Hydrobiologia (2005) 551:147–157 J.N. Beisel, L. Hoffmann, L. Triest & P. Usseglio-Polatera (eds), Ecology and Disturbances of Aquatic Systems DOI 10.1007/s10750-005-4457-y
Springer 2005 Response of Elodea nuttallii (Planch.) H. St. John to manual harvesting in the North-East of France Fiorant Di Nino*, Gabrielle Thiébaut & Serge Muller Laboratoire de Biodiversite´ & Fonctionnement des Ecosyste`mes, Universite´ de Metz, Avenue Ge´ne´ral Delestraint, 57070, Metz, France (*Author for correspondence: E-mail: fiorant_dinino@yahoo.fr) Key words: invasive aquatic plant, Elodea nuttallii, morphological traits, stream, management Abstract Elodea nuttallii (Planch). H. St John is an introduced aquatic macrophyte which was first observed in France in the early 1950s. The impact of two frequencies of harvesting on the biomass and regrowth strategy of this invasive species was evaluated by assessment of morphological traits monthly from February to October 2003. The effect of this management on the floristic biodiversity was also analysed. Harvesting caused a drastic reduction of biomass of E. nuttallii. Two harvests caused almost total disappearance of E. nuttallii. Furthermore, no significant difference was observed in the architecture of E. nuttallii between an unharvested site and harvested site. In one year, harvest did not allow the development of native aquatic plants. Introduction As a result of the increased influence of man on aquatic systems, many waterways in the world have become eutrophic and unwanted growth of aquatic invasive vegetation has become a considerable problem. Native to temperate North America, Elodea nuttallii (Planch.) H. St John was first introduced into Europe in 1939 (Wolff, 1980; Simpson, 1984) and has received far less investigations into its biology than other invasive species. In Europe, E. nuttallii was first identified in 1955 (Sell, 1959). Only female plants were observed, introduced certainly via the trade in live aquarium plants (Cook & Urmi-Köning, 1985), legal or otherwise. Apparently, E. nuttallii is actively spreading in many parts of Europe and seems to be replacing Elodea canadensis Michaux in many localities (Mériaux & Géhu, 1979; Simpson, 1990; Thiébaut et al., 1997; Barrat-Segretain, 2001; Tremp, 2001; Demierre & Perfetta, 2002). Dispersal has mostly been by stem fragments floating downstream. Vegetative buds are more easily distributed between catchments than stem fragments by wildlife. The continued spread of E. nuttallii is likely encouraged by eutrophication (Grime, 1988). E. nuttallii grows in still or slow flowing eutrophic waters. It is often found in species poor macrophyte communities subject to boat traffic, management and in eutrophic ditches. It is tolerant of disturbance, oil pollution, metal pollution and salinity up to 14 per thousand (Sabbatini & Murphy, 1996; BarratSegretain, 2001; Newman, 2001). Its important biomass varied from 500 to 800 g Dry Weight/m2 in lakes (Kunii, 1984; Ozimek et al., 1990). Dense stands of macrophytes have several negative consequences on the balance of the hydrosystem, for example the decomposition of E. nuttallii at the end of the growth season inducing a secondary eutrophication. Conducing to an intense bacterial metabolism produces anoxic, reducing conditions, which results in decreased 148 rates of mineralization and in the accumulation of fermentation endproducts that are toxic to many plants (Santamaria, 2002). Jones et al. (1996) established that the stands of E. nuttallii greatly restricted water movement which, together with the plantÕs photosynthetic and respiratory activity, resulted in a highly structured water column with very steep dissolved gas and pH gradients through the stands. The impact of the spread of E. nuttallii on biodiversity was relatively unknown. Finally, invasion of E. nuttallii caused very important economic problems. Effectively the important biomass produced by E. nuttallii modifies water flow, often increases the risk of adjacent land flooding, causes disagreements for human activities (navigation, fishing, tourism) and induces important cost for the management (Demierre & Perfetta, 2002). In many bodies of water, it has been necessary to control overabundant aquatic plants. There are several methods of managing aquatic plants: mechanical or manual harvesting, biological control, changing the aquatic environment and chemical control. The management techniques chosen must be appropriate both to the type of weed problem and to the uses and function of the body water. Chemical control (Diquat and Acrolein) are used in New South Wales or in Australia (Cook & Urmi-Köning, 1985; Bowmer et al., 1995), but it does not solved the problem of the secondary eutrophication. That is why Newman (2001) suggested that remove by mechanical means following by application of herbicide (Diquat) or a biological control option by using Grass Carp (Ctenopharyngodon idella), were the best options in England. However several herbicides seem to require long contact time for effective control, making management difficult in flowing waters (Bowmer et al., 1995), and grass carp consumption also lead to eutrophication because fits inefficient digestion of macrophyte material. To regulate the spreading of E. nuttallii in Lake Léman, harvest is used (Demierre & Perfetta, 2002). To our knowledge, no research on the impact of harvest of E. nuttallii in flowing shallow waters has been done. To evaluate the impact of harvesting on the invasive E. nuttallii and precisely investigate the process of regrowth, an approach based on measurements of morphological traits was used. In this paper, we aim to determine: (i) the impact of the number of harvests on E. nuttallii regrowth, (ii) which regrowth strategy E. nuttallii adopts, through measurement of morphological traits, (iii) the impact of harvest of E. nuttallii stands on the floristic biodiversity. Materials and methods Study area The study was performed in the Vosges mountain, in the Northern Vosges (NE France). The landscape pattern consists of sandstone mountains of 200–580 m in altitude topped by rock conglomerate, surrounded by steep cliffs. The regional climate is sub continental. Winters are cold, with more than 100 days of frost and an annual temperature of 8.6 C. Summer is relatively hot. The mean rainfall is 900 mm. The streams are subject to eutrophication (Muller, 1990; Thiébaut & Muller, 1998). The mean sources of pollution are fish farms and domestic sewage. A biomonitoring of flowing waters by aquatic macrophytes was realized since 1993 (Thiébaut & Muller, 1998, 1999). The invasive species E. nuttallii colonized the streams of this area since the end of 1970s (Muller, 1990; Thiébaut & Muller, 1999). The population of E. nuttallii are clonal in Northern Vosges streams (Di Nino, 2002). The sampling sites located in the Falkensteinbach stream (49 1¢ N, 7 23¢ E), were characterized by overabundance of E. nuttallii (mean cover percentage visually estimated between 70 and 90% in July by imaging a birdÕs eye view of the channel). A 100 m length of stream was chosen. Two spot-checks (Reference site, experimental site E divided in two sub-units: E1 and E2) located at 45 m intervals (buffer zone) were selected (Fig. 1). Materials Elodea is a genus of perennials with submerged leaves and floating flowers. The leaves are in whorls of 3 and sessile. Leaves usually folded along the midrib, somewhat recurved, with undulate margins. E. nuttallii over winters as prostrate shoots which start to regenerate new lateral shoots 149 Figure 1. Description of the experimental site. as the temperature reaches 10 C (Kunii, 1981, 1982). The shoots grow rapidly towards the surface without branching when they form a densely branched canopy (Fig. 2). Physical features (width, water velocity, depth) and aquatic vegetation were recorded monthly from February to October 2003 at each site (Reference site, experimental sites E1 and E2). 24 h after sample collection). Alkalinity was determined by titration (AFNOR, 1990). Conductivity and pH were measured using a combined glass electrode and corrected for temperature (25 C). Reactive soluble phosphorus and ammonia were analysed using spectrophotometer (single reagent ascorbic acid technique for phosphorus, and indophenolÕs technique for ammonia, AFNOR, 1990). Samples for nitrate, sulfate and chloride analyses were determined in the laboratory with ion chromatography. Chemical survey of the water Experimental protocol In mid-stream, 500 ml of water were collected monthly from the end of February to the end of October 2003. Analyses were performed immediately upon returning to the laboratory (less than The factor tested was the number of harvests: Physical features – one total harvest was practised on E1 and E2 on February 26, 150 Figure 2. Diagram illustrating E. nuttallii and its morphological traits. – a second total harvest was realised on E2 on May 26. In the east of France, E. nuttallii starts to regenerate at the end of February. Its low biomass in February favours the harvest (Kunii, 1984; Di Nino, 2002). A preliminary study showed that fragmentation of the plant begins in June in Vosges mountain (Di Nino, 2002), we choose May for the second harvest to reduce the dispersion of the species. During the harvest, to avoid the dispersal by floating stem fragments, a netting was placed a few metres downstream the experimental area. After the harvest, regrowth and biomass production were surveyed each month until the end of experiment (October 26). Biomass production Ten plots (0.2 m2 area/plot) were randomly placed each month in each site (reference, E1 and E2). The vegetation of plot was dug out manually by species. E. nuttallii was weighted separately. Three replicates of E. nuttallii were dried at 65 C for 3 days. Results were expressed in Dry Weight/m2. Regrowth strategy Thirty plants were collected each month in each site (reference, E1 and E2). Apical shoots of 3 cm length, corresponding to the optimal growth area, was cut off. Lateral shoots included the initial lateral which developed from the nodes on the apical original shoot and the others lateral which was a development either from the same nodes, or from the nodes on the lateral shoots (Kunii, 1981). Nine morphological traits were measured of each plant by a ruler (Fig. 2): – trait 1: Main shoot length – 2: Lateral shoot length (initial + secondary shoots) – 3: Number of lateral shoots (initial shoot) – 4: Length of total shoot (main + lateral) – 5: Density. It corresponded to the ratio between dried biomass of the plant and length of total shoot. – 6: Length of ten internodes after the cut of 3 cm apex. A preliminary statistical study showed that leaves from the sixth whorl is the most representative leaf of the ten internodes (Di Nino, 2002). – 7: Length of a leaf located at the sixth whorl – 8: width of a leaf located at the sixth whorl – 9: Surface of a leaf located at the sixth whorl. One leaf on this sixth whorl is cut, fixed on a paper with sailor tape. Surface was calculated by using logician Scion image V. 1.63. Statistical analysis Data were analysed using Minitab. After the verification of the normal distribution of the 151 parameter and homogeneity of variance, ANOVA were used to show difference between population and evolution during the seasonal growth. The significance level for each comparison was adjusted according to them by the Bonferroni method to p < 0.05. Results Chemical characteristics of the water The water was neutral (pH = 6.95 ± 0.12), buffered (alkalinity = 291 ± 29 leq/l), low mineral content (conductivity = 71 ± 6 lS/cm). Sampling sites were characterised by a high nitrogen concentration (NNH+ and 4 = 109 ± 40 lg/l) a moderate concentration of phosphate (PPO3) 4 = 37 ± 10 lg/l). During the experimental period, these chemical characteristics were stable (Table 2). Physical features The total surface of the harvested sites was 150 m2 (30 m length · 5 m width) against 170 m2 (36 m length · 4.70 m width) for the reference site. At the beginning of the experiment, the main physical features of the two sampling sites (E1, E2) and reference site were homogenous (Table 1). In the end of summer, depth was higher in reference site than in the two harvested sites, whereas the mean flow velocity was lower. The flow velocity and the depth of the two harvested sites were similar after May (Table 1). Impact of harvesting on the biomass and the regrowth of E. nuttallii Biomass production The lowest biomass was measured in March (DW = 10 g/m2), whereas the highest was obtained in August (DW = 822 g/m2) in the reference site. The harvest had a significant impact on the production of biomass. There was a significant difference in the biomass produced among one harvest and two harvests. The second harvest in May reduced the biomass of E. nuttallii to a mean Table 1. Mean physical features of the experimental site Physical features Depth (m) Flow velocity (m s)1) Month Reference site E1 (one harvest February E2 (two harvest Feb 03 and 03) May 03 Mini Maxi Mean value Mini Maxi Mean value Mini Maxi Mean value 26/2/03 0.10 0.70 0.35 ± 0.13 0.12 0.61 0.39 ± 0.14 0.12 0.58 0.32 ± 0.10 26/3/03 26/4/03 0.10 0.01 0.70 0.65 0.35 ± 0.13 0.31 ± 0.16 0.12 0.12 0.61 0.53 0.39 ± 0.14 0.30 ± 0.13 0.12 0.12 0.58 0.43 0.32 ± 0.10 0.26 ± 0.10 26/5/03 0.08 0.65 0.38 ± 0.16 0.15 0.60 0.33 ± 0.12 0.05 0.42 0.27 ± 0.09 26/6/03 0.10 0.87 0.42 ± 0.20 0.15 0.50 0.30 ± 0.10 0.18 0.42 0.27 ± 0.08 26/7/03 0.10 0.90 0.49 ± 0.19 0.18 0.50 0.31 ± 0.06 0.10 0.40 0.28 ± 0.07 26/8/03 0.15 1.02 0.53 ± 0.21 0.20 0.51 0.33 ± 0.1 0.15 0.51 0.32 ± 0.11 26/9/03 0.10 0.90 0.45 ± 0.22 0.10 0.40 0.26 ± 0.09 0.18 0.48 0.27 ± 0.10 26/10/03 0.12 1.06 0.45 ± 0.23 0.08 0.55 0.32 ± 0.12 0.08 0.40 0.28 ±0.10 26/2/03 26/3/03 0.40 0.40 0.40 0.40 0.40 ± 0.00 0.40 ± 0.00 0.40 0.40 0.40 0.40 0.40 ± 0.00 0.40 ± 0.00 0.40 0.40 0.40 0.40 0.40 ± 0.00 0.40 ±0.00 26/4/03 0.32 0.43 0.39 ± 0.06 0.24 0.45 0.34 ± 0.11 0.24 0.45 0.34 ± 0.11 26/5/03 0.22 0.62 0.43 ± 0.17 0.37 0.45 0.42 ± 0.05 0.37 0.45 0.42 ± 0.05 26/6/03 0.26 0.30 0.27 ± 0.02 0.25 0.30 0.28 ± 0.03 0.25 0.30 0.28 ± 0.03 26/7/03 0.27 0.34 0.30 ± 0.04 0.33 0.40 0.36 ± 0.04 0.33 0.40 0.36 ± 0.04 26/8/03 0.25 0.33 0.28 ± 0.04 0.32 0.40 0.37 ± 0.04 0.32 0.40 0.37 ± 0.04 26/9/03 0.26 0.32 0.30 ± 0.03 0.32 0.40 0.36 ± 0.04 0.32 0.40 0.36 ± 0.04 26/10/03 0.37 0.48 0.42 ± 0.06 0.36 0.40 0.38 ± 0.02 0.36 0.40 0.38 ± 0.02 152 Table 2. Physico-chemical composition of water pH Conductivity Alkalinity P-PO3) 4 NNH+ 4 NNO)3 SSO2) 4 Cl) (lS/cm) (leq/l) (lg/l) (lg/l) (mg/l) (mg/l) (mg/l) 26/2/03 6.97 74 250 15 121 0.72 9.94 5.92 26/3/03 26/4/03 6.98 7.01 71 61 254 314 41 31 193 74 0.57 0.57 10.45 9.75 5.94 5.82 26/5/03 6.99 71 320 45 115 0.48 9.25 5.39 26/6/03 6.99 69 285 33 126 0.59 9.85 5.77 26/7/03 7.13 85 308 48 97 0.36 8.22 5.36 26/8/03 6.70 69 260 41 50 0.54 8.39 5.74 26/9/03 6.93 71 308 40 105 0.48 8.88 5.73 26/10/03 6.85 68 318 37 97 0.60 9.60 5.63 Mean value Std 6.95 0.12 71 6 291 29 37 10 109 40 0.55 0.10 9.37 0.75 5.70 0.21 level of 14 g DW/m2 in July in E2 against 120 g DW/m2 in E1 and 565 g DW/m2 in the reference site. No stands of E. nuttallii were found after July in site E2 (Table 3). Only some individuals were present. Regrowth strategy Significant differences in morphological traits appeared among the dates for five traits (1, 2, 3, 4 and 6). A significant reduction of the length response (traits 1, 2, 3, 4, 6) was observed in the two experimental sites in August (ANOVA, p < 0.05). These morphological traits were the highest in August and September in reference site (Fig. 3). Relationships between species after the regrowth At the beginning of the study, the biodiversity was low. Elodea nuttallii was the dominant species. Four other species were recorded: Elodea canadensis, Ranunculus peltatus, Callitriche platycarpa and Fontinalis antipyretica in less than 1% of the stream. At the end of the experimental period, the cover percentage of native macrophytes did not increase. The exotic E. canadensis disappeared in the harvested sites and F. antipyretica was not found (Table 4). The decrease of E. nuttallii stands did not allow the development of native aquatic plants such as R. peltatus. Table 3. Biomass production Month Discussion Dry weight g/m2 Reference E1 (one harvest E2 (two harvest site February 03) Feb 03 and May 03) 26/2/03 5 5 5 26/3/03 10 2 2 26/4/03 90 2 2 26/5/03 51 32 32 26/6/03 26/7/03 330 565 180 120 1 14 26/8/03 822 54 1 26/9/03 610 101 0 26/10/03 567 60 0 Mean value (n = 10). Impact of harvesting on the biomass and regrowth of E. nuttallii No significant difference was established for biological traits after one or two harvests. Our results corroborated partially the conclusions of Abernethy et al. (1996) that showed no significant change for length response after one cut and only 44% reduction after two cuts. Harvests caused no morphological change in the architecture of regrown plants in our area, except in August. In August, a significant reduction of growth of plants was established. E. nuttallii appeared as a Figure 3. Morphology on the regrown plants of E. nuttallii. Temporal changes of nine different morphological traits: trait 1: main shoot length; 2: lateral shoot length; 3: number of lateral shoots (initial + secondary shoots); 4: length of total shoot (main + lateral); 5: density; 6: length of ten internodes; 7: length of a leaf located of the sixth whorl; 8: width of a leaf located of the sixth whorl; 9: surface of a leaf located of the sixth whorl. The significance level for each comparison was adjusted according to the Bonferroni method ( p < 0.05) and indicated by the letters (A, B, C, D). 153 154 Table 4. Aquatic vegetation survey Month Vegetation cover (%) Reference site E1 (One harvest February 03) E2 (Two harvest Feb 03 and May 03) Species: E. nuttallii E. canadensis Ranunculus Callitriche E. nuttallii E. canadensis Ranunculus Callitriche E. nuttallii E. canadensis Ranunculus Callitriche peltatus platycarpa & peltatus platycarpa & peltatus platycarpa & C. hamulata C. hamulata C. hamulata 26/02/03 20 1 0 0 20 1 0 0 20 1 0 0 26/03/03 40 1 0 0 3 0 0 0 3 0 0 0 26/04/03 20 1 4 4 3 0 0 2 3 0 0 2 26/05/03 20 1 4 4 20 0 2 5 20 0 2 5 26/06/03 60 1 0 2 35 0 0 2 5 0 0 2 26/07/03 70 26/08/03 90 1 1 0 0 1 4 35 15 0 0 0 0 2 0 5 3 0 0 0 0 2 0 26/09/03 80 1 0 4 20 0 0 0 5 0 0 0 26/10/03 70 1 0 2 15 0 2 2 3 0 2 2 Estimation of vegetation cover in percent. 155 disturbance-tolerant species. The plant did not adopt the prostrate form characteristic of overwintering in the end of experiment in October in Northern Vosges stream. E. nuttallii grows on yearly cycle in Northern Vosges streams. The biomass response of Elodea was more marked in our area (reduction of 94 and 100% after one and two harvests, respectively) than in the study of Abernethy et al. (1996), which measure biomass reductions of 41 and 59% after one and two cuts, respectively. In our study, the maximum of biomass was obtained in August in accordance with literature data (Kunii, 1984; Best & Dassen, 1987; Newman, 2001). After July, biomass will be reduced by washout in the experimental sites E1 and E2 and in lesser extend in reference site. Harvesting induced modification of physical characteristics of the stream. The stream, overrun with sand in harvested sites, was characterized by a highest water velocity and lowest depth. However, dense stands of E. nuttallii reduced flow velocity in reference site. Relationships between E. nuttallii and other species Differences in biological traits of the two Elodea species E. canadensis and E. nuttallii are particularly important to consider in the analysis of the invasive or competitive success of the species (Williamson, 1996). Barrat-Segretain et al. (2002) showed few differences in traits (regeneration and colonisation of vegetative fragments, resistance to water current, herbivory) between the two Elodea species. The displacement of E. canadensis by E. nuttallii as usually observed in field could not be explained by morphological traits or by physiological differences (Jones et al., 2000). For example, no clear differences in photosynthetic behaviour were observed between the Elodea species (James et al., 1999). However, the species E. nuttallii seems to be less sensitive to ammonium and had higher phosphorus storage ability than E. canadensis (Rolland & Trémolières, 1995; Robach et al. 1995). It had a higher growth rate than E. canadensis both in field and under laboratory conditions (Simpson, 1990; Eugelink 1998). An invading species such as E. nuttallii may be able to exploit the unused resource even though its ecology is not fundamentally different from that of the native species Callitriche platycarpa. Thiebaut & Muller (2003) showed that Elodea nuttallii had higher phosphorus storage ability than C. platycarpa in Northern Vosges streams. A competition for resources between native species (C. platycarpa, R. peltatus) and alien species such as E. nuttallii was suggested in our streams (Garbey et al., 2003; Thiébaut & Muller, 2003). The spread of E. nuttallii seems to be the cause of the disappearance of Myriophyllum alterniflorum, in Northern Vosges stream (Thiebaut et al., 1997) and the regression of Potamogeton compressus in lake Kawaguchi (Nagasaka et al., 2002). However, the loss of biodiversity induced by E. nuttalliiÕs spread was not clearly established. These results are in concordance with the study of Tremp (2001). Is harvest an efficient tool to manage E. nuttallii? The kind and biomass of plants vary in different aquatic environments – canals, streams, rivers, lakes, ponds marshes and wetlands. The use to which a body of water is being put determines the management objectives, and whether there is a need for the management or control of aquatic plants. There is a choice between total control and some form of selective control. Elodea appeared to be less susceptible to cutting-based weed control measures than Myriophyllum spicatum, a native species (Abernethy et al., 1996). From the practical management point of view, the results of the study of Garbey et al. (2003) imply that the disturbance-causing weed control measure will tend to favour species with stronger disturbance – tolerant strategies, such as E. nuttallii. Newman (2001) considered that the effectiveness of mechanical control depended on the date of the harvest. During June, the roots of E. nuttallii die and in September the plant attains maximum biomass. For him, cutting before the end of June will require a second cut later in the season and to limit the amount of biomass required to be harvested it is also necessary to cut before September. Sabbatini & Murphy (1996) using a multivariate approach, showed that E. nuttallii has a strong tolerance of management based on disturbance, such as cutting. Cutting, specially mechanical control, could induce a reduction of the biomass 156 of indigenous plants and allow Elodea to spread to new areas because harvest break up the plant. However harvesting can be quite useful in areas where the weed is already established as in Northern Vosges streams, or when the weed will disperse into areas unfavourable to its survival (Bowmer et al., 1995). An other solution was to do nothing and to ‘‘wait and see’’. After a spreading period, E. canadensis became rare in our area. E. nuttallii will probably have a similar invasion pattern than E. canadensis. A noticeable decline in E. nuttallii indeed was also reported after the peak of the outburst in JapanÕs lake (Nagasaka et al., 2002). E. nuttallii populations exhibited a genetic uniformity that made them vulnerable to attack by fungi or pathogens. However, eutrophication increases E. nuttalliiÕs invasibility. Growth of E. nuttallii was favoured by nitrogen level (Ozimek et al., 1990, 1993; Best et al., 1996). No environmental factor could limit the spread of E. nuttallii in our area. Conclusion Harvesting caused a drastic reduction of biomass of E. nuttallii. After two harvests E. nuttallii almost disappeared. However, no effect of harvest was observed on the architecture of regrown plants except in August. In the end of the year, the impact of harvest on biodiversity was low and did not favour the development of native aquatic plants. Further work is needed to improve our knowledge to estimate the ecological risk of harvesting on biodiversity and on ecosystem function. The risk of adverse side-effects for users of the water and for the ecosystem health must always be taken into account. Accordingly, aquatic weed management system must be developed which are socially and environmentally acceptable. Acknowledgements The assistance of Muriel Julita was greatly appreciated. This study was funded by the Northern Vosges Biosphere Reserve. This project is sponsored by the French Ministry of Ecology and Sustainable Development Program ‘‘Biological Invasions’’. References Abernethy, V. J., M. R. Sabbatini & K. J. Murphy, 1996. Response of Elodea canadensis Michx. and Myriophyllum spicatum L to shade, cutting and competition in experimental culture. Hydrobiologia 340: 219–224. Association Française de NORmalisation (AFNOR), 1990. Recueil de normes françaises. Eaux. Méthodes dÕessais. 4 ème ed. Paris. Barrat-Segretain, M. -H., 2001. Invasive species in the Rhône River floodplain (France): replacement of Elodea canadensis Michaux by E. nuttallii St. John in two former river channels. Archiv fur Hydrobiologie 152: 237–251. Barrat-Segretain, M. -H., A. Elger, P. Sagnes & S. Puijalon, 2002. Comparison of three life-history of invasive Elodea canadensis Michx and Elodea nuttallii (Planch) H. St. John. Aquatic Botany 74: 299–313. Best, E. P. & J. H. A. Dassen, 1987. A seasonal study of growth characteristics, and the levels of carbohydrates and proteins in Elodea nuttallii, Polygonum amphibium and Phragmites australis. Aquatic Botany 28: 353–372. Best, E. P. H., H. Woltman & F. H. H. Jacobs, 1996. Sedimentrelated growth limitation of Elodea nuttallii as indicated by a fertilization experiment. Freshwater Biology 36: 33–44. Bowmer, K. H., S. W. L. Jacobs & G. R. Sainty, 1995. Identification, Biology and Management of Elodea canadensis, Hydrocharitaceae. Journal of Aquatic Plant Management 33: 13–19. Cook, C. D. K. & K. Urmi-König, 1985. A revision of the genus Elodea (Hydrocharitaceae). Aquatic Botany 21: 111– 156. Demierre A., & J. Perfetta, 2002. Gestion du faucardage des macrophytes sur les rives genevoises du Léman (Suisse). Proceedings of the 11th EWRS International Symposium on aquatic Weeds, Moliets et Maâ (France), Septembre 2–6 septembre 2002, 345–347. Di Nino, F., 2002. Caractérisation morphogénétique des élodées de Lorraine et de la Plaine dÕAlsace. Univesité de Metz (France). DEA Toxicologie de lÕEnvironnement, 41 pp. Eugelink, A. H., 1998. Phosphorus uptake and active growth of Elodea canadensis Michx. and Elodea nuttallii (Planch.) St. John. Water Science and Technology 37: 59–65. Garbey C., G. Thiébaut, S. Muller, 2003. Impact of manual spring harvesting on the regrowth of a spreading aquatic plant: Ranunculus peltatus Schrank Archiv fur Hydrobiologie 156(2): 271–286. Grime, J. P., 1988. The CRS model of primary plant strategies: origins, implications, and tests. In L. D. Gottlieb & S. K. Jain (eds), Plant Evolutionary Biology. Chapman & Hall, London, 371–393. James, C. S., J. W. Eaton & K. Hardwick, 1999. Competition between the three submerged macrophytes, Elodea canadensis Michx, Elodea nuttallii (Planch.) St. John and Lagarosiphon major (Ridl.) Moss. Hydrobiologia 415: 35–40. Jones, J. I. & K. J. W. Hardwick Eaton, 1996. Diurnal carbon restrictions on the photosynthesis of dense stands of Elodea nuttallii (Planch.) St. John. Hydrobiologia 340: 11–16. Jones, J. I. & J. W. K. Eaton Hardwick, 2000. The effect of changing environmental variables in the surrounding water 157 on the physiology of Elodea nuttallii. Aquatic Botany 66: 115–129. Kunii, H., 1981. Characteristics of the winter growth of detached Elodea nuttallii (Planch) St. John in Japan. Aquatic Botany 11: 57–66. Kunii, H., 1982. The critical temperature for the active growth of Elodea nuttallii (Planch.) St. John. Japanese Journal of Ecology 32: 111–112. Kunii, H., 1984. Seasonal growth and profile structure development of Elodea nuttallii (Planch.) St.John in pond OjagaIke, Japan. Aquatic Botany 18: 239–247. Meriaux, J. -L., & J. -M., Gehu, 1979. Réactions des groupements aquatiques et subaquatiques aux changements de lÕenvironnement. Epharmonie 1979. Tüxen, Cramer in der A.R Gantner Verlag Kommanditgesellschaft, 121–142. Muller, S., 1990. Une séquence de groupements végétaux bioindicateurs dÕeutrophisation croissante des cours dÕeau faiblement minéralisés des Basses Vosges gréseuses du Nord. Comptes Rendus de lÕAcadémie des Sciences Paris 310: 509–514. Nagasaka, M., K. Yoshizawa, K. Ariizumi & K. Hirabayashi, 2002. Temporal changes and vertical distribution of macrophytes in Lake Kawaguchi. Oecologia 3: 107–114. Newman, J., 2001. NuttallÕs pondweed. Centre for Aquatic Plant Management information 28. Ozimek, T., R. Gulati & E. van Donk, 1990. Can macrophytes be useful in biomanipulation of lakes? The lake Zwemlust example. Hydrobiologia 200/201: 399–407. Ozimek, T., E. Van Donk & R. D. Gulati, 1993. Growth and nutrient uptake by two species of Elodea in experimental conditions and their role in nutrient accumulation in a macrophyte-dominated lake. Hydrobiologia 251: 13–18. Rolland, T. & M. Tremolières, 1995. The role of ammonium in the distribution of two species of Elodea. Acta Botanica Gallica 142: 733–739. Robach, F., I. Hajnsek, I. Eglin & M. Tremolières, 1995. Phosphorus sources for aquatic macrophytes in running waters:water or sediment?. Acta botanica Gallica 142: 719–731. Sabbatini, M. R. & K. J. Murphy, 1996. Submerged plant survival strategies in relation to management and environmental pressures in drainage channel habitats. Hydrobiologia 340: 191–195. Santamaria, L., 2002. Why are most aquatic plants widely disturbed? Dispersal, clonal growth and small-scale heterogeneity in a stressfull environment. Acta Oecologica 23: 137–154. Sell, Y., 1959. Étude comparative de quelques espèces du genre Elodea à propos de lÕapparition à Strasbourg et ses environs dÕune espèce nouvelle pour lÕEurope continentale. Bulletin de lÕAssociation Philomatique dÕAlsace Lorraine 10: 121–133. Simpson, D. A., 1984. A short history of the introduction and spread of Elodea Michx. in The British Isles. Watsonia 15: 1–9. Simpson, D. A., 1990. Displacement of Elodea canadensis Michx. by Elodea nuttallii (Planch.) St. John in the British Isles. Watsonia 18: 173–177. Thiébaut, G. & S. Muller, 1998. The impact of eutrophication on aquatic macrophyte diversity in weakly mineralised streams in the Northern Vosges mountains (N-E, France). Biodiversity and Conservation 7: 1051–1068. Thiébaut, G. & S. Muller, 1999. A macrophyte communities sequence as an indicator of eutrophication and acidification levels in weakly mineralised streams in North-Eastern France. Hydrobiologia 410: 17–24. Thiébaut, G. & S. Muller, 2003. Linking phosphorus pools of water, sediment and macrophytes in running waters. International Journal of Limnology 39: 307–316. Thiébaut, G., T. Rolland, F. Robach, M. Trémolières & S. Muller, 1997. Quelques conséquences de lÕintroduction de deux espèces de macrophytes, Elodea canadensis Michaux et Elodea nuttallii St. John, dans les écosystèmes aquatiques continentaux:exemple de la Plaine dÕAlsace et des Vosges du Nord (Nord-Est de la France). Bulletin Français de la Pêche et de la Pisciculture 344/345: 441–452. Tremp, H., 2001. Standörtliche Differenzierung der Vorkommen von Elodea canadensis Michx.und Elodea nuttallii (Planch.) St. John in Gewässern der badischen Oberrheinebene Ber. Inst. Landschafts- Pflanzenökologie Univ. Hohenheim 10: 19–32. Williamson, M., 1996. Biological Invasions. Chapman and Hall, London. Wolff, P., 1980. Die Hydrilleae (Hydrocharitaceae) in Europa. Gött. Flor. Rundbr 14: 33–56.