]. N. Am. Benthol. Soc., 1992, 11(2):16S by The North American Benthological Society
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1 [Volume 11 Bedrock outcrop A B P i, C = Coleoptera thornburghae, Optioservus >., Anchytarsus bicolor. lymphomyiidae, Ormosia j, nr. Pedicia, Pilaria spp., ]. N. Am. Benthol. Soc., 199, 11():16S by The North American Benthological Society Aquatic hyphomycetes in insecticide-treated and untreated streams KELLER SUBERKROPP Department of Biology, Box 87344, University of Alabama, Tuscaloosa, Alabama USA ]. BRUCE WALLACE Department of Entomology, University of Georgia, Athens, Georgia 36 USA Abstract. We compared the aquatic hyphomycete assemblage in a small headwater stream, where both shredder abundances and production had been dramatically reduced by the insecticide methoxychlor, with the aquatic hyphomycete assemblages in two reference streams containing high abundances of insect shredders. Concentrations of conidia being transported in the water of the treated stream were higher than those in the reference streams during much of the year (8 of 13 samples taken every 4 wk). The species composition (both number of species and the percent each contributed to the total) of conidia in transport was similar among the three streams. Aquatic hyphomycete assemblages on maple leaves colonized at 4-wk intervals over an annual cycle exhibited a similar pattern in that fungi sporulated at higher frequencies in the treated stream than in the reference streams, but the fungal species composition was similar in the three streams. Key words: aquatic hyphomycetes, shredders, streams, methoxychlor, leaf litter, fungi. Studies of the interactions between leafshredding invertebrates and fungi colonizing leaves in streams have concentrated on how fungal species composition, biomass, and activity affect the feeding of shredders (Barlocher 1985, Suberkropp 199), but have paid little attention to the effects that shredder feeding might have on the fungal assemblages growing on leaves. Barlocher (198, 198) used litter bags with different mesh sizes to compare aquatic hyphomycete assemblages occurring on litter protected from and exposed to shredders. Aquatic hyphomycete assemblages on litter exposed to shredders (i.e., in coarse-meshed bags) produced fewer conidia and had lower species richness than those protected from shredders (in fine-meshed bags). Shredder feeding affected total production of conidia by (1) reducing mass-specific rates of sporulation, and () increasing litter breakdown rates which allowed less time for sporulation to occur (Barlocher 198). Shredder feeding lowered fungal species richness primarily by eliminating rare species that occur late on litter protected from shredder feeding (Barlocher 198). Our study was carried out as part of a larger investigation examining the roles of invertebrates in leaf litter processing. Our primary objective was to use a whole-stream manipulation 165 to examine the effects of shredders on aquatic hyphomycete assemblages. We compared the aquatic hyphomycetes occurring in a headwater stream in which shredder densities had been experimentally reduced by seasonal treatment with the insecticide methoxychlor with those in two reference streams that contained high shredder densities. During the final year of a 3-yr insecticide treatment, we assessed aquatic hyphomycete assemblages in the three streams by determining (1) the concentrations and species composition of aquatic hyphomycete conidia in the water and () the frequencies of aquatic hyphomycetes sporulating on maple leaves placed in each stream at 4-wk intervals. Methods The three study streams drain Catchments 53, 54, and 55 in the Coweeta Hydrologic Laboratory (US Forest Service) in southwestern North Carolina. These streams are Ist-order, headwater streams, which are heavily shaded by mixed oak-hickory forest with a dense understory of rhododendron. All streams have similar catchment areas, annual discharges, and thermal regimes. Dissolved nutrient concentrations are very low (NO 3 -N concentrations <5 ftg/l, PO t -P concentrations < 5 ;ag/l; J. B. Wallace
2 166 K. SUBERKROPP AND J. B. WALLACE [Volume ] and W. T. Swank, Coweeta Hydrologic Laboratory, unpublished data). The streams have been described in more detail by Cuffney and Wallace (1988), Cuffney et al. (199) and Wallace et al. (1991b). From December 1985 through October 1988, C 54 received quarterly applications of methoxychlor. Seasonal treatments of C 54 with methoxychlor were accomplished by spraying methoxychlor at the rate of 1 mg/l (based on discharge measured at the flume on each date) for 4 h. Maximum concentration of methoxychlor in stream water, however, reached only 14 ftg/l and dropped to less than jig/l within 31 h of termination of the treatment (Wallace et al. 1989). After the first two applications, sediments had concentrations ranging from.38 to 11.7 fig methoxychlor per gram dry weight. This treatment resulted in massive insect drift and a drastic reduction in the benthic insect community. During the treatment period, few shredders were detected in leaf packs or associated with litter in this stream. C 53 had received treatment with methoxychlor for 1 yr in 198, and had recovered to pretreatment levels of shredder biomass, leaf-processing rates, and FPOM production by 198 (Wallace et al. 1986). It served as a reference stream, together with C 55 which had never been treated with methoxychlor. Concentrations of aquatic hyphomycete conidia in transport were measured at a flume at the bottom of each catchment by filtering.5-1.-l aliquots of water through membrane filters (5-fim pore size). Filters were fixed and stained with.1% trypan blue in lactic acid (Iqbal and Webster 1973). In the laboratory, 1 fields of each filter were examined microscopically, and the number and species composition of the conidia determined. Three filters from each stream were prepared on four dates during 1987 and at approximately 4-wk intervals from April 1988 through March Since only one stream (C 54) was treated with methoxychlor in this study, replication was lacking and effects of the treatment could not be analyzed with inferential statistics. Standard errors were calculated using data from the three filters taken from each stream at each date to indicate variation among these subsamples. Similarity of species occurring in different streams was examined with percentage similarity (P) calculated as P = minimum (p,;, p i ) where p n is the percentage of species i in stream 1 and pa is the percentage of species i in stream. Percentages were summed over all species (Krebs 1989). From April 1988 through March 1989, mesh bags (5x5 mm mesh) containing 1-15 g airdried autumn-shed red maple (Acer rubrum) leaves were placed in each stream at 4-wk intervals, with the exception of the period from 5 June-3 July, when no samples were taken. These leaves were used as baits (sensu Shearer and Lane 1983) to assess the assemblages of aquatic hyphomycetes colonizing a particular type of leaf throughout the year in each stream. Following exposure in each stream for 4 wk, disks (.7 cm diameter) were cut from the leaves from one litter bag from each stream, incubated for 1 d in stream water, and fixed in lactophenol. Later, disks were stained with trypan blue in lactophenol and the surfaces of 1 disks from each sample were scanned for the presence of sporulating aquatic hyphomycetes (Suberkropp 1984). The percentage of disks on which conidiophores of a species was observed producing conidia was calculated as the frequency of occurrence of that species. The density of conidiophores of each species on each leaf disk was also estimated (1 = low density: one to few conidiophores on one portion of the disk; = medium density: conidiophores observed on several parts of the disk; 3 = high density: conidiophores observed over most of the disk surface; Suberkropp 1984). Results Concentrations of aquatic hyphomycete conidia in transport in C 54, the treated stream, were 3-5 times higher than those in the reference streams from April-June 1988 and times higher during July, September, November, and December 1988 (Fig. 1). At other sampling dates, concentrations of conidia in the treated stream were similar to one or both of the reference streams. Concentrations of conidia in all three streams exhibited small peaks in January Overall, the species composition and percentages of aquatic hyphomycete conidia in transport were similar in all three streams (Table 1). Percent similarities calculated from these data averaged over the entire year suggest that the spora in the treated stream, C 54, were more en -D cco enu o CO TD "c OO 3! FIG. 1. nidia in I two refer resents ft 4-wk inte May, 5 J and 1 D in similar t were to spora in other (P for each out mo< in the t to C 55 major sj sented, stream sigmoic tified o: unideni /un long;, botto of T. st change: streams of A. te of the s several general 54 and the tre; sistentl in at le
3 199] FUNGI IN AN INSECTICIDE-TREATED STREAM 167 a) en u o \ cd c O o C 53 C 54 C 55 A M J J A S O N D J F M FIG. 1. Concentrations of aquatic hyphomycete conidia in transport in the treated stream (C 54) and two reference streams (C 53 and C 55). Each bar represents the mean +1 SE of triplicate filters taken at 4-wk intervals. Sample dates were 4 Apr, 3 Apr, 8 May, 5 Jun, 3 Jul, 18 Aug, 15 Sep, 15 Oct, 1 Nov, and 1 Dec in 1988, and 14 Jan, 11 Feb, and 1 Mar in similar to the spora in C 55 (P = 83%) than they were to the spora in C 53 (P = 71%) or than the spora in the two reference streams were to each other (P = 7%). Percent similarities calculated for each sample date also suggest that throughout most of the year, the species composition in the treated stream (C 54) was more similar to C 55 than either was to C 53. Four of the major species (cf. Table 1) in transport are presented as percent of the total conidia in each stream on each sample date in Figure. Most sigmoid conidia could not be positively identified on filters. However, the majority of the unidentified sigmoid conidia that were 6-1 /tm long appeared to be Flagellospora curvula (Fig., bottom panel). These conidia, as well as those of T. septatus, exhibited pronounced seasonal changes in all three streams. Differences among streams are also evident. For example/ conidia of A. tetradadia constituted a larger percentage of the spora in C 53 and C 54 than in C 55 on several sample dates, and conidia of T. septatus generally occurred at higher percentages in C 54 and C 55 than in C 53. Conidia of species in the treated stream (C 54) did not exhibit consistently higher or lower percentages than found in at least one of the reference streams, particularly during the time when concentrations of conidia in the treated stream were much higher (April-July, Fig. 1) than those in the reference streams. However, during August and September, percentages of conidia of T. septatus were higher, and during January and February, percentages of sigmoid conidia were lower in C 54 than in both reference streams (Fig. ). Frequencies of sporulation by aquatic hyphomycetes on maple leaves were generally low, but frequencies in the treated stream were higher than those in the reference streams (Fig. 3). This is especially evident for the two dominant species, Articulospora tetradadia and Alatospora acuminata. Composition of species colonizing maple leaves did not differ greatly among the streams. The species of Triscelophorus seen sporulating on leaves produced much smaller conidia than those of T. septatus, a major species of the conidia in transport, and was tentatively identified as Triscelophorus konajensis Sridhar & Kaveriappa. The densities of conidiophores of aquatic hyphomycetes were extremely low on leaves from all streams. In 9% of the obser- C3 C 53 ffl C 54 I C 55 A. tetradadia A M J J A S O N D J F FIG.. Articulospora tetradadia, Alatospora acuminata, Triscelophorus septatus, and sigmoid (6-1 um) conidia as percent of the total conidia in transport in the treated stream (C 54) and two reference streams (C 53 and C 55) at each sample date. The sigmoid conidia are thought to be primarily Flagellospora curvula. Sample dates correspond to those in Figure 1.
4 168 K. SUBERKROPP AND J. B. WALLACE [Volume ] TABLE 1. Average species composition of aquatic hyphomycete conidia in transport as percent of total in the treated stream (C 54) and two reference streams (C 53 and 55). Fungal species C 53 C 54 C 55 Alatospora acuminata Ingold A. flagellata (Gonczol) Marvanova 1..5 Anguillospora filiformis Greathead Articulospora tetracladia Ingold Casaresia sphagnorum Fragoso Clavariopsis aquatica de Wild Clavatospora longibrachiata (Ingold) Marvanova & Nilsson...5 Culicidospora gravida Petersen.5.3 Geniculospora inflata (Ingold) Nilsson ex Marvanova & Nilsson.7.3 Heliscus lugdunensis Sacc. & Therry Lemonniera aquatica de Wild Lemonniera sp..5.. Lunulospora curoula Ingold Mycocentrospora sp...3 Tetrabrunneospora ellissii Dyko Tetrachaetum elegans Ingold Tetracladium setigemm (Grove) Ingold Tricladium chaetocladium Ingold Tripospermum sp..5.4 Triscelophorus septatus Wolfe Triscelophorus spp Unidentified Sigmoid (<6jtm long) Sigmoid (6-1 jim) Sigmoid (> 1 MHI) Tetraradiate Triradiate Tetraradiate Al vations of conidiophores on leaf disks from ref- ing on other environmental conditions (Hoderence streams, densities were estimated to be kinson 1976). Sridhar and Kaveriappa (1986) low (density = 1, see Methods); in the remain- found that 14 species of aquatic hyphomycetes der, they were medium (=). In 73% of the ob- growing on leaf litter sporulated in the presservations of conidiophores on leaf disks from ence of 5 mg/l of the insecticide benzene hexathe treated stream, densities were low (=1); in chloride, but were differentially inhibited by 4%, they were medium (=); and in 3%, they higher concentrations. Given the brief appliwere high (=3)., cation periods and the low concentrations of methoxychlor (<15 Mg/L) used in the present Discussion study, we do not think that the observed changes in the aquatic hyphomycete assembleges were The effects of methoxychlor on aquatic hy- due to direct effects of methoxychlor. We conphomycetes have not been determined. How- elude that the stimulation of the aquatic hyever, another insecticide, DDT, which is struc- phomycetes that we observed in the treated turally similar to methoxychlor, has been found stream is indirect and primarily due to the abto have no effect on the growth of several aquat- sence of shredders and their feeding activity, ic hyphomycete species at concentrations less Insecticide treatment caused massive declines than mg/l (Dalton et al. 197). At higher in shredders colonizing litterbags in the treated concentrations, DDT can have a variety of ef- stream, whereas the two reference streams confects (both stimulatory and inhibitory) depend- tained high densities of shredders (Cuffney et al. 199 nual sh 93% (' treatme shredde (3.34 to Wallace a sepan in each AFDM/ lows: A andc: 15.7, C March =.4 of Geo shredd much 1 than ir highes Januar The the tre of litte the tw Wallac ment I the tre in the Based ter in concei shouk andth In the sporu (Barlo greate in the strean (8ofl prese: year ( tions alway It is j of lee trapp untre late charg streai treatt
5 [Volume 11 sport as percent of total in C C icntal conditions (Hodand Kaveriappa (1986) f aquatic hyphomycetes sporulated in the presisecticide benzene hexa- 'erentially inhibited by Given the brief appli- low concentrations of ;/L) used in the present iat the observed changes ycete assemblages were methoxychlor. We contion of the aquatic hybserved in the treated >rimarily due to the abtheir feeding activity, caused massive declines litterbags in the treated y reference streams conf shredders (Cuffney et 199] FUNGI IN AN INSECTICIDE-TREATED STREAM 169 al. 199). Based on benthic samples, average annual shredder abundances in C 54 declined by 93% (67 to 149 individuals/m ) from Yr 1 (pretreatment) to Yr (first treatment year), and shredder production declined by more than 87% (3.34 to.43 g AFDM nr yr-'; Lugthart and Wallace 199). During the period of our study, a separate decomposition study was conducted in each stream. Average shredder biomass (mg AFDM/bag) in red maple leaf bags was as follows: April-June 1988: C 53 = 17.4, C 54 =.6, and C 55 = 16.4; July-November 1988: C 53 = 15.7, C 54 =.3, and C 55 = 17.6; and January- March 1989: C 53 = 3.7, C 54 = 4.1, and C 55 =.4 (K. Chung and J. B. Wallace, University of Georgia, unpublished data). Consequently, shredders were present throughout the year at much higher biomass in the reference streams than in the treated stream. In all streams, the highest biomass of shredders occurred during January-March. The lack of shredders and their feeding in the treated stream led to lower breakdown rates of litter and production of FPOM compared with the two reference streams (Cuffney et al. 199, Wallace et al. 1991b). By the third year of treatment (1988), the concentration of leaf litter in the treated stream was more than double that in the reference streams (Wallace et al. 1991a). Based on the effects of shredder feeding on litter in leaf packs (Barlocher 198), the greater concentrations of leaf litter in the treated stream should provide more substrate for fungal growth and therefore allow more conidium production. In the absence of shredder feeding, rates of sporulation per g leaf tissue may also increase (Barlocher 198). These effects should lead to greater concentrations of conidia in transport in the treated stream than in the two reference streams. This was the case for most of the year (8 of 13 monthly samples). Since shredders were present in the reference streams throughout the year (see above), it is not clear why concentrations of conidia in the treated stream were not always higher than those in the reference stream. It is possible that the increased accumulations of leaf litter in the treated stream effectively trapped and retained more conidia than in the untreated streams. We also note that during the late summer and autumn of 1988 when discharge and concentrations of conidia in all streams were low, differences between the treated and reference stream were small (Fig. Frequency (^) 1UU CD C 53 C 54 C 55 - A. tetraciaaia 4 r» A. acuminata n n. x n tt VkrikM & m T. elegans ci * r rm ft nm 5 I Triscelophorus sp. x 3 r " «A M J J A S O N D J F M FIG. 3. Frequencies of sporulation by the dominant aquatic hyphomycete species (Articulosporu tetrucladia, Alatospora acuminata, Tetrachaetum elegans, and Triscelophorus sp.) on maple leaves that had been colonized in the treated stream (C 54) or in one of the two reference streams (C 53 and C 55) for 4 wk. Litter bags were removed from streams every 4 wk starting on 3 Apr 1988 with the exception of 3 Jul 1988 when no data (x) were obtained. 1). However, discharge and concentrations of conidia were not significantly correlated over the entire annual cycle in any of the streams. We found that the frequencies and densities of aquatic hyphomycete conidiophores on maple leaves were higher in the treated stream than in the two reference streams. This may reflect greater rates of sporulation in the absence of invertebrate activity (Barlocher 198) rather than higher fungal biomass or activity since respiration rates (per unit mass) of microorganisms associated with leaf litter, wood, and sediments have not been found to be significantly different in the three streams (Cuffney et al. 199). In general, annual maximum concentrations (1-3/L) of aquatic hyphomycete conidia in the three streams examined in this study were at the low end of the range (8-, conidia/ L) that has been found in other woodland streams (Iqbal and Webster 1973, Wood-Eggenschwiler and Barlocher 1983, Shearer and Webster 1985, Thomas et al. 1989, Suberkropp 1991). In addition, seasonal patterns in concentrations of conidia differed from patterns that have been noted for other temperate streams in that maximum concentrations in the Coweeta streams
6 17 K. SUBERKROPP AND J. B. WALLACE [Volume 11 occurred in late winter-spring (January-April) rather than during the period of autumn leaf inputs (October-December; Iqbal and Webster 1973, Barlocher and Rosset 1981). Frequencies and densities of sporulating structures on leaves incubated in the Coweeta streams were also low in comparison with other streams (e.g., Suberkropp 1984). The reason for these differences is unknown, but all streams examined in this study had extremely low concentrations of nutrients in comparison with most streams in which aquatic hyphomycetes have previously been studied. Nutrient concentrations have been suggested to affect rates of sporulation by aquatic hyphomycetes (Suberkropp 1991), and the low nutrient concentrations in these Coweeta streams may be responsible for the low levels of aquatic hyphomycetes both on leaves and as conidia in the water. Barlocher (198) noted higher species richness in aquatic hyphomycete assemblages on leaf litter that was protected from shredder feeding and attributed this to the elimination of late, rare species by shredders. We did not find an increase in the species richness of aquatic hyphomycetes in the treated stream as a result of the elimination of shredders. This may be due to the high concentrations of leaf litter in all streams, even those with shredders. If leaves, particularly those that are processed slowly (such as rhododendron), persist for long periods of time, they may provide refugia for the late, rare species that never have time to appear in shortterm studies of individual leaf packs (Barlocher 198). A number of laboratory studies have demonstrated that shredders have the capability to forage selectively for different fungal species (Barlocher 1985, Suberkropp 199). For trichopteran shredders, the basic units of food selection are patches of fungi within a leaf (Arsuffi and Suberkropp 1985). Although our study did not examine aquatic hyphomycete assemblages at this scale, we would expect the relative abundances of certain aquatic hyphomycete species in the treated stream to differ from those in the reference streams if selective feeding by shredders was widespread. For example, if shredders preferentially fed on certain fungal species, we would expect their biomass to be reduced leading to lower conidium production by these species in the reference streams than in the treated stream. Consequently, conidia of these species should be present as lower percentages of the total in the reference streams than in the treated stream. Conversely, if certain fungal species were unpalatable to shredders, the percentages of their conidia should be higher in the reference streams than in the treated stream. Since fungal species (cf. Fig. ) generally did not exhibit such patterns (two exceptions noted in Results), and the percent similarities for species composition and abundances of conidia in transport did not suggest large differences between the treated and reference streams (Table 1), we found little evidence to suggest that selective foraging had a large enough impact to alter the fungal species composition in these streams. Further research examining this question at a finer scale (e.g., within or between leaves) is needed to determine if selective feeding by shredders can have other effects on the fungi colonizing leaves in streams. Acknowledgements We thank Alice A. Gibson, Beth Goldowitz, Keun Chung, and Dr. G. }. Lugthart for technical assistance. Drs. T. L. Arsuffi, M. E. Gurtz, R. J. Mackay, and an anonymous reviewer provided constructive comments on an earlier version of the paper. This research was supported by a grant (BSR ) from the National Science Foundation. Literature Cited ARSUFFI, T. L., AND K. SUBERKROPP Selective feeding by caddisfly (Trichoptera) detritivores on leaves with fungal colonized patches. Oikos 45: BARLOCHER, F Leaf-eating invertebrates as competitors of aquatic hyphomycetes. Oecologia 47: BARLOCHER, F Conidium production from leaves and needles in four streams. Canadian Journal of Botany 6: BARLOCHER, F The role of fungi in the nutrition of stream invertebrates. Botanical Journal of the Linnean Society 91: BARLOCHER, F., AND J. ROSSET Aquatic hyphomycete spora of two Black Forest and two Swiss Jura streams. Transactions of the British Mycological Society 76: CUFFNEY, T. F., AND J. B. WALLACE Particulate organic matter export from headwater streams: discrete versus continuous measurement. Cana-
7 199] FUNGI IN AN INSECTICIDE-TREATED STREAM 171 dian Journal of Fisheries and Aquatic Sciences 45:1-16. CUFFNEY, T. F., J. B. WALLACE, AND G. J. LUGTHART Experimental evidence quantifying the role of benthic invertebrates in organic matter dynamics of headwater streams. Freshwater Biology 3: DALTON, S. A., M. HODKINSON, AND K. A. SMITH Interactions between DDT and river fungi. I. Effects of p,p'-ddt on the growth of aquatic hyphomycetes. Applied Microbiology : HODKINSON, M Interactions between aquatic fungi and DDT. Pages in E. B. G. Jones (editor). Recent advances in aquatic mycology. John Wiley & Sons, Inc., New York. IQBAL, S., AND J. WEBSTER Aquatic hyphomycete spora of the River Exe and its tributaries. Transactions of the British Mycological Society 61: KREBS, C. J Ecological methodology. Harper & Row, New York. LUGTHART, G. J., AND J. B. WALLACE Effects of disturbance on benthic functional structure and production in mountain streams. Journal of the North American Benthological Society 11: SHEARER, C. A., AND L. C. LANE Comparison of three techniques for the study of aquatic hyphomycete communities. Mycologia 75: SHEARER, C. A., AND J. WEBSTER Aquatic hyphomycete communities in the River Teign. I. Longitudinal distribution patterns. Transactions of the British Mycological Society 84: SRIDHAR, K. R., AND K. M. KAVERIAPPA Effect of pesticides on sporulation and spore germination of water-borne hyphomycetes. Pages in R. C. Dalella, M. N. Madhyastha, and J. Mohan (editors). Environmental biology, coastal ecosystem. Academy of Environmental Biology, India. SUBERKROPP, K Effect of temperature on seasonal occurrence of aquatic hyphomycetes. Transactions of the British Mycological Society 8:53-6. SUBERKROPP, K Relationships between growth and sporulation of aquatic hyphomycetes on decomposing leaf litter. Mycological Research 95: SUBERKROPP, K Interactions with invertebrates. Pages in F. Barlocher (editor). The ecology of aquatic hyphomycetes. Springer, Heidelberg (in press). THOMAS, K., G. A. CHILVERS, AND R. H. NORRIS Seasonal occurrence of conidia of aquatic hyphomycetes (Fungi) in Lees Creek, Australian Capital Territory. Australian Journal of Marine and Freshwater Research 4:11-3. WALLACE, J. B., T. F. CUFFNEY, B. S. GOLDOWITZ, K. CHUNG, AND G. J. LUGTHART. 199 la. Long-term studies of the influence of invertebrate manipulations and drought on participate organic matter export from headwater streams. Verhandlungen der Internationalen Vereinigung fur Theoretische und Angewandte Limnologie 4: WALLACE, J. B., T. F. CUFFNEY, J. R. WEBSTER, G. J. LUGTHART, K. CHUNG, AND B. S. GOLDOWITZ. 1991b. Export of fine organic particles from headwater streams: effects of season, extreme discharges, and invertebrate manipulation. Limnology and Oceanography 36:67-68.! WALLACE, J. B., G. J. LUGTHART, T. F. CUFFNEY, AND G. A. SCHURR The impact of repeated insecticidal treatments on drift and benthos of a headwater stream. Hydrobiologia 179: WALLACE, J. B., D. S. VOGEL, AND T. F. CUFFNEY Recovery of a headwater stream from insecticideinduced community disturbance. Journal of the North American Benthological Society 5: WOOD-EGGENSCHWIUER, S., AND F. BARLOCHER Aquatic hyphomycetes in sixteen streams in France, Germany and Switzerland. Transactions of the British Mycological Society 81: Received: 1 November 1991 Accepted: February 199
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