AOBPreview originally published online on August 21, 2003
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Annals of Botany 92: 547-556, 2003
© 2003 Annals of Botany Company
Exposure to Asulox Inhibits the Growth of Mosses
,11 School of Biological Sciences, 3.614 Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK and 2 Natural History Museum, Cromwell Road, London SW7 5BD, UK
* For correspondence: Fax: 0161-2753938, e-mail l.sheffield{at}man.ac.uk Present address: Manchester Metropolitan University. Department of Environmental and Geographical Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK
Received: 9 October 2002;; Returned for revision: 21 November 2002. Accepted: 13 June 2003; Published electronically: 21 August 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Asulox is a herbicide used to control bracken. Its effects on mosses were investigated to ascertain whether exposure proved as detrimental as found in parallel studies on pteridophytes. Mature gametophytes of 18 mosses were exposed to a range of concentrations of Asulox under standard conditions and the effects on growth monitored. Plants were cut to a standard length, exposed to Asulox solution for 24 h, grown for 3 weeks and total elongation (main stem and branches) measured. EC50 values were calculated and species ranked according to sensitivity. The effects of exposure on total elongation were compared with those on main stem elongation alone. Under the conditions tested, the total elongation of all species was inhibited after exposure to Asulox. The amount of elongation observed after exposure was different for different species and inhibition of elongation occurred at different exposure concentrations. A single regression equation was not adequate to describe the dose response curves of all species tested. An ability to produce secondary branches may confer increased tolerance to Asulox exposure. It is concluded that mosses suffer detrimental effects after exposure to Asulox at concentrations similar to those that affect fern gametophytes such as bracken.
Key words: Asulox, asulam, bryophyte, moss, growth, elongation, response curves, hormesis.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bryophytes have a global distribution and play an important role in ecosystem development and function (Tan and Pocs, 2000). They are the primary form of carbon storage in many northern ecosystems (O’Neill, 2000) and are important in nutrient sequestration, water retention, the regulation of soil temperature and pH (Vitt, 2000). Mosses have been used as experimental models; for example, Syntrichia ruralis (Hedw.) F. Weber & D. Mohr (Oliver et al., 2000) and Physcomitrella patens (Hedw.) Bruch & Schimp. (Cove et al., 1997), and as biomonitors and bioindicators of heavy metal pollution (e.g. Markert et al., 1996a, b; Siebert et al., 1996). They have proved invaluable in investigations on the effects of atmospheric deposition of nitrogen and sulfur-containing compounds on uplands (for a review, see Bates, 2000). Brown et al. (1986), Mabb (1989) and Newmaster et al. (1999) all reported significant effects of exposure of mosses to the herbicides dichlorophen, paraquat, 2,4-D, ferrous sulfate, trichlor and glyphosate but, in general, the effects of herbicides on moss growth and survival have been little studied and are poorly understood. The effects of changing land management practices on native species and biodiversity have become clearer recently (for an overview, see Hindmarch and Pienkowski, 1997), and a decline in arable field species of bryophytes has been noted (Smith, 2001). The potential effects of agricultural herbicides on bryophyte communities has therefore been identified as of critical importance (Porley, 2001).
Asulam [methyl (4-aminophenyl sulfonyl) carbamate] is a systemic herbicide used extensively in many parts of the world to control the spread of bracken (Pteridium aquilinum (L.) Kuhn) (Rhone-Poulenc, undated). It is applied as the water-soluble sodium salt Asulox by helicopter, ground-based vehicles or hand-operated knapsack sprayers (Rhone-Poulenc, undated). Asulox has been approved for large-scale aerial use since 1974 (Soper, 1996) and current figures for aerial spraying with Asulox in Britain are between 5000 and 8000 ha per annum, the majority of which occurs in Scotland and northern England (Pakeman et al., 2000). Field application rate is 4400 gai (grams active ingredient) ha–1, equivalent to approx. 100 gai l–1 for aerial spraying. Application with a wetting agent is recommended by the manufacturer (Rhone-Poulenc, undated), but local practice varies (N. Hawkings-Byass, pers. comm.).
The effects of Asulox on plants has been studied in field-based, glasshouse and laboratory experiments over the past 25 years. Ferns have been shown to be particularly sensitive to Asulox exposure in drift (Marrs and Frost, 1996), overspray (Horrill et al., 1978; Sheffield et al., 2003) and solution (Keary et al., 2000; Sheffield, 2002). There has been no recent work on the effects of Asulox on bryophytes, but early field experiments indicated that mosses differ markedly from each other in their sensitivity to the herbicide (Horrill et al., 1978). The ubiquitous nature of bryophytes and their substantial presence as part of the biodiversity within and around bracken stands (Rodwell, 1991, 1992; Sheffield et al., 2003) means that it is imperative to establish (a) whether all bryophytes are similarly sensitive and (b) whether invasive, keystone and other important species are more or less sensitive than bracken to Asulox exposure.
The extent of exposure to herbicide of non-target species under field conditions depends on many factors. These include the climatic conditions at the time of application, the size and angle of incidence of the spray droplets and the situation of the non-target plants (Hawkings-Byass, 2000; Robinson and Page, 2000). Habitat structure often precludes some of the most sensitive species from exposure and the combination of information on inherent sensitivity and likelihood of exposure can provide a basis for the estimation of the risk of exposure to specific plants (Robinson and Page, 2000). Identifying the inherent sensitivity of species to Asulox exposure is fraught with difficulties but attempts have been made. Breeze et al. (1992) calculated ED10 and ED50 values for 14 angiosperms exposed to single droplets of Asulox. Sheffield (2002) and Keary et al. (2000) found eight ferns to be more sensitive to Asulox than the target fern bracken, and similar experiments by Sheffield et al. (2003) ranked Rumex acetosa L., a commonly used bioassay subject in Asulox field trials, to be more sensitive than Agrostis capillaris L. or Holcus lanatus L.
The aim of this study was to expose mature gametophytes of a wide variety of mosses to a range of Asulox concentrations under controlled, fully defined conditions. The null hypotheses were (a) that exposure to Asulox would have no effect on the total elongation of the species tested and (b) that all species would be similarly sensitive to Asulox exposure. A secondary aim was to determine whether susceptibility could be linked to growth form and/or an ability of the moss species to produce secondary branches.
The approach was adapted from that used by Keary et al. (2000) for the exposure of fern gametophytes. The objectives were to (a) assess the mosses after exposure to Asulox and categorize their relative sensitivity and (b) to relate sensitivity to particular growth forms, phylogeny and ecology. The study comprised two experiments carried out in succession, one with a 3-week and the other with a 6-week growing period following exposure to Asulox.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Eighteen species of mosses were collected from various locations in Britain as listed in Table 1. Details of taxonomy and ecology are presented in Table 2. Species identifications were verified by F. J. Rumsey (NHM) or S. R. Edwards (MANCH) and voucher specimens placed in MANCH. Plants were stored hydrated at 4 (±2) °C in sealed containers for a maximum of 5 months until used.
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Experiment 1: assessment of responses to 24-h Asulox exposure on moss explants after 3 weeks growth
Experiment 1 was carried out May–August 2000. For all species, healthy shoots were selected, apical regions were cut to standard lengths to include the majority of photosynthetic material and, where present, secondary branches were removed. The explants were exposed to a minimum of five of a possible 11 aqueous concentrations of Asulox (see Table 1) always including a control of de-ionized water (0 gai l–1 Asulox) to ensure that the plants grew under the conditions used. Ten explants per flask were immersed in 100 ml Asulox solution (without addition of a wetting agent) on an orbital shaker (100 rpm) for 24 h, then washed in copious amounts of de-ionized water. The explants were grown for 3 weeks on green shade netting (hole size: 4 x 7 mm), over filter paper saturated with de-ionized water in sealed wavin culture dishes (Lab Associates, The Netherlands) at 23 (±2) °C (75 µmol m–2 s–1 PAR, 16/8 h cycle) with small ventilation holes (approx. 1 mm) in the lid. Pleurocarpous species were laid flat on the netting, acrocarps were inserted upright through the holes. The explants were sprayed five times a week with a solution of artificial rainwater (adapted from Meade, 1982) to provide mineral nutrients. Excess solution was drained before new was added. After 3 weeks the total elongation of each explant (main stem and branch elongation) was measured with a ruler. Measurements of total elongation were used as an indication of bryophyte response to Asulox treatment as pilot experiments showed this to be a parameter inhibited by Asulox exposure that generated reproducible measurements for a wide range of species (Lawton, 2000). EC50 values were calculated to compare between species’ sensitivity to Asulox. As the data were continuous (i.e. growth, rather than mortality data) the EC50 values were defined as the concentration at which elongation was 50 % of the control plants (Forbes, 1993).
Experiment 2: assessment of responses to 24-h Asulox exposure on different moss growth forms
Experiment 2 was undertaken March–June 2001. The methods followed those of Experiment 1, except that the explants were grown for 6 weeks after exposure to Asulox, in some cases different initial explant lengths were used and the plants were watered with artificial rainwater solution five times during the first week and thereafter with de-ionized water four times a weeks and with rainwater solution once weekly. All species were exposed to the same eight Asulox concentrations between 0 and 12·5 gai l–1. An exposure rate of 100 gai l–1 was not used, as none of the species survived that exposure rate in Experiment 1. At the end of the experiment, main stem elongation and total elongation (main stem and branch elongation) were measured with a ruler.
For both experiments, the length of explant used, numbers of replicates and exposure concentrations of Asulox solution are indicated in Table 1.
Statistical analysis
Experiment 1.
Elongation data for each species were analysed separately by one-way ANOVA with Tukey HSD post-hoc tests (for error degrees of freedom, see Table 1). EC50 values were calculated using two methods. The first method was a linear regression technique, where the data were first expressed as proportion inhibition compared with the control response and then probit transformed. The transformed data were plotted against log10 concentration and a linear regression analysis performed (OECD, 1984; Forbes, 1993). As probit transformation can only be performed on data values >0 and <1, those points 
0 and 
1 were substituted with 0·001 and 0·999, respectively. The linear regression analysis could not be performed on two species (Cratoneuron filicinum and Eurhynchium praelongum). The second method was a non-linear regression technique. Logistic curves were fitted to the data according to Seber and Wild (1989) and Seefeldt et al. (1995). The upper and lower asymptote were fixed at the mean control values and zero respectively. Non-linear regression analysis could not be performed on two species (Cratoneuron filicinum and Rhytidiadelphus squarrosus). EC50 estimates, confidence limits and R2 values are shown in Table 3.
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Experiment 2.
Main stem elongation and total elongation data for each species were analysed separately by one-way ANOVA with randomized block design and Tukey HSD post hoc tests (for error degrees of freedom, see Table 1).
All analyses were carried out using either SPSS 10.1 or SYSTAT 10 statistical packages.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Experiment 1
All species tested showed a significant (P < 0·001) decrease in total elongation compared with the controls at a minimum of one Asulox concentration and the majority failed to grow after exposure levels of about 10 gai l–1 Asulox, but the response between 0 and 10 gai l–1 was different for different species (see Fig. 1). One species (W. fluitans) showed a significant increase in elongation compared with the controls at 2 gai l–1 Asulox (P < 0·05) before a significant decrease in elongation was observed at concentrations of 8 gai l–1 and above (P < 0·001). Explants for all species with severely inhibited elongation also showed signs of physical damage. Their stems often lacked chlorophyll, appearing yellow or brown and were soft to the touch. Severely affected explants were prone to disintegration with handing. Growth of the majority of control plants was firm, healthy and green.
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For most of the species tested, the probit-transformed linear regression explained the dose response best. However, the response of five species was better explained by logistic curves (see Table 3). The range of predicted EC50 values was similar for both techniques (0·1–9 gai l–1) with the most (P. commune) and least (W. flutians) sensitive species consistently predicted. Values for species of intermediate sensitivity were broadly but not exactly consistent between the models.
Experiment 2
H. jutlandicum, E. praelongum, R. squarrosus and C. introflexus all produced a substantial number of side branches during the 6-week growing period, where as P. commune produced very few. Three of the five species tested showed main stem elongation to be more severely affected by Asulox exposure than total elongation, with significant differences from the control plants occurring at lower exposure concentrations (Fig. 2). Of these, two were pleurocarps (R. squarrosus and H. jutlandicum) and one was an acrocarp (C. introflexus). P. commune (acrocarp) showed main stem and total elongation to be equally affected by Asulox exposure, whilst E. praelongum (pleurocarp) showed no significant effects of exposure at all.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Inhibition of total elongation and dose response curves
Exposure to Asulox inhibited the total elongation of all of the moss species tested in the first experiment. The amount of total elongation produced after Asulox exposure was different for different species and inhibition of total elongation occurred at different exposure concentrations.
The inability to fit a single regression model to all species tested is in line with work of previous authors (e.g. Breeze et al., 1992), and highlights the problems associated with the direct comparison of single values, such as EC50, to indicate absolute species’ sensitivity. A number of factors can influence dose response data, e.g. initial health and size of the test plants, measurements taken, exposure time, plant density and the penetration rate of the toxin (see Breeze et al., 1992; Humphry et al., 2001), and there are no obvious explanations for the different response curves determined herein. While the regression methods employed were unable to determine consistent EC50 values for those species of intermediate sensitivity, the most and least sensitive species and the effective range of concentration were consistently predicted between methods (see Table 3). The lack of congruity for species of intermediate sensitivity is likely to be due to variability of the data or insufficient concentration resolution. The disparity in sensitivity between moss species subjected to herbicide exposure concurs with results reported in Horrill et al. (1978), Atkinson et al. (1980) and by Brown (1992).
Evidence of hormesis
W. fluitans was the only species to show a significant increase in elongation after exposure to Asulox. This response is an example of hormesis—the stimulation of growth at low levels of toxins or stress. Hormesis has been reported in a large number and a wide range of toxicological studies, including the effects of herbicides on plants (Stebbing, 1998; Calabrese et al., 1999; Schabenberger et al., 1999; Parsons, 2001). The phenomenon is not well understood, but has been attributed to low levels of potential toxins or stress causing a perturbation and then an overcompensation of the mechanisms controlling the measurable response. Deleterious effects have subsequently been observed at higher exposure levels (e.g. Stebbing, 1998; Calabrese et al., 1999).
Ecological, morphological and phylogenetic influences
The differences in the responses of the 18 moss species to Asulox exposure are not co-incident with a single ecological or morphological factor. The more sensitive species tended to be those with a preference for wet habitats (e.g. Sphagnum spp., P. commune), but the aquatic species W. fluitans was the most tolerant tested (see Table 3). It is worthy of note that both Sphagnum and Polytrichum species are phylogenetically distant from other species of moss (Newton et al., 2000) and the differences that have led to this taxonomic distance could be a factor in explaining their relative sensitivity to Asulox exposure.
Polytrichum species have prominent lamellae on their ventral leaf surfaces (Scheirer and Dolan, 1983) which increases the relative surface area (Thomas et al., 1996). The lamellar margins are wax-coated to prevent the uptake of surface water, but contain small parallel openings (diameter approx. 0·6–7·8 µm) to allow for gas exchange (Thomas et al., 1996). The saturation of inter-lamellar spaces of P. commune after vacuum infiltration has been reported (Thomas et al., 1996) and it is suggested that the 24-h exposure time used in this experiment could result in the flooding of the inter-lamellar spaces, with a consequent increase in surface area exposed and hence sensitivity to Asulox. In these experiments, no wetting agent was added to the Asulox solution. Addition of a wetting agent would be likely to increase the permeability of the herbicide through any surface wax, thereby potentially increasing sensitivity to exposure.
Polytrichum species have a well-developed hydroid and leptoid system, which efficiently transports dissolved solutes to all regions of the plant (Scheirer, 1983). The anionic and water-soluble Asulox solution could be expected to be transported through the plant via the hydroids, and effective internal transport may also be a factor in the sensitivity of P. commune to Asulox.
The high cation exchange capacity (CEC) of Sphagnum (Clymo, 1963) is unlikely to have a large influence on the effect of Asulox, as this is applied in the anionic form (Rhone-Poulenc, undated). Mabb (1989) reported that in experiments on R. squarrosus, anionic herbicides do not bind to the cell walls in large quantities and that their action appeared to be dependent on immediate uptake into cells. The porose cells of the Sphagnaceae, however, greatly increase the surface area adjacent to living cells directly in contact with solution (Smith, 1978), and thus effective surface area exposed to Asulox.
Of the five species tested in Experiment 2, three showed main stem elongation to be more sensitive to Asulox exposure than total elongation. P. commune did not produce prolific branches and was highly sensitive to exposure. R. squarrosus, H. jutlandicum and E. praelongum are pleurocarps with highly branching growth forms. E. praelongum showed no effects of exposure compared with the control plants. The difference in sensitivity of this species between the two experiments is suggested to be due to discrepancies in experimental procedure such as storage time, time of collection, initial explant length and growth period. R. squarrosus and H. jutlandicum, however, both showed stem elongation to be more susceptible to Asulox exposure than total elongation. C. introflexus is an acropcarp with a prolific ability to produce branches from the main stem, and a reputation as a non-native invasive species in the northern hemisphere (Hill et al., 1992). The results of Experiment 2 suggest, first, that not all potential meristems are inhibited by 24-h exposure to low concentrations of Asulox and, secondly, that the ability to produce secondary branches, rather than growth form per se, may confer increased tolerance to Asulox.
Comparison with laboratory experiments
The exposure methods used herein entailed total immersion in herbicide solution, the aim of which was to establish whether all species responded in the same manner after exposure to Asulox under strictly controlled and reproducible conditions. All of the moss species tested herein showed the first detrimental effects of Asulox exposure between concentrations of 0·01 and 10 gai l–1 and most species did not grow after exposure to 10 gai l–1 Asulox. This indicates that, under identical test conditions, mosses suffer detrimental effects after exposure to Asulox at concentrations similar to those that affect grass and R. acetosa seedlings, and the fern gametophytes tested by Keary et al. (2000), Sheffield (2002) and Sheffield et al. (2003).
Relevance to field exposure
The current study, Keary et al. (2000) and Sheffield (2002) all exposed moss or fern gametophytes in Asulox solution. Field exposure to Asulox would generally be in the form of spray droplets and thus the effective field dosage of Asulox received per plant is likely to be considerably less than that received by immersion in solution. While the dominant life form of ferns is the sporophyte, the dominant form for mosses is the gametophyte. Although direct comparisons with field exposure cannot be made from these data, the results from laboratory exposed moss gametophytes are more relevant to field conditions than the laboratory exposed fern gametophytes. Given that the sensitivity of fern sporophytes under field conditions has been demonstrated (Horrill et al., 1978), and until adequate field trials on the effects of Asulox on bryophytes are undertaken, it is suggested that mosses are potentially sensitive to Asulox exposure under field conditions.
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ACKNOWLEDGEMENTS |
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We thank Roderick Robinson for his helpful advice and guidance, Bayer CropScience for providing the Asulox, United Utilities for allowing collection of material and J. G. Duckett, J. W. Bates and D. H. Brown for helpful comments on an earlier version of this manuscript. Funding for this project was provided by English Nature, with whom J.R. holds a Natural Environment Research Council (UK)/CASE studentship.
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