skip to main content


Title: Connections and Feedback: Aquatic, Plant, and Soil Microbiomes in Heterogeneous and Changing Environments
Abstract Plant, soil, and aquatic microbiomes interact, but scientists often study them independently. Integrating knowledge across these traditionally separate subdisciplines will generate better understanding of microbial ecological properties. Interactions among plant, soil, and aquatic microbiomes, as well as anthropogenic factors, influence important ecosystem processes, including greenhouse gas fluxes, crop production, nonnative species control, and nutrient flux from terrestrial to aquatic habitats. Terrestrial microbiomes influence nutrient retention and particle movement, thereby influencing the composition and functioning of aquatic microbiomes, which, themselves, govern water quality, and the potential for harmful algal blooms. Understanding how microbiomes drive links among terrestrial (plant and soil) and aquatic habitats will inform management decisions influencing ecosystem services. In the present article, we synthesize knowledge of microbiomes from traditionally disparate fields and how they mediate connections across physically separated systems. We identify knowledge gaps currently limiting our abilities to actualize microbiome management approaches for addressing environmental problems and optimize ecosystem services.  more » « less
Award ID(s):
1656006
NSF-PAR ID:
10228098
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
BioScience
Volume:
70
Issue:
7
ISSN:
0006-3568
Page Range / eLocation ID:
548 to 562
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. BACKGROUND The availability of nitrogen (N) to plants and microbes has a major influence on the structure and function of ecosystems. Because N is an essential component of plant proteins, low N availability constrains the growth of plants and herbivores. To increase N availability, humans apply large amounts of fertilizer to agricultural systems. Losses from these systems, combined with atmospheric deposition of fossil fuel combustion products, introduce copious quantities of reactive N into ecosystems. The negative consequences of these anthropogenic N inputs—such as ecosystem eutrophication and reductions in terrestrial and aquatic biodiversity—are well documented. Yet although N availability is increasing in many locations, reactive N inputs are not evenly distributed globally. Furthermore, experiments and theory also suggest that global change factors such as elevated atmospheric CO 2 , rising temperatures, and altered precipitation and disturbance regimes can reduce the availability of N to plants and microbes in many terrestrial ecosystems. This can occur through increases in biotic demand for N or reductions in its supply to organisms. Reductions in N availability can be observed via several metrics, including lowered nitrogen concentrations ([N]) and isotope ratios (δ 15 N) in plant tissue, reduced rates of N mineralization, and reduced terrestrial N export to aquatic systems. However, a comprehensive synthesis of N availability metrics, outside of experimental settings and capable of revealing large-scale trends, has not yet been carried out. ADVANCES A growing body of observations confirms that N availability is declining in many nonagricultural ecosystems worldwide. Studies have demonstrated declining wood δ 15 N in forests across the continental US, declining foliar [N] in European forests, declining foliar [N] and δ 15 N in North American grasslands, and declining [N] in pollen from the US and southern Canada. This evidence is consistent with observed global-scale declines in foliar δ 15 N and [N] since 1980. Long-term monitoring of soil-based N availability indicators in unmanipulated systems is rare. However, forest studies in the northeast US have demonstrated decades-long decreases in soil N cycling and N exports to air and water, even in the face of elevated atmospheric N deposition. Collectively, these studies suggest a sustained decline in N availability across a range of terrestrial ecosystems, dating at least as far back as the early 20th century. Elevated atmospheric CO 2 levels are likely a main driver of declines in N availability. Terrestrial plants are now uniformly exposed to ~50% more of this essential resource than they were just 150 years ago, and experimentally exposing plants to elevated CO 2 often reduces foliar [N] as well as plant-available soil N. In addition, globally-rising temperatures may raise soil N supply in some systems but may also increase N losses and lead to lower foliar [N]. Changes in other ecosystem drivers—such as local climate patterns, N deposition rates, and disturbance regimes—individually affect smaller areas but may have important cumulative effects on global N availability. OUTLOOK Given the importance of N to ecosystem functioning, a decline in available N is likely to have far-reaching consequences. Reduced N availability likely constrains the response of plants to elevated CO 2 and the ability of ecosystems to sequester carbon. Because herbivore growth and reproduction scale with protein intake, declining foliar [N] may be contributing to widely reported declines in insect populations and may be negatively affecting the growth of grazing livestock and herbivorous wild mammals. Spatial and temporal patterns in N availability are not yet fully understood, particularly outside of Europe and North America. Developments in remote sensing, accompanied by additional historical reconstructions of N availability from tree rings, herbarium specimens, and sediments, will show how N availability trajectories vary among ecosystems. Such assessment and monitoring efforts need to be complemented by further experimental and theoretical investigations into the causes of declining N availability, its implications for global carbon sequestration, and how its effects propagate through food webs. Responses will need to involve reducing N demand via lowering atmospheric CO 2 concentrations, and/or increasing N supply. Successfully mitigating and adapting to declining N availability will require a broader understanding that this phenomenon is occurring alongside the more widely recognized issue of anthropogenic eutrophication. Intercalibration of isotopic records from leaves, tree rings, and lake sediments suggests that N availability in many terrestrial ecosystems has steadily declined since the beginning of the industrial era. Reductions in N availability may affect many aspects of ecosystem functioning, including carbon sequestration and herbivore nutrition. Shaded areas indicate 80% prediction intervals; marker size is proportional to the number of measurements in each annual mean. Isotope data: (tree ring) K. K. McLauchlan et al. , Sci. Rep. 7 , 7856 (2017); (lake sediment) G. W. Holtgrieve et al. , Science 334 , 1545–1548 (2011); (foliar) J. M. Craine et al. , Nat. Ecol. Evol. 2 , 1735–1744 (2018) 
    more » « less
  2. Abstract Over the past several decades, we have increased our understanding of the influences of plant genetics on associated communities and ecosystem functions. These influences have been shown at both broad spatial scales and across many plant families, creating an active subdiscipline of ecology research focused on genes‐to‐ecosystems connections. One complex aspect of plant genetics is the distinction between males and females in dioecious plants. The genetic determinants of plant sex are poorly understood for most plants, but the influences of plant sex on morphological, physiological, and chemical plant traits are well‐studied. We argue that these plant traits, controlled by plant sex, may have wide‐reaching influences on both terrestrial and aquatic communities and ecosystem processes, particularly for riparian plants. Here we systematically review the influences of plant sex on plant traits, influences of plant traits on terrestrial community members, and how interactions between plant traits and terrestrial community members can influence terrestrial ecosystem functions in riparian forests. We then extend these influences into adjacent aquatic ecosystem functions and aquatic communities to explore how plant sex might influence linked terrestrial‐aquatic systems as well as the physical structure of riparian systems. This review highlights data gaps in empirical studies exploring the direct influences of plant sex on communities and ecosystems but draws inference from community and ecosystem genetics. Overall, this review highlights how variation by plant sex has implications for climate change adaptations in riparian habitats, the evolution and range shifts of riparian species and the methods used for conserving and restoring riparian systems. 
    more » « less
  3. Abstract

    The potential for animals to modify spatial patterns of nutrient limitation for autotrophs and habitat availability for other members of their communities is increasingly recognized. However, net trophic effects of consumers acting as ecosystem engineers remain poorly known. The American AlligatorAlligator mississippiensisis an abundant predator capable of dramatic modifications of physical habitat through the creation and maintenance of pond‐like basins, but its role in influencing community structure and nutrient dynamics is less appreciated.

    We investigated if alligators engineer differences in nutrient availability and changes to community structure by their creation of ‘alligator ponds’ compared to the surrounding phosphorus (P)‐limited oligotrophic marsh.

    We used a halo sampling design of three distinct habitats extending outward from 10 active alligator ponds across a hydrological gradient in the Everglades, USA. We performed nutrient analysis on basal food‐web resources and quantitative community analyses, and stoichiometric analyses on plants and animals.

    Our findings demonstrate that alligators act as ecosystem engineers and enhance food‐web heterogeneity by increasing nutrient availability, manipulating physical structure and altering algal, plant and animal communities. Flocculent detritus, an unconsolidated layer of particulate organic matter and soil, showed strong patterns of P enrichment in ponds. Higher P availability in alligator ponds also resulted in bottom‐up trophic transfer of nutrients as evidenced by higher growth rates (lower N:P) for plants and aquatic consumers. Edge habitats surrounding alligator ponds contained the most diverse communities of invertebrates and plants, but low total abundance of fishes, likely driven by high densities of emergent macrophytes. Pond communities exhibited higher abundance of fish compared to edge habitat and were dominated by compositions of small invertebrates that track high nutrient availability in the water column. Marshes contained high numbers of animals that are closely tied to periphyton mats, which were absent from other habitats.

    Alligator‐engineered habitats are ecologically important by providing nutrient‐enriched ‘hotspots’ in an oligotrophic system, habitat heterogeneity to marshes, and refuges for other fauna during seasonal disturbances. This work adds to growing evidence that efforts to model community dynamics should routinely consider animal‐mediated bottom‐up processes like ecosystem engineering.

     
    more » « less
  4. Abstract

    The National Ecological Observatory Network Terrestrial Observation System (NEON TOS) produces open‐access data products that allow data users to investigate the impact of change drivers on key “sentinel” taxa and soils. The spatial and temporal sampling strategy that coordinates implementation of these protocols enables integration across TOS products and with products generated by NEON aquatic, remote sensing, and terrestrial instrument subsystems. Here, we illustrate the plots and sampling units that make up the physical foundation of a NEON TOS site, and we describe the scales (subplot, plot, airshed, and site) at which sampling is spatially colocated across protocols and subsystems. We also describe how moderate resolution imaging spectroradiometer‐enhanced vegetation index (MODIS‐EVI) phenology data are used to temporally coordinate TOS sampling within and across years at the continental scale of the observatory. Individually, TOS protocols produce data products that provide insight into populations, communities, and ecosystem processes. Within the spatial and temporal framework that guides cross‐protocol implementation, the ability to draw inference across data products is enhanced. To illustrate this point, we develop an example using R software that links two TOS data products collected with different temporal frequencies at both plot and site spatial scales. A thorough understanding of how TOS protocols are integrated with each other in space and time, and with other NEON subsystems, is necessary to leverage NEON data products to maximum effect. For example, a researcher must understand the spatial and temporal scales at which soil biogeochemistry data, soil microbe biomass data, and plant litter production and chemistry data may be combined to quantify soil nutrient stocks and fluxes across NEON sites. We present clear links among TOS protocols and across NEON subsystems that will enhance the utility of NEON TOS data products for the data user community.

     
    more » « less
  5. Abstract

    Imaging spectroscopy provides the opportunity to incorporate leaf and canopy optical data into ecological studies, but the extent to which remote sensing of vegetation can enhance the study of belowground processes is not well understood. In terrestrial systems, aboveground and belowground vegetation quantity and quality are coupled, and both influence belowground microbial processes and nutrient cycling. We hypothesized that ecosystem productivity, and the chemical, structural and phylogenetic‐functional composition of plant communities would be detectable with remote sensing and could be used to predict belowground plant and soil processes in two grassland biodiversity experiments: the BioDIV experiment at Cedar Creek Ecosystem Science Reserve in Minnesota and the Wood River Nature Conservancy experiment in Nebraska. We tested whether aboveground vegetation chemistry and productivity, as detected from airborne sensors, predict soil properties, microbial processes and community composition. Imaging spectroscopy data were used to map aboveground biomass, green vegetation cover, functional traits and phylogenetic‐functional community composition of vegetation. We examined the relationships between the image‐derived variables and soil carbon and nitrogen concentration, microbial community composition, biomass and extracellular enzyme activity, and soil processes, including net nitrogen mineralization. In the BioDIV experiment—which has low overall diversity and productivity despite high variation in each—belowground processes were driven mainly by variation in the amount of organic matter inputs to soils. As a consequence, soil respiration, microbial biomass and enzyme activity, and fungal and bacterial composition and diversity were significantly predicted by remotely sensed vegetation cover and biomass. In contrast, at Wood River—where plant diversity and productivity were consistently higher—belowground processes were driven mainly by variation in the quality of aboveground inputs to soils. Consequently, remotely sensed functional, chemical and phylogenetic composition of vegetation predicted belowground extracellular enzyme activity, microbial biomass, and net nitrogen mineralization rates but aboveground biomass (or cover) did not. The contrasting associations between the quantity (productivity) and quality (composition) of aboveground inputs with belowground soil attributes provide a basis for using imaging spectroscopy to understand belowground processes across productivity gradients in grassland systems. However, a mechanistic understanding of how above and belowground components interact among different ecosystems remains critical to extending these results broadly.

     
    more » « less