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Towards a predictive framework for biocrust mediation of plant performance: A meta‐analysis

Understanding the importance of biotic interactions in driving the distribution and abundance of species is a central goal of plant ecology. Early vascular plants likely colonized land occupied by biocrusts — photoautotrophic, surface‐dwelling soil communities comprised of cyanobacteria, bryophytes, lichens and fungi — suggesting biotic interactions between biocrusts and plants have been at play for some 2,000 million years. Today, biocrusts coexist with plants in dryland ecosystems worldwide, and have been shown to both facilitate or inhibit plant species performance depending on ecological context. Yet, the factors that drive the direction and magnitude of these effects remain largely unknown. We conducted a meta‐analysis of plant responses to biocrusts using a global dataset encompassing 1,004 studies from six continents. Meta‐analysis revealed there is no simple positive or negative effect of biocrusts on plants. Rather, plant responses differ by biocrust composition and plant species traits and vary across plant ontogeny. Moss‐dominated biocrusts facilitated, while lichen‐dominated biocrusts inhibited overall plant performance. Plant responses also varied among plant functional groups: C 4 grasses received greater benefits from biocrusts compared to C 3 grasses, and plants without N‐fixing symbionts responded more positively to biocrusts than plants with N‐fixing symbionts. Biocrusts decreased germination but facilitated growth of non‐native plant species. Synthesis . Results suggest that interspecific variation in plant responses to biocrusts, contingent on biocrust type, plant traits, and ontogeny can have strong impacts on plant species performance. These findings have important implications for understanding biocrust contributions to plant productivity and community assembly processes in ecosystems worldwide.

Journal of Ecology

Plant effects on and response to soil microbes in native and non-native Phragmites australis

Plant–soil feedbacks (PSFs) mediate plant community dynamics and may plausibly facilitate plant invasions. Microbially mediated PSFs are defined by plant effects on soil microbes and subsequent changes in plant performance (responses), both positive and negative. For microbial interactions to benefit invasive plants disproportionately, native and invasive plants must either (1) have different effects on and responses to soil microbial communities or (2) only respond differently to similar microbial communities. In other words, invasive plants do not need to cultivate different microbial communities than natives if they respond differently to them. However, effects and responses are not often explored separately, making it difficult to determine the underlying causes of performance differences. We performed a reciprocal-transplant PSF experiment with multiple microbial inhibition treatments to determine how native and non-native lineages of Phragmites australis affect and respond to soil bacteria, fungi, and oomycetes. Non-native Phragmites is a large, fast-growing, cosmopolitan invasive plant, whereas the North American native variety is comparatively smaller, slower growing, and typically considered a desirable wetland plant. We identified the effects of each plant lineage on soil microbes using DNA meta-barcoding and linked plant responses to microbial communities. Both Phragmites lineages displayed equally weak, insignificant PSFs. We found evidence of slight differential effects on microbial community composition, but no significant differential plant responses. Soils conditioned by each lineage differed only slightly in bacterial community composition, but not in fungal composition. Additionally, native and non-native Phragmites lineages did not significantly differ in their response to similar soil microbial communities. Neither lineage appreciably differed when plant biomass was compared between those grown in sterile and live soils. Targeted microbial inhibitor treatments revealed both lineages were negatively impacted by soil bacteria, but the negative response was stronger in non-native Phragmites . These observations were opposite of expectations from invasion theory and imply that the success of non-native Phragmites , relative to the native lineage, does not result from its interaction with soil microorganisms. More broadly, quantifying plant effects on, and responses to soil microbes separately provides detailed and nuanced insight into plant-microbial interactions and their role in invasions, which could inform management outcomes for invasive plants.

Ecological Applications

Southwest Exotic Mapping Program 2007: Occurrence summary and maps of select invasive, non-native plants in Arizona

An important aspect of management of invasive, non-native plants (invasive plants) is information on the type, location, and magnitude of infestations. Regional development of this information requires an integrated program of data collection, management, and delivery. The Southwest Exotic Plant Mapping Program (SWEMP), coordinated through the U.S. Geological Survey’s Southwest Biological Science Center, annually compiles occurrence records for infestations of invasive plants. Operating since 1998, the SWEMP team has accepted occurrence records contributed voluntarily by federal, tribal, state, and private collaborators and has compiled these contributions accumulatively with previous versions of SWEMP. The SWEMP 2007 regional database update, SWEMP07, contains 62,000 records for 221 plant species with records dating as far back as 1911 and up to December, 2006. Records include invasive plants in Arizona, eastern California, Colorado, New Mexico, and Utah. SWEMP07 is available through the Southwest Exotic Plant Information Clearinghouse ( http://sbsc.wr.usgs.gov/research/projects/swepic/swepic.asp , click SWEMP). Not all invasive plants are non-native and not all invasive plants are even invasive. The Arizona Invasive Species Advisory Council (2006) defined an invasive species as “a species that is (1) non-native to the ecosystem under consideration and, (2) whose introduction causes or is likely to cause economic or environmental harm, or harm to human health”. SWEMP uses the U.S. Department of Agriculture PLANTS database ( http://plants.usda.gov/ ) to determine if a plant is native or not to Arizona. As SWEMP does not independently assess the current or potential impact of invasive plants, we include most non-native plant records contributed. We have not included agricultural crops that are non-native, for example apples, oranges, etc. In this open-file-report, we use the SWEMP07 update to summarize the occurrence of invasive plants in Arizona and present distribution maps for a select invasive plants in Arizona. We use the word occurrence purposefully instead of the word distribution. The SWEMP07 database only provides an estimate of the actual distribution of invasive plants in Arizona. The information provided is a first approximation of the state-wide extent of invasive plant distribution.

Open-File Report

Status and limiting factors of two rare plant species in dry montane communities of Hawai`i Volcanoes National Park.

Two rare plants native to montane dry forests and woodland communities of Hawai`i Volcanoes National Park (HAVO) were studied for more than two years to determine their stand structure, short-term mortality rates, patterns of reproductive phenology, success of fruit production, floral visitor composition, seed germination rates in the greenhouse, and survival of both natural and planted seedlings. Phyllostegia stachyoides , a shrubby Hawaiian mint (Lamiaceae) that is a species of concern, was studied within two small kīpuka at a natural population on the park’s Mauna Loa Strip, and three plantings at sites along the Mauna Loa Road were also monitored. Silene hawaiiensis , a threatened shrub species in the pink family (Caryophyllaceae), was monitored at two natural populations, one on Mauna Loa at the Three Trees Kīpuka and the second on Kīlauea Crater Rim south of Halema`uma`u. Silene hawaiiensis plantings were also made inside and outside ungulate exclosures at the park’s Kahuku Unit Phyllostegia stachyoides appeared to have a relatively stable natural population in HAVO with approximately 19% adult plant mortality over three years and recruitment of natural seedlings. Despite high mortality (~98%), some seedlings persisted for more than a year, and recruitment of new plants into the population exceeded the losses of adult plants. Flowering and fruiting phenology was annual and seasonal with peak appearance of buds and flowers in spring and greatest abundance of mature fruit in the summer and fall. Successful production of green fruit from buds and flowers was very high (45%), and green fruit transitioned to mature fruit at a rate of 17.8%. Five insect species were observed visiting flowers, and those with the greatest visitation rates were the alien hover fly Allograpta obliqua (Syrphidae) and the endemic yellowfaced bee Hylaeus difficilis (Colletidae). Both insect species were shown to be carrying pollen of P. stachyoides . Seed germination rates in the greenhouse were variable but ranged as high as 80.4%. Mortality of seedlings planted at three sites along the Mauna Loa Road was very high (~90%) within 2–3 years of planting. There was no significant difference in the mortality or growth of seedlings planted in areas with little grass compared to those in adjacent areas with high grass cover. Silene hawaiiensis had a stable population structure at the Mauna Loa study area, but its population structure at the Kīlauea study site was flat to declining. Mortality of adult plants was low on Mauna Loa (6.5%), but was greater than 30% at the Kīlauea Crater Rim site. Among regularly monitored plants at the Kīlauea site, losses were observed in all size classes between 2006 and 2008. Natural seedling recruitment was observed in stand structure plots at both sites between 2006 and 2007, but numbers of seedlings were low and did not compensate for losses of adult plants. Reproductive phenology was annual with buds and flowers observed in summer and fall, and fruit formed in the fall and winter. The production of immature fruit capsules from buds and flowers was high (51.2%) and tagged immature fruit became mature fruit at a high rate of 66.7%. Floral visitation rates were very low in timed observations and only three insect species were identified visiting S. hawaiiensis flowers: native yellow-faced bees Hylaeus difficilis and H. volcanicus , and the alien hover fly Allograpta exotica . A seed dispersal experiment at the Kīlauea Crater Rim site demonstrated that wind dispersed seeds could travel at least 40 m from S. hawaiiensis plants with mature open capsules. Seed germination rates varied from 7.0 to 73.0% in greenhouse trials. Mortality of planted seedlings at Kahuku was not significantly greater outside ungulate exclosures than inside, but growth in height and production of reproductive structures was significantly greater in protected areas inside exclosures. In the current study, the seedling stage was the most vulnerable part of the life cycle for both P . stachyoides and S. hawaiiensis , and low seedling recruitment appeared to be the most important limiting factor for these species

Hawaii

Associational effects of plant ontogeny on damage by a specialist insect herbivore

Intraspecific variation in plant traits is a major cause of variation in herbivore feeding and performance. Plant defensive traits change as a plant grows, such that ontogeny may account for a substantial portion of intraspecific trait variation. We tested how the ontogenic stage of an individual plant, of an individual in the context of its neighboring plants, and of a patch of plants with mixed or uniform stages affect plant–herbivore interactions. To do this, we conducted an experimental study of the interactions between Lepidium draba , a perennial brassicaceous weed, and Plutella xylostella , a common herbivore of L. draba . We found that L. draba foliar glucosinolates, secondary metabolites often implicated in defense, decreased in concentration with plant age. In single-stage patches, herbivores performed similarly on L. draba plants of different ages. Furthermore, we found no difference in the cumulative performance of herbivores reared on mixed- or even-staged patches of L. draba . However, in mixed-stage patches, the damage experienced by a focal plant depended on the stage of neighboring plants, suggesting a preference hierarchy of the herbivore among plant stages. In our study, the amount of herbivory depended on the ontogenic neighborhood in which the plant grew. However, from the herbivore’s perspective, variation in plant ontogenic stage was unimportant to its success in terms of feeding rate and final weight.

Oecologia

Demographic estimation methods for plants with dormancy

Demographic studies in plants appear simple because unlike animals, plants do not run away. Plant individuals can be marked with, e.g., plastic tags, but often the coordinates of an individual may be sufficient to identify it. Vascular plants in temperate latitudes have a pronounced seasonal life–cycle, so most plant demographers survey their study plots once a year often during or shortly after flowering. Life–states are pervasive in plants, hence the results of a demographic study for an individual can be summarized in a familiar encounter history, such as 0VFVVF000. A zero means that an individual was not seen in a year and a letter denotes its state for years when it was seen aboveground. V and F here stand for vegetative and flowering states, respectively. Probabilities of survival and state transitions can then be obtained by mere counting. Problems arise when there is an unobservable dormant state, i.e., when plants may stay belowground for one or more growing seasons. Encounter histories such as 0VF00F000 may then occur where the meaning of zeroes becomes ambiguous. A zero can either mean a dead or a dormant plant. Various ad hoc methods in wide use among plant ecologists have made strong assumptions about when a zero should be equated to a dormant individual. These methods have never been compared among each other. In our talk and in Kéry et al. (submitted), we show that these ad hoc estimators provide spurious estimates of survival and should not be used. In contrast, if detection probabilities for aboveground plants are known or can be estimated, capturerecapture (CR) models can be used to estimate probabilities of survival and state–transitions and the fraction of the population that is dormant. We have used this approach in two studies of terrestrial orchids, Cleistes bifaria (Kéry et al., submitted) and Cypripedium reginae (Kéry & Gregg, submitted) in West Virginia, U.S.A. For Cleistes, our data comprised one population with a total of 620 marked ramets over 10 years, and for Cypripedium , two populations with 98 and 258 marked ramets over 11 years. We chose the ramet (= single stem or shoot) as the demographic unit of our study since there was no way distinguishing among genets (genet = genetical individual, i.e., the “individual” that animal ecologists are mostly concerned with). This will introduce some non–independence into the data, which can nevertheless be dealt with easily by correcting variances for overdispersion. Using ramets instead of genets has the further advantage that individuals can be assigned to a state such as flowering or vegetative in an unambiguous manner. This is not possible when genets are the demographic units. In all three populations, auxiliary data was available to show that detection probability of aboveground plants was m 0.995 We fitted multistate models in program MARK by specifying three states (D, V, F), even though the dormant state D does not occur in the encounter histories. Detection probability is fixed at 1 for the vegetative (V) and the flowering state (F) and at zero for the dormant state (D). Rates of survival and of state transitions as well as slopes of covariate relationships can be estimated and LRT or the AIC machinery be used to select among models. To estimate the fraction of the population in the unobservable dormant state, the encounter histories are collapsed to 0 (plant not observed aboveground) and 1 (plant observed aboveground). The Cormack–Jolly–Seber model without constraints on detection probability is used to estimate detection probability, the complement of which is the estimated fraction of the population in the dormant state. Parameter identifiability is an important issue in multi state models. We used the Catchpole–Morgan–Freeman approach to determine which parameters are estimable in principle in our multi state models. Most of 15 tested models were indeed estimable with the notable exception of the most general model, which has fully interactive state- and time-dependent survival and state transition rates. This model would become identifiable if at least some plants would be excavated in years when they do not show up aboveground. Our analyses for three analyzed populations of Cleistes and Cypripedium yielded annual ramet survival rates ranging from 0.86–0.96. Estimates of the average fraction dormant ranged from 0.02–0.30, but with up to half a population in the dormant state in some years. Ultrastructural modeling enables interesting hypotheses to be tested about the relationships of demographic rates with climatic covariates for instance. Such covariate modeling makes the CR approach particularly interesting for evolutionary–ecological questions about, e.g., the adaptive significance of the dormant state.

Animal Biodiversity and Conservation

Vascular plant and vertebrate species richness in national parks of the eastern United States

Given the estimates that species diversity is diminishing at 50-100 times the normal rate, it is critical that we be able to evaluate changes in species richness in order to make informed decisions for conserving species diversity. In this study, we examined the potential of vascular plant species richness to be used as a surrogate for vertebrate species richness in the classes of amphibians, reptiles, birds, and mammals. Vascular plants, as primary producers, represent the biotic starting point for ecological community structure and are the logical place to start for understanding vertebrate species associations. We used data collected by the United States (US) National Park Service (NPS) on species presence within parks in the eastern US to estimate simple linear regressions between plant species richness and vertebrate richness. Because environmental factors may also influence species diversity, we performed simple linear regressions of species richness versus natural logarithm of park area, park latitude, mean annual precipitation, mean annual temperature, and human population density surrounding the parks. We then combined plant species richness and environmental variables in multiple regressions to determine the variables that remained as significant predictors of vertebrate species richness. As expected, we detected significant relationships between plant species richness and amphibian, bird, and mammal species richness. In some cases, plant species richness was predicted by park area alone. Species richness of mammals was only related to plant species richness. Reptile species richness, on the other hand, was related to plant species richness, park latitude and annual precipitation, while amphibian species richness was related to park latitude, park area, and plant species richness. Thus, plant species richness predicted species richness of different vertebrate groups to varying degrees and should not be used exclusively as a surrogate for vertebrate species richness. Plant species richness should be included with other variables such as area and climate when considering strategies to manage and conserve species in US National Parks. It is not always appropriate to draw conclusions about analyses of taxonomic surrogates from one area to another. Two patterns evident from the linear regressions were the increase in species richness with the increase of park area and with increase of vascular plant species richness. To test whether there were differences in these patterns among networks, we used analysis of covariance (ANCOVA). Differences among networks were detected only in bird species richness versus plant species richness and for all taxa except mammals for vertebrate species richness versus park area. Some of these results may be due to small sample size among networks, and therefore, low statistical power. Other factors that could have contributed to these results were differences in average park area and habitat heterogeneity among networks, latitudinal gradients, low variation in mean annual precipitation, and different use of vegetation by migratory species. Based on these results we recommend that management of biodiversity be approached from local and site specific criteria rather than applying management directives derived from other regions of the US. It is also recommended that analyses similar to those presented here be conducted for all national parks, once data become available for all networks in the US, to gain a better understanding of how vascular plant species richness, area, and vertebrate species richness are related in the US.

Natural Resource Technical Report NPS/NCR/NCRO/NRT

Hotter temperatures alter riparian plant outcomes under regulated river conditions

Climate change and river regulation alter environmental controls on riparian plant occurrence and cover worldwide. Simultaneous changes to river flow and air temperature could result in unanticipated plant responses to novel environmental conditions. Increasing temperature could alter riparian plant response to hydrology and other factors, while river regulation may exacerbate environmental stress through novel flows like those resulting from power generation. Further, plant establishment and growth may require differing conditions, which may be decoupled by novel conditions. Using a large dataset that spans a natural 5°C mean annual temperature (MAT) gradient and a Bayesian model that integrates plant occurrence and cover, we address four questions: (1) Does hotter MAT modify plant response to hydrology, substrate composition, topography, and cover of co-occurring plant species? (2) Does the timing of hydropower tides benefit some species over others? (3) Does dam-induced erosion hinder riparian species more than upland species? (4) Do occurrence and cover respond to different environmental variables, allowing for decoupling of life history processes? We addressed these questions with data collected along 364 km of the Colorado River downstream of Glen Canyon Dam, Arizona, United States of America. Occurrence and cover class were recorded in >10,000 plots from 2016 to 2020, along with environmental covariates that repeat across the climate gradient. For 36 species, plant occurrence and cover were modeled with respect to MAT, hydrology, substrate, topography, other plant cover, and their interactions with MAT. There were four key results. (1) Increasing MAT will not only directly influence plants but will mediate their responses to the environment, including greater dependence on stable water supplies. (2) The timing of hydropower tides shapes plant community composition. (3) Dam-related erosion has an outsized effect on riparian species, which could lead to a loss of regionally unique plant species. (4) For all species, the most important covariates driving occurrence differed from those for cover, suggesting the potential for these life stages to be decoupled. Not only will climate change and river regulation independently alter plant distributions, interactions among hotter temperature, dam-controlled flow patterns, and limited fine sediments will determine which species flourish or perish under future conditions.

Arizona

Intraspecific variation mediates density dependence in a genetically diverse plant species

Interactions between neighboring plants are critical for biodiversity maintenance in plant populations and communities. Intraspecific trait variation and genome duplication are common in plant species and can drive eco-evolutionary dynamics through genotype-mediated plant–plant interactions. However, few studies have examined how species-wide intraspecific variation may alter interactions between neighboring plants. We investigate how subspecies and ploidy variation in a genetically diverse species, big sagebrush ( Artemisia tridentata ), can alter the demographic outcomes of plant interactions. Using a replicated, long-term common garden experiment that represents range-wide diversity of A. tridentata , we ask how intraspecific variation, environment, and stand age mediate neighbor effects on plant growth and survival. Spatially explicit models revealed that ploidy variation and subspecies identity can mediate plant–plant interactions but that the effect size varied in time and across experimental sites. We found that demographic impacts of neighbor effects were strongest during early stages of stand development and in sites with greater growth rates. Within subspecies, tetraploid populations showed greater tolerance to neighbor crowding compared to their diploid variants. Our findings provide evidence that intraspecific variation related to genome size and subspecies identity impacts spatial demography in a genetically diverse plant species. Accounting for intraspecific variation in studies of conspecific density dependence will improve our understanding of how local populations will respond to novel genotypes and biotic interaction regimes. As introduction of novel genotypes into local populations becomes more common, quantifying demographic processes in genetically diverse populations will help predict long-term consequences of plant–plant interactions.

Idaho, Utah