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Mycologia, 96(1), 2004, pp. 57-65.
© 2004 by The Mycological Society of America

Effects of whole-stream nutrient enrichment on the concentration and abundance of aquatic hyphomycete conidia in transport


Vladislav Gulis 1
Keller Suberkropp

     Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama 35487

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

The concentrations and relative abundances of aquatic hyphomycete conidia in water were followed during a three-year study in two headwater streams at Coweeta Hydrologic Laboratory, North Carolina, using the membrane-filtration technique. After a one-year pretreatment period, one of the streams was enriched continuously with inorganic nutrients (N+P) for two years while the other stream served as the reference. This ecosystem-level nutrient manipulation resulted in concentrations of aquatic hyphomycete conidia in the water of the treated stream that were 4.5–6.9 times higher than the concentrations observed during the pretreatment period and in the reference stream. Nutrient enrichment led to an increase in the number of fungal species detected on each sampling date. Changes in dominance patterns and relative abundances of individual species also were detected after treatment. Nutrient addition stimulates the reproductive activity of aquatic hyphomycetes, their colonization success and fungal-mediated leaf-litter decomposition. Such changes in the activity of the fungal community might affect higher trophic levels in lotic ecosystems.

Key words: community structure, freshwater fungi, nitrogen, phosphorus, seasonal pattern


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Aquatic hyphomycetes play a key role in the decomposition of plant litter entering woodland streams from riparian vegetation (Suberkropp and Klug 1976Citation, Bärlocher and Kendrick 1981Citation, Bärlocher 1992Citation). These fungi colonize substrata, sporulate underwater, and their conidia are well adapted for dispersal by water currents (Webster and Descals 1981Citation). In laboratory experiments, conidia production may account for 8–12% of leaf mass loss (Suberkropp 1991Citation); lower values (2–4%) have been calculated for fungal communities in streams (Findlay and Arsuffi 1989Citation, Suberkropp 1991Citation).

It was hypothesized that aquatic hyphomycetes might obtain inorganic nutrients (nitrogen and phosphorus) not only from their organic substrata (leaf litter, wood debris, etc.) but also directly from water passing by (Suberkropp 1995Citation, Suberkropp and Chauvet 1995Citation). Later, studies in laboratory microcosms demonstrated that elevated concentrations of nitrate and phosphate in water stimulate overall fungal activity and conidia production (Suberkropp 1998Citation, Sridhar and Bärlocher 2000Citation).

The aim of this study was to examine the effects of long-term, whole-stream nutrient enrichment on the community structure of aquatic hyphomycetes from concentrations of conidia in the water and to compare these data with those from a pretreatment period and a reference stream. Because most aquatic hyphomycetes form characteristic tetraradiate, branched or filiform conidia, the elegant technique introduced by Iqbal and Webster (1973)Citation to characterize aquatic hyphomycete communities in streams was used. It consists basically of passing a known amount of water through membrane filters and subsequently identifying and counting conidia trapped on the filter. The underlying assumption is that assemblages of conidia in transport reflect those developed on submerged organic substrata (Bärlocher 1982Citation); some conidia, however, may be introduced from terrestrial habitats (Bandoni 1981Citation, Sridhar and Bärlocher 1993Citation).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
The study was conducted at two headwater streams draining catchments 53 and 54 at the Coweeta Hydrologic Laboratory, Macon County, North Carolina. They drain south-facing slopes covered by mixed deciduous forest in the southern Appalachian Mountains at an elevation of ca 850 m. Because the dense understory of Rhododendron maximum L. results in year-round shading, the streams are primarily heterotrophic, i.e., they rely on allochthonous organic matter and energy. These streams are small (average discharge about 2 L s-1), circumneutral, softwater and contain low nutrient concentrations (NO3-N + NH4-N < 29 µg L-1, soluble reactive phosphorus (SRP) < 9 µg L-1, J. Benstead, pers comm). Streams are located about 300 m apart, and their physical and hydrochemical characteristics are very similar (Cuffney et al 1990Citation, Wallace et al 1999Citation). Water temperature during the study was continuously monitored with Optic StowAway temperature probes (Onset Computer Corp.).

Pretreatment observations of both streams were initiated in Apr 1999, and nutrient addition was started in stream 54 on 11 Jul 2000, while stream 53 continued to serve as a reference. Treatment stream 54 was enriched with nitrogen and phosphorus (ammonium nitrate and potassium phosphate) with a pump 145 m above the sampling site that added a concentrated solution into a pipe fed with stream water that was laid in the streambed and continued to within 10 m of the downstream flume. The amount of nutrients added was proportional to instantaneous discharge and was controlled by a data logger. The pipe had 18 openings (an average of 8 m apart) down the stream, letting nutrient solution drip into the stream over its entire length (Gulis and Suberkropp 2003aCitation). Nutrient addition resulted in elevated ammonium-N (100 µg L-1, mean during 24 mo of treatment), nitrate-N (283 µg L-1) and SRP (46 µg L-1) that was determined from five water samples taken at approximately 25 m intervals along the stream twice a month (J. Benstead, pers comm).

To determine concentrations and species composition of aquatic hyphomycete conidia, water samples were taken monthly over a 3 yr period (Apr 1999–Jul 2002) at flumes 135 and 190 m downstream from the source of streams 53 and 54, respectively. Triplicate samples of stream water (300–500 mL) were filtered through membrane filters (5 µm pore size, Millipore) at streamside (Iqbal and Webster 1973Citation), and conidia were stained with trypan blue in lactic acid (0.1%). Filters were taken to the laboratory where conidia were identified and counted (150 fields, Leitz Laborlux, 160x). Different amounts of water were filtered and subjected to counts of conidia on each date, due to the highly variable concentrations of suspended solids that interfered with conidia observation and according to anticipated conidia concentrations. To meaningfully compare species richness, we adjusted all conidia counts to the smallest sample volume (3 x 300 mL) and used rarefaction (Krebs 1989Citation) to calculate the expected number of species corresponding to the adjusted number of conidia in each sample. In other words, we chose to use the volume of water sampled and not the number of conidia (individuals) to standardize species richness (see Bärlocher and Graça 2002Citation for discussion).

Mean aquatic hyphomycete conidia concentrations and numbers of species in the water of stream 53 and 54 were compared both before and after treatment periods with paired t-tests. Conidia concentrations were log10 transformed before analyses. To find out whether treatment indeed caused the changes in conidia concentrations, we performed randomized intervention analysis (RIA, Carpenter et al 1989Citation). Despite recent criticism (Murtaugh 2002Citation), we believe that this analysis was appropriate in our case because the three half-series means (mean pretreatment conidia concentrations in both streams and mean post-treatment concentration in the reference stream) were very similar and temporal differences between streams were not clearly pronounced. Sorensen's quantitative similarity indexes (Magurran 1988Citation) were calculated as:


where S is the number of species, xik is the relative abundance of species k in stream i. Evenness of conidia distribution among taxa and Shannon-Wiener diversity index were calculated as:


where E is evenness, H is Shannon-Weaver index, S is the number of species, pi is the relative abundance of species i in the community. Cluster and correspondence analyses based on mean relative abundances of dominant fungal species (abundance >5% in any stream/treatment combination, nine species total) were carried out to ordinate four stream/treatment combinations and analyze what changes in fungal species/abundances led to the differences observed. Statistical analyses were done with Statistica 5.5 (StatSoft Inc., Tulsa, Oklahoma).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Water temperatures were very similar in the two streams throughout the study (Fig. 1). Although the concentration of aquatic hyphomycete conidia in stream water from 53 and 54 fluctuated rather erratically during the pretreatment period in 1999–2000, mean conidia concentrations in the two streams were not significantly different (paired t-test, P = 0.084, Fig. 2A). In 2000–2002, when nutrients were continuously added to stream 54, the difference in mean conidia concentration between reference and treatment streams was highly significant (P < 0.0001, Fig. 2A). On the basis of the comparison of pretreatment and treatment data for both streams, RIA indicated that the treatment had an effect on conidia concentrations in the water (P < 0.0001). Nutrient enrichment resulted in higher conidia concentrations on each sampling date in stream 54 in comparison to 53. Seasonal patterns with higher conidia concentrations in the autumn and early winter also was more pronounced in the treatment stream.



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  		FIG. 1. Average daily water temperatures of stream 53 and 54 during the study.

 


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  		FIG. 2. Conidia concentration (A) and species richness (B) of aquatic hyphomycetes in water of stream 53 and 54. Symbols indicate mean ± 1 SE. Means for stream 53 (dashed) and 54 (solid lines) are presented for before and after treatment periods

 
A total of 51 taxa of aquatic and water-borne hyphomycetes were detected in the two streams during the study (Table I). The mean numbers of species per sampling date (sample volume adjusted, rarefied data) were nearly equal and not significantly different in stream 53 and 54 during the pretreatment period (paired t-test, P = 0.896, Fig. 2B, Table II). However, the mean number of species per sampling date was higher in stream 54 compared to stream 53 during the treatment period (paired t-test, P < 0.0001). Species richness of aquatic hyphomycetes determined from water samples was affected positively by nutrient enrichment in stream 54 (RIA, P = 0.002). Temporal fluctuations in species richness were similar in both streams during the treatment period and generally corresponded to seasonal patterns in conidia concentration (cf. Fig. 2A and B).


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  		TABLE I. Aquatic hyphomycete conidia assemblages (mean of percent contributions at each sampling date) in water from stream 53 (reference) and 54 (treatment) before (Apr 1999–Jul 2000) and during (Jul 2000–Jul 2002) the addition of nutrients to stream 54

 

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  		TABLE II. Comparison of aquatic hyphomycete communities of stream 53 (reference) and 54 (treatment) before and after nutrient addition was started in 54. Standard errors are included for mean conidia concentrations and number of species

 
Five and seven species of aquatic hyphomycetes dominated the conidia pool (mean percent contribution >5% during study period) in stream 53 and 54, respectively. The relative abundances of the dominant species are illustrated in Fig. 3. The top-ranked species in both streams was Alatospora acuminata (28 and 18% of total conidia in stream 53 and 54, respectively, but see note to Table I for explanation). The most notable difference in community structure of aquatic hyphomycete conidia between streams throughout the observation period was the nearly total absence of Lunulospora curvula from stream 53, whereas in 54 it was a codominant species at least in the pretreatment year (Table I, Fig. 3). Nutrient enrichment resulted in shifts in relative abundances of some aquatic hyphomycetes in stream 54. Triscelophorus monosporus and L. curvula were common during the pretreatment period in warmer seasons and in the summer (2000) when the enrichment was started but nearly disappeared afterward. In contrast, Tricladium chaetocladium and Tetrachaetum elegans increased their contribution to the total conidia pool after nutrient addition started (Table I, Fig. 3).



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  		FIG. 3. Relative abundance of dominant aquatic hyphomycetes (as conidia in transport) in streams 53 and 54 throughout the study. Data for Alatospora acuminata and small sigmoid conidia were combined (see note to Table I).

 
Despite the fact that we observed changes in dominant species and the relative contributions of individual fungal species to the total conidia pool, species richness, diversity and evenness of conidia distribution among taxa were similar in all four stream/treatment combinations (Table II). The similarity indices between fungal assemblages, however, indicate that changes in aquatic hyphomycete community structure occurred after nutrient enrichment.

Cluster and correspondence analyses also reflected changes in aquatic hyphomycete communities that took place after nutrient enrichment and allowed separation of the "54 after" fungal assemblage (Fig. 4). Increases in relative abundances of the conidia of Anguillospora filiformis, Tetrachaetum elegans and Tricladium chaetocladium were associated with nutrient addition (Table I, Fig. 4). Overall, 70.0 and 27.3% of the inertia were explained by dimension 1 and 2, respectively, of the correspondence analysis.



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  		FIG. 4. Cluster and correspondence analyses of four stream/treatment combinations based on mean relative abundances of conidia of nine dominant species of aquatic hyphomycetes. Clustering based on Pearson correlation coefficient and unweighted pair-group average method. Solid circles on correspondence analysis plot represent communities, crosses plot fungal taxa are abbreviated as: AA = Alatospora acuminata, AF = Anguillospora filiformis, AT = Articulospora tetracladia, FC = Flagellospora curvula, LC = Lunulospora curvula, TE = Tetrachaetum elegans, TC = Tricladium chaetocladium, TK = Triscelophorus konajensis, TM = T. monosporus

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
In our study, we achieved 13- and fivefold mean increases in nitrogen and phosphorus concentrations in the treatment stream that led to 4.5–6.9 times higher mean conidia concentrations during the treatment period in comparison to pretreatment period and the reference stream (Fig. 2A, Table II). The maximum conidia concentration recorded in stream 54 was 22 000 spores L-1, which is similar to some of the higher concentrations reported for other streams (cf. 22 000 spores L-1, Shearer and Webster 1985aCitation; 25 000 spores L-1, Suberkropp 1991Citation; 18 000 spores L-1, Suberkropp 1997Citation; 24 000 spores L-1, Gönczöl and Révay 1998Citation).

In addition to nutrient concentrations, two important factors that affect production of conidia are temperature (cf. Figs. 1 and 2A) and presence of leaf litter in the stream. Headwater streams at Coweeta have relatively high leaf-litter standing stocks throughout the year (Suberkropp, unpubl data). This, coupled with naturally very low N and P concentrations and relatively warm winter temperatures, results in small fluctuations in conidia concentrations throughout the year (stream 53, Fig. 2A, cf. Suberkropp and Wallace 1992Citation) rather than large peaks during the autumn-winter that are common in many temperate streams (Iqbal and Webster 1973Citation, Bärlocher and Rosset 1981Citation, Shearer and Webster 1985bCitation, Suberkropp 1997Citation, Gönczöl and Révay 1999Citation, Bärlocher 2000Citation). Nutrient enrichment of stream 54, however, led to clear seasonal peaks coinciding with or lagging slightly behind the main leaf-litter inputs in autumn (stream 54 Nov 2000 and 2001, Fig. 2A). Smaller peaks were also observed in spring.

Several studies have provided indications that water chemistry and inorganic nutrients in particular, affect conidia production to a greater extent than fungal biomass accrual and microbially mediated leaf-litter decomposition (Suberkropp 1995Citation, Suberkropp and Chauvet 1995Citation, Grattan and Suberkropp 2001Citation). These observations also were confirmed by experiments in laboratory microcosms (Suberkropp 1998Citation, Sridhar and Bärlocher 2000Citation). Increased concentrations of conidia in streams with high nutrient concentrations should result in more efficient/faster colonization of new substrata. Once established on plant litter, fungi grow faster with higher nutrient availability (Grattan and Suberkropp 2001Citation, Gulis and Suberkropp 2003aCitation) and because of their relatively short lifecycle soon produce more conidia. This stimulation of fungal activity leads to the faster disappearance of leaf litter from the stream, which might affect leaf-shredding invertebrates and stream food webs.

Aquatic hyphomycetes allocate up to 80% of their production to conidia (Suberkropp 1991Citation), and the proportion can vary depending on nutrient availability (Suberkropp 1995Citation). Because fungal yield coefficients for decomposing submerged leaf litter were estimated to vary between 1–31%, being higher (15–31%) at increased nutrient availability (Suberkropp 1991Citation, 1995Citation, Weyers and Suberkropp 1996Citation, Sridhar and Bärlocher 2000Citation, Gulis and Suberkropp 2003bCitation, cCitation), this results in a significant amount of leaf carbon being lost as conidia. In laboratory microcosms, Articulospora tetracladia converted 1.5 and 12% of leaf mass loss to conidia at low and high nutrient concentrations, respectively (Gulis and Suberkropp 2003cCitation). For leaf litter colonized by a natural microbial assemblage in a headwater stream and then incubated in laboratory microcosms at different levels of nutrients, the difference was even greater—0.04 and 4.0% of leaf mass loss was converted to conidia at low and high N and P concentrations, respectively (Gulis and Suberkropp 2003bCitation). Consequently, in streams with higher nutrient concentrations, more conidia, i.e., more fine-particulate organic carbon, will be produced with the potential to be transported out of a stream and lost to local food webs.

Species richness of aquatic hyphomycetes in stream 54 after nutrient addition was higher than in the reference stream on each sampling date after late fall 2000 (Fig. 2B). This presumably was due to uneven increase in sporulation by aquatic hyphomycetes that enhanced the detection of rare species. We also noticed shifts in the relative contributions of the dominant species (Fig. 3). In contrast, Sridhar and Bärlocher (2000)Citation did not find shifts in species composition in response to nutrient addition in a laboratory experiment. It is not clear why elevated nutrient concentrations affected the relative abundances of some dominant species. We noted that all three species that significantly increased in abundance after nutrient addition (Anguillospora filiformis, Tetrachaetum elegans and Tricladium chaetocladium; Table I, Fig. 4) have relatively large conidia in comparison to spore size of species dominant during pretreatment period or in the reference stream (Alatospora acuminata and Articulospora tetracladia). Perhaps production of conidia with higher biovolume requires additional inorganic nutrient supply because it has been suggested that N and P obtained from the water are mainly shunted to sporulation by aquatic hyphomycetes (Suberkropp 1998Citation). Additional studies on the physiological requirements of particular species are needed to address this question. Interspecific interactions also may be modified at different nutrient levels.

The effects of long-term, whole-stream, nutrient enrichment on aquatic fungi has received little attention in the literature. We previously compared fungal biomass, leaf-litter decomposition and aquatic hyphomycete conidia in transport in the upstream, unenriched reach of stream 54 with that occurring in the nutrient-enriched downstream reach in a shorter (8 mo) study (Gulis and Suberkropp 2003aCitation). Concentrations of conidia were higher in the downstream reach, and some shifts in dominance pattern similar to those observed in our study occurred. It is evident from the results of these studies that nutrient enrichment of a small woodland stream (including anthropogenic eutrophication) can result in higher concentrations of aquatic hyphomycete conidia in transport and changes in fungal community structure. Because these changes are coupled to faster leaf-litter colonization, higher decomposition rates (Gulis and Suberkropp 2003aCitation) and presumably increased transport of fine particulate organic matter downstream, such enrichment might have consequences for the invertebrate fauna feeding on submerged decaying organic matter and on the higher trophic levels in such streams.


   ACKNOWLEDGMENTS
 
We are grateful to H. Weyers for help with sample collection and J. Benstead for providing long-term nutrient data for both streams. This work was supported in part under NSF-NATO Postdoctoral Fellowship in Science and Engineering awarded to VG and by NSF grant DEB 9806610.


   FOOTNOTES
 
1 Current address: Institute of Marine Research, Department of Zoology, University of Coimbra, 3004-517 Coimbra, Portugal. E-mail: vgulis{at}ci.uc.pt Back

Accepted for publication May 30, 2003.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Bandoni RJ., 1981 Aquatic Hyphomycetes from terrestrial litter. In: Wicklow DT, Carroll GC, eds. The fungal community: its organization and role in the ecosystem. New York: Marcel Dekker. p 693–708

Bärlocher F., 1982 Conidium production from leaves and needles in four streams. Can J Bot 60:1487-1494

———, ed 1992 The ecology of aquatic hyphomycetes. Berlin: Springer-Verlag. 225 p

———. 2000 Water-borne conidia of aquatic hyphomycetes: seasonal and yearly patterns in Catamaran Brook, New Brunswick, Canada. Can J Bot 78:157-167

———, Graça MAS., 2002 Exotic riparian vegetation lowers fungal diversity but not leaf decomposition in Portuguese streams. Freshw Biol 47:1123-1135

———, Kendrick B., 1981 Role of aquatic hyphomycetes in the trophic structure of streams. In: Wicklow DT, Carroll GC, eds. The fungal community: its organization and role in the ecosystem. New York: Marcel Dekker. p 743–760

———, Rosset J., 1981 Aquatic hyphomycete spora of two Black Forest and two Swiss Jura streams. Trans Br Mycol Soc 76:479-483

Carpenter SR, Frost TM, Heisey D, Kratz TK., 1989 Randomized intervention analysis and the interpretation of whole-ecosystem experiments. Ecology 70:1142-1152

Cuffney TF, Wallace JB, Lugthart GJ., 1990 Experimental evidence quantifying the role of benthic invertebrates in organic matter dynamics of headwater streams. Freshw Biol 23:281-299

Findlay SE, Arsuffi TL., 1989 Microbial growth and detritus transformations during decomposition of leaf litter in a stream. Freshw Biol 21:261-269

Gönczöl J, Révay Á., 1998 Aquatic hyphomycetes in a tributary of the Morgó stream, Börzsöny Mts., NE Hungary. Studia Bot Hung 29:5-16

———, ———. 1999 Studies on the aquatic Hyphomycetes of the Morgó stream, Hungary. II. Seasonal periodicity of conidial populations. Arch Hydrobiol 144:495-508

Grattan RM, Suberkropp K., 2001 Effects of nutrient enrichment on yellow poplar leaf decomposition and fungal activity in streams. J N Am Benthol Soc 20:33-43

Gulis V, Suberkropp K., 2003a Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123-134

———, ———. 2003b Effect of inorganic nutrients on relative contributions of fungi and bacteria to carbon flow from submerged decomposing leaf litter. Microb Ecol 45:11-19[Medline]

———, ———. 2003c Interactions between stream fungi and bacteria associated with decomposing leaf litter at different levels of nutrient availability. Aquat Microb Ecol 30:149-157

Iqbal SH, Webster J., 1973 Aquatic hyphomycete spora of the River Exe and its tributaries. Trans Br Mycol Soc 61:331-346

Krebs CJ., 1989 Ecological methodology. New York: Harper and Row Publishers. 654 p

Magurran AE., 1988 Ecological diversity and its measurement. Princeton: Princeton University Press. 179 p

Murtaugh PA., 2002 On rejection rates of paired intervention analysis. Ecology 83:1752-1761

Shearer CA, Webster J., 1985a Aquatic hyphomycete communities in the River Teign. I. Longitudinal distribution patterns. Trans Br Mycol Soc 84:489-501

———, ———. 1985b Aquatic hyphomycete communities in the River Teign. II. Temporal distribution patterns. Trans Br Mycol Soc 84:503-507

Sridhar KR, Bärlocher F., 1993 Aquatic hyphomycetes on leaf litter in and near a stream in Nova Scotia, Canada. Mycol Res 97:1530-1535

———, ———. 2000 Initial colonization, nutrient supply, and fungal activity on leaves decaying in streams. Appl Environ Microbiol 66:1114-1119[Abstract/Free Full Text]

Suberkropp K., 1991 Relationships between growth and sporulation of aquatic hyphomycetes on decomposing leaf litter. Mycol Res 95:843-850

———. 1995 The influence of nutrients on fungal growth, productivity, and sporulation during leaf breakdown in streams. Can J Bot 73: (Suppl. 1) S1361-S1369

———. 1997 Annual production of leaf-decaying fungi in a woodland stream. Freshw Biol 38:169-178

———. 1998 Effect of dissolved nutrients on two aquatic hyphomycetes growing on leaf litter. Mycol Res 102:998-1002

———, Chauvet E., 1995 Regulation of leaf breakdown by fungi in streams: influences of water chemistry. Ecology 76:1433-1445

———, Klug MJ., 1976 Fungi and bacteria associated with leaves during processing in a woodland stream. Ecology 57:707-719

———, Wallace JB., 1992 Aquatic hyphomycetes in insecticide-treated and untreated streams. J N Am Benthol Soc 11:165-171

Wallace JB, Eggert SL, Meyer JD, Webster JR., 1999 Effects of resource limitation on a detrital-based ecosystem. Ecol Monogr 69:409-442

Webster J, Descals E., 1981 Morphology, distribution, and ecology of conidial fungi in freshwater habitats. In: Cole GT, Kendrick B, eds. Biology of conidial fungi. Vol. 1. New York: Academic Press. p 295–355

Weyers HS, Suberkropp K., 1996 Fungal and bacterial production during the breakdown of yellow poplar leaves in two streams. J N Am Benthol Soc 15:408-420




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