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Comparison of usefulness of three types of artificial substrata (glass, wood and plastic) when studying settlement patterns of periphyton in lakes of different trophic status
Journal of Microbiological Methods 45 Ž2001. 167–170 www.elsevier.comrlocaterjmicmeth
Comparison of usefulness of three types of artificial substrata žglass, wood and plastic/ when studying settlement patterns of periphyton in lakes of different trophic status Roman A. Danilov ) , N.G.A. Ekelund Department of Natural and EnÕironmental Sciences, Mid Sweden UniÕersity, 871 88 Harnosand, Sweden ¨ ¨ Received 16 October 2000; received in revised form 20 October 2000; accepted 22 February 2001
Abstract Usefulness of three types of artificial substrata Žglass, wood and plastic. was tested when studying settlement patterns of periphyton in lakes of different trophic status. Strictly eu-, meso- and oligotrophic lakes in central Sweden were chosen as objects of the study. Glass slides, glass tubes, pieces of plastic ŽPVC. and pieces of wood of similar dimensions were placed for 9 weeks in July–August vertically 3 cm above bottom at a total depth of ca. 30 cm. Substrata were located at well-illuminated places without any other submerged objects Žlike macrophytes and stones., which could potentially affect colonisation patterns by algae. Periphyton communities, which colonised both the glass tubes and the pieces of wood tested, were specific enough to enable a clear classification of the lakes studied in eu-, meso- and oligotrophic. Glass tubes turned out to be the most favourable substratum when investigating settlement patterns of periphyton in this study. Although also colonised by periphytic species, wood did not support the same diversity and abundance of species as glass did. No algae were detected on the plastics studied. The plastics were covered entirely by a slime layer of bacteria. It is discussed if the nature of plastics could have some inhibitory effects on algal growth or the slime layer itself may have prevented settlement of algal spores. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Artificial substrata; Periphyton; Trophic status
1. Introduction Periphytic algal communities considerably contribute to primary production in aquatic ecosystems. The sensitivity of periphyton to environmental factors and biologically active substances has been well documented, thus making periphyton a favourable bioassay object Že.g., Smolar et al., 1998; Genter and
) Corresponding author. Tel.: q46-611-86292; fax: q46-61186160. E-mail address: [email protected] ŽR.A. Danilov..
Lehman, 2000; Kinross et al., 2000.. Periphytic algae can also be successfully used for removal of excessive nutrients, metals and toxic substances, hence improving water quality ŽVymazal, 1988; Hill et al., 2000.. Therefore, a question of great interest is, which substrata are the most favourable for different periphytic taxa. Although questioned some decades ago, interactions between algae and substrata became evident ŽWetzel, 1983.. A lot of studies have been performed to compare the usefulness of different natural and artificial substrata for attached algae. However, as pointed out by Cattaneo and Amireault Ž1992., the results of the most com-
0167-7012r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 7 0 1 2 Ž 0 1 . 0 0 2 4 7 - 0
168
R.A. DaniloÕ, N.G.A. Ekelundr Journal of Microbiological Methods 45 (2001) 167–170
parative studies are contradictory. They conclude that Athis contradiction has two probable sources: authors evaluate their results differently in relation to the goals of their study, and the performance of substrata may depend on the environment studied and methods used.B Glass slides were used over decades and remained probably the most popular artificial substrata. Not seldom different plastics were applied during the recent decades. As natural substrata introduced stones are used in epilithon studies while wood seems to be underestimated Žfor review see Aloi, 1990; Cattaneo and Amireault, 1992.. Both the natures of a substratum and environmental factors Žwith nutrients playing a crucial role. define which taxa will colonise it ŽSmoot et al., 1998; Danilov and Ekelund, 2000.. The aims of this study were: Ž1. to investigate differences between periphyton algal communities colonising glass, plastic and wood substrates in lakes of different trophic status Žeu-, meso- and oligotrophic.; Ž2. to reveal which substratum would be preferable when estimating trophic conditions within lakes using periphyton as bioindicators.
tom at a total depth of ca. 30 cm. All substrata tested were cleaned with 99% ethanol prior to incubation. The substrata Žthree samples of each type. were located at well-illuminated places without any other submerged objects Žlike macrophytes and stones. which could potentially affect colonisation patterns by algae. Algal communities were sampled after 9 weeks of exposure in August 2000 and immediately examined in the laboratory without any fixation. The patches of the same size Ž1 cm2 . were scraped randomly from the surface of the substrata used and analysed for algal cells present. Three patches were scraped from each substratum to enable statistical significance of data. The frequency of each species present was determined according to relative units: 1 —occasional, 2—rare, 3—frequent, 4—dominant Že.g., Smolar et al., 1998; Danilov and Ekelund, 2000.. The lakes were compared using similarity index based on Euclidean distance algorithm and species presence–absence data in the computer package Minitab 13.0 ŽDanilov and Ekelund, 2000..
3. Results and discussion 2. Material and methods Trophic status of the lakes was defined according to total phosphorus concentration Ž Ptot ., where the lakes with Ptot less than 15 mg ly1 were considered as oligotrophic, between 15 and 25 mg ly1 as mesotrophic and above 25 mg ly1 as eutrophic, respectively. As study objects, five lakes with different trophic conditions were chosen: two eutrophic— Ž Ptot s 29 mg ly1 . and Sjalandssjon Kindborgstjarnen ¨ ¨ ¨ y1 Ž Ptot s 56 mg l ., one mesotrophic—Valasjon ¨ Ž Ptot s 18 mg ly 1 ., and two oligotrophic— Bastusjon ¨ Ž Ptot s 9 mg ly1 . and Haggsjon ¨ ¨ Ž Ptot s 11 mg ly1 .. All lakes were located at the same latitude Ž62854X N. in Vasternorrlands region of Swe¨ den. The data of Ptot were obtained using Autoanalyser ŽTechnicon Traacs 80. and kindly supplied by the County Administration, Harnosand. The criterion ¨ ¨ for the choice of the lakes studied was unambiguously definitive trophic conditions. Glass slides, glass tubes, pieces of plastic ŽPVC. and pieces of wood Žwillow and pine. of similar dimensions were placed vertically 3 cm above bot-
Periphyton assemblages on substrata tested were identical in the eutrophic lakes. The same was true for the oligotrophic lakes investigated. Thus, the results presented in Table 1 deal entirely with eu-, meso- and oligotrophic conditions without splitting them into individual lakes. Two species of Gomphonema ŽBacillariophyceae. were found while the distribution of Gomphonema oliÕaceum was entirely restricted to the eutrophic lakes ŽTable 1.. G. constrictum colonised the substrata used in the mesoand oligotrophic lakes. If present, the species of Gomphonema were found both on pieces of wood and glass tubes, although glass tubes seemed to be more preferable Žhigher abundance.. All identified species of Chlorophyceae belonged to multicellular algae. However, only Cladophora glomerata was found in the eutrophic lakes Žon the glass tubes but not on the pieces of wood. but in huge numbers. The highest abundance of Chlorophyceae Žfive species. was detected on the glass tubes under mesotrophic conditions. However, entirely Coleochaete pulÕinata could also colonise wood. In oligotrophic lakes,
R.A. DaniloÕ, N.G.A. Ekelundr Journal of Microbiological Methods 45 (2001) 167–170
169
Table 1 List of periphyton taxa found on different submerged substrata after 9 weeks exposure in lakes of different trophic status Species
Eutrophic Glass
Chlorophyceae C. glomerata ŽL.. Kutz. ¨ Col. pulÕinata Breb. ´ Mougeotia sp. Rhizoclonium hieroglyphicum ŽAg.. Kuetz. Rhizoclonium sp. Ulothrix tenerrima Kuetz. Bacillariophyceae G. constrictum Ehr. G. oliÕaceum Breb. ´
Mesotrophic Wood
Oligotrophic
Glass
Wood
1 2 3 1 4
1
1
1
Glass
Wood
3
1
2
1
4
2
1
relative high density of Mougeotia sp. population was observed on the glass tubes. The same algae were present on the pieces of wood but in considerably less numbers. The sensitivity of periphyton to nutrient level is evident, thus the differences in distribution of different algae species observed in our study are not surprising ŽRosemond, 1994; Smoot et al., 1998; Klug and Fisher, 2000.. The capacity of Cladophora sp. to reach nuisance levels in eutrophicated waters is well-documented ŽDodds and Gudder, 1992.. This fact explains the dominance of C. glomerata in the eutrophic lakes studied. Chlorophyceae were reported in the literature to dominate often periphyton communities in waters of both acid and alkali pH ŽRosemond, 1994; Meegan and Perry, 1996.. Keeping in mind that moderate nutrient levels would
provide the most favourable conditions for development of diverse algae species, the highest species abundance detected under mesotrophic conditions is not surprising. However, our results show that the nature of substratum can considerably affect patterns of colonisation by periphytic algae. No growth of algae was observed on the plastics used Žtherefore, not shown in Table 1.. The plastics were covered entirely by a slime layer of bacteria Žthis layer was not visible on the pieces of wood or glass tubes tested.. One possible explanation to this fact could be the nature of plastics thus having some inhibitory effects on algal growth ŽWetzel, 1983.. On the other hand, the slime layer itself may have prevented settlement of algal spores. This result is contradictory to those summarised by Cattaneo and Amireault Ž1992. where
Fig. 1. Resolution between lakes of different trophic level based on periphyton settlement patterns on artificial substrata: Ža. glass tubes; Žb. pieces of wood. O—oligotrophic, M—mesotrophic, E—eutrophic lakes.
170
R.A. DaniloÕ, N.G.A. Ekelundr Journal of Microbiological Methods 45 (2001) 167–170
plastics were considered to be favourable artificial substrata for periphyton studies. Glass tubes seemed to be the most favourable substratum for colonisation by periphytic algae. This result coincides well with those reported earlier by numerous authors in the literature Žfor review see Aloi, 1990.. However, while common in natural aquatic environments, wood as substratum does not seem to be tested properly ŽSladeckova, ` ` 1962; Aloi, 1990; Cattaneo and Amireault, 1992.. Thus, we made an attempt to fill this gap. As presented in Table 1, the pieces of wood tested did not turn out to be a favourable substrate in our study. However, this fact can eventually depend on the duration of experiments. Both short-duration and long-duration experiments were considered Ždepending on authors. as the most favourable in case of periphyton Že.g., Smoot et al., 1998; Kinross et al., 2000.. We believe that exposures less than 60 days could lead to erratic conclusions about settlement patterns of periphyton Že.g., Biggs, 1988.. Periphyton communities, which colonised both the glass tubes and the pieces of wood tested, were specific enough to enable a clear classification of the lakes studied in eu-, meso- and oligotrophic ŽFig. 1a,b.. The clustering algorithm applied was proven to be one of the most favourable when estimating trophic conditions in lakes based on natural periphytic communities ŽDanilov and Ekelund, 2000..
References Aloi, J.E., 1990. A critical review of recent freshwater periphyton field methods. Can. J. Fish. Aquat. Sci. 47, 656–670. Biggs, B.J.F., 1988. Artificial substrate exposure times for periphyton biomass estimate in rivers. N. Z. J. Mar. Freshwater Res. 22, 507–515. Cattaneo, A., Amireault, M.C., 1992. How artificial are artificial
substrata for periphyton? J. North Am. Benthol. Soc. 11, 244–256. Danilov, R.A., Ekelund, N.G.A., 2000. The use of epiphyton and epilithon data as a base for calculating ecological indices in monitoring of eutrophication in lakes in central Sweden. Sci. Total Environ. 248, 63–70. Dodds, W.K., Gudder, D.A., 1992. The ecology of Cladophora. J. Phycol. 28, 415–427. Genter, R.B., Lehman, R.M., 2000. Metal toxicity inferred from algal population density, heterotrophic substrate use and fatty acid profile in a small stream. Environ. Toxicol. Chem. 19, 869–878. Hill, B.H., Willingham, W.T., Parrish, L.P., McFarland, B.H., 2000. Periphyton community responses to elevated metal concentrations in a Rocky Mountain stream. Hydrobiologia 428, 161–169. Kinross, J.H., Read, P.A., Christofi, N., 2000. The influence of pH and aluminium on the growth of filamentous algae in artificial streams. Arch. Hydrobiol. 149, 67–86. Klug, J.L., Fisher, J.M., 2000. Factors influencing the growth of Mougeotia in experimentally acidified mesocosms. Can. J. Fish. Aquat. Sci. 57, 538–547. Meegan, S.K., Perry, S.A., 1996. Periphyton communities in headwater streams of different water chemistry in the central Appalachian Mountains. J. Freshwater Ecol. 11, 247–256. Rosemond, A.D., 1994. Multiple factors limit seasonal variation in periphyton in a forest stream. J. North Am. Benthol. Soc. 13, 333–344. Sladeckova, ` ` A., 1962. Limnological investigation methods for the periphyton ŽAaufwuchsB . community. Bot. Rev. 28, 286–350. Smolar, N., Vrhovsek, D., Kosi, G., 1998. Effects of low flow on periphyton in three different types of streams in Slovenia. In: Bretschko, G., Helesic, ˇ J. ŽEds.., Advances in River Bottom Ecology. Backhuys Publishers, Leiden, The Netherlands, pp. 107–116. Smoot, J.C., Langworthy, D.E., Levy, M., 1998. Periphyton growth on submerged artificial substrate as a predictor of phytoplankton response to nutrient enrichment. J. Microbiol. Methods 32, 11–19. Vymazal, J., 1988. The use of periphyton communities for nutrient removal from polluted streams. Hydrobiologia 166, 225– 237. Wetzel, R.G., 1983. Attached algal-substrata interactions: fact or myth, and when and how? In: Wetzel, R.G. ŽEd.., Periphyton of Freshwater Ecosystems. Dr. W. Junk Publishers, The Hague, pp. 207–215.
Comparison of usefulness of three types of artificial substrata žglass, wood and plastic/ when studying settlement patterns of periphyton in lakes of different trophic status Roman A. Danilov ) , N.G.A. Ekelund Department of Natural and EnÕironmental Sciences, Mid Sweden UniÕersity, 871 88 Harnosand, Sweden ¨ ¨ Received 16 October 2000; received in revised form 20 October 2000; accepted 22 February 2001
Abstract Usefulness of three types of artificial substrata Žglass, wood and plastic. was tested when studying settlement patterns of periphyton in lakes of different trophic status. Strictly eu-, meso- and oligotrophic lakes in central Sweden were chosen as objects of the study. Glass slides, glass tubes, pieces of plastic ŽPVC. and pieces of wood of similar dimensions were placed for 9 weeks in July–August vertically 3 cm above bottom at a total depth of ca. 30 cm. Substrata were located at well-illuminated places without any other submerged objects Žlike macrophytes and stones., which could potentially affect colonisation patterns by algae. Periphyton communities, which colonised both the glass tubes and the pieces of wood tested, were specific enough to enable a clear classification of the lakes studied in eu-, meso- and oligotrophic. Glass tubes turned out to be the most favourable substratum when investigating settlement patterns of periphyton in this study. Although also colonised by periphytic species, wood did not support the same diversity and abundance of species as glass did. No algae were detected on the plastics studied. The plastics were covered entirely by a slime layer of bacteria. It is discussed if the nature of plastics could have some inhibitory effects on algal growth or the slime layer itself may have prevented settlement of algal spores. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Artificial substrata; Periphyton; Trophic status
1. Introduction Periphytic algal communities considerably contribute to primary production in aquatic ecosystems. The sensitivity of periphyton to environmental factors and biologically active substances has been well documented, thus making periphyton a favourable bioassay object Že.g., Smolar et al., 1998; Genter and
) Corresponding author. Tel.: q46-611-86292; fax: q46-61186160. E-mail address: [email protected] ŽR.A. Danilov..
Lehman, 2000; Kinross et al., 2000.. Periphytic algae can also be successfully used for removal of excessive nutrients, metals and toxic substances, hence improving water quality ŽVymazal, 1988; Hill et al., 2000.. Therefore, a question of great interest is, which substrata are the most favourable for different periphytic taxa. Although questioned some decades ago, interactions between algae and substrata became evident ŽWetzel, 1983.. A lot of studies have been performed to compare the usefulness of different natural and artificial substrata for attached algae. However, as pointed out by Cattaneo and Amireault Ž1992., the results of the most com-
0167-7012r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 7 0 1 2 Ž 0 1 . 0 0 2 4 7 - 0
168
R.A. DaniloÕ, N.G.A. Ekelundr Journal of Microbiological Methods 45 (2001) 167–170
parative studies are contradictory. They conclude that Athis contradiction has two probable sources: authors evaluate their results differently in relation to the goals of their study, and the performance of substrata may depend on the environment studied and methods used.B Glass slides were used over decades and remained probably the most popular artificial substrata. Not seldom different plastics were applied during the recent decades. As natural substrata introduced stones are used in epilithon studies while wood seems to be underestimated Žfor review see Aloi, 1990; Cattaneo and Amireault, 1992.. Both the natures of a substratum and environmental factors Žwith nutrients playing a crucial role. define which taxa will colonise it ŽSmoot et al., 1998; Danilov and Ekelund, 2000.. The aims of this study were: Ž1. to investigate differences between periphyton algal communities colonising glass, plastic and wood substrates in lakes of different trophic status Žeu-, meso- and oligotrophic.; Ž2. to reveal which substratum would be preferable when estimating trophic conditions within lakes using periphyton as bioindicators.
tom at a total depth of ca. 30 cm. All substrata tested were cleaned with 99% ethanol prior to incubation. The substrata Žthree samples of each type. were located at well-illuminated places without any other submerged objects Žlike macrophytes and stones. which could potentially affect colonisation patterns by algae. Algal communities were sampled after 9 weeks of exposure in August 2000 and immediately examined in the laboratory without any fixation. The patches of the same size Ž1 cm2 . were scraped randomly from the surface of the substrata used and analysed for algal cells present. Three patches were scraped from each substratum to enable statistical significance of data. The frequency of each species present was determined according to relative units: 1 —occasional, 2—rare, 3—frequent, 4—dominant Že.g., Smolar et al., 1998; Danilov and Ekelund, 2000.. The lakes were compared using similarity index based on Euclidean distance algorithm and species presence–absence data in the computer package Minitab 13.0 ŽDanilov and Ekelund, 2000..
3. Results and discussion 2. Material and methods Trophic status of the lakes was defined according to total phosphorus concentration Ž Ptot ., where the lakes with Ptot less than 15 mg ly1 were considered as oligotrophic, between 15 and 25 mg ly1 as mesotrophic and above 25 mg ly1 as eutrophic, respectively. As study objects, five lakes with different trophic conditions were chosen: two eutrophic— Ž Ptot s 29 mg ly1 . and Sjalandssjon Kindborgstjarnen ¨ ¨ ¨ y1 Ž Ptot s 56 mg l ., one mesotrophic—Valasjon ¨ Ž Ptot s 18 mg ly 1 ., and two oligotrophic— Bastusjon ¨ Ž Ptot s 9 mg ly1 . and Haggsjon ¨ ¨ Ž Ptot s 11 mg ly1 .. All lakes were located at the same latitude Ž62854X N. in Vasternorrlands region of Swe¨ den. The data of Ptot were obtained using Autoanalyser ŽTechnicon Traacs 80. and kindly supplied by the County Administration, Harnosand. The criterion ¨ ¨ for the choice of the lakes studied was unambiguously definitive trophic conditions. Glass slides, glass tubes, pieces of plastic ŽPVC. and pieces of wood Žwillow and pine. of similar dimensions were placed vertically 3 cm above bot-
Periphyton assemblages on substrata tested were identical in the eutrophic lakes. The same was true for the oligotrophic lakes investigated. Thus, the results presented in Table 1 deal entirely with eu-, meso- and oligotrophic conditions without splitting them into individual lakes. Two species of Gomphonema ŽBacillariophyceae. were found while the distribution of Gomphonema oliÕaceum was entirely restricted to the eutrophic lakes ŽTable 1.. G. constrictum colonised the substrata used in the mesoand oligotrophic lakes. If present, the species of Gomphonema were found both on pieces of wood and glass tubes, although glass tubes seemed to be more preferable Žhigher abundance.. All identified species of Chlorophyceae belonged to multicellular algae. However, only Cladophora glomerata was found in the eutrophic lakes Žon the glass tubes but not on the pieces of wood. but in huge numbers. The highest abundance of Chlorophyceae Žfive species. was detected on the glass tubes under mesotrophic conditions. However, entirely Coleochaete pulÕinata could also colonise wood. In oligotrophic lakes,
R.A. DaniloÕ, N.G.A. Ekelundr Journal of Microbiological Methods 45 (2001) 167–170
169
Table 1 List of periphyton taxa found on different submerged substrata after 9 weeks exposure in lakes of different trophic status Species
Eutrophic Glass
Chlorophyceae C. glomerata ŽL.. Kutz. ¨ Col. pulÕinata Breb. ´ Mougeotia sp. Rhizoclonium hieroglyphicum ŽAg.. Kuetz. Rhizoclonium sp. Ulothrix tenerrima Kuetz. Bacillariophyceae G. constrictum Ehr. G. oliÕaceum Breb. ´
Mesotrophic Wood
Oligotrophic
Glass
Wood
1 2 3 1 4
1
1
1
Glass
Wood
3
1
2
1
4
2
1
relative high density of Mougeotia sp. population was observed on the glass tubes. The same algae were present on the pieces of wood but in considerably less numbers. The sensitivity of periphyton to nutrient level is evident, thus the differences in distribution of different algae species observed in our study are not surprising ŽRosemond, 1994; Smoot et al., 1998; Klug and Fisher, 2000.. The capacity of Cladophora sp. to reach nuisance levels in eutrophicated waters is well-documented ŽDodds and Gudder, 1992.. This fact explains the dominance of C. glomerata in the eutrophic lakes studied. Chlorophyceae were reported in the literature to dominate often periphyton communities in waters of both acid and alkali pH ŽRosemond, 1994; Meegan and Perry, 1996.. Keeping in mind that moderate nutrient levels would
provide the most favourable conditions for development of diverse algae species, the highest species abundance detected under mesotrophic conditions is not surprising. However, our results show that the nature of substratum can considerably affect patterns of colonisation by periphytic algae. No growth of algae was observed on the plastics used Žtherefore, not shown in Table 1.. The plastics were covered entirely by a slime layer of bacteria Žthis layer was not visible on the pieces of wood or glass tubes tested.. One possible explanation to this fact could be the nature of plastics thus having some inhibitory effects on algal growth ŽWetzel, 1983.. On the other hand, the slime layer itself may have prevented settlement of algal spores. This result is contradictory to those summarised by Cattaneo and Amireault Ž1992. where
Fig. 1. Resolution between lakes of different trophic level based on periphyton settlement patterns on artificial substrata: Ža. glass tubes; Žb. pieces of wood. O—oligotrophic, M—mesotrophic, E—eutrophic lakes.
170
R.A. DaniloÕ, N.G.A. Ekelundr Journal of Microbiological Methods 45 (2001) 167–170
plastics were considered to be favourable artificial substrata for periphyton studies. Glass tubes seemed to be the most favourable substratum for colonisation by periphytic algae. This result coincides well with those reported earlier by numerous authors in the literature Žfor review see Aloi, 1990.. However, while common in natural aquatic environments, wood as substratum does not seem to be tested properly ŽSladeckova, ` ` 1962; Aloi, 1990; Cattaneo and Amireault, 1992.. Thus, we made an attempt to fill this gap. As presented in Table 1, the pieces of wood tested did not turn out to be a favourable substrate in our study. However, this fact can eventually depend on the duration of experiments. Both short-duration and long-duration experiments were considered Ždepending on authors. as the most favourable in case of periphyton Že.g., Smoot et al., 1998; Kinross et al., 2000.. We believe that exposures less than 60 days could lead to erratic conclusions about settlement patterns of periphyton Že.g., Biggs, 1988.. Periphyton communities, which colonised both the glass tubes and the pieces of wood tested, were specific enough to enable a clear classification of the lakes studied in eu-, meso- and oligotrophic ŽFig. 1a,b.. The clustering algorithm applied was proven to be one of the most favourable when estimating trophic conditions in lakes based on natural periphytic communities ŽDanilov and Ekelund, 2000..
References Aloi, J.E., 1990. A critical review of recent freshwater periphyton field methods. Can. J. Fish. Aquat. Sci. 47, 656–670. Biggs, B.J.F., 1988. Artificial substrate exposure times for periphyton biomass estimate in rivers. N. Z. J. Mar. Freshwater Res. 22, 507–515. Cattaneo, A., Amireault, M.C., 1992. How artificial are artificial
substrata for periphyton? J. North Am. Benthol. Soc. 11, 244–256. Danilov, R.A., Ekelund, N.G.A., 2000. The use of epiphyton and epilithon data as a base for calculating ecological indices in monitoring of eutrophication in lakes in central Sweden. Sci. Total Environ. 248, 63–70. Dodds, W.K., Gudder, D.A., 1992. The ecology of Cladophora. J. Phycol. 28, 415–427. Genter, R.B., Lehman, R.M., 2000. Metal toxicity inferred from algal population density, heterotrophic substrate use and fatty acid profile in a small stream. Environ. Toxicol. Chem. 19, 869–878. Hill, B.H., Willingham, W.T., Parrish, L.P., McFarland, B.H., 2000. Periphyton community responses to elevated metal concentrations in a Rocky Mountain stream. Hydrobiologia 428, 161–169. Kinross, J.H., Read, P.A., Christofi, N., 2000. The influence of pH and aluminium on the growth of filamentous algae in artificial streams. Arch. Hydrobiol. 149, 67–86. Klug, J.L., Fisher, J.M., 2000. Factors influencing the growth of Mougeotia in experimentally acidified mesocosms. Can. J. Fish. Aquat. Sci. 57, 538–547. Meegan, S.K., Perry, S.A., 1996. Periphyton communities in headwater streams of different water chemistry in the central Appalachian Mountains. J. Freshwater Ecol. 11, 247–256. Rosemond, A.D., 1994. Multiple factors limit seasonal variation in periphyton in a forest stream. J. North Am. Benthol. Soc. 13, 333–344. Sladeckova, ` ` A., 1962. Limnological investigation methods for the periphyton ŽAaufwuchsB . community. Bot. Rev. 28, 286–350. Smolar, N., Vrhovsek, D., Kosi, G., 1998. Effects of low flow on periphyton in three different types of streams in Slovenia. In: Bretschko, G., Helesic, ˇ J. ŽEds.., Advances in River Bottom Ecology. Backhuys Publishers, Leiden, The Netherlands, pp. 107–116. Smoot, J.C., Langworthy, D.E., Levy, M., 1998. Periphyton growth on submerged artificial substrate as a predictor of phytoplankton response to nutrient enrichment. J. Microbiol. Methods 32, 11–19. Vymazal, J., 1988. The use of periphyton communities for nutrient removal from polluted streams. Hydrobiologia 166, 225– 237. Wetzel, R.G., 1983. Attached algal-substrata interactions: fact or myth, and when and how? In: Wetzel, R.G. ŽEd.., Periphyton of Freshwater Ecosystems. Dr. W. Junk Publishers, The Hague, pp. 207–215.