Eric Chauvet

Importance of Stream Microfungi in Controlling Breakdown Rates of Leaf Litter

Breakdown of seven leaf species covering a broad range of litter qualities (lignin: 7-31% of leaf dry mass; tannin: 0.0-6.7%; nitrogen: 0.5-2.6%; phosphorus: 0.0 17- 0.094%) and dynamics of fungal biomass and reproductive activity were studied in a softwater mountain stream. Litter breakdown proceeded at exponential rates k ranging from 0.0042 d-l (evergreen oak) to 0.0515 d-l (ash). Fungal colonization of litter was generally rapid, with the fungus-specific indicator molecule ergosterol increasing from initially negligible concentrations to 375-859 pug/g of detrital mass. Using species-specific factors relating ergosterol concentrations to mycelial dry mass, maximum fungal biomass associated with litter was estimated as 61-155 mg/g of total system mass. Minimum estimates of net mycelial production during active growth varied between 0.3 and 3.8 mg g-I d-l, and maximum sporulation rates of aquatic hyphomycetes ranged from 760 to 7500 conidia mg- I d-l. Initially, reproductive activity was largely synchronized with increases in ergosterol concentrations, but it declined dramatically after peak sporulation rates were reached, whereas ergosterol concentrations levelled off or decreased at consid- erably slower rates. Periods of highest fungal productivity were thus limited to an initial breakdown stage of 2-8 wk. Strong correlations were found between the exponential breakdown coefficient and each of three parameters reflecting fungal activity in leaf litter, that is, maximum ergosterol concentration (P = 0.002, r = 0.96), net mycelial production (P = 0.02, r = 0.92), and sporulation rate (P < 0.001, r = 0.99). The initial lignin content of leaves was also significantly correlated with the rate constant k (P = 0.02, r = -0.83), suggesting that lignin was the primary factor determining litter quality and thus breakdown rate. The correlation was even stronger when data were logarithmically transformed (P < 0.01, r = -0.95). Tannin concentration was significantly correlated with k only when two high-lignin species were excluded from the analysis (P = 0.19, r = -0.56 compared with P = 0.05, r = -0.88), while initial concentrations of phosphorus (P = 0.17, r = 0.58) and particularly nitrogen (P = 0.82, r = 0.06) were poor predictors of litter decomposability. These results suggest that the initial lignin content of leaves controlled litter breakdown rate through a kinetic limitation of carbon sources for saprotrophic microfungi. The de- composer activity of these organisms, in turn, would then have governed breakdown rates. In doing this, fungi produced substantial amounts of both mycelial and conidial biomass that was potentially available to higher trophic levels of the food web.

A perspective on leaf litter breakdown in streams

Leaf litter breakdown, a critical ecosystem level process in streams and other aquatic environments , has been conceptualized using models borrowed from terrestrial systems. We argue that current views of the process in fresh waters need to be conceptually improved. Specifically, we think the idea that breakdown proceeds in three distinct temporal stages (leaching, conditioning, fragmentation) has been over emphasized. Leaching, the massive loss of soluble leaf components within 24 h after immersion, is generally considered to constitute a well-defined first stage. Recent evidence suggests, however, that the initial solute losses are largely an effect of the un natural drying procedures to which experimental leaves are normally subjected. Fresh leaf litter does lose solutes when immersed,but gradually throughout the breakdown process rather than instantly upon wetting. Conditioning, the second breakdown stage, describes the enhancement of leaf palatability for detritivores by microbial colonization, and is thus ultimately targeted towards a group of organisms (which contribute to litter degradation) rather than addressing the breakdown process per se. Furthermore,conditioning implies a key role for detritivorous invertebrates and underrates the established direct degradative activity of microbial decomposers. If, thus, leaching and conditioning are not generally useful operators to describe portions of the litter breakdown process in freshwaters, the traditional concept, which emphasises leaching, conditioning and fragmentation as three sequential stages, loses much of its appeal. Consequently, we propose a new conceptual model, in which the coincidence and interplay of various subprocesses of litter breakdown is more strongly recognized. In this model, we propose to view the process in terms of the products of litter breakdown-as a complement to the usual perspective which focuses on litter mass loss. Six primary breakdown products are considered : bacterial, fungal and shredder biomass; dissolved organic matter; fine-particulate organic matter; and inorganic mineralization products such as CO2, NH+ and PO3-. We present a scheme illustrating the hypothesized formation of these products throughout breakdown. However, to improve understanding of the process, application of the proposed conceptual framework in experimental work is necessary.

A case for using litter breakdown to assess functional stream integrity

Assessment of the condition of ecosystems is a critical prerequisite for alleviating effects of the multiple anthropogenic stresses imposed on them. For stream ecosystems, a multitude of approaches has been proposed for this purpose. However, they all rest on the assessment of structural attributes, even though it is generally recognized that adequate characterization of ecosystems requires information on both structure (pattern) and function (process). Therefore, we propose a complementary approach to stream assessment based on evaluating ecosystem level processes. Leaf litter breakdown is a prime candidate to consider in this context. This is because of the pivotal role that allochthonous litter plays in streams, the demonstrated effects of anthropogenic perturbations on litter breakdown, and the relative ease of implementation. Leaf breakdown is governed by a variety of internal and external factors that complicate the partitioning of effects due to anthropogenic stress and natural variability (background noise), thus potentially limiting the sensitivity and robustness of litter breakdown assays. However, internal regulation factors can be controlled by standardizing assessment procedures, while variability due to external factors can be accounted for by stream classification and/or a comparative approach (e.g., downstream-upstream comparisons). Composite parameters such as ratios of break- down rates in fine-mesh and coarse-mesh bags may further increase the power of litter breakdown assays. Analyses may also be extended to include both leaf-associated decomposer assemblages (i.e., structural measures) and processes (i.e., additional functional measures). Significant efforts are required for developing standard assessment schemes as refined as extant procedures based on structural stream attributes (e.g., structure of macroinvertebrate assemblages). These efforts are nevertheless worthwhile in view of the new dimension that is added to current assessment procedures when functional elements are incorporated.

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.

Continental-scale effects of nutrient pollution on stream ecosystem functioning.

Reading the Leaves Excess inputs of nutrients—a type of pollution known as eutrophication—threatens biodiversity and water quality in rivers and streams. Woodward et al. (p. 1438; see the Perspective by Palmer and Febria) studied how one key ecosystem process—leaf-litter decomposition—responds to eutrophication across a large nutrient pollution gradient in 100 European streams. Leaf breakdown was stimulated by low to moderate nutrient concentrations but was inhibited at high rates of nutrient loading. Leaf-litter breakdown rates across 100 European streams offer insights into ecosystem health during eutrophication. Excessive nutrient loading is a major threat to aquatic ecosystems worldwide that leads to profound changes in aquatic biodiversity and biogeochemical processes. Systematic quantitative assessment of functional ecosystem measures for river networks is, however, lacking, especially at continental scales. Here, we narrow this gap by means of a pan-European field experiment on a fundamental ecosystem process—leaf-litter breakdown—in 100 streams across a greater than 1000-fold nutrient gradient. Dramatically slowed breakdown at both extremes of the gradient indicated strong nutrient limitation in unaffected systems, potential for strong stimulation in moderately altered systems, and inhibition in highly polluted streams. This large-scale response pattern emphasizes the need to complement established structural approaches (such as water chemistry, hydrogeomorphology, and biological diversity metrics) with functional measures (such as litter-breakdown rate, whole-system metabolism, and nutrient spiraling) for assessing ecosystem health.

The Role of Biodiversity in the Functioning of Freshwater and Marine Benthic Ecosystems

Abstract Empirical studies investigating the role of species diversity in sustaining ecosystem processes have focused primarily on terrestrial plant and soil communities. Eighteen representative studies drawn from post-1999 literature specifically examined how changes in biodiversity affect benthic ecosystem processes. Results from these small-scale, low-diversity manipulative studies indicate that the effects of changes in biodiversity (mostly synonymous with local species richness) are highly variable over space and time and frequently depend on specific biological traits or functional roles of individual species. Future studies of freshwater and marine ecosystems will require the development of new experimental designs at larger spatial and temporal scales. Furthermore, to successfully integrate field and laboratory studies, the derivation of realistic models and appropriate experiments will require approaches different from those already used in terrestrial systems.

Magnitude and variability of process rates in fungal diversity-litter decomposition relationships

There is compelling evidence that losses in plant diversity can alter ecosystem functioning, particularly by reducing primary production. However, impacts of biodiversity loss on decomposition, the complementary process in the carbon cycle, are highly uncertain. By manipulating fungal decomposer diversity in stream microcosm experiments we found that rates of litter decomposition and associated fungal spore production are unaffected by changes in decomposer diversity under benign and harsher environmental conditions. This result calls for caution when generalizing outcomes of biodiversity experiments across systems. In contrast to their magnitude, the variability of process rates among communities increased when species numbers were reduced. This was most likely caused by a portfolio effect (i.e. statistical averaging), with the uneven species distribution typical of natural communities tending to weaken that effect. Curbing species extinctions to maintain ecosystem functioning thus can be important even in situations where process rates are unaffected.

Breakdown of leaf litter in a neotropical stream

We investigated the breakdown of 2 leaf species, Croton gossypifolius (Euphorbiaceae) and Clidemia sp. (Melastomataceae), in a 4th-order neotropical stream (Andean Mountains, southwestern Colombia) using leaf bags over a 6-wk period. We determined the initial leaf chemical composition and followed the change in content of organic matter, C, N, and ergosterol, the sporulation activity of aquatic hyphomycetes, and the structure and composition of leaf-associated aquatic hyphomycetes and macroinvertebrates. Both leaf species decomposed rapidly (k = 0.0651 and 0.0235/d, respectively); Croton lost 95% of its initial mass within 4 wk compared to 54% for Clidemia. These high rates were probably related to the stable and moderately high water temperature (19°C), favoring strong biological activity. Up to 2300 and 1500 invertebrates per leaf bag were found on Croton and Clidemia leaves after 10 and 16 d, respectively. Shredders accounted for <5% of the total numbers and biomass. Fungal biomass peaked at 8.4 and 9.6% of the detrital mass of the 2 leaf species, suggesting that fungi contributed considerably to leaf mass loss. The difference in breakdown rates between leaf species was consistent with the earlier peaks in ergosterol and sporulation rate in Croton (10 d vs 16 d in Clidemia) and the faster colonization of Croton by macroinvertebrates. The softer texture, lower tannin content, and higher N content were partly responsible for the faster breakdown of Croton leaves. The rapid breakdown of leaf litter, combined with a low influence by shredders, is in accordance with previous findings. The high fungal activity associated with rapid leaf breakdown appears to be characteristic of leaf processing in tropical streams.

A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration

The decomposition of plant litter is one of the most important ecosystem processes in the biosphere and is particularly sensitive to climate warming. Aquatic ecosystems are well suited to studying warming effects on decomposition because the otherwise confounding influence of moisture is constant. By using a latitudinal temperature gradient in an unprecedented global experiment in streams, we found that climate warming will likely hasten microbial litter decomposition and produce an equivalent decline in detritivore-mediated decomposition rates. As a result, overall decomposition rates should remain unchanged. Nevertheless, the process would be profoundly altered, because the shift in importance from detritivores to microbes in warm climates would likely increase CO(2) production and decrease the generation and sequestration of recalcitrant organic particles. In view of recent estimates showing that inland waters are a significant component of the global carbon cycle, this implies consequences for global biogeochemistry and a possible positive climate feedback.

Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition

Diel temperature oscillations are a nearly ubiquitous phenomenon, with amplitudes predicted to change along with mean temperatures under global-warming scenarios. Impact assessments of global warming have largely disregarded diel temperature oscillations, even though key processes in ecosystems, such as decomposition, may be affected. We tested the effect of a 5 degrees C temperature increase with and without diel oscillations on litter decomposition by fungal communities in stream microcosms. Five temperature regimes with identical thermal sums (degree days) were applied: constant 3 degrees and 8 degrees C; diel temperature oscillations of 5 degrees C around each mean; and oscillations of 9 degrees C around 8 degrees C. Temperature oscillations around 8 degrees C (warming scenario), but not 3 degrees C (ambient scenario), accelerated decomposition by 18% (5 degrees C oscillations) and 31% (9 degrees C oscillations), respectively, compared to the constant temperature regime at 8 degrees C. Community structure was not affected by oscillating temperatures, although the rise in mean temperature from 3 degrees to 8 degrees C consistently shifted the relative abundance of species. A simple model using temperature-growth responses of the dominant fungal decomposers accurately described the experimentally observed pattern, indicating that the effect of temperature oscillations on decomposition in our warming scenario was caused by strong curvilinear responses of species to warming at low temperature, particularly of the species becoming most abundant at 8 degrees C (Tetracladium marchalianum). These findings underscore the need to consider species-specific temperature characteristics in concert with changes in communities when assessing consequences of global warming on ecosystem processes.