspecifics.

Oikos

Plant phenolics and absorption features in vegetation reflectance spectra near 1.66 μm

Past laboratory and field studies have quantified phenolic substances in vegetative matter from reflectance measurements for understanding plant response to herbivores and insect predation. Past remote sensing studies on phenolics have evaluated crop quality and vegetation patterns caused by bedrock geology and associated variations in soil geochemistry. We examined spectra of pure phenolic compounds, common plant biochemical constituents, dry leaves, fresh leaves, and plant canopies for direct evidence of absorption features attributable to plant phenolics. Using spectral feature analysis with continuum removal, we observed that a narrow feature at 1.66 μm is persistent in spectra of manzanita, sumac, red maple, sugar maple, tea, and other species. This feature was consistent with absorption caused by aromatic C- H bonds in the chemical structure of phenolic compounds and non-hydroxylated aromatics. Because of overlapping absorption by water, the feature was weaker in fresh leaf and canopy spectra compared to dry leaf measurements. Simple linear regressions of feature depth and feature area with polyphenol concentration in tea resulted in high correlations and low errors (% phenol by dry weight) at the dry leaf ( r 2 = 0.95, RMSE = 1.0%, n = 56), fresh leaf ( r 2 = 0.79, RMSE = 2.1%, n = 56), and canopy ( r 2 = 0.78, RMSE = 1.0%, n = 13) levels of measurement. Spectra of leaves, needles, and canopies of big sagebrush and evergreens exhibited a weak absorption feature centered near 1.63 μm, short ward of the phenolic compounds, possibly consistent with terpenes. This study demonstrates that subtle variation in vegetation spectra in the shortwave infrared can directly indicate biochemical constituents and be used to quantify them. Phenolics are of lesser abundance compared to the major plant constituents but, nonetheless, have important plant functions and ecological significance. Additional research is needed to advance our understanding of the spectral influences of plant phenolics and terpenes relative to dominant leaf biochemistry (water, chlorophyll, protein/nitrogen, cellulose, and lignin).

International Journal of Applied Earth Observation

Restoration for resilience: The role of plant-microbial interactions and seed provenance in ecological restoration

With global efforts to restore grassland ecosystems, researchers and land management practitioners are working to reconstruct habitat that will persist and withstand stresses associated with climate change. Part of these efforts involve movement of plant material potentially adapted to future climate conditions from native habitat or seed production locations to a new restoration site. Restoration practice often follows this plant-centered, top-down approach. However, we suggest that restoration of belowground interactions, namely between plants and arbuscular mycorrhizal fungi or rhizobia, is important for restoring resilient grasslands. In this synthesis we highlight these interactions and offer insight into how their restoration might be included in current grassland restoration practice. Ultimately, restoration of belowground interactions may contribute to grassland habitat that can withstand and respond to future climate uncertainties.

Natural Areas Journal

Landscape genomics of Sphaeralcea ambigua in the Mojave Desert: a multivariate, spatially-explicit approach to guide ecological restoration

Local adaptation influences plant species’ responses to climate change and their performance in ecological restoration. Fine-scale physiological or phenological adaptations that direct demographic processes may drive intraspecific variability when baseline environmental conditions change. Landscape genomics characterize adaptive differentiation by identifying environmental drivers of adaptive genetic variability and mapping the associated landscape patterns. We applied such an approach to Sphaeralcea ambigua , an important restoration plant in the arid southwestern United States, by analyzing variation at 153 amplified fragment length polymorphism loci in the context of environmental gradients separating 47 Mojave Desert populations. We identified 37 potentially adaptive loci through a combination of genome scan approaches. We then used a generalized dissimilarity model (GDM) to relate variability in potentially adaptive loci with spatial gradients in temperature, precipitation, and topography. We identified non-linear thresholds in loci frequencies driven by summer maximum temperature and water stress, along with continuous variation corresponding to temperature seasonality. Two GDM-based approaches for mapping predicted patterns of local adaptation are compared. Additionally, we assess uncertainty in spatial interpolations through a novel spatial bootstrapping approach. Our study presents robust, accessible methods for deriving spatially-explicit models of adaptive genetic variability in non-model species that will inform climate change modelling and ecological restoration.

California, Nevada

“Naturalness” in designated Wilderness: Long-term changes in non-native plant dynamics on campsites, Boundary Waters, Minnesota

Wilderness areas in the United States are preserved for their untrammeled naturalness and opportunities for unconfined recreation. The Boundary Waters Canoe Area Wilderness has these qualities, but long-term recreation visitation pressures on campsites can cause significant ecological changes. This article explores changes on campsites, specifically examining non-native plant ecology over 3 decades. The research replicates a 1982 study analyzing vegetation composition and cover on campsites and environmentally paired controls. Camping activities have removed substantial tree cover on campsites, altering their ecological conditions and perceived wilderness character. Over the span of 32 years, the number of non-native plant species found on campsites has not risen, although their mean relative cover has increased significantly and they have spread to more sites. Of the 23 non-native herbs and grasses found on the campsites, only Cirsium arvense is considered a noxious weed by the state of Minnesota. Other noninvasive, non-native plants fall into a gray area in the context of "naturalness" for an area protected as Wilderness because they provide some positive ecological services even as they degrade wilderness character. Thus, wilderness managers face a difficult challenge in coping with the long-term impacts of visitor use on wilderness conditions and character.

Minnesota

IPANE: Could New England's Early Detection Network benefit eastern Canada?

The Invasive Plant Analysis of New England (IPANE: ipane.org) is a multifaceted approach to regional early detection of invasive plants. IPANE, was founded in 2001 to create a comprehensive six state New England regional partnership to: minimize the ecological damage caused by invasive plants; provide reliable and accessible educational material; maintain a network of professional and trained volunteers to gather information and to locate new incursions; provide a web-accessible database and maps of invasive and potentially invasive plants; conduct and encourage research on the biology and ecology of invasive plants; and, use program-generated data to develop predictive distribution models for the region. This program uses the synergy of all the components to create a regional early detection and rapid assessment network to curtail new invasions before they become widespread on the regional landscape. IPANE is a model for the United States Geological Survey National Early Detection Network Toolbox, a compendium of information developed for use by Network partners. In addition, an Early Detection Alert system has been developed to inform key federal and state agency staff, conservation organizations, and those with vegetation management responsibilities about new or potential invaders to the region. These include current and anticipated distribution, diagnostic characters, images, pertinent biological and control information, and key contacts. Most of the non-native species currently considered invasive by IPANE appear to be spreading into New England from the south or west. IPANE is strategically placed to act as an advanced warning system for the 5 provinces of Eastern and Maritime Canada. At the meeting held in Nova Scotia in September 2007, this idea was suggested to attendees from 4 of these 5 provinces and the Canadian government. By expanding its alert systems, IPANE could serve as a focal point for Early Detection information moving in any direction and tie Eastern Canada into the National Early Detection Network of the United States.

Conference Paper

Post-fire vegetation response in a repeatedly burned low-elevation sagebrush steppe protected area provides insights about resilience and invasion resistance

Sagebrush steppe ecosystems are threatened by human land-use legacies, biological invasions, and altered fire and climate dynamics. Steppe protected areas are therefore of heightened conservation importance but are few and vulnerable to the same impacts broadly affecting sagebrush steppe. To address this problem, sagebrush steppe conservation science is increasingly emphasizing a focus on resilience to fire and resistance to non-native annual grass invasion as a decision framework. It is well-established that the positive feedback loop between fire and annual grass invasion is the driving process of most contemporary steppe degradation. We use a newly developed ordinal zero-augmented beta regression model fit to large-sample vegetation monitoring data from John Day Fossil Beds National Monument, USA, spanning 7 years to evaluate fire responses of two native perennial foundation bunchgrasses and two non-native invasive annual grasses in a repeatedly burned, historically grazed, and inherently low-resilient protected area. We structured our model hierarchically to support inferences about variation among ecological site types and over time after also accounting for growing-season water deficit, fine-scale topographic variation, and burn severity. We use a state-and-transition conceptual diagram and abundances of plants listed in ecological site reference conditions to formalize our hypothesis of fire-accelerated transition to ecologically novel annual grassland. Notably, big sagebrush ( Artemisia tridentata ) and other woody species were entirely removed by fire. The two perennial grasses, bluebunch wheatgrass ( Pseudoroegneria spicata ) and Thurber's needlegrass ( Achnatherum thurberianum ) exhibited fire resiliency, with no apparent trend after fire. The two annual grasses, cheatgrass ( Bromus tectorum ) and medusahead ( Taeniatherum caput-medusae ), increased in response to burn severity, most notably medusahead. Surprisingly, we found no variation in grass cover among ecological sites, suggesting fire-driven homogenization as shrubs were removed and annual grasses became dominant. We found contrasting responses among all four grass species along gradients of topography and water deficit, informative to protected-area conservation strategies. The fine-grained influence of topography was particularly important to variation in cover among species and provides a foothold for conservation in low-resilient, aridic steppe. Broadly, our study demonstrates how to operationalize resilience and resistance concepts for protected areas by integrating empirical data with conceptual and statistical models.

Oregon

Resprouting and seeding hypotheses: A test of the gap-dependent model using resprouting and obligate seeding subspecies of Arctostaphylos

Ecological factors favoring either postfire resprouting or postfire obligate seeding in plants have received considerable attention recently. Three ecological models have been proposed to explain patterns of these two life history types. In this study, we test these three models using data from California chaparral. We take an innovative approach to testing these models by not testing community or landscape patterns, but instead, investigating vegetation structure characteristic of four pairs of resprouting and (non-resprouting) obligate seeding subspecies of Arctostaphylos (Ericaceae), a dominant and diverse shrub genus in California chaparral. Data were analyzed for percentage bare ground, elevation, annual precipitation, number of fires, and time between fires and were compared independently for each subspecies pair. Results were consistently supportive of the gap-dependent model suggesting that obligate seeders are favored when post-disturbance gaps are large. Results were inconclusive or contrary to expectations for both of the other two models.

Plant Ecology

Spartina alterniflora genotype influences facilitation and suppression of high marsh species colonizing an early successional salt marsh

Genetically based phenotypic and ecotypic variation in a dominant plant species can influence ecological functions and patterns of recruitment by other species in plant communities. However, the nature and degree of importance of genotypic differences is poorly understood in most systems. The dominant salt marsh species, Spartina alterniflora , is known to induce facilitative and competitive effects in different plant species, and the outcomes of interactions can be affected by nutrients and flooding stress. Clonal genotypes, which maintained their different plant architecture phenotypes throughout 31 months of a field experiment, underwent considerable genet‐specific senescence in their centres over the last 12 months. Different clonal genotypes and different locations (robust edges vs. senescent centres) permitted significantly different levels of light penetration of the canopy (14.8–77.6%), thus establishing spatial heterogeneity for this important environmental factor. S. alterniflora clonal genotype influenced the degree of suppression of the previously dominant Salicornia bigelovii as well as facilitation of recruitment and growth by other plant species. Aster subulatus and Atriplex patula performed better in Spartina clone centres, and experienced reduced growth in Salicornia ‐dominated areas. Four other high marsh species ( Borrichia frutescens , Aster tenuifolius , Iva frutescens and Limonium carolinianum ) colonized only into Spartina clones but not into the Salicornia ‐dominated area. These results suggest that differences in clone size, centre senescence, stem density, height, total stem length and biomass in different genotypes of a dominant marsh plant species can influence recruitment and growth of other plant species. The spatial pattern of habitat heterogeneity is, at least in part, dependent on the genotypic diversity, and possibly the genetic diversity, of such foundation species. We hypothesize that as genotypic diversity increases in populations of a dominant plant species like S. alterniflora , the number and diversity of interactions with other species will increase as well.

Journal of Ecology

Ecological islands: Conserving biodiversity hotspots in a changing climate

For decades, botanists have recognized that rare plants are clustered into ecological “islands”: small and isolated habitat patches produced by landscape features such as sinkholes and bedrock outcrops. Insular ecosystems often provide unusually stressful microhabitats for plant growth (eg because of thin soils, high temperatures, extreme pH, or limited nutrients) to which rare species are specially adapted. Climate-driven shifts to these stressors may undermine the competitive advantage of stress-adapted species, allowing them to be displaced by competitors, or may overwhelm their coping strategies altogether. Special features of insular ecosystems—such as extreme habitat fragmentation and association with unusual landscape features—may also affect their climate sensitivity and adaptive capacity. To predict and manage these changes, a simple conceptual framework is presented based on a synthesis of over 300 site-level studies. Using this framework, conservation efforts can leverage existing ecological knowledge to anticipate changes in particular microhabitats and design targeted strategies for conserving rare species.

Frontiers in Ecology and the Environment

Interactions among invasive plants: Lessons from Hawai‘i

Most ecosystems have multiple-plant invaders rather than single-plant invaders, yet ecological studies and management actions focus largely on single invader species. There is a need for general principles regarding invader interactions across varying environmental conditions, so that secondary invasions can be anticipated and managers can allocate resources toward pretreatment or postremoval actions. By reviewing removal experiments conducted in three Hawaiian ecosystems (a dry tropical forest, a seasonally dry mesic forest, and a lowland wet forest), we evaluate the roles environmental harshness, priority effects, productivity potential, and species interactions have in influencing secondary invasions, defined here as invasions that are influenced either positively (facilitation) or negatively (inhibition/priority effects) by existing invaders. We generate a conceptual model with a surprise index to describe whether long-term plant invader composition and dominance is predictable or stochastic after a system perturbation such as a removal experiment. Under extremely low resource availability, the surprise index is low, whereas under intermediate-level resource environments, invader dominance is more stochastic and the surprise index is high. At high resource levels, the surprise index is intermediate: Invaders are likely abundant in the environment but their response to a perturbation is more predictable than at intermediate resource levels. We suggest further testing across environmental gradients to determine key variables that dictate the predictability of postremoval invader composition.

Hawai'i

Novel plant communities limit the effects of a managed flood to restore riparian forests along a large regulated river

Dam releases used to create downstream flows that mimic historic floods in timing, peak magnitude and recession rate are touted as key tools for restoring riparian vegetation on large regulated rivers. We analysed a flood on the 5th‐order Green River below Flaming Gorge Dam, Colorado, in a broad alluvial valley where Fremont cottonwood riparian forests have senesced and little recruitment has occurred since dam completion in 1962. The stable post dam flow regime triggered the development of novel riparian communities with dense herbaceous plant cover. We monitored cottonwood recruitment on landforms inundated by a managed flood equal in magnitude and timing to the average pre‐dam flood. To understand the potential for using managed floods as a riparian restoration tool, we implemented a controlled and replicated experiment to test the effects of artificially modified ground layer vegetation on cottonwood seedling establishment. Treatments to remove herbaceous vegetation and create bare ground included herbicide application (H), ploughing (P), and herbicide plus ploughing (H + P). Treatment improved seedling establishment. Initial seedling densities on treated areas were as much as 1200% higher than on neighbouring control (C) areas, but varied over three orders of magnitude among the five locations where manipulations were replicated. Only two replicates showed the expected seedling density rank of (H + P) > P > H> C. Few seedlings established in control plots and none survived 1 year. Seedling density was strongly affected by seed rain density. Herbivory affected growth and survivorship of recruits, and few survived nine growing seasons. Our results suggest that the novel plant communities are ecologically and geomorphically resistant to change. Managed flooding alone, using flows equal to the pre‐dam mean annual peak flood, is an ineffective riparian restoration tool where such ecosystem states are present and floods cannot create new habitat for seedling establishment. This problem significantly limits long‐term river and riparian management options.

Colorado