Coupled Shifts in Ectomycorrhizal Communities and Plant Uptake of Organic Nitrogen Along a Soil Gradient: An Isotopic Perspective

Ecosystems - Plants associating with mutualistic ectomycorrhizal (ECM) fungi may directly obtain nitrogen (N) bound in soil organic matter (N-SOM). However, the contribution of N-SOM to plant...     

Effects of Organic Enrichment of Mine Spoil on Growth and Nutrient Uptake in Oak Seedlings Inoculated with Selected Ectomycorrhizal Fungi

Abstract Poor growth of Quercus robur L. (oak) trees has been reported on mine sites where overburden and subsoil have been used in the reinstatement of surface layers. This stunting has been attributed to a lack of macronutrients and to an adverse soil environment for root growth and mycorrhizal development. Growth, mineral nutrition, and ectomycorrhizal colonization of Q. robur seedlings were studied in an experiment carried out under controlled growing conditions in which mine spoil material was enriched with a leaf litter mulch. Enrichment of mine spoil material was found to produce a significant increase in growth and foliar N concentrations of oak seedlings. Inoculation with three taxa of ectomycorrhizal fungi did not benefit seedlings when mine spoil was the only substrate, possibly due to the poor physical properties of the unamended spoil and lack of nutrients. Inoculation with two taxa, Laccaria laccata and Hebeloma crustuliniforme, isolated from 3‐year‐old trees produced a significant stimulation of growth in the organically enriched treatment, which was believed to be due to greater uptake of mineralized N. However, Cortinarius anomalus isolated from fruit bodies associated with a 15‐year‐old tree did not increase biomass. The presence of organic matter was found to result in a significant stimulation of mycorrhizal infection by both inoculum and contaminant mycobionts. Recommendations are made for improving the establishment and growth of oak seedlings on reinstated sites.     

Role of Arbuscular Mycorrhizal Fungi in Uptake of Phosphorus and Nitrogen From Soil

Abstract

Colonization of plant roots by arbuscular mycorrhizal fungi can greatly increase the plant uptake of phosphorus and nitrogen. The most prominent contribution of arbuscular mycorrhizal fungi to plant growth is due to uptake of nutrients by extraradical mycorrhizal hyphae. Quantification of hyphal nutrient uptake has become possible by the use of soil boxes with separated growing zones for roots and hyphae. Many (but not all) tested fungal isolates increased phosphorus and nitrogen uptake of the plant by absorbing phosphate, ammonium, and nitrate from soil. However, compared with the nutrient demand of the plant for growth, the contribution of arbuscular mycorrhizal fungi to plant phosphorus uptake is usually much larger than the contribution to plant nitrogen uptake. The utilization of soil nutrients may depend more on efficient uptake of phosphate, nitrate, and ammonium from the soil solution even at low supply concentrations than on mobilization processes in the hyphosphere. In contrast to ectomycorrhizal fungi, nonsoluble nutrient sources in soil are used only to a limited extent by hyphae of arbuscular mycorrhizal fungi. Side effects of mycorrhizal colonization on, for example, plant health or root activity may also influence plant nutrient uptake.     

Temporal Shifts in Plant Diversity Effects on Carbon and Nitrogen Dynamics During Litter Decomposition in a Mediterranean Shrubland Exposed to Reduced Precipitation

Ecosystems - Climate and plant diversity are major determinants of carbon (C) and nitrogen (N) dynamics in decomposing plant litter. However, the direction and extent to which these dynamics are...     

Nitrogen Isotope Patterns in Alaskan Black Spruce Reflect Organic Nitrogen Sources and the Activity of Ectomycorrhizal Fungi

Global patterns in soil, plant, and fungal stable isotopes of N (δ¹⁵N) show promise as integrated metrics of N cycling, particularly the activity of ectomycorrhizal (ECM) fungi. At small spatial scales, however, it remains difficult to differentiate the underlying causes of plant δ¹⁵N variability and this limits the application of such measurements to better understand N cycling. We conducted a landscape-scale analysis of δ¹⁵N values from 31 putatively N-limited monospecific black spruce (Picea mariana) stands in central Alaska to assess the two main hypothesized sources of plant δ¹⁵N variation: differing sources and ECM fractionation. We found roughly 20% of the variability in black spruce foliar N and δ¹⁵N values to be correlated with the concentration and δ¹⁵N values of soil NH₄ ⁺ and dissolved organic N (DON) pools, respectively. However, ¹⁵N-based mixing models from 24 of the stands suggested that fractionation by ECM fungi obscures the ¹⁵N signature of soil N pools. Models, regressions, and N abundance data all suggested that increasing dependence on soil DON to meet black spruce growth demands predicates increasing reliance on ECM-derived N and that black spruce, on average, received 53% of its N from ECM fungi. Future research should partition the δ¹⁵N values within the soil DON pool to determine how choice of soil δ¹⁵N values influence modeled ECM activity. The C balance of boreal forests is tightly linked to N cycling and δ¹⁵N values may be useful metrics of changes to these connections.     

Nitrogen Addition in a Tibetan Alpine Meadow Increases Intraspecific Variability in Nitrogen Uptake,Leading to Increased Community-level Nitrogen Uptake

Ecosystems - Plant nitrogen (N) uptake is a critical ecosystem function, especially when terrestrial ecosystems are threatened worldwide by increasing anthropogenic N deposition. However, the...     

Intein-mediated site-specific conjugation of Quantum Dots to proteins in vivo

We describe an intein based method to site-specifically conjugate Quantum Dots (QDs) to target proteins in vivo. This approach allows the covalent conjugation of any nanostructure and/or nanodevice to any protein and thus the targeting of such material to any intracellular compartment or signalling complex within the cells of the developing embryo. We genetically fused a pleckstrin-homology (PH) domain with the N-terminus half of a split intein (I_N). The C-terminus half (I_C) of the intein was conjugated to QDs in vitro. I_C-QD's and RNA encoding PH-I_N were microinjected into Xenopus embryos. In vivo intein-splicing resulted in fully functional QD-PH conjugates that could be monitored in real time within live embryos. Use of Near Infra Red (NIR)-emitting QDs allowed monitoring of QD-conjugates within the embryo at depths where EGFP is undetectable demonstrating the advantages of QD's for this type of experiment. In conclusion, we have developed a novel in vivo methodology for the site-specific conjugation of QD's and other artificial structures to target proteins in different intracellular compartments and signaling complexes.     

Nitrogen Uptake by Trees and Mycorrhizal Fungi in a Successional Northern Temperate Forest: Insights from Multiple Isotopic Methods

Forest succession may cause changes in nitrogen (N) availability, vegetation and fungal community composition that affect N uptake by trees and their mycorrhizal symbionts. Understanding how these changes affect the functioning of the mycorrhizal symbiosis is of interest to ecosystem ecology because of the fundamental roles mycorrhizae play in providing nutrition to trees and structuring forest ecosystems. We investigated changes in tree and mycorrhizal fungal community composition, the availability and uptake of N by trees and mycorrhizal fungi in a forest undergoing a successional transition (age-related loss of early successional tree taxa). In this system, 82–96% of mycorrhizal hyphae were ectomycorrhizal (EM). As biomass production of arbuscular mycorrhizal (AM) trees increased, AM hyphae comprised a significantly greater proportion of total fungal hyphae, and the EM contribution to the N requirement of EM-associated tree taxa declined from greater than 75% to less than 60%. Increasing N availability was associated with lower EM hyphal foraging and ¹⁵N tracer uptake, yet the EM-associated later-successional species Quercus rubra was nonetheless a stronger competitor for ¹⁵N than AM-associated Acer rubrum, likely due to the more extensive nature of the persistent EM hyphal network. These results indicate that successional increases in N availability and co-dominance by AM-associated trees have increased the importance of AM fungi in the mycorrhizal community, while down-regulating EM N acquisition and transfer processes. This work advances understanding of linkages between tree and fungal community composition, and indicates that successional changes in N availability may affect competition between tree taxa with divergent resource acquisition strategies.     

High Rate of Uptake of Organic Nitrogen Compounds by Prochlorococcus Cyanobacteria as a Key to Their Dominance in Oligotrophic Oceanic Waters

Direct evidence that marine cyanobacteria take up organic nitrogen compounds in situ at high rates is reported. About 33% of the total bacterioplankton turnover of amino acids, determined with a representative [³⁵S]methionine precursor and flow sorting, can be assigned to Prochlorococcus spp. and 3% can be assigned to Synechococcus spp. in the oligotrophic and mesotrophic parts of the Arabian Sea, respectively. This finding may provide a mechanism for Prochlorococcus' competitive dominance over both strictly autotrophic algae and other bacteria in oligotrophic regions sustained by nutrient remineralization via a microbial loop.     

Characteristics of the Integrated Electromyogram in Individuals Exposed to Long-Term Vibration

The functional state of the forearm muscles in individuals exposed to long-term vibration (dressers with a duration of current employment of 7–15 years, n = 12) was assessed using turn–amplitude analysis of the integrated surface electromyogram (EMG), the nerve conduction velocity test, and the conventional motor unit action potential electromyographic test. A significant increase in the EMG amplitude and the number of turns upon graded effort, as well as a decrease in the maximal ratio of the number of turns to the average amplitude of the electromyogram from the right m. flexor carpi radialis of the dressers, was revealed, which is indicative of secondary muscular disorders connected with the specific features of the occupational movement pattern and long-term exposure to vibration.     

Increased Diversity of Arbuscular Mycorrhizal Fungi in a Long-Term Field Experiment via Application of Organic Amendments to a Semiarid Degraded Soil

In this study, we tested whether communities of arbuscular mycorrhizal (AM) fungi associated with roots of plant species forming vegetative cover as well as some soil parameters (amounts of phosphatase and glomalin-related soil protein, microbial biomass C and N concentrations, amount of P available, and aggregate stability) were affected by different amounts (control, 6.5 kg m⁻², 13.0 kg m⁻², 19.5 kg m⁻², and 26.0 kg m⁻²) of an urban refuse (UR) 19 years after its application to a highly eroded, semiarid soil. The AM fungal small-subunit (SSU) rRNA genes were subjected to PCR, cloning, single-stranded conformation polymorphism analysis, sequencing, and phylogenetic analyses. One hundred sixteen SSU rRNA sequences were analyzed, and nine AM fungal types belonging to Glomus groups A and B were identified: three of them were present in all the plots that had received UR, and six appeared to be specific to certain amendment doses. The community of AM fungi was more diverse after the application of the different amounts of UR. The values of all the soil parameters analyzed increased proportionally with the dose of amendment applied. In conclusion, the application of organic wastes enhanced soil microbial activities and aggregation, and the AM fungal diversity increased, particularly when a moderate dose of UR (13.0 kg m⁻²) was applied.The semiarid Mediterranean areas of Southeastern Spain are affected by environmental degradation and erosive processes due to the fact that they are characterized by a set of climatic conditions that includes irregular and scarce rainfall and long, dry, and hot summers. Under these conditions, the soil organic matter content decreases, and the availability of nutrients and water for plants is reduced. Consequently, soil productivity decreases, levels of below-ground microbially diverse populations decline, and the water deficit limits plant growth so that the vegetation cover of natural soils cannot be sustained. Therefore, the development of revegetation techniques to reduce erosion, to remediate the effects of degradation, and, thus, to allow the restoration of biodiversity is needed. It was previously demonstrated that the application of organic amendments, such as urban refuse (UR), to soil increases the organic matter content of soil and improves the quality and productivity of degraded soils (17, 44, 57). Also, it was previously shown that the organic residues yield an improvement in levels of microbially diverse populations in the soil (43).A substantial part of the soil microbial communities belongs to the arbuscular mycorrhizal (AM) fungi, an ancient group of fungi belonging to the phylum Glomeromycota (49), which form mutualistic associations with the roots of the majority of land plants. These fungi have a variety of beneficial effects on their host plants, such as increasing the uptake of mineral nutrients, particularly phosphorus and nitrogen (41, 52); reduction of pathogen infections (7); improvement of water relations (12) and soil stability (58); and the limitation of heavy metal uptake (34). It is evident that AM fungi are an important factor contributing to the maintenance of terrestrial ecosystem functioning. Studies have shown that the diversity of AM fungal populations in the soil can affect plant diversity and productivity and ecosystem stability (62). Therefore, information on the species composition of the AM fungal community in roots is important for an understanding of mycorrhizal function as well as for the effective management and preservation of the diversity of AM fungal populations in ecological field studies.Thanks to advances in molecular techniques in recent years, it is possible to apply PCR-based molecular methods in order to analyze the diversity of AM fungi colonizing the roots of an individual plant at any given time. Traditional identification based on spore morphology is often problematic, and the abundance of spores in the soil may not accurately reflect AM fungal community composition and dynamics (8). The single-stranded conformation polymorphism (SSCP) approach is a very sensitive and reproducible technique for analyzing the sequence diversity of AM fungi within roots (30). This method is based on nucleotide differences between homologous sequence strands, which are detected by electrophoresis of single-stranded DNA under nondenaturing conditions (38).It is known that the application of organic amendments can have a positive effect on the proliferation of natural AM fungi in crop systems (20, 26). The stimulatory effects of the addition of organic matter on the development of AM fungi could be related to an improvement in the extensive network of AM fungal mycelium in the soil. In this way, the colonized plants are able to effectively exploit nutrients and water from soil (52). Moreover, AM fungi are able to exploit nutrients released by the mineralization of organic matter due to the activities of mineralizing microorganisms (28). However, there are many previous reports that showed a strong negative impact on the presence of AM fungal populations and mycorrhizal colonization when composted urban waste was added to the soil (19, 46). Also, research using trap cultures of host plants showed a decrease in the level of diversity of AM fungal species in soils amended with sewage sludge (25, 61).In a previous study carried out in 1992 at the site that is also the subject of the current work, Roldán and Albaladejo (43) found that the application of UR decreased levels of AM fungal populations in the first year after amendment; however, they observed an increase in levels of these populations 3 years after the addition. We hypothesized that after a long period of time, the application of UR could alter the diversity of AM fungal populations in a highly eroded, semiarid soil and that this effect could be influenced by the refuse application rate. In order to verify this hypothesis, we studied the diversity of the AM fungi associated with the roots of plant species forming the vegetative cover of five plots that received different amounts of UR 19 years after the amendment. Also, we determined whether there was an improvement in soil quality parameters related to soil microbial activity.     

Nitrogen Uptake During One Year in Subarctic Plant Functional Groups and in Microbes After Long-Term Warming and Fertilization

For the first time in an arctic long-term warming and fertilization experiment, the short-term (days) and longer-term (month and year) nitrogen (N) uptake and allocation in plants, microbes, and soil pools were studied, with ¹⁵N-labeling of an organic nitrogen form, glycine. The long-term warming and fertilization had no marked effect on soil inorganic N content, but both dissolved organic N (DON) and plant biomass did increase after fertilization. Soil microbes initially immobilized most of the added ¹⁵N, but in the following months, they lost two-thirds, while label concentration in plants increased. After a year, however, the ¹⁵N recovered in microbes was still 10-fold higher than that in the plant biomass, showing the high importance of soil microbes in nutrient retention in arctic ecosystems, irrespective of the impact of long-term warming or fertilization. The effects of the treatments on the uptake of label by deciduous shrubs and evergreens paralleled that of their N pool sizes, suggesting that their N uptake potential was unaffected by long-term warming and fertilizer addition. Mosses and herbs had high uptake potential but in fertilized plots they took up less ¹⁵N, that is, they were N saturated. The fraction of ¹⁵N in microbes tended to decrease after fertilization, but this was an effect of higher N pool dilution after 1 month and a year, and not due to lower initial uptake. Although the concentration of soil inorganic N did not change after fertilization, both increased DON and the results of the ¹⁵N label addition showed that the N availability in the ecosystem had increased. By contrast, warming had little effect on soil N pools and microbial ¹⁵N uptake, and, hence, had no detectable effects on ¹⁵N accumulation.     

Commensal Interactions in a Dual-Species Biofilm Exposed to Mixed Organic Compounds

There is limited knowledge of interspecies interactions in biofilm communities. In this study, Pseudomonas sp. strain GJ1, a 2-chloroethanol (2-CE)-degrading organism, and Pseudomonas putida DMP1, a p-cresol-degrading organism, produced distinct biofilms in response to model mixed waste streams composed of 2-CE and various p-cresol concentrations. The two organisms maintained a commensal relationship, with DMP1 mitigating the inhibitory effects of p-cresol on GJ1. A triple-labeling technique compatible with confocal microscopy was used to investigate the influence of toxicant concentrations on biofilm morphology, species distribution, and exopolysaccharide production. Single-species biofilms of GJ1 shifted from loosely associated cell clusters connected by exopolysaccharide to densely packed structures as the p-cresol concentrations increased, and biofilm formation was severely inhibited at high p-cresol concentrations. In contrast, GJ1 was abundant when associated with DMP1 in a dual-species biofilm at all p-cresol concentrations, although at high p-cresol concentrations it was present only in regions of the biofilm where it was surrounded by DMP1. Evidence in support of a commensal relationship between DMP1 and GJ1 was obtained by comparing GJ1-DMP1 biofilms with dual-species biofilms containing GJ1 and Escherichia coli ATCC 33456, an adhesive strain that does not mineralize p-cresol. Additionally, the data indicated that only tower-like cell structures in the GJ1-DMP1 biofilm produced exopolysaccharide, in contrast to the uniform distribution of EPS in the single-species GJ1 biofilm.     

The Role of Negative Charge in the Delivery of Quantum Dots to Neurons

Despite our extensive knowledge of the structure of negatively charged cell surface proteoglycans and sialoglycoconjugates in the brain, we have little understanding of how their negative charge contributes to brain function. We have previously shown that intensely photoluminescent 9-nm diameter quantum dots (QDs) with a CdSe core, a ZnS shell, and a negatively charged compact molecular ligand coating (CL4) selectively target neurons rather than glia. We now provide an explanation for this selective neuronal delivery. In this study, we compared three zwitterionic QD coatings differing only in their regions of positive or negative charge, as well as a positively charged (NH₂) polyethylene glycol (PEG) coat, for their ability to deliver the cell-membrane-penetrating chaperone lipopeptide JB577 (WG(Palmitoyl)VKIKKP₉G₂H₆) to individual cells in neonatal rat hippocampal slices. We confirm both that preferential uptake in neurons, and the lack of uptake in glia, is strongly associated with having a region of greater negative charge on the QD coating. In addition, the role of negatively charged chondroitin sulfate of the extracellular matrix (ECM) in restricting uptake was further suggested by digesting neonatal rat hippocampal slices with chondroitinase ABC and showing increased uptake of QDs by oligodendrocytes. Treatment still did not affect uptake in astrocytes or microglia. Finally, the future potential of using QDs as vehicles for trafficking proteins into cells continues to show promise, as we show that by administering a histidine-tagged green fluorescent protein (eGFP-His₆) to hippocampal slices, we can observe neuronal uptake of GFP.     

Long-Term Regional Shifts in Plant Community Composition Are Largely Explained by Local Deer Impact Experiments

The fact that herbivores and predators exert top-down effects to alter community composition and dynamics at lower trophic levels is no longer controversial, yet we still lack evidence of the full nature, extent, and longer-term effects of these impacts. Here, we use results from a set of replicated experiments on the local impacts of white-tailed deer to evaluate the extent to which such impacts could account for half-century shifts in forest plant communities across the upper Midwest, USA. We measured species'' responses to deer at four sites using 10–20 year-old deer exclosures. Among common species, eight were more abundant outside the exclosures, seven were commoner inside, and 16 had similar abundances in- and outside. Deer herbivory greatly increased the abundance of ferns and graminoids and doubled the abundance of exotic plants. In contrast, deer greatly reduced tree regeneration, shrub cover (100–200 fold in two species), plant height, plant reproduction, and the abundance of forbs. None of 36 focal species increased in reproduction or grew taller in the presence of deer, contrary to expectations. We compared these results to data on 50-year regional shifts in species abundances across 62 sites. The effects of herbivory by white-tailed deer accurately account for many of the long-term regional shifts observed in species'' abundances (R² = 0.41). These results support the conjecture that deer impacts have driven many of the regional shifts in forest understory cover and composition observed in recent decades. Our ability to link results from shorter-term, local experiments to regional long-term studies of ecological change strengthens the inferences we can draw from both approaches.     

Modification of Spontaneous Emission Rates of Self-assembled CdSe Quantum Dots by Coupling to Hybrid Optical Nanoantennas

Plasmonics - The spontaneous emission of a light source can be modified by tailoring its local density of optical states. Indeed, this concept has been commonly utilized to enhance the spontaneous...     

Ecological Consequences of Long-Term Exposure of Anabaena variabilis (Cyanophyceae) to Shifts in Environmental Factors

Cultures of Anabaena variabilis were exposed to different light intensities, and the time course of photoadaptation was measured by photosynthetic rate and changes in pigmentation. A shift down in intensity of 284 μEin · m⁻² · sec⁻¹ caused a temporary decrease in the photosynthetic response followed by gradual adaptation to the new conditions. Final chlorophyll a and carotenoid concentrations were reached after 1 day, although other physiological indicators showed that adaptation required 4 days. The parameter I_k was shown to be the best indicator of photoadaptation. A shift up in light intensity of the same magnitude also required 4 days for complete photoadaptation by the culture, although chlorophyll and carotenoid concentrations stabilized within 1 day. A shift down in light intensity of 392 μEin · m⁻² · sec⁻¹ resulted in a temporary attempt to adapt followed by collapse of the population. This demonstrates an apparent threshold in the magnitude of the shift in light intensity which will permit successful adaptation. Simultaneous changes in light intensity and temperature also adversely affected culture populations. Our observations present a possible cause for the decline or prevention of an algal bloom under a fluctuating light regime and suggest that it may be possible to predict this decline as a result of synoptic weather patterns or hydrodynamic influences.     

Escherichia coli Behavior in the Presence of Organic Matter Released by Algae Exposed to Water Treatment Chemicals

When exposed to oxidation, algae release dissolved organic matter with significant carbohydrate (52%) and biodegradable (55 to 74%) fractions. This study examined whether algal organic matter (AOM) added in drinking water can compromise water biological stability by supporting bacterial survival. Escherichia coli (1.3 × 10⁵ cells ml⁻¹) was inoculated in sterile dechlorinated tap water supplemented with various qualities of organic substrate, such as the organic matter coming from chlorinated algae, ozonated algae, and acetate (model molecule) to add 0.2 ± 0.1 mg of biodegradable dissolved organic carbon (BDOC) liter⁻¹. Despite equivalent levels of BDOC, E. coli behavior depended on the source of the added organic matter. The addition of AOM from chlorinated algae led to an E. coli growth equivalent to that in nonsupplemented tap water; the addition of AOM from ozonated algae allowed a 4- to 12-fold increase in E. coli proliferation compared to nonsupplemented tap water. Under our experimental conditions, 0.1 mg of algal BDOC was sufficient to support E. coli growth, whereas the 0.7 mg of BDOC liter⁻¹ initially present in drinking water and an additional 0.2 mg of BDOC acetate liter⁻¹ were not sufficient. Better maintenance of E. coli cultivability was also observed when AOM was added; cultivability was even increased after addition of AOM from ozonated algae. AOM, likely to be present in treatment plants during algal blooms, and thus potentially in the treated water may compromise water biological stability.     

Ubiquity of Insect-Derived Nitrogen Transfer to Plants by Endophytic Insect-Pathogenic Fungi: an Additional Branch of the Soil Nitrogen Cycle

The study of symbiotic nitrogen transfer in soil has largely focused on nitrogen-fixing bacteria. Vascular plants can lose a substantial amount of their nitrogen through insect herbivory. Previously, we showed that plants were able to reacquire nitrogen from insects through a partnership with the endophytic, insect-pathogenic fungus Metarhizium robertsii. That is, the endophytic capability and insect pathogenicity of M. robertsii are coupled so that the fungus acts as a conduit to provide insect-derived nitrogen to plant hosts. Here, we assess the ubiquity of this nitrogen transfer in five Metarhizium species representing those with broad (M. robertsii, M. brunneum, and M. guizhouense) and narrower insect host ranges (M. acridum and M. flavoviride), as well as the insect-pathogenic fungi Beauveria bassiana and Lecanicillium lecanii. Insects were injected with ¹⁵N-labeled nitrogen, and we tracked the incorporation of ¹⁵N into two dicots, haricot bean (Phaseolus vulgaris) and soybean (Glycine max), and two monocots, switchgrass (Panicum virgatum) and wheat (Triticum aestivum), in the presence of these fungi in soil microcosms. All Metarhizium species and B. bassiana but not L. lecanii showed the capacity to transfer nitrogen to plants, although to various degrees. Endophytic association by these fungi increased overall plant productivity. We also showed that in the field, where microbial competition is potentially high, M. robertsii was able to transfer insect-derived nitrogen to plants. Metarhizium spp. and B. bassiana have a worldwide distribution with high soil abundance and may play an important role in the ecological cycling of insect nitrogen back to plant communities.