Despite decades of research, the associations between plants and their mycorrhizal fungi remain poorly understood. In ecosystems with a mix of arbuscular mycorrhizal (AM) and ectomycorrhizal (EM)-associated trees, tree species richness and tree mycorrhizal association may shape mycorrhizal fungal communities and below-ground processes. Utilizing a long-term biodiversity-ecosystem function experiment at the Smithsonian Environmental Research Center (SERC), we investigated how tree species richness (1, 4, 12 species) and tree mycorrhizal association (AM, EM, mixed) influence the diversity and composition of the soil microbiome. We further assessed how above- and below-ground taxonomic and functional diversity influence soil characteristics. We hypothesized that soil microbial communities would be more strongly driven by tree mycorrhizal association than tree species richness and that both tree mycorrhizal association and fungal diversity would affect soil characteristics. Tree mycorrhizal type influenced EM fungal richness, diversity and turnover more strongly than tree species richness, with tree mycorrhizal association effects on turnover 2.4 times greater. Conversely, tree species richness led to a significant increase in AM hyphal length, while AM fungal relative abundance was linked to mycorrhizal association. Neither tree species richness nor tree mycorrhizal association directly impacted soil characteristics. Instead, shifts in fungal diversity and composition affected soil characteristics. 3. AM fungal richness was positively associated with acid phosphatase (AP) extracellular enzyme activity (EEA), whereas AM fungal hyphal lengths were positively associated with N-acetyl-glucosaminidase (NAG) EEA. The AP EEA was negatively correlated with inorganic phosphate (PO43-) concentrations in soils whereas NAG EEA was positively correlated with inorganic nitrate (NO3-). 4. Shifts in the composition of saprotrophic and pathogenic fungi correlated with soil organic carbon (SOC) stocks, suggesting SOC decomposition rate, rather than accumulation, drove carbon storage in these plots. Synthesis. By jointly manipulating tree species richness and tree mycorrhizal association, we demonstrated that mycorrhizal associations drive EM fungal diversity and composition and AM fungal abundance while indirectly influencing soil characteristics via below-ground microbiomes. As global change alters plant and fungal diversity and guild structure, understanding the universality of these above- and below-ground linkages will be critical for predicting ecosystem-level responses.
Soil organic matter (SOM) is primarily derived from leaf and root inputs, but the relative contributions of each are difficult to study without the use of isotopic tracers. Furthermore, associations between trees and mycorrhizal fungi can influence the production and persistence of SOM. We quantified tree inputs and carbon and nitrogen content of three SOM fractions - free and occluded particulate organic matter (fPOM and oPOM, respectively), and mineral-associated organic matter (MAOM) - in a tree common garden in Maryland, USA, where the trees and soil have distinct isotopic signatures due to prior use of the land as a cornfield. We found that stem basal area was not associated with concentrations of carbon (C) in any SOM pool but that fine root biomass was positively related to the proportion of tree-derived MAOM-C. POM was positively associated with leaf litter carbon : nitrogen ratio (C : N), but tree-derived MAOM was not associated with fine root C : N. Tree mycorrhizal type did not influence the relative importance of leaf and root-derived SOM. Our results indicate that leaf litter and fine roots have distinct roles on POM and MAOM formation, respectively, and that these effects are consistent across tree mycorrhizal associations in early stand development.
Forest canopy complexity (i.e., the three-dimensional structure of the canopy) is often associated with increased species diversity as well as high primary productivity across natural forests. However, canopy complexity, tree diversity, and productivity are often confounded in natural forests, and the mechanisms of these relationships remain unclear. Here, we used two large tree diversity experiments in North America to assess three hypotheses: (1) increasing tree diversity leads to increased canopy complexity, (2) canopy complexity is positively related to tree productivity, and (3) the relationship between tree diversity and tree productivity is indirect and driven by the positive effects of canopy complexity. We found that increasing tree diversity from monocultures to mixtures of 12 species increases canopy complexity and productivity by up to 71% and 73%, respectively. Moreover, structural equation modeling indicates that the effects of tree diversity on productivity are indirect and mediated primarily by changes in internal canopy complexity. Ultimately, we suggest that increasing canopy complexity can be a major mechanism by which tree diversity enhances productivity in young forests.
The tree diversity–productivity relationship is key to effective forest restoration and management; however, it remains unclear what role foliar chemical diversity and interactions between trees and their enemies play in driving this relationship. Trees produce chemical metabolites in their leaves that impact herbivory and pathogen infection. If trees alter the diversity of metabolites they produce when grown in more diverse communities, this could impact interactions with herbivores and pathogens. Ultimately, these tropic interactions with plant enemies, mediated by chemical diversity, could be important drivers of diversity–productivity relationships. Using a large‐scale tree diversity experiment, we used a focal tree sampling design from 14 species across a gradient of tree species richness to assess the role of foliar chemicals and trophic interactions in the diversity–productivity relationship. We used untargeted metabolomics to measure foliar phytochemical diversity, monitored tree–enemy interactions, including foliar fungal pathogens, caterpillar communities and deer browsing, and modelled their relationship to tree growth using path analysis. We unravelled significant evidence for top‐down mediation of the diversity–productivity relationship driven primarily by herbivores rather than foliar pathogens and contrasting effects of foliar chemical diversity on different enemy types. Individual trees growing in more diverse communities had higher phytochemical diversity and higher caterpillar richness, but lower leaf fungal pathogen richness. Leaf phytochemical diversity was positively associated with caterpillar richness and fungal pathogen richness, but negatively associated with browsing by white‐tailed deer ( Odocoileus virginianus ). Path analysis revealed that phytochemical diversity, caterpillar richness, insect damage and deer damage—but not foliar pathogens—all mediated positive indirect effects of tree richness on tree growth rate. Synthesis . We highlight the significant mediation of diversity–productivity relationships via contrasting effects of phytochemical diversity on plant–enemy interactions. Ultimately, our study underscores the importance of incorporating trophic interactions into biodiversity–ecosystem function studies.
Determining the factors that set species' range limits is of critical importance in an era of rapid climate and biotic change. Mangroves dominate global tropical coastlines, but their subtropical range limits are thought to be mainly constrained by cold air. However, several tropical mangrove range limits are conspicuously warm, arid, and dominated by cold water countercurrents. Despite speculation that the combination of cold water and aridity controls these range limits, investigations of this phenomenon are rare. Here, we conducted an experimental study examining the separate and interactive effects of cold water and aridity on survival, growth, and ecophysiological traits of three mangrove species from the arid, countercurrent range limit in Baja California, Mexico. It is one of the few range edges worldwide where red and white mangroves (Rhizophora mangle and Laguncularia racemosa, respectively), not the putatively stress-tolerant black mangroves (Avicennia germinans), are the most poleward distributed mangroves, providing further opportunity to examine how mangrove ecophysiological traits affect species-specific range limits. Black mangroves were surprisingly intolerant of cold water regardless of aridity, with no seedlings surviving in the lowest water temperature (13 degrees C) after 8 months. In contrast, both white and red mangrove seedlings were able to survive at 13 degrees C when humidity was 65% (but not 40%). In cold water and arid conditions, leaf stomatal conductance was consistently lowest for white mangroves, intermediate for red mangroves, and highest for black mangroves, suggesting that white mangroves were the most resistant to transpiration water loss in the arid conditions typical of Baja. Similarly, when exposed to drought after the eight-month experiment, white mangroves grown in cold water survived longer than red and black mangroves. Synthesis: Ultimately, our results suggest that the species-specific range limits of mangroves in Baja California reflects their species-specific adaptations (or lack thereof) to cold water and aridity, with white and red mangroves surprisingly outperforming black mangroves. Further, the difference in our results compared to the same species in other ranges underscores the need to incorporate species and range-specific traits when conducting distribution modelling to predict the effects of climate change on organism range limits.
Tree plantings have the potential to increase species diversity and sequester carbon, yet planting failure and early mortality pose significant barriers to their success. Biodiversity‐ecosystem function theory suggests that diverse tree plantings could improve survival outcomes through either the portfolio or facilitation effect, yet there remain few tests of this hypothesis. Here, we use a large‐scale tree‐diversity experiment (BiodiversiTREE), with monitoring of nearly 8,000 individual trees to test whether (1) tree species diversity increases survival rates, (2) tree diversity stabilizes the risk of planting failure, and/or (3) diversity effects are important relative to other common drivers of seedling mortality (e.g. herbivory and soil moisture). We found that only species identity significantly impacted the likelihood of survival, not plant functional diversity nor plot species richness nor phylogenetic diversity. There were minor effects of elevation and soil moisture on survival, but both explained a very small amount of variation in the data (r2marg ≤ 0.011). Higher tree diversity did, however, strongly reduce variation in survival across plots, with nearly 2‐fold higher coefficients of variation in monocultures (30.4%, 28.4–32.6% 95% bootstrapped confidence interval) compared to 4‐ (16.3%, 13.8–18.7%) and 12‐species plots (12.8%, 10.8–14.7%). Ultimately, our results suggest that employing diverse species can lower the risk of planting failure (i.e. the portfolio effect), but that species selection still plays a large role in early establishment.
Biodiversity within ecological communities has been shown to influence plant resistance and tolerance to herbivory, and may strongly interact with climate change. However, the effects of diversity within microbial symbionts on their plant hosts' responses to herbivores is less well documented, particularly within the context of agricultural systems. Here we examine the interactive effects of rhizobial diversity and drought in promoting soybean resistance and tolerance to insect and mammalian herbivores in an outdoor pot experiment. We demonstrate that soybean plants provided with a diverse mixture of rhizobial strains experience 30% less damage by chewing insect herbivores under both drought (reduced watering and increased temperature) and ambient weather conditions, as well as half as much colonization by aphids under drought conditions. This effect was not due to the presence of any particularly beneficial rhizobial strain (i.e., not a selection effect), but rather due to an enhanced benefit provided by the rhizobial strains in combination (i.e., a complementarity effect). No effects of rhizobial diversity were observed on the rate of defoliation by rabbits. While rhizobial diversity did affect soybean resistance to insect herbivores, these differences in insect damage did not carry through to affect soybean growth or final yield. Thus, soybean plants exhibited high tolerance to herbivory regardless of our experimentally imposed rhizobial diversity or drought treatments. With future projections for increased pest outbreaks and drought, understanding the factors that can sustainably enhance agricultural yield is critical. Our results suggest that promoting rhizobial diversity within soybean agriculture may be one nature-based solution to promote the resistance of this critical crop to insect pests.
Introduced invasive plants are a major environmental problem, but public interest in invasive plants is generally considered low compared to climate change and threatened flagship species, hindering support for effective management and policy. To understand what does drive public interest in invasive plants in the US, we investigated Google Trends search data from 2010 to 2020 for 209 introduced plant species found in the continental US. Using a phylogenetically-controlled structural equation model, we investigated three hypothesized drivers of interest: (1) plant abundance as quantified by national and state-level occurrence records in the Global Biodiversity Information Facility, (2) four key plant traits that might influence plant conspicuousness to the general public: ornamental use, human health risks, monoculture formation, and plants with positive economic value, and (3) media coverage, in particular the volume and sentiment of news articles over the same 10-year period. Public search interest was highest for the most abundant introduced species and those with human health risks, but significantly lower for ornamentals. News coverage was mostly negatively toned and disproportionately focused on a relatively small group of widespread invasive species, with significantly lower and more positively-worded coverage of ornamentals. Ultimately, we suggest that a narrow emphasis on a few highly covered ‘notorious’ invasive plant species, with lower and more positive coverage of ornamental introduced species, could send mixed messages and weaken public awareness of the threats of biological invasions. However, the generally strong linkages between public search interest and media coverage of invasive plants suggests ample opportunity to improve messaging and increase public awareness.
Abstract Internet search data can accurately assess the intensity of public interest in environmental issues. Although invasive plants are a major environmental problem, public interest in invasive plants is generally considered low compared to climate change and threatened flagship species. To understand what drives public interest in invasive plants in the US, we investigated Google Trends search data from 2010 to 2020 for 210 invasive plant species found in the continental US. We investigated three hypothesized drivers of interest: (1) plant abundance as quantified by national and state-level occurrence records in the Global Biodiversity Information Facility, (2) media coverage, in particular the volume and tone of news articles over the same 10-year period, and (3) five key plant traits that might influence plant conspicuousness to the general public: ornamental use, human health risks, monoculture formation, plants with positive economic value, and time since introduction. Google search interest was positively but indirectly influenced by species’ state and national level abundance patterns. In contrast, public search interest was most strongly and directly determined by species with greater human health risk and enhanced media coverage (through the number and tone of published articles). Ultimately, this suggests that enhanced media coverage of invasive plant species, particularly articles that detail their negative impacts, could generate increased public awareness for biological invasions.
Acute resource pulses can have dramatic legacies for organismal growth, but the legacy effects of resource pulses on broader aspects of community structure and ecosystem processes are less understood. Mass emergence of periodical cicadas (Magicicada spp.) provides an excellent opportunity to shed light on the influence of resource pulses on community and ecosystem dynamics: the adults emerge every 13 or 17 years in vast numbers over much of eastern North America, with a smaller but still significant number becoming incorporated into forest food webs. To study the potential effects of such arthropod resource pulse on primary production and belowground food webs, we added adult cicada bodies to the soil surface surrounding sycamore trees and assessed soil carbon and nitrogen concentrations, plant-available nutrients, abundance and community composition of soil fauna occupying various trophic levels, decomposition rate of plant litter after 50 and 100 days, and tree performance for 4 years. Contrary to previous studies, we did not find significant cicada effects on tree performance despite observing higher plant-available nutrient levels on cicada addition plots. Cicada addition did change the community composition of soil nematodes and increased the abundance of bacterial- and fungal-feeding nematodes, while plant feeders, omnivores, and predators were not influenced. Altogether, acute resource pulses from decomposing cicadas propagated belowground to soil microbial-feeding invertebrates and stimulated nutrient mineralization in the soil, but these effects did not transfer up to affect tree performance. We conclude that, despite their influence on soil food web and processes they carry out, even massive resource pulses from arthropods do not necessarily translate to NPP, supporting the view that ephemeral nutrient pulses can be attenuated relatively quickly despite being relatively large in magnitude.
The influence of resource pulse induced by periodical cicada bodies on soil fauna (nematodes and mites) communities, decomposition, soil nutrients, soil C and N, and American sycamore tree performance. See the "Metadata" tab in the Excel file for more details.
Macroclimatic changes are expected to radically alter coastal wetland ecosystems in the coming century. The trajectory of the response to climate warming may differ based on other concomitantly changing abiotic variables such as soil salinity and relative humidity. Thus, understanding plant responses to multiple interacting stressors is required to accurately predict coastal wetland shifts under climate change. The ongoing poleward shift of mangrove range limits has been linked with a reduction in freeze events, yet interactions between low temperature and other abiotic stressors remain underexplored. We grew two common mangroves (Avicennia germinans and Rhizophora mangle, n = 1222) from propagules for 10 months in environmental growth chambers under experimentally manipulated temperature, salinity, and relative humidity treatments that reflected the range of conditions these species experience in the field. We measured variation in growth and physiological characteristics before, during, and after low temperature exposure. For both species, resistance and resilience to low temperature stress were mediated by salinity and relative humidity conditions. Chronic chilling at 10 °C caused widespread reduction in seedling stem elongation rate, altered leaf gas exchange rates, and increased mortality, particularly under high salinity and low humidity conditions. Additional exposure to an overnight freeze (−4 °C) had relatively minor impacts. Five months after exposure to low temperatures, some R. mangle exhibited the capacity to recover from severe cold damage, but only under optimal humidity and salinity conditions. Although A. germinans were generally more resistant to low temperature stress, severely damaged plants did not recover, even in low salinity and high humidity conditions. We contend that current and future mangrove range limits are the result of interactions between multiple abiotic stressors including temperature, salinity, and relative humidity. Consequently, future modelling approaches to predicting range shifts under climate change need to consider multiple concomitantly changing abiotic variables and their interactions.
The role of tree diversity in restored forests and its impact on key ecological processes like growth and resistance to herbivory has become increasingly important. We analyzed height growth and white-tailed deer Odocoileus virginianus browsing damage to saplings of 16 broadleaved tree species in a large-scale (13 ha) reforestation experiment in Maryland, USA, where we manipulated tree diversity in 70 1,225-m2 plots. After four growing seasons, higher plot-level tree richness led to increased deer browsing damage (i.e., associational susceptibility). Despite increased deer damage to saplings in mixed plots, tree richness had no overall effect on sapling height growth. However, diversity-height relationships were related to species functional traits. Light demanding species with large leaves and faster growth rates had reduced heights in mixtures, whereas shade-tolerant, slower-growing species generally had either increased or unchanged height growth in diverse tree communities, likely related to increased canopy closure in mixtures relative to monocultures. We show that tree diversity can improve growth of late successional species despite exacerbated mammalian herbivore damage. By facilitating the establishment of species with a range of life-history strategies, increased tree diversity may enhance ecosystem multi-functionality in the early stages of forest restoration.
Abstract Ecological release from herbivory due to chemical novelty is commonly predicted to facilitate biological invasions by plants, but has not been tested on a community scale. We used metabolomics based on mass spectrometry molecular networks to assess the novelty of foliar secondary chemistry of 15 invasive plant species compared to 46 native species at a site in eastern North America. Locally, invasive species were more chemically distinctive than natives. Among the 15 invasive species, the more chemically distinct were less preferred by insect herbivores and less browsed by deer. Finally, an assessment of invasion frequency in 2,505 forest plots in the Atlantic coastal plain revealed that, regionally, invasive species that were less preferred by insect herbivores, less browsed by white‐tailed deer, and chemically distinct relative to the native plant community occurred more frequently in survey plots. Our results suggest that chemically mediated release from herbivores contributes to many successful invasions.