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The effects of barley straw (Hordeum vulgare) on the growth of freshwater algae
Bioresource Technology 96 (2005) 1788–1795
The effects of barley straw (Hordeum vulgare) on the growth of freshwater algae M.D. Ferrier
a,*
, B.R. Butler Sr. b, D.E. Terlizzi c, R.V. Lacouture
d
a
Department of Biology, Hood College, Frederick, MD 21701, United States Maryland Cooperative Extension, University of Maryland, 700 Agriculture Center, Westminster, MD 21157, United States University of Maryland Sea Grant Extension Program, Center of Marine Biotechnology, 701 E. Pratt St Baltimore, MD 21202, United States d Morgan State University Estuarine Research Center, 10545 Mackall Rd., St Leonard, MD 20685, United States b
c
Received 17 June 2003; received in revised form 14 January 2005; accepted 14 January 2005 Available online 7 March 2005
Abstract Bioassays were conducted to determine the efficacy of barley straw liquor in controlling algal growth of 12 freshwater species of algae representing three divisions. Barley straw liquor inhibited the growth of three nuisance algae common in freshwater: Synura petersenii, Dinobyron sp., and Microcystis aeruginosa. However, Selenastrum capricornutum, Spirogyra sp., Oscillatoria lutea var. contorta, and Navicula sp. had significantly increased growth in the presence of straw liquor. The growth of the remainder, Ulothrix fimbriata, Scenedesmus quadricauda, Chlorella vulgaris, Anabaena flos-aquae, and Synedra sp. showed no significant difference from controls. In a related field study, we treated four of six ponds with barley straw and monitored their chlorophyll a levels for one growing season. While phytoplankton populations in all ponds decreased in midsummer, the phytoplankton biomass in treated ponds did not differ significantly from that of control ponds, suggesting that the application of barley straw had no effect on algal growth in these systems. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Algicide; Algae control; Barley straw; Inhibition; Stimulation
1. Introduction Various forms of unicellular, filamentous, and colonial freshwater algae pose management problems in ponds, lakes, and reservoirs. Algae may interfere with pond uses or lead to environmental problems both directly as a consequence of excessive algal biomass and indirectly due to the algicide treatments used in their control. Filamentous algae clog pumps, screens, and emitters in agricultural irrigation systems. Many algal forms create off-flavors in potable water (Barrett et al., 1996). These unpleasant tastes and odors reduce the *
Corresponding author. Tel.: +1 301 696 3660; fax: +1 301 696 3667. E-mail address: [email protected] (M.D. Ferrier).
0960-8524/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2005.01.021
water intake of livestock and can render water from reservoirs unfit for human consumption (Gangstad, 1986; Vymazal, 1995). Remedial efforts to reduce the effects of algal blooms in reservoirs (e.g. filtering or chlorinating the water) have met with limited success since species such as Synura sp. and Anabaena sp. release oils during chlorination creating additional taste and odor problems (Vymazal, 1995). Mat-forming species also can hinder recreational fishing and swimming, and are considered unsightly by the general public (Newman, 1999). Anecdotal evidence of the ability of barley straw to control algal growth was observed as early as 1980 (Welch et al., 1990). Subsequent work demonstrated the addition of barley straw to a pond does not kill algae
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already present, but prevents the growth of new algal cells (Newman, 1999). This algistatic activity is produced on immersion and during decomposition of straw in a well-oxygenated environment. Decomposing barley straw has been shown to control a wide range of algae in freshwater systems including unicellular, filamentous and colonial forms (Gibson et al., 1990; Martin and Ridge, 1999). Research to date shows that control occurs in key algal divisions including cyanobacteria (e.g. Microcystis aeruginosa, Newman and Barrett, 1993), diatoms (e.g. Asterionella sp. and Tabellaria sp., Barrett et al., 1996; Martin and Ridge, 1999) chlorophytes, (e.g. Cladophora glomerata, Welch et al., 1990) and various desmid species (Martin and Ridge, 1999). However, it appears that responses to barley straw in the laboratory are species-specific with no consistent pattern of inhibition within any algal division. Moreover, plant residues, including barley straw, are known to stimulate algal growth in some species (Rice, 1986; Butler, 1998; Martin and Ridge, 1999). Although laboratory studies have indicated that decomposing barley straw is not inhibitory to all algal species, many field studies in the United Kingdom have demonstrated its successful use as an algistatic agent (Barrett et al., 1996; Everall and Lees, 1996, 1997; Caffrey and Monahan, 1999; Ridge et al., 1999). However, consistent control of algal growth by decomposing barley straw has not been found in initial field studies in the US (Lembi, 2002). The goals of this investigation were to: (1) document the effect of barley straw liquor on the growth of a variety of freshwater unialgal cultures; (2) assess the effect of barley straw liquor in the presence and absence of associated microbial communities and straw detritus; and (3) determine whether barley straw is inhibitory to natural phytoplankton communities in central Maryland ponds.
2. Methods 2.1. Preparation of barley straw extract Liquor (leachate) from decomposing barley straw was prepared according to Gibson et al. (1990) by placing 360 g of barley straw (chopped into 2-cm lengths) in 18 l of reverse-osmosis (RO) water in a new polyethylene bucket with a lid. An aquarium air pump was used to provide constant aeration to the decomposing straw. The decomposing straw was incubated at room temperature for sixty days before being used for bioassays. 2.2. Laboratory bioassays of unialgal cultures Twelve species of algae, representing three divisions, were selected for bioassays. These species are representa-
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tive of algae that at times present management problems in freshwater impoundments in the northeastern United States and/or have been previously reported as species of algae that are affected by decomposing barley straw (Table 1). Algal cultures were obtained from the collection of the University of Texas and from the Carolina Biological Supply Company. Cultures were transferred to sterile 500 ml flasks containing 250 ml of a Tris-buffered nutrient medium (Alga-Gro, Carolina Biological Supply, Burlington, NC) and placed in a growth chamber at 20 °C with a 12 h light/12 h dark photoperiod and PAR of 65.4 lmol m 2 s 1. As soon as cultures exhibited substantial growth, aliquots from them were used to initiate bioassays. Bioassays were performed in sterile screw-cap tubes containing 25 ml of liquid. Each tube received 7 ml of algal inoculum, and 9 ml of sterile nutrient medium (Alga-Gro, initial pH = 7.10). In addition, 4 tubes for each algal species received 9 ml of sterile-filtered barley straw liquor (pore size 0.22 lm) and 4 tubes received 9 ml of unfiltered barley straw liquor with 5 pieces of straw 1.5 cm long. These volumes of liquor are equivalent to the leached decomposition products from a barley straw concentration of 7.2 g dry mass of barley straw per liter. Four control tubes received 9 ml of sterile RO water to achieve an equal final volume with the treatments. All tubes were lightly capped to allow gasexchange and maintained in a growth chamber on a 12 h light/12 h dark cycle with a light period irradiance of 65.4 lmol m 2 s 1 PAR and a temperature of 21– 22 °C. Each tube was swirled approximately every 48 h to promote gas-exchange and resuspend settled algae. The bioassays were terminated after two weeks. The 25 ml samples were glass-fiber filtered (Gelman AE; effective pore size 0.7 lm) and stabilized with MgCO3 for chlorophyll analysis. All filters were immediately placed on ice and quickly transferred to 20 °C until analysis (<4 weeks). The filters were extracted in 90% acetone and chlorophyll a (Chl a) was determined spectrophotometrically at 665 nm after correction for particulates and phaeo-pigments (Parsons et al., 1984). After two weeks of growth, the mean algal biomass (as Chl a) in the control and barley straw treatments was compared for each species using an ANOVA. If means were determined to be significantly different, a TukeyÕs HSD was employed to discern where differences in means occurred. For those data sets not meeting the assumption of homoscedasticity (Dinobryon sp. and Synura petersenii), means of control and barley straw treatments were compared using a Kruskal–Wallis test. In cases where significant differences were found, pairwise comparisons using a Mann–Whitney U-test were employed to identify which treatments were different from the control.
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Table 1 Species selected for bioassays with extract of decomposed barley straw Algae
Division
Potential management implicationa
Previously documented responseb to barley straw or related materials in members of the same genus
Ulothrix fimbriata
Chlorophyta
Can lower DO
U. trentonense
Scenedesmus quadricauda
Chlorophyta
Can lower DO
S. subspicatus + (Martin and Ridge, 1999) Scenedesmus sp. (Ball et al., 2001) Scenedesmus sp. +/ (Choe and Jung, 2002)
Selenastrum capricornutum
Chlorophyta
Can lower DO
S. capricornutum
Spirogyra sp.
Chlorophyta
Mat-forming Filter-clogging
Spirogyra sp.
Chlorella vulgaris
Chlorophyta
Can lower DO Filter-clogging
C. vulgaris (Gibson et al., 1990) Chlorella sp. (Pillinger et al., 1992) C. vulgaris (Ridge and Pillinger, 1996) Chlorella sp. (Ridge et al., 1999)
Microcystis aeruginosa
Cyanophyta
Toxic Taste and odor
M. aeruginosa (Pillinger et al., 1992) M. aeruginosa (Newman and Barrett, 1993) M. aeruginosa (Ridge and Pillinger, 1996) M. aeruginosa (Martin and Ridge, 1999) M. aeruginosa (Ridge et al., 1999) Microcystis sp. (Ball et al., 2001) Microcystis sp. +/ (Choe and Jung, 2002)
Oscillatoria lutea var. contorta
Cyanophyta
Off-flavor in fish Filter-clogging
O. tenius (Everall and Lees, 1997) O. animalis + (Martin and Ridge, 1999) O. redekei (Martin and Ridge, 1999)
Anabaena flos-aquae
Cyanophyta
Toxic Filter-clogging Taste and odor
A. cylindrica + (Martin and Ridge, 1999) A. flos-aquae (Martin and Ridge, 1999)
Navicula sp.
Chrysophyta (diatom)
Filter-clogging
None reported
Synedra sp.
Chrysophyta (diatom)
Taste and odor Filter-clogging
None reported
Synura petersenii
Chrysophyta
Taste and odor
None reported
Dinobryon sp.
Chrysophyta
Taste and odor
None reported
(Gibson et al., 1990)
(Gibson et al., 1990)
(Gibson et al., 1990)
Previous responses of algae to straw, straw extract, or other potentially alleopathic plant materials is noted. a Source: APHA (1975). b ‘‘ ’’ indicates reported inhibition, ‘‘+’’ indicates reported growth enhancement.
2.3. Field application of barley straw Six ponds in central Maryland were monitored to examine the effects of decomposing barley straw on algal biomass. The ponds ranged in size from 0.2 to 1.6 ha with average depths from 1.8 to 4.3 m. All of the ponds were mesotrophic to eutrophic, exhibited low alkalinity (total alkalinity less than 50 mg l 1), and were of neutral pH to slightly acidic. These ponds frequently had exhibited problematic algal growth in the past. Several had been treated with either diquat or copper sulfate in previous years to control nuisance algal species. Four of the six ponds were randomly selected for treatment with barley straw. The remaining two control ponds were untreated. Each treated pond received an application of straw equivalent to 112 kg ha 1. The straw bales were loosened to allow water circulation through the bale and promote aerobic decomposition. Loosened bales were wrapped in netting and deployed
evenly around the pond at or near the waterÕs surface and at least 3 m from the shore. Just prior to deploying the straw (21 May 1998), all ponds were evaluated for phytoplankton biomass. Five to eight water samples were taken from each pond at a depth of 25 cm approximately 2 m from shore. The samples from each pond were pooled and analyzed for Chl a by the method described previously. After the application of straw, algal biomass was evaluated in the ponds biweekly using this protocol until 10 September 1998.
3. Results 3.1. Effects of straw on growth of unialgal cultures Frequent visual evaluation indicated that control cultures of all algal species grew substantially during the
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two week incubation period. Therefore, Chl a levels in treated cultures that were lower than those of their untreated counterparts were indicative of growth inhibition by barley straw liquor. Growth of Microcystis aeruginosa, Dinobryon sp., and Synura petersenii were all significantly (p < 0.05) inhibited by barley straw (Fig. 1). S. petersenii was completely inhibited in all straw treatments with Chl a undetectable at the end of the two-week incubation. Likewise, M. aeruginosa was significantly inhibited by barley straw. Both sterile-filtered liquor and unfiltered straw treatments exhibited inhibition in S. petersenii and M. aeruginosa. Growth of Dinobryon sp. was reduced in both straw treatments but only the sterilefiltered liquor treatment exhibited significant inhibition. Since initial levels of Chl a were not measured in any cultures, the mode of inhibition observed in the cases of M. aeruginosa and Dinobryon sp. may have been either algistatic or algicidal. However, the complete disappearance of S. petersenii from treated cultures indi-
cates that the action of barley straw in this case was likely algicidal. Selenastrum capricornutum, Spirogyra sp., Oscillatoria lutea var. contorta, and Navicula sp. exhibited significantly (p < 0.05) increased growth in the presence of at least one of the barley straw treatments (Fig. 2). Unfiltered liquor significantly stimulated growth in all four species. Sterile-filtered extract significantly increased the growth of Navicula sp. and Selenastrum capricornutum but significantly inhibited the growth of Spirogyra sp. The growth of Oscillatoria lutea var. contorta was unaffected by sterile-filtered liquor.
Fig. 1. Mean algal biomass (expressed as chlorophyll a concentration) of species inhibited by barley straw. Replicate cultures were maintained in nutrient media, media augmented with unfiltered barley straw extract, or sterile-filtered barley straw extract. Error bars represent ±1 standard deviation. * Treatment different from control with p 6 0.05; ** treatment different from control with p 6 0.01.
Fig. 2. Mean algal biomass (expressed as chlorophyll a concentration) of species stimulated by barley straw. Replicate cultures were maintained in nutrient media, media augmented with unfiltered barley straw extract, or sterile-filtered barley straw extract. Error bars represent ±1 standard deviation. * Treatment different from control with p 6 0.05; ** treatment different from control with p 6 0.01.
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The growth of Anabaena flos-aquae, Chlorella vulgaris, Ulothrix fimbriata, Synedra sp. and Scenedesmus quadricauda was not significantly affected by the presence of barley straw (Fig. 3). Though non-significant, Anabaena flos-aquae and Chlorella vulgaris grown in the presence of barley straw displayed slightly greater growth than their respective controls. 3.2. Field applications of straw The average algal biomass in both treated and control ponds declined rapidly after the initial algal sampling (Fig. 4). Algal biomass remained low in all ponds until mid-August when a small second period
1000
Chlorophyll a Content (µg L-1)
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Control Ponds
800
Straw-treated Ponds
600 400
200
0
May
June
July
August
Sept
Month Fig. 4. Average chlorophyll a concentrations from control ponds (n = 2) and ponds treated with barley straw (n = 4). Dotted line indicates the date of barley straw application to treated ponds. Control pond averages were not significantly different from those of ponds treated with barley straw on any sampling date. (Standard deviations not shown.)
of growth was evident. At each sampling the variation in mean algal biomass among treated and control ponds was very large (coefficients of variation from 36% to 157% and from 33% to 141% for treated and control ponds, respectively). Consequently, the average biomass in treated versus control ponds was not significantly different during any sampling throughout the summer.
4. Discussion 4.1. Algal species vary in response to straw
Fig. 3. Mean algal biomass (expressed as chlorophyll a concentration) of species unaffected by barley straw. Replicate cultures were maintained in nutrient media, media augmented with unfiltered barley straw extract, or sterile-filtered barley straw extract. Error bars represent ±1 standard deviation.
Rotted barley straw and liquors from decomposing straw are effective in inhibiting the growth of some species of nuisance algae in laboratory cultures. This study reiterates the finding that the growth of Microcystis aeruginosa, which is implicated in taste and odor problems as well as being a potential producer of toxins, is consistently inhibited by barley straw (Pillinger et al., 1992; Newman and Barrett, 1993; Ridge and Pillinger, 1996; Martin and Ridge, 1999; Ridge et al., 1999; Ball et al., 2001). This is the first report of growth inhibition in both Synura petersenii and Dinobryon sp. In a survey of 174 utilities, flagellated chrysophytes such as these accounted for 14% of the taste and odor problems in drinking water supplies (Casitas Municipal Water District, 1987), particularly water supplies emanating from colder mesotrophic to marginally eutrophic reservoirs (Hoehn, 1998). Thus, barley straw may offer a new method for mitigating water supply problems that stem from the growth of these chrysophytes. The responses of laboratory algal cultures to the presence of barley straw in this study were often different
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from those observed previously for the same species or members of the same genus. For example, the growth of Selenastrum capricornutum and Anabeana flos-aquae were stimulated in the present study but found to be inhibited by rotting straw in earlier studies (Gibson et al., 1990; Martin and Ridge, 1999). Similarly, both rotted straw (Gibson et al., 1990) and leachate from unrotted straw (Ridge and Pillinger, 1996) inhibited the growth of Chlorella vulgaris; however, its growth was unaffected in this study. The response of diatoms to compounds produced during the decomposition of barley straw also varies widely. The diatom species in this study were either unaffected (Synedra sp.) or stimulated (Navicula sp.) by barley straw. In a field study, Barrett et al. (1996) suggest that barley straw inhibited diatom growth. Likewise, Tabellaria flocculosa and Asterionella formosa exhibited growth inhibition in the presence of decomposing straw (Martin and Ridge, 1999). However, the growth of Nitzschia filiformis var. conferta was stimulated by barley straw (Martin and Ridge, 1999). Some diatoms may exhibit tolerance to suspected inhibitors produced by straw. For example, the marine diatom, Thallassiosira sp. was observed to grow in the presence of phenolic compounds (Loveli et al., 2002). Growth of Ulothrix fimbriata and Scenedesmus quadricauda were not affected by barley straw in this study. The growth of Oscillatoria lutea var. contorta was stimulated. Although previous studies did not employ these species, other species in these same genera responded differently in every case (see Table 1) (Gibson et al., 1990; Everall and Lees, 1997; Martin and Ridge, 1999; Ball et al., 2001). It appears likely that growth responses to decomposing barley straw are, at a minimum, species-specific. Differences in response among strains of the same species, with the exception of Microcystis aeruginosa (Martin and Ridge, 1999), have not been widely investigated. Although taxonomic differences may account for some of the differences observed between the current study and previous work, other factors also may be important when comparing results among laboratory bioassays using barley straw. Straw dosage can be critical in eliciting growth responses (Martin and Ridge, 1999). However, in the current study, bioassays contained liquor doses equivalent to 7200 g m 3 (dry mass of straw)—a dosage considered sufficient to cause inhibition in even slightly susceptible algal species (Martin and Ridge, 1999). The age and conditions under which rotted straw is prepared can also affect bioassay results. The current study employed straw that was aerobically decomposed for two months. This time period was sufficient to elicit significant growth inhibition in Cladophora glomerata in a previous study (Gibson et al., 1990); however, maximum inhibition in that study was observed after six
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months of decomposition. Additional studies are needed to further elucidate the temporal variability in inhibitory activity of decomposing straw relative to individual algal species. 4.2. The nature of inhibiting and stimulating compounds Although the current study sheds no light on the chemical makeup of algal growth inhibitors in decomposing barley straw, it appears that straw inhibitors produced after two months of decomposition remained stable and active over the 2-week bioassay. Sterilefiltered liquor (containing neither microbes from the decomposing straw nor fine particles of detrital straw) was capable of inhibiting all three algal species that exhibited significantly reduced growth (Fig. 1). Other studies have reported similar persistence of inhibitory activity after filtration (Gibson et al., 1990; Ball et al., 2001). However, Ridge et al. (1999) found that, while ‘‘early phase’’ (less than 90 days) decomposition of oak leaves produced inhibitors that persisted in the absence of fine particulate leaf material, inhibitors from ‘‘late phase’’ decomposition sometimes required the presence of fine particles to elicit inhibition in bioassays. It appears that the nature (type and quantity) of the inhibitory substances in decomposing straw may vary over the course of the strawÕs decomposition. While bioassay-guided fractionation of chemical constituents from decomposing straw may not be helpful in elucidating the identities of inhibitory compounds during later phases of decomposition (Pillinger et al., 1994), it may be a productive approach for identifying inhibitory compounds that are released from straw during the early phases of decomposition. The ability of components from rotting barley straw to stimulate growth of some algal species was first reported over a decade ago (Barrett and Newman, 1992), yet this aspect of its effect has received little attention. Martin and Ridge (1999) observed significant growth stimulation in Nitzschia filiformis var. conferta, Scenedesmus subspicatus, Anabaena cylindrica and Oscillatoria animalis when incubated in media containing rotted barley straw. Terlizzi et al. (2002) reported growth stimulation in cultures of three estuarine dinoflagellates (Gyrodinium instriatum, Prorocentrum minimum, and P. micans) treated with barley straw. Similarly, products from other plants (wheat, Ball et al., 2001; oak leaves, Ridge et al., 1999; and needles and chips of pine and Korean pine, Choe and Jung, 2002) stimulate algal growth at least during some stages of decomposition. Moreover, even decomposition products from plants that cause growth inhibition in Microcystis sp. and Scenedesmus sp. at higher dosages (barley straw, rice straw, mugwort, and chrysanthemum) exhibit a shift toward stimulation at lower concentrations (Choe and Jung, 2002).
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During the current study, the stimulatory nature of rotting barley straw was generally most pronounced in treatments containing bits of straw rather than sterilefiltered liquor (Fig. 2), while sterile-filtered liquor still elicited lesser levels of stimulation in the cases of Navicula sp. and Selenastrum capricornutum. These differences suggest that stimulatory components from two-monthold decomposing straw may be somewhat labile and in need of constant replenishment during the bioassay. 4.3. Field studies of barley straw application While the results of laboratory barley straw bioassays often do not translate directly into outcomes of straw applications in the field (Lembi, 2002), one would expect that, given the species-specific inhibitory and stimulatory nature of rotting straw exhibited in this study and elsewhere (Martin and Ridge, 1999), natural algal communities treated with straw would exhibit shifts in species composition as well as either increases or decreases in total biomass. With one exception (Kelly and Smith, 1996), all published reports of field applications of barley straw have indicated an overall decline in algal biomass without a notable shift in species composition. However, Brownlee et al. (2003) recently reported a lack of overall decline in algal biomass from some freshwater and brackish water samples treated with barley straw but a shift in species dominance in those samples. Most reported field studies of the effect of decomposing barley straw on algal growth have been conducted as management experiments that involved a single pond, canal, or reservoir (Welch et al., 1990; Ridge and Barrett, 1992; Everall and Lees, 1997; Barrett et al., 1999; Caffrey and Monahan, 1999). The efficacy of straw applications in these studies was assessed either by comparing algal growth in treated waters with that upstream of the application or by making pre- and post-treatment comparisons of algal growth at the same location. As these authors point out, the lack of replication and absence of legitimate controls in these studies make definitive conclusions concerning the effectiveness of field applications of barley straw difficult. In the current study, although phytoplankton biomass (as measured by Chl a) declined in ponds treated with barley straw, similar declines were seen in ponds that received no straw. Likewise, observations of floating filamentous algal mats made at the time of phytoplankton samplings indicated a general decline in surface coverage by mats throughout the summer in both treated and control ponds. These simultaneous declines in biomass, coupled with considerable between-pond variation in both treated and control groups, cannot be used to support the premise that barley straw inhibited the growth of algae in these systems. Similarly, Kelly and Smith (1996) were unable to demonstrate that barley straw retarded algal growth in a small, eutrophic Scottish loch.
The dosage employed in this study (112 kg ha 1) is at the lower limit of recommended dosages for small ponds (Newman, 1999; Butler et al., 2001; Lembi, 2002). It may be that greater amounts of straw in treated ponds would have resulted in more easily discernable differences in chlorophyll a levels when compared with control ponds. Future field studies of the effect of rotting barley straw on algal growth need to be designed in ways that evaluate system-to-system variation as well as allow for comparisons with simultaneously run controls. Field experiments that employ replicate experimental ponds (e.g. Nicholls and Taylor, 1995) or mesocosms deployed in natural systems would provide these opportunities. 4.4. Conclusion The current study and results of previous researchers (Kelly and Smith, 1996; Martin and Ridge, 1999; Terlizzi et al., 2002) challenge the view that barley straw is an effective broad-spectrum treatment for nuisance algae. Rather, this work suggests that barley straw may be of value in the treatment of specific algae. Selective inhibition and stimulation of algal species suggests barley straw treatment may alter the species composition of phytoplankton communities.
Acknowledgements We thank Irene Ridge for helpful discussions of this work. Financial support was provided by the University of Maryland College of Agriculture and Natural Resources and the Whitaker Foundation.
References Ball, A.S., Williams, M., Vincent, D., Robinson, J., 2001. Algal growth control by a barley straw extract. Bioresour. Technol. 77, 177–181. Barrett, P.R.F., Newman, J.R., 1992. Algal growth inhibition by rotting barley straw (Abstract). Br. Phycol. J. 27, 83–84. Barrett, P.R.F., Curnow, J.C., Littlejohn, J.W., 1996. The control of diatom and cyanobacterial blooms in reservoirs using barley straw. Hydrobiologia 340, 307–311. Barrett, P.R.F., Littlejohn, J.W., Curnow, J., 1999. Long-term algal control in a reservoir using barley straw. Hydrobiologia 415, 309– 313. Brownlee, E.F., Sellner, S.G., Sellner, K.G., 2003. Effects of barley straw (Hordeum vulgare) on freshwater and brackish phytoplankton and cyanobacteria. J. Appl. Phycol. 15, 525–531. Butler, B.R., 1998. Examination of the effects of barley straw (Hordeum vulgare) on freshwater algae in the field and laboratory. MS thesis; Hood College, Frederick, MD, USA. Butler, B., Terlizzi, D., Ferrier, D., 2001. Barley straw: a potential method of algae control in ponds. Publication No. UM-SG-MAP2001-02. Maryland Sea Grant Extension Program, College Park, MD.
M.D. Ferrier et al. / Bioresource Technology 96 (2005) 1788–1795 Caffrey, J.M., Monahan, C., 1999. Filamentous algal control using barley straw. Hydrobiologia 415, 315–318. Casitas Municipal Water District, 1987. Current methodology for control of algae in reservoirs. AWWA Research Foundation, American Water Works Association, Denver, CO. Choe, S., Jung, I., 2002. Growth inhibition of freshwater algae by ester compounds released from rotted plants. J. Ind. Eng. Chem. 8, 297– 304. Everall, N.C., Lees, D.R., 1996. The use of barley straw to control general and blue-green algal growth in a Derbyshire reservoir. Wat. Res. 30, 269–276. Everall, N.C., Lees, D.R., 1997. The identification and significance of chemicals released from decomposing barley straw during reservoir algal control. Wat. Res. 31, 614–620. Gangstad, E.O., 1986. Freshwater Vegetation Management. Thomas Publications, Fresno, CA. Gibson, M.T., Welch, I.M., Barrett, P.R.F., Ridge, I, 1990. Barley straw as an inhibitor of algal growth II: laboratory studies. J. Appl. Phycol. 2, 241–248. Hoehn, R.C., 1998. Biological aspects of taste and odor problems in drinking water (abstract). AWWARF Taste and Odor Workshop, Chicago, IL. Available from:. Kelly, L.A., Smith, S., 1996. The nutrient budget of a small eutrophic loch and the effectiveness of straw bales in controlling algal blooms. Freshwater Biol. 36, 411–418. Lembi, C., 2002. Barley straw for algae control. Aquatic Plant Management Publication APM-1-W. Purdue University, South Bend, IN. Available from: . Loveli, C.R., Eriksen, N.T., Lewitus, A.J., Chen, Y.P., 2002. Resistance of the marine diatom Thalassiosira sp. to toxicity of phenolic compounds. Mar. Ecol. Prog. Ser. 229, 11–18. Martin, D., Ridge, I., 1999. The relative sensitivity of algae to decomposing barley straw. J. Appl. Phycol. 11, 285–291.
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Newman, J., 1999. Control of algae with straw. Information Sheet 3. IACR—Centre for Aquatic Plant Management. Sonning, Berkshire, UK. Newman, J.R., Barrett, P.R.F., 1993. Control of Microcystis aeruginosa by decomposing barley straw. J. Aquatic. Plant Manag. 31, 353–355. Nicholls, K.H., Taylor, R.G., 1995. Experimental use of barley straw for algae control in Ontario ponds (Abstract). Lake Reserv. Manage. 11, 175. Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York. Pillinger, J.M., Cooper, J.A., Ridge, I., Barrett, P.R.F., 1992. Barley straw as an inhibitor of algae growth III: the role of fungal decomposition. J. Appl. Phycol. 4, 353–355. Pillinger, J.M., Cooper, J.A., Ridge, I., 1994. Role of phenolic compounds in the antialgal activity of barley straw. J. Chem. Ecol. 20, 1557–1569. Rice, E.L., 1986. Allelopathic growth stimulation. In: Putnam, A.R, Tang, C.-S. (Eds.), The Science of Allelopathy. John Wiley and Sons, New York. Ridge, I., Barrett, P.R.F., 1992. Algal control with barley straw. Aspects Appl. Biol. 29, 457–462. Ridge, I., Pillinger, J.M., 1996. Towards understanding the nature of algal inhibitors from barley straw. Hydrobiologia 340, 301–305. Ridge, I., Walters, J., Street, M., 1999. Algal growth control by terrestrial leaf litter: a realistic tool. Hydrobiologia 395/396, 173–180. Terlizzi, D.E., Ferrier, M.D., Armbrester, E.A., Anlauf, K.A., 2002. Inhibition of dinoflagellate growth by extracts of barley straw (Hordeum vulgare). J. Appl. Phycol. 14, 275–280. Vymazal, J., 1995. Algae and Element Cycling in Wetlands. Lewis Publishers, Boca Raton, FL. Welch, I.M., Barrett, P.R.F., Gibson, M.T., Ridge, I., 1990. Barley straw as an inhibitor of algae growth I: studies in the Chesterfield Canal. J. Appl. Phycol. 2, 231–239.
The effects of barley straw (Hordeum vulgare) on the growth of freshwater algae M.D. Ferrier
a,*
, B.R. Butler Sr. b, D.E. Terlizzi c, R.V. Lacouture
d
a
Department of Biology, Hood College, Frederick, MD 21701, United States Maryland Cooperative Extension, University of Maryland, 700 Agriculture Center, Westminster, MD 21157, United States University of Maryland Sea Grant Extension Program, Center of Marine Biotechnology, 701 E. Pratt St Baltimore, MD 21202, United States d Morgan State University Estuarine Research Center, 10545 Mackall Rd., St Leonard, MD 20685, United States b
c
Received 17 June 2003; received in revised form 14 January 2005; accepted 14 January 2005 Available online 7 March 2005
Abstract Bioassays were conducted to determine the efficacy of barley straw liquor in controlling algal growth of 12 freshwater species of algae representing three divisions. Barley straw liquor inhibited the growth of three nuisance algae common in freshwater: Synura petersenii, Dinobyron sp., and Microcystis aeruginosa. However, Selenastrum capricornutum, Spirogyra sp., Oscillatoria lutea var. contorta, and Navicula sp. had significantly increased growth in the presence of straw liquor. The growth of the remainder, Ulothrix fimbriata, Scenedesmus quadricauda, Chlorella vulgaris, Anabaena flos-aquae, and Synedra sp. showed no significant difference from controls. In a related field study, we treated four of six ponds with barley straw and monitored their chlorophyll a levels for one growing season. While phytoplankton populations in all ponds decreased in midsummer, the phytoplankton biomass in treated ponds did not differ significantly from that of control ponds, suggesting that the application of barley straw had no effect on algal growth in these systems. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Algicide; Algae control; Barley straw; Inhibition; Stimulation
1. Introduction Various forms of unicellular, filamentous, and colonial freshwater algae pose management problems in ponds, lakes, and reservoirs. Algae may interfere with pond uses or lead to environmental problems both directly as a consequence of excessive algal biomass and indirectly due to the algicide treatments used in their control. Filamentous algae clog pumps, screens, and emitters in agricultural irrigation systems. Many algal forms create off-flavors in potable water (Barrett et al., 1996). These unpleasant tastes and odors reduce the *
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0960-8524/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2005.01.021
water intake of livestock and can render water from reservoirs unfit for human consumption (Gangstad, 1986; Vymazal, 1995). Remedial efforts to reduce the effects of algal blooms in reservoirs (e.g. filtering or chlorinating the water) have met with limited success since species such as Synura sp. and Anabaena sp. release oils during chlorination creating additional taste and odor problems (Vymazal, 1995). Mat-forming species also can hinder recreational fishing and swimming, and are considered unsightly by the general public (Newman, 1999). Anecdotal evidence of the ability of barley straw to control algal growth was observed as early as 1980 (Welch et al., 1990). Subsequent work demonstrated the addition of barley straw to a pond does not kill algae
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already present, but prevents the growth of new algal cells (Newman, 1999). This algistatic activity is produced on immersion and during decomposition of straw in a well-oxygenated environment. Decomposing barley straw has been shown to control a wide range of algae in freshwater systems including unicellular, filamentous and colonial forms (Gibson et al., 1990; Martin and Ridge, 1999). Research to date shows that control occurs in key algal divisions including cyanobacteria (e.g. Microcystis aeruginosa, Newman and Barrett, 1993), diatoms (e.g. Asterionella sp. and Tabellaria sp., Barrett et al., 1996; Martin and Ridge, 1999) chlorophytes, (e.g. Cladophora glomerata, Welch et al., 1990) and various desmid species (Martin and Ridge, 1999). However, it appears that responses to barley straw in the laboratory are species-specific with no consistent pattern of inhibition within any algal division. Moreover, plant residues, including barley straw, are known to stimulate algal growth in some species (Rice, 1986; Butler, 1998; Martin and Ridge, 1999). Although laboratory studies have indicated that decomposing barley straw is not inhibitory to all algal species, many field studies in the United Kingdom have demonstrated its successful use as an algistatic agent (Barrett et al., 1996; Everall and Lees, 1996, 1997; Caffrey and Monahan, 1999; Ridge et al., 1999). However, consistent control of algal growth by decomposing barley straw has not been found in initial field studies in the US (Lembi, 2002). The goals of this investigation were to: (1) document the effect of barley straw liquor on the growth of a variety of freshwater unialgal cultures; (2) assess the effect of barley straw liquor in the presence and absence of associated microbial communities and straw detritus; and (3) determine whether barley straw is inhibitory to natural phytoplankton communities in central Maryland ponds.
2. Methods 2.1. Preparation of barley straw extract Liquor (leachate) from decomposing barley straw was prepared according to Gibson et al. (1990) by placing 360 g of barley straw (chopped into 2-cm lengths) in 18 l of reverse-osmosis (RO) water in a new polyethylene bucket with a lid. An aquarium air pump was used to provide constant aeration to the decomposing straw. The decomposing straw was incubated at room temperature for sixty days before being used for bioassays. 2.2. Laboratory bioassays of unialgal cultures Twelve species of algae, representing three divisions, were selected for bioassays. These species are representa-
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tive of algae that at times present management problems in freshwater impoundments in the northeastern United States and/or have been previously reported as species of algae that are affected by decomposing barley straw (Table 1). Algal cultures were obtained from the collection of the University of Texas and from the Carolina Biological Supply Company. Cultures were transferred to sterile 500 ml flasks containing 250 ml of a Tris-buffered nutrient medium (Alga-Gro, Carolina Biological Supply, Burlington, NC) and placed in a growth chamber at 20 °C with a 12 h light/12 h dark photoperiod and PAR of 65.4 lmol m 2 s 1. As soon as cultures exhibited substantial growth, aliquots from them were used to initiate bioassays. Bioassays were performed in sterile screw-cap tubes containing 25 ml of liquid. Each tube received 7 ml of algal inoculum, and 9 ml of sterile nutrient medium (Alga-Gro, initial pH = 7.10). In addition, 4 tubes for each algal species received 9 ml of sterile-filtered barley straw liquor (pore size 0.22 lm) and 4 tubes received 9 ml of unfiltered barley straw liquor with 5 pieces of straw 1.5 cm long. These volumes of liquor are equivalent to the leached decomposition products from a barley straw concentration of 7.2 g dry mass of barley straw per liter. Four control tubes received 9 ml of sterile RO water to achieve an equal final volume with the treatments. All tubes were lightly capped to allow gasexchange and maintained in a growth chamber on a 12 h light/12 h dark cycle with a light period irradiance of 65.4 lmol m 2 s 1 PAR and a temperature of 21– 22 °C. Each tube was swirled approximately every 48 h to promote gas-exchange and resuspend settled algae. The bioassays were terminated after two weeks. The 25 ml samples were glass-fiber filtered (Gelman AE; effective pore size 0.7 lm) and stabilized with MgCO3 for chlorophyll analysis. All filters were immediately placed on ice and quickly transferred to 20 °C until analysis (<4 weeks). The filters were extracted in 90% acetone and chlorophyll a (Chl a) was determined spectrophotometrically at 665 nm after correction for particulates and phaeo-pigments (Parsons et al., 1984). After two weeks of growth, the mean algal biomass (as Chl a) in the control and barley straw treatments was compared for each species using an ANOVA. If means were determined to be significantly different, a TukeyÕs HSD was employed to discern where differences in means occurred. For those data sets not meeting the assumption of homoscedasticity (Dinobryon sp. and Synura petersenii), means of control and barley straw treatments were compared using a Kruskal–Wallis test. In cases where significant differences were found, pairwise comparisons using a Mann–Whitney U-test were employed to identify which treatments were different from the control.
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Table 1 Species selected for bioassays with extract of decomposed barley straw Algae
Division
Potential management implicationa
Previously documented responseb to barley straw or related materials in members of the same genus
Ulothrix fimbriata
Chlorophyta
Can lower DO
U. trentonense
Scenedesmus quadricauda
Chlorophyta
Can lower DO
S. subspicatus + (Martin and Ridge, 1999) Scenedesmus sp. (Ball et al., 2001) Scenedesmus sp. +/ (Choe and Jung, 2002)
Selenastrum capricornutum
Chlorophyta
Can lower DO
S. capricornutum
Spirogyra sp.
Chlorophyta
Mat-forming Filter-clogging
Spirogyra sp.
Chlorella vulgaris
Chlorophyta
Can lower DO Filter-clogging
C. vulgaris (Gibson et al., 1990) Chlorella sp. (Pillinger et al., 1992) C. vulgaris (Ridge and Pillinger, 1996) Chlorella sp. (Ridge et al., 1999)
Microcystis aeruginosa
Cyanophyta
Toxic Taste and odor
M. aeruginosa (Pillinger et al., 1992) M. aeruginosa (Newman and Barrett, 1993) M. aeruginosa (Ridge and Pillinger, 1996) M. aeruginosa (Martin and Ridge, 1999) M. aeruginosa (Ridge et al., 1999) Microcystis sp. (Ball et al., 2001) Microcystis sp. +/ (Choe and Jung, 2002)
Oscillatoria lutea var. contorta
Cyanophyta
Off-flavor in fish Filter-clogging
O. tenius (Everall and Lees, 1997) O. animalis + (Martin and Ridge, 1999) O. redekei (Martin and Ridge, 1999)
Anabaena flos-aquae
Cyanophyta
Toxic Filter-clogging Taste and odor
A. cylindrica + (Martin and Ridge, 1999) A. flos-aquae (Martin and Ridge, 1999)
Navicula sp.
Chrysophyta (diatom)
Filter-clogging
None reported
Synedra sp.
Chrysophyta (diatom)
Taste and odor Filter-clogging
None reported
Synura petersenii
Chrysophyta
Taste and odor
None reported
Dinobryon sp.
Chrysophyta
Taste and odor
None reported
(Gibson et al., 1990)
(Gibson et al., 1990)
(Gibson et al., 1990)
Previous responses of algae to straw, straw extract, or other potentially alleopathic plant materials is noted. a Source: APHA (1975). b ‘‘ ’’ indicates reported inhibition, ‘‘+’’ indicates reported growth enhancement.
2.3. Field application of barley straw Six ponds in central Maryland were monitored to examine the effects of decomposing barley straw on algal biomass. The ponds ranged in size from 0.2 to 1.6 ha with average depths from 1.8 to 4.3 m. All of the ponds were mesotrophic to eutrophic, exhibited low alkalinity (total alkalinity less than 50 mg l 1), and were of neutral pH to slightly acidic. These ponds frequently had exhibited problematic algal growth in the past. Several had been treated with either diquat or copper sulfate in previous years to control nuisance algal species. Four of the six ponds were randomly selected for treatment with barley straw. The remaining two control ponds were untreated. Each treated pond received an application of straw equivalent to 112 kg ha 1. The straw bales were loosened to allow water circulation through the bale and promote aerobic decomposition. Loosened bales were wrapped in netting and deployed
evenly around the pond at or near the waterÕs surface and at least 3 m from the shore. Just prior to deploying the straw (21 May 1998), all ponds were evaluated for phytoplankton biomass. Five to eight water samples were taken from each pond at a depth of 25 cm approximately 2 m from shore. The samples from each pond were pooled and analyzed for Chl a by the method described previously. After the application of straw, algal biomass was evaluated in the ponds biweekly using this protocol until 10 September 1998.
3. Results 3.1. Effects of straw on growth of unialgal cultures Frequent visual evaluation indicated that control cultures of all algal species grew substantially during the
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two week incubation period. Therefore, Chl a levels in treated cultures that were lower than those of their untreated counterparts were indicative of growth inhibition by barley straw liquor. Growth of Microcystis aeruginosa, Dinobryon sp., and Synura petersenii were all significantly (p < 0.05) inhibited by barley straw (Fig. 1). S. petersenii was completely inhibited in all straw treatments with Chl a undetectable at the end of the two-week incubation. Likewise, M. aeruginosa was significantly inhibited by barley straw. Both sterile-filtered liquor and unfiltered straw treatments exhibited inhibition in S. petersenii and M. aeruginosa. Growth of Dinobryon sp. was reduced in both straw treatments but only the sterilefiltered liquor treatment exhibited significant inhibition. Since initial levels of Chl a were not measured in any cultures, the mode of inhibition observed in the cases of M. aeruginosa and Dinobryon sp. may have been either algistatic or algicidal. However, the complete disappearance of S. petersenii from treated cultures indi-
cates that the action of barley straw in this case was likely algicidal. Selenastrum capricornutum, Spirogyra sp., Oscillatoria lutea var. contorta, and Navicula sp. exhibited significantly (p < 0.05) increased growth in the presence of at least one of the barley straw treatments (Fig. 2). Unfiltered liquor significantly stimulated growth in all four species. Sterile-filtered extract significantly increased the growth of Navicula sp. and Selenastrum capricornutum but significantly inhibited the growth of Spirogyra sp. The growth of Oscillatoria lutea var. contorta was unaffected by sterile-filtered liquor.
Fig. 1. Mean algal biomass (expressed as chlorophyll a concentration) of species inhibited by barley straw. Replicate cultures were maintained in nutrient media, media augmented with unfiltered barley straw extract, or sterile-filtered barley straw extract. Error bars represent ±1 standard deviation. * Treatment different from control with p 6 0.05; ** treatment different from control with p 6 0.01.
Fig. 2. Mean algal biomass (expressed as chlorophyll a concentration) of species stimulated by barley straw. Replicate cultures were maintained in nutrient media, media augmented with unfiltered barley straw extract, or sterile-filtered barley straw extract. Error bars represent ±1 standard deviation. * Treatment different from control with p 6 0.05; ** treatment different from control with p 6 0.01.
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The growth of Anabaena flos-aquae, Chlorella vulgaris, Ulothrix fimbriata, Synedra sp. and Scenedesmus quadricauda was not significantly affected by the presence of barley straw (Fig. 3). Though non-significant, Anabaena flos-aquae and Chlorella vulgaris grown in the presence of barley straw displayed slightly greater growth than their respective controls. 3.2. Field applications of straw The average algal biomass in both treated and control ponds declined rapidly after the initial algal sampling (Fig. 4). Algal biomass remained low in all ponds until mid-August when a small second period
1000
Chlorophyll a Content (µg L-1)
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Control Ponds
800
Straw-treated Ponds
600 400
200
0
May
June
July
August
Sept
Month Fig. 4. Average chlorophyll a concentrations from control ponds (n = 2) and ponds treated with barley straw (n = 4). Dotted line indicates the date of barley straw application to treated ponds. Control pond averages were not significantly different from those of ponds treated with barley straw on any sampling date. (Standard deviations not shown.)
of growth was evident. At each sampling the variation in mean algal biomass among treated and control ponds was very large (coefficients of variation from 36% to 157% and from 33% to 141% for treated and control ponds, respectively). Consequently, the average biomass in treated versus control ponds was not significantly different during any sampling throughout the summer.
4. Discussion 4.1. Algal species vary in response to straw
Fig. 3. Mean algal biomass (expressed as chlorophyll a concentration) of species unaffected by barley straw. Replicate cultures were maintained in nutrient media, media augmented with unfiltered barley straw extract, or sterile-filtered barley straw extract. Error bars represent ±1 standard deviation.
Rotted barley straw and liquors from decomposing straw are effective in inhibiting the growth of some species of nuisance algae in laboratory cultures. This study reiterates the finding that the growth of Microcystis aeruginosa, which is implicated in taste and odor problems as well as being a potential producer of toxins, is consistently inhibited by barley straw (Pillinger et al., 1992; Newman and Barrett, 1993; Ridge and Pillinger, 1996; Martin and Ridge, 1999; Ridge et al., 1999; Ball et al., 2001). This is the first report of growth inhibition in both Synura petersenii and Dinobryon sp. In a survey of 174 utilities, flagellated chrysophytes such as these accounted for 14% of the taste and odor problems in drinking water supplies (Casitas Municipal Water District, 1987), particularly water supplies emanating from colder mesotrophic to marginally eutrophic reservoirs (Hoehn, 1998). Thus, barley straw may offer a new method for mitigating water supply problems that stem from the growth of these chrysophytes. The responses of laboratory algal cultures to the presence of barley straw in this study were often different
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from those observed previously for the same species or members of the same genus. For example, the growth of Selenastrum capricornutum and Anabeana flos-aquae were stimulated in the present study but found to be inhibited by rotting straw in earlier studies (Gibson et al., 1990; Martin and Ridge, 1999). Similarly, both rotted straw (Gibson et al., 1990) and leachate from unrotted straw (Ridge and Pillinger, 1996) inhibited the growth of Chlorella vulgaris; however, its growth was unaffected in this study. The response of diatoms to compounds produced during the decomposition of barley straw also varies widely. The diatom species in this study were either unaffected (Synedra sp.) or stimulated (Navicula sp.) by barley straw. In a field study, Barrett et al. (1996) suggest that barley straw inhibited diatom growth. Likewise, Tabellaria flocculosa and Asterionella formosa exhibited growth inhibition in the presence of decomposing straw (Martin and Ridge, 1999). However, the growth of Nitzschia filiformis var. conferta was stimulated by barley straw (Martin and Ridge, 1999). Some diatoms may exhibit tolerance to suspected inhibitors produced by straw. For example, the marine diatom, Thallassiosira sp. was observed to grow in the presence of phenolic compounds (Loveli et al., 2002). Growth of Ulothrix fimbriata and Scenedesmus quadricauda were not affected by barley straw in this study. The growth of Oscillatoria lutea var. contorta was stimulated. Although previous studies did not employ these species, other species in these same genera responded differently in every case (see Table 1) (Gibson et al., 1990; Everall and Lees, 1997; Martin and Ridge, 1999; Ball et al., 2001). It appears likely that growth responses to decomposing barley straw are, at a minimum, species-specific. Differences in response among strains of the same species, with the exception of Microcystis aeruginosa (Martin and Ridge, 1999), have not been widely investigated. Although taxonomic differences may account for some of the differences observed between the current study and previous work, other factors also may be important when comparing results among laboratory bioassays using barley straw. Straw dosage can be critical in eliciting growth responses (Martin and Ridge, 1999). However, in the current study, bioassays contained liquor doses equivalent to 7200 g m 3 (dry mass of straw)—a dosage considered sufficient to cause inhibition in even slightly susceptible algal species (Martin and Ridge, 1999). The age and conditions under which rotted straw is prepared can also affect bioassay results. The current study employed straw that was aerobically decomposed for two months. This time period was sufficient to elicit significant growth inhibition in Cladophora glomerata in a previous study (Gibson et al., 1990); however, maximum inhibition in that study was observed after six
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months of decomposition. Additional studies are needed to further elucidate the temporal variability in inhibitory activity of decomposing straw relative to individual algal species. 4.2. The nature of inhibiting and stimulating compounds Although the current study sheds no light on the chemical makeup of algal growth inhibitors in decomposing barley straw, it appears that straw inhibitors produced after two months of decomposition remained stable and active over the 2-week bioassay. Sterilefiltered liquor (containing neither microbes from the decomposing straw nor fine particles of detrital straw) was capable of inhibiting all three algal species that exhibited significantly reduced growth (Fig. 1). Other studies have reported similar persistence of inhibitory activity after filtration (Gibson et al., 1990; Ball et al., 2001). However, Ridge et al. (1999) found that, while ‘‘early phase’’ (less than 90 days) decomposition of oak leaves produced inhibitors that persisted in the absence of fine particulate leaf material, inhibitors from ‘‘late phase’’ decomposition sometimes required the presence of fine particles to elicit inhibition in bioassays. It appears that the nature (type and quantity) of the inhibitory substances in decomposing straw may vary over the course of the strawÕs decomposition. While bioassay-guided fractionation of chemical constituents from decomposing straw may not be helpful in elucidating the identities of inhibitory compounds during later phases of decomposition (Pillinger et al., 1994), it may be a productive approach for identifying inhibitory compounds that are released from straw during the early phases of decomposition. The ability of components from rotting barley straw to stimulate growth of some algal species was first reported over a decade ago (Barrett and Newman, 1992), yet this aspect of its effect has received little attention. Martin and Ridge (1999) observed significant growth stimulation in Nitzschia filiformis var. conferta, Scenedesmus subspicatus, Anabaena cylindrica and Oscillatoria animalis when incubated in media containing rotted barley straw. Terlizzi et al. (2002) reported growth stimulation in cultures of three estuarine dinoflagellates (Gyrodinium instriatum, Prorocentrum minimum, and P. micans) treated with barley straw. Similarly, products from other plants (wheat, Ball et al., 2001; oak leaves, Ridge et al., 1999; and needles and chips of pine and Korean pine, Choe and Jung, 2002) stimulate algal growth at least during some stages of decomposition. Moreover, even decomposition products from plants that cause growth inhibition in Microcystis sp. and Scenedesmus sp. at higher dosages (barley straw, rice straw, mugwort, and chrysanthemum) exhibit a shift toward stimulation at lower concentrations (Choe and Jung, 2002).
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During the current study, the stimulatory nature of rotting barley straw was generally most pronounced in treatments containing bits of straw rather than sterilefiltered liquor (Fig. 2), while sterile-filtered liquor still elicited lesser levels of stimulation in the cases of Navicula sp. and Selenastrum capricornutum. These differences suggest that stimulatory components from two-monthold decomposing straw may be somewhat labile and in need of constant replenishment during the bioassay. 4.3. Field studies of barley straw application While the results of laboratory barley straw bioassays often do not translate directly into outcomes of straw applications in the field (Lembi, 2002), one would expect that, given the species-specific inhibitory and stimulatory nature of rotting straw exhibited in this study and elsewhere (Martin and Ridge, 1999), natural algal communities treated with straw would exhibit shifts in species composition as well as either increases or decreases in total biomass. With one exception (Kelly and Smith, 1996), all published reports of field applications of barley straw have indicated an overall decline in algal biomass without a notable shift in species composition. However, Brownlee et al. (2003) recently reported a lack of overall decline in algal biomass from some freshwater and brackish water samples treated with barley straw but a shift in species dominance in those samples. Most reported field studies of the effect of decomposing barley straw on algal growth have been conducted as management experiments that involved a single pond, canal, or reservoir (Welch et al., 1990; Ridge and Barrett, 1992; Everall and Lees, 1997; Barrett et al., 1999; Caffrey and Monahan, 1999). The efficacy of straw applications in these studies was assessed either by comparing algal growth in treated waters with that upstream of the application or by making pre- and post-treatment comparisons of algal growth at the same location. As these authors point out, the lack of replication and absence of legitimate controls in these studies make definitive conclusions concerning the effectiveness of field applications of barley straw difficult. In the current study, although phytoplankton biomass (as measured by Chl a) declined in ponds treated with barley straw, similar declines were seen in ponds that received no straw. Likewise, observations of floating filamentous algal mats made at the time of phytoplankton samplings indicated a general decline in surface coverage by mats throughout the summer in both treated and control ponds. These simultaneous declines in biomass, coupled with considerable between-pond variation in both treated and control groups, cannot be used to support the premise that barley straw inhibited the growth of algae in these systems. Similarly, Kelly and Smith (1996) were unable to demonstrate that barley straw retarded algal growth in a small, eutrophic Scottish loch.
The dosage employed in this study (112 kg ha 1) is at the lower limit of recommended dosages for small ponds (Newman, 1999; Butler et al., 2001; Lembi, 2002). It may be that greater amounts of straw in treated ponds would have resulted in more easily discernable differences in chlorophyll a levels when compared with control ponds. Future field studies of the effect of rotting barley straw on algal growth need to be designed in ways that evaluate system-to-system variation as well as allow for comparisons with simultaneously run controls. Field experiments that employ replicate experimental ponds (e.g. Nicholls and Taylor, 1995) or mesocosms deployed in natural systems would provide these opportunities. 4.4. Conclusion The current study and results of previous researchers (Kelly and Smith, 1996; Martin and Ridge, 1999; Terlizzi et al., 2002) challenge the view that barley straw is an effective broad-spectrum treatment for nuisance algae. Rather, this work suggests that barley straw may be of value in the treatment of specific algae. Selective inhibition and stimulation of algal species suggests barley straw treatment may alter the species composition of phytoplankton communities.
Acknowledgements We thank Irene Ridge for helpful discussions of this work. Financial support was provided by the University of Maryland College of Agriculture and Natural Resources and the Whitaker Foundation.
References Ball, A.S., Williams, M., Vincent, D., Robinson, J., 2001. Algal growth control by a barley straw extract. Bioresour. Technol. 77, 177–181. Barrett, P.R.F., Newman, J.R., 1992. Algal growth inhibition by rotting barley straw (Abstract). Br. Phycol. J. 27, 83–84. Barrett, P.R.F., Curnow, J.C., Littlejohn, J.W., 1996. The control of diatom and cyanobacterial blooms in reservoirs using barley straw. Hydrobiologia 340, 307–311. Barrett, P.R.F., Littlejohn, J.W., Curnow, J., 1999. Long-term algal control in a reservoir using barley straw. Hydrobiologia 415, 309– 313. Brownlee, E.F., Sellner, S.G., Sellner, K.G., 2003. Effects of barley straw (Hordeum vulgare) on freshwater and brackish phytoplankton and cyanobacteria. J. Appl. Phycol. 15, 525–531. Butler, B.R., 1998. Examination of the effects of barley straw (Hordeum vulgare) on freshwater algae in the field and laboratory. MS thesis; Hood College, Frederick, MD, USA. Butler, B., Terlizzi, D., Ferrier, D., 2001. Barley straw: a potential method of algae control in ponds. Publication No. UM-SG-MAP2001-02. Maryland Sea Grant Extension Program, College Park, MD.
M.D. Ferrier et al. / Bioresource Technology 96 (2005) 1788–1795 Caffrey, J.M., Monahan, C., 1999. Filamentous algal control using barley straw. Hydrobiologia 415, 315–318. Casitas Municipal Water District, 1987. Current methodology for control of algae in reservoirs. AWWA Research Foundation, American Water Works Association, Denver, CO. Choe, S., Jung, I., 2002. Growth inhibition of freshwater algae by ester compounds released from rotted plants. J. Ind. Eng. Chem. 8, 297– 304. Everall, N.C., Lees, D.R., 1996. The use of barley straw to control general and blue-green algal growth in a Derbyshire reservoir. Wat. Res. 30, 269–276. Everall, N.C., Lees, D.R., 1997. The identification and significance of chemicals released from decomposing barley straw during reservoir algal control. Wat. Res. 31, 614–620. Gangstad, E.O., 1986. Freshwater Vegetation Management. Thomas Publications, Fresno, CA. Gibson, M.T., Welch, I.M., Barrett, P.R.F., Ridge, I, 1990. Barley straw as an inhibitor of algal growth II: laboratory studies. J. Appl. Phycol. 2, 241–248. Hoehn, R.C., 1998. Biological aspects of taste and odor problems in drinking water (abstract). AWWARF Taste and Odor Workshop, Chicago, IL. Available from:
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Newman, J., 1999. Control of algae with straw. Information Sheet 3. IACR—Centre for Aquatic Plant Management. Sonning, Berkshire, UK. Newman, J.R., Barrett, P.R.F., 1993. Control of Microcystis aeruginosa by decomposing barley straw. J. Aquatic. Plant Manag. 31, 353–355. Nicholls, K.H., Taylor, R.G., 1995. Experimental use of barley straw for algae control in Ontario ponds (Abstract). Lake Reserv. Manage. 11, 175. Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York. Pillinger, J.M., Cooper, J.A., Ridge, I., Barrett, P.R.F., 1992. Barley straw as an inhibitor of algae growth III: the role of fungal decomposition. J. Appl. Phycol. 4, 353–355. Pillinger, J.M., Cooper, J.A., Ridge, I., 1994. Role of phenolic compounds in the antialgal activity of barley straw. J. Chem. Ecol. 20, 1557–1569. Rice, E.L., 1986. Allelopathic growth stimulation. In: Putnam, A.R, Tang, C.-S. (Eds.), The Science of Allelopathy. John Wiley and Sons, New York. Ridge, I., Barrett, P.R.F., 1992. Algal control with barley straw. Aspects Appl. Biol. 29, 457–462. Ridge, I., Pillinger, J.M., 1996. Towards understanding the nature of algal inhibitors from barley straw. Hydrobiologia 340, 301–305. Ridge, I., Walters, J., Street, M., 1999. Algal growth control by terrestrial leaf litter: a realistic tool. Hydrobiologia 395/396, 173–180. Terlizzi, D.E., Ferrier, M.D., Armbrester, E.A., Anlauf, K.A., 2002. Inhibition of dinoflagellate growth by extracts of barley straw (Hordeum vulgare). J. Appl. Phycol. 14, 275–280. Vymazal, J., 1995. Algae and Element Cycling in Wetlands. Lewis Publishers, Boca Raton, FL. Welch, I.M., Barrett, P.R.F., Gibson, M.T., Ridge, I., 1990. Barley straw as an inhibitor of algae growth I: studies in the Chesterfield Canal. J. Appl. Phycol. 2, 231–239.