Keller Suberkropp

Regulation of Leaf Breakdown by Fungi in Streams: Influences of Water Chemistry

We examined the influence of stream water chemistry on relationships between fungal activity and breakdown rates of yellow poplar (Liriodendron tulipifera) leaves in eight streams that varied with respect to pH and nutrient (nitrate and phosphate) con- centrations. We also performed a reciprocal exchange experiment of leaves that had been colonized by microorganisms in two streams with contrasting water chemistries. Decom- poser activity varied greatly depending on the stream in which the leaves were placed. Variation in breakdown rates of yellow poplar leaves was over 9-fold maximum ATP concentrations associated with leaves varied as much as 8-fold, and maximum sporulation rates of fungi associated with leaves varied over 80-fold among streams. Among all streams, nitrate, phosphate, and temperature were positively correlated with one another and with decomposer biomass and activity. When hardwater streams were analyzed separately, nitrate concentration was the only variable that was significantly correlated with all measures of microbial activity and leaf breakdown. Consequently, nitrate concentration appeared to explain much of the variation we detected among streams. Responses to the reciprocal exchange experiment were rapid, with significant changes occurring within the first 5 d after the transfer. Leaves transferred from the hardwater stream containing relatively high concentrations of nitrate and phosphate to the softwater stream containing low concentra- tions of nutrients exhibited by large decreases in both ATP concentrations and sporulation rates, whereas ATP concentrations and sporulation rates increased when leaves received the reciprocal transfer. The fungi associated with decomposing leaves in streams appear to obtain a significant portion of their nutrients (e.g., nitrogen and phosphorus) from the water passing over the leaf surface. These results indicate that the chemistry of the water can be an important regulator of leaf breakdown in streams by affecting the activity of decomposer fungi.

Relationships between growth and sporulation of aquatic hyphomycetes on decomposing leaf litter

The dynamics of changes in microbial biomass (ATP concentrations), respiration rates and sporulation rates of aquatic hyphomycetes associated with tulip poplar leaf disks in two streams with different water chemistry were compared with the activities of a dominant fungal species from each stream growing on sterilized leaf disks in the laboratory. Aquatic hyphomycetes sporulated at maximum rates after 15–19 d in both stream and laboratory studies. Sporulation occurred during periods of increasing biomass and respiration indicating a close relationship between growth and sporulation in these fungi. Leaf disks decomposing in the hardwater stream supported greater biomass, activity and number of species than those decomposing in the softwaer stream. Fungi colonizing leaf disks in the laboratory exhibited higher ATP concentrations and sporulation rates than the communities from either stream. These differences appear to be related to water chemistry, particularly N and P concentrations. Organic matter budgets calculated for the two species grown in the laboratory indicated that growth yield coefficients were 0·15–0·23 g g −1 and net production efficiencies ranged from 24 to 46 %. A significant portion of fungal production was converted into conidia by both fungi.

Fungal and Bacterial Production during the Breakdown of Yellow Poplar Leaves in 2 Streams

We compared the production and biomass of fungi with that of bacteria during the breakdown of yellow poplar leaves (Liriodendron tulipifera) in 2 streams that differed in water chemistry. The hardwater stream contained higher concentrations of nutrients (N and P) than the softwater stream. Fungal biomass (determined from ergosterol concentrations), production (determined from rates of [14C]acetate incorporation into ergosterol), and sporulation rates associated with leaves were greater in the hardwater stream than in the softwater stream. Bacterial biomass (determined from direct counts and cell volume estimates) was similar on leaves in both streams, but bacterial production (determined from rates of [3H]leucine incorporation into protein) was greater on leaves in the hardwater stream than in the softwater stream. Fungal biomass associated with leaves was always much greater than bacterial biomass (385-1236× in the hardwater stream, 32-185× in the softwater stream) during leaf breakdown. Fungal production reached maximum values within the first 2 wk after leaves were submerged in the hardwater stream. In the softwater stream, fungal production was low and remained relatively constant throughout the study with a minimum occurring after 28 d. In both streams, bacterial production increased throughout leaf breakdown. Even so, with the exception of 1 date, production of fungi was greater (2-108× in the hardwater stream and 0.9-35× in the softwater stream) than bacterial production during leaf breakdown. On the basis of both biomass and production, fungi played a greater role than bacteria in the breakdown of yellow poplar leaves in these streams.

Effect of Inorganic Nutrients on Relative Contributions of Fungi and Bacteria to Carbon Flow from Submerged Decomposing Leaf Litter

The relative contributions of fungi and bacteria to carbon flow from submerged decaying plant litter at different levels of inorganic nutrients (N and P) were studied. We estimated leaf mass loss, fungal and bacterial biomass and production, and microbial respiration and constructed partial carbon budgets for red maple leaf disks precolonized in a stream and then incubated in laboratory microcosms at two levels of nutrients. Patterns of carbon flow for leaf disks colonized with the full microbial assemblage were compared with those colonized by bacteria but in which fungi were greatly reduced by placing leaf disks in colonization chambers sealed with membrane filters to exclude aquatic hyphomycete conidia but not bacterial cells. On leaves colonized by the full microbial assemblage, elevated nutrient concentrations stimulated fungi and bacteria to a similar degree. Peak fungal and bacterial biomass increased by factors of 3.9 and 4.0; cumulative production was 3.9 and 5.1 times higher in the high nutrient in comparison with the low nutrient treatment, respectively. Fungi dominated the total microbial biomass (98.4 to 99.8%) and cumulative production (97.3 and 96.5%), and the fungal yield coefficient exceeded that of bacteria by a factor of 36 and 27 in low- and high-nutrient treatments, respectively. Consequently, the dominant role of fungi in leaf decomposition did not change as a result of nutrient manipulation. Carbon budgets indicated that 8% of leaf carbon loss in the low-nutrient treatment and 17% in the high-nutrient treatment were channeled to microbial (essentially fungal) production. Nutrient enrichment had a positive effect on rate of leaf decomposition only in microcosms with full microbial assemblages. In treatments where fungal colonization was reduced, cumulative bacterial production did not change significantly at either nutrient level and leaf decomposition rate was negatively affected (high nutrients), suggesting that bacterial participation in carbon flow from decaying leaf litter is low regardless of the presence of fungi and nutrient availability. Moreover, 1.5 and 2.3 times higher yield coefficients of bacteria in the reduced fungal treatments at low and high nutrients, respectively (percentage of leaf carbon loss channeled to bacterial production), suggest that bacteria are subjected to strong competition with fungi for resources available in leaf litter.

Effects of nutrient enrichment on yellow poplar leaf decomposition and fungal activity in streams

We examined the effect of nutrient addition on rates of decomposition, ergosterol concentrations (as a measure of fungal biomass), and rates of fungal sporulation associated with yellow poplar (Liriodendron tulipifera L.) leaf disks in 3 streams that differed in water chemistry. We carried out these studies in flow-through channels that received additions of KH2PO4, NaNO3, both nutrients, or controls with no additions. When limiting nutrients were added to the water in all 3 streams, leaf-decaying fungi responded and decomposition rates increased. Two streams, Walker Branch and Payne Creek, contained low concentrations of both inorganic N (<40 μg/L) and P (<16 μg/L). In these streams, rates of leaf decomposition, concentrations of fungal biomass, and rates of sporulation were stimulated only when N and P were added together, indicating that these nutrients potentially colimited fungal activity. The other stream, Little Schultz Creek, contained low concentrations of P (<5 μg/L), but higher concentrations of N (65–200 μg/L) than Walker Branch and Payne Creek. Rates of leaf decomposition, fungal biomass, and sporulation were stimulated by P addition and when both nutrients were added together, indicating potential limition of fungal activity by P in this stream. Results from all 3 streams provide direct experimental evidence that leaf-decaying fungi can use nutrients dissolved in stream water and that, in some streams, rates of leaf decomposition are stimulated by the addition of these nutrients.

URBANIZATION AFFECTS STREAM ECOSYSTEM FUNCTION BY ALTERING HYDROLOGY, CHEMISTRY, AND BIOTIC RICHNESS

Catchment urbanization can alter physical, chemical, and biological attributes of stream ecosystems. In particular, changes in land use may affect the dynamics of organic matter decomposition, a measure of ecosystem function. We examined leaf-litter decomposition in 18 tributaries of the St. Johns River, Florida, USA. Land use in all 18 catchments ranged from 0% to 93% urban which translated to 0% to 66% total impervious area (TIA). Using a litter-bag technique, we measured mass loss, fungal biomass, and macroinvertebrate biomass for two leaf species (red maple [Acer rubrum] and sweetgum [Liquidambar styraciflua]). Rates of litter mass loss, which ranged from 0.01 to 0.05 per day for red maple and 0.006 to 0.018 per day for sweetgum, increased with impervious catchment area to levels of approximately 30-40% TIA and then decreased as impervious catchment area exceeded 40% TIA. Fungal biomass was also highest in streams draining catchments with intermediate levels of TIA. Macroinvertebrate biomass ranged from 17 to 354 mg/bag for red maple and from 15 to 399 mg/bag for sweetgum. Snail biomass and snail and total invertebrate richness were strongly related to breakdown rates among streams regardless of leaf species. Land-use and physical, chemical, and biological variables were highly intercorrelated. Principal-components analysis was therefore used to reduce the variables into several orthogonal axes. Using stepwise regression, we found that flow regime, snail biomass, snail and total invertebrate richness, and metal and nutrient content (which varied in a nonlinear manner with impervious surface area) were likely factors affecting litter breakdown rates in these streams.

Effect of dissolved nutrients on two aquatic hyphomycetes growing on leaf litter

Concentrations of potassium nitrate, potassium phosphate, or calcium chloride were varied in stream-simulating microcosms containing leaf discs colonized by the aquatic hyphomycetes Anguillospora filiformis or Lunulospora curvula. Cumulative conidium production of the fungi determined from rates of sporulation at 2 d intervals was stimulated by increasing concentrations of both potassium nitrate and potassium phosphate but not by calcium chloride. Leaf weight loss was also stimulated by increasing concentrations of potassium nitrate and potassium phosphate. The amount of fungal biomass (determined as ATP concentrations) associated with leaf discs increased significantly only in the treatments in which A. filiformis received increasing concentrations of potassium nitrate. These results indicate that as aquatic hyphomycetes grow on leaf litter, they can obtain at least a portion of their inorganic nutrition from the water flowing over the leaves. They also suggest that sporulation is more sensitive to changes in nutrient concentrations than growth.

Experimental nutrient additions accelerate terrestrial carbon loss from stream ecosystems

Carbon kicked out by nutrients Excess nutrients added to streams result in net carbon loss from aquatic ecosystems. Nitrogen and phosphorus are known to fuel increases in algal carbon. Now, Rosemond et al. show that nutrients stimulate losses of terrestrially derived carbon (e.g., from twigs and leaves). The authors monitored several multiyear experiments on headwater forest streams in the United States. Some of these streams had extra nitrogen and phosphorus added at levels that are now common in many streams and lakes. To successfully manage river ecosystems, we need to take into account nutrient pollution effects on multiple carbon pathways. Science, this issue p. 1142 Terrestrial carbon is rapidly lost from stream ecosystems as a result of nutrient enrichment. Nutrient pollution of freshwater ecosystems results in predictable increases in carbon (C) sequestration by algae. Tests of nutrient enrichment on the fates of terrestrial organic C, which supports riverine food webs and is a source of CO2, are lacking. Using whole-stream nitrogen (N) and phosphorus (P) additions spanning the equivalent of 27 years, we found that average terrestrial organic C residence time was reduced by ~50% as compared to reference conditions as a result of nutrient pollution. Annual inputs of terrestrial organic C were rapidly depleted via release of detrital food webs from N and P co-limitation. This magnitude of terrestrial C loss can potentially exceed predicted algal C gains with nutrient enrichment across large parts of river networks, diminishing associated ecosystem services.

Nutrient enrichment alters storage and fluxes of detritus in a headwater stream ecosystem.

Responses of detrital pathways to nutrients may differ fundamentally from pathways involving living plants: basal carbon resources can potentially decrease rather than increase with nutrient enrichment. Despite the potential for nutrients to accelerate heterotrophic processes and fluxes of detritus, few studies have examined detritus-nutrient dynamics at whole-ecosystem scales. We quantified organic matter (OM) budgets over three consecutive years in two detritus-based Appalachian (U.S.A.) streams. After the first year, we began enriching one stream with low-level nitrogen and phosphorus inputs. Subsequent effects of nutrients on outputs of different OM compartments were determined using randomized intervention analysis. Nutrient addition did not affect dissolved or coarse particulate OM export but had dramatic effects on fine particulate OM (FPOM) export at all discharges relative to the reference stream. After two years of enrichment, FPOM export was 340% higher in the treatment stream but had decreased by 36% in the reference stream relative to pretreatment export. Ecosystem respiration, the dominant carbon output in these systems, also increased in the treatment stream relative to the reference, but these changes were smaller in magnitude than those in FPOM export. Nutrient enrichment accelerated rates of OM processing, transformation, and export, potentially altering food-web dynamics and ecosystem stability in the long term. The results of our large-scale manipulation of a detrital ecosystem parallel those from analogous studies of soils, in which net loss of organic carbon has often been shown to result from experimental nutrient addition at the plot scale. Streams are useful model systems in which to test the effects of nutrients on ecosystem-scale detrital dynamics because they allow both the tracking of OM conversion along longitudinal continua and the integrated measurement of fluxes of transformed material through downstream sites.

Fungal Growth, Production, and Sporulation during Leaf Decomposition in Two Streams

ABSTRACT I examined the activity of fungi associated with yellow poplar (Liriodendron tulipifera) and white oak (Quercus alba) leaves in two streams that differed in pH and alkalinity (a hardwater stream [pH 8.0] and a softwater stream [pH 6.7]) and contained low concentrations of dissolved nitrogen (<35 μg liter−1) and phosphorus (<3 μg liter−1). The leaves of each species decomposed faster in the hardwater stream (decomposition rates, 0.010 and 0.007 day−1 for yellow poplar and oak, respectively) than in the softwater stream (decomposition rates, 0.005 and 0.004 day−1 for yellow poplar and oak, respectively). However, within each stream, the rates of decomposition of the leaves of the two species were not significantly different. During the decomposition of leaves, the fungal biomasses determined from ergosterol concentrations, the production rates determined from rates of incorporation of [14C]acetate into ergosterol, and the sporulation rates associated with leaves were dynamic, typically increasing to maxima and then declining. The maximum rates of fungal production and sporulation associated with yellow poplar leaves were greater than the corresponding rates associated with white oak leaves in the hardwater stream but not in the softwater stream. The maximum rates of fungal production associated with the leaves of the two species were higher in the hardwater stream (5.8 mg g−1 day−1 on yellow poplar leaves and 3.1 mg g−1 day−1 on oak leaves) than in the softwater stream (1.6 mg g−1day−1 on yellow poplar leaves and 0.9 mg g−1day−1 on oak leaves), suggesting that effects of water chemistry other than the N and P concentrations, such as pH or alkalinity, may be important in regulating fungal activity in streams. In contrast, the amount of fungal biomass (as determined from ergosterol concentrations) on yellow poplar leaves was greater in the softwater stream (12.8% of detrital mass) than in the hardwater stream (9.6% of detrital mass). This appeared to be due to the decreased amount of fungal biomass that was converted to conidia and released from the leaf detritus in the softwater stream.