Aquatic Botany 81 (2005) 245251 www.elsevier.

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Growth limitation of Lemna minor due to high plant density

Steven M. Driever, Egbert H. van Nes *, Rudi M.M. Roijackers
Department of Environmental Sciences, Aquatic Ecology and Water Quality Management Group, Wageningen University, P.O. Box 8080, NL-6700 DD Wageningen, The Netherlands Received 4 March 2004; received in revised form 11 October 2004; accepted 6 December 2004

Abstract The effect of high population densities on the growth rate of Lemna minor (L.) was studied under laboratory conditions at 23 8C in a medium with sufcient nutrients. At high population densities, we found a non-linear decreasing growth rate with increasing L. minor density. Above a L. minor biomass of ca. 180 g dry weight (DW) m2, the net growth rate became negative. At a density of 9 g DW m2, a maximum relative growth rate of ca. 0.3 d1 was found. At very low densities (<9 g m2), we observed an inverse density dependence (or Allee effect). Probably, this lower growth rate was due to lower local temperatures within such partly covered L. minor decks. On the basis of these experimental results and literature data, a simple model was created. To test the model, the density of duckweed in three different Dutch ditches was monitored for 9 weeks in spring. Within this period, full coverage of the ditches by duckweed was reached. The maximum density increased with rising air temperature. The model described the eld data well, suggesting that crowding is an important factor in limitation of duckweed growth. # 2005 Elsevier B.V. All rights reserved.
Keywords: Lemnaceae; Crowding; Biomass; Growth rate; Model; Inverse density dependence

1. Introduction In eutrophic ditches and ponds, duckweeds (Lemnaceae) often form dense oating mats (Landolt, 1986). The biodiversity of such systems is usually low, as the water under
* Corresponding author. Tel.: +31 317 482733; fax: +31 317 484411. E-mail address: egbert.vannes@wur.nl (E.H.van. Nes). 0304-3770/$ see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2004.12.002

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Lemnaceae mats often becomes too anoxic for sh and macrofauna to survive (Janse and Van Puijenbroek, 1998). Due to competition for light, also submerged macrophytes usually cannot coexist with Lemnaceae. The duckweed mats may be persistent and it is suggested that Lemnaceae dominance is a self-stabilizing state (Scheffer et al., 2003). In (sub)tropical areas, other free-oating plants such as water hyacinth (Eichhornia crassipes Solms) can form an even larger threat to biodiversity (Mehra et al., 1999). To control free-oating Lemnacea, insight in the growth dynamics is necessary. Several abiotic factors have been studied intensively such as nutrients and temperature. Lemnacea need high phosphorus and nitrogen loadings (Portielje and Roijackers, 1995). With increasing temperature, the growth rate increases approximately linearly up to an optimum (Landolt, 1986). Duckweed may deplete nutrients (Scheffer et al., 2003) and can change conductivity and pH of the water (McLay, 1976). This way they change their own growth conditions (Landolt and Kandeler, 1987). Relatively little attention has been paid to cause of intraspecic competition within mats of Lemnacea and the effect on their growth. We studied the effect of crowding on the growth rate of Lemna minor in the laboratory. L. minor was grown in different densities, varying from low to high, in a medium with sufcient nutrients. From the results of this experiment, a simple model was constructed to explore the factors involved in growth of L. minor. To validate the model, we monitored three Lemna-dominated ditches near Wageningen (The Netherlands) for 9 weeks.

2. Materials and methods 2.1. Crowding experiment The growth rate of L. minor was determined under laboratory conditions (23 8C, a 14-h photoperiod and an irradiance of 180 mmol m2 s1 PAR). The plants were grown on a liquid medium based on Smart and Barko (1985), optimised for Lemnacea by Szabo et al. (2003). A series of different densities was used (5.5, 9.5, 90, 180 and 915 g dry weight (DW) m2). For each treatment, six replicates were applied. The initial biomass was determined as fresh weight. The plants were placed in vertical cylinders (height 10 cm, diameter 5.9 cm), which were placed in 2-l aquaria lled with medium (Szabo et al., 2003). After day 4, the cylinders were placed in a basin with fresh medium. After day 7, the experiment was stopped and the fresh weight and dry weight (24 h at 70 8C) of L. minor were measured. The initial dry weight was calculated using the dry weight to fresh weight ratio at the end of the experiment. The relative growth rate was calculated assuming exponential growth. 2.2. Model A simple model was constructed to describe the effect of crowding, temperature and nutrients: dB B r f T; B; N; P l B dt (1)

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The variation in time of the biomass of L. minor (B in g DW m2) was modelled as the function of the maximum growth rate (r). The gross production was modied by a limitation function ( f(T, B, N, P)), which was a function of air temperature (T), biomass (B) and nutrients (N and P). Furthermore, the production was corrected for the loss (l), which included mortality, predation and respiration. The limitation function ( f(T, B, N, P)) was dened as: f T; B; N; P T Tmin N P hB Topt Tmin N hN P hP B hB (2)

Temperature (T) limitation was assumed to be linear from the minimum temperature (Tmin, 5 8C) up to the optimum temperature (Topt, 26 8C) (Landolt, 1986; Landolt and Kandeler, 1987). Nutrient limitation of ammonia and nitrate (N) and ortho-phosphate (P) were modelled as Monod-type functions, with the following half saturation values: hN = 0.04 mg N l1 and hP = 0.05 mg P l1 (Luond, 1980). The limiting effect of biomass was simply assumed to be another Monod-type function dependent on biomass B and with a half saturation hB, which was determined during this study. 2.3. Field observations Three ditches in the surroundings of Wageningen, The Netherlands, were selected. In all ditches L. minor was present at the start of the monitoring period. For a period of 9 weeks (AprilJuly 2003) biomass was measured in approximately 14-days intervals using stratied sampling. The water surface of the ditch was divided by eye into three strata, i.e. 020%, 2180% and 81100% coverage. The strata were drawn on a map and within each stratum, 10 random sampling coordinates were drawn. The biomass in the stratum with 0 20% coverage was neglected. Duckweed was sampled using a method after McLay (1974). A 10 cm 10 cm gauze covered iron square was positioned horizontally under the L. minor cover. The square was lifted up through the cover of plants. All biomass not accounting for L. minor was removed by hand and dry weight was determined (24 h at 70 8C). Water samples for chemical analyses of N and P were taken at the last three sampling dates. NNO3 + NNO2, NNH4+ and PPO43 were analysed using a Technicon Autoanalyser II. Air temperature data were obtained from a nearby weather station.

3. Results 3.1. Crowding Growth rates of L. minor decreasing with increasing density (Fig. 1). The highest growth rate of 0.30 d1 was observed at a biomass of 10 g DW m2. Remarkably, the lowest biomass (5 g DW m2) had a signicantly lower growth rate of 0.23 d1 (MannWhitney P < 0.008). The highest densities of 180 g DW m2 and 915 g DW m2 showed a negative net growth rate of 0.02 and 0.08 d1, respectively. These experimental data were used to calibrate the model, assuming no nutrient limitation. The maximum growth rate, r, was

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Fig. 1. Growth rate as a function of the initial biomass of L. minor (g DW m2). Dots indicate the measured growth rate. The solid line represents the curve described by the model at a constant temperature of 23 8C.

obtained by extrapolation and was corrected for the optimum temperature of 26 8C (0.41 d1). The half saturation constant, hB, (26 g DW m2) was calculated from the equilibrium biomass. The resulting model was used to describe the net relative growth for different biomasses (Fig. 1). 3.2. Field Fig. 2 shows the eld data and model prediction for each ditch. Growth rate, r, was tted for each ditch separately assuming different limiting factors for each ditch. With an increase in air temperature (day 4247; Fig. 2), the duckweed biomass in all ditches increased, as the model predicted. For f N (N) and f P (P), the assumption was made that nutrients were not limiting (Table 1), supported by the fact that L. minor was present at the start of the sampling period.

4. Discussion Using a combination of a laboratory-scale experiment and a simple model, we obtained insight in the growth dynamics of L. minor in the eld. The laboratory experiment showed the relation between crowding and growth rate. We were able to model eld growth in Dutch ditches, suggesting that we captured the main processes in the model. Yet several processes were neglected or oversimplied in the model. For instance, the model assumed that the plants were homogenous distributed over the ditch. In reality, this is usually not true because of the inuence of birds and wind (Dufeld and Edwards, 1981). Indeed the distribution of L. minor in the sampled ditches was very heterogeneous, also within the three strata. In the model the loss, l, was assumed to be constant for all ditches (0.05), which equals a lifetime of about 35 days, a realistic value for individual fronds (Landolt, 1986). The loss included respiration, grazing and mortality implicitly. It was neglected that respiration is

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Fig. 2. Biomass (g DW m2) of L. minor in three ditches and maximum air temperature (8C) from day 0 (17 April 2003) to day 63 (18 June 2003). Field data are indicated as black squares, open triangles and black dots for Opheusden, Zetten and Sinderhoeve, respectively with standard errors (N = 10). Model output is shown as a dashed and dotted line, dashed line and solid line for Opheusden, Zetten and Sinderhoeve, respectively. Maximum air temperature is indicated by the dotted line.

strongly dependent on temperature. Differences between ditches in grazing pressure by birds and invertebrates were not known and could not be accounted for in the mortality rates. The inuences of temperature, crowding and decomposition on mortality are unknown. In our model, we used air temperature instead of water temperature. It is known that temperature can vary widely between water, air and within oating mats (Dale and Gillespie, 1976), so we assumed that the temperature of the fronds in the upper layers is better described by the maximum air temperature than by the water temperature. Despite these simplications, the negative effect of crowding on growth rate was accurately described in the model. The density dependent reduction of growth rate was
Table 1 Characteristics of the ditches Characteristic Length (m) Width (m) Depth (m) Sediment NNH4+ (mg l1) NNO3 (mg l1) PPO43 (mg l1) Sinderhoeve 40.0 3.0 1.6 Sand 0.07 (0.03) 0.05 (0.05) 0.42(0.56) Zetten 45.5 1.83.0 0.5 Clay 0.08 (0.01) 0.04 (0.03) 0.51 (0.68) Opheusden 48.0 0.7 0.4 Clay 0.14(0.10) 0.99(1.38) 1.62 (0.65)

The nutrient levels are mean values for the last three sampling dates.

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clearly not linear, like in logistic growth, but it decreased approximately logarithmically. It could well be described as a Monod-type growth limitation by biomass. The mechanism causing this density dependency is not completely clear. In a dense mat, fronds are piled up in several layers. One could expect that in such case layers can be subdivided into two parts: an upper part with nutrient limitation and a lower part with light limitation (Clatworthy and Harper, 1962) or CO2 limitation. However, since we observed only decompositon in the lower parts, it seems not very likely that nutrient limitation of the upper part was a major factor. The laboratory experiments suggested that there is an inverse density dependence at low densities. In waters partly covered by L. minor (biomass below 9.5 g DW m2), the relative growth rate increased signicantly with increasing Lemna density. A likely explanation for this effect seems to be the increase of temperature in a closed deck, due to solar radiation (Dale and Gillespie, 1976). In this way, there is facilitation at low densities once there is full coverage, i.e. the higher temperature within the mat will increase the relative growth rate. For other oating plants, a similar facilitation may occur. For instance, the tropical oating Salvenia molesta is known to increase temperature locally (Room and Kerr, 1983).

Acknowledgements We thank Gertie Arts and Dick Belgers from Alterra (Wageningen, NL) for useful suggestions and discussions and Frank van Herpen, who helped a great deal with the practical work.

References
Clatworthy, J.N., Harper, J.L., 1962. Comparative biology of closely related species living in same area. 5. Interand intraspecic interference within cultures of Lemna spp. and Salvinia natans. J. Exp. Bot. 13, 307324. Dale, H.M., Gillespie, T., 1976. Inuence of oating vascular plants on diurnal uctuations of temperature near water surface in early spring. Hydrobiologia 49, 245256. Dufeld, A.N., Edwards, R.W., 1981. Predicting the distribution of Lemna spp.in a complex system of drainage channels. In: Proceedings of the Association of Applied Biologists Conference Aquatic Weeds and their Controls, pp. 5965. Janse, J.H., Van Puijenbroek, P.J.T.M., 1998. Effects of eutrophication in drainage ditches. Environ. Pollut. 102 (Suppl. 1), 547552. Landolt, E., 1986. Biosystematic Investigations in the Family of Duckweeds (Lemnaceae) (vol. 2), The Family of LemnaceaeA Monographic Study, vol. 1. Veroff. Geobot. Inst.ETH, Zurich. Landolt, E., Kandeler, R., 1987. Biosystematic Investigations in the Family of Duckweeds (Lemnaceae) (vol.4), The Family of the LemnaceaeA Monographic Study, vol. 2. Veroff. Geobot. Inst. ETH, Zurich. Luond, A., 1980. Effects of nitrogen and phosphorus upon the growth of some Lemnaceae. In: Landolt, E. (Ed.), Biosystematic Investigations in the Family of Duckweeds (Lemnaceae), vol. 1. Veroff. Geobot. Inst. ETH Zurich, Zurich, pp. 118141. McLay, C.L., 1974. The distribution of duckweed Lemna perpusilia in a small Southern California lake: an experimental approach. Ecology 55, 262276. McLay, C.L., 1976. The effect of pH on the population growth of three species of duckweed: Spirodela oligorrhiza Lemna minor and Wolfa arrhiza.. Freshwater Biol. 6, 125136.

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Mehra, A., Farago, M.E., Banerjee, D.K., Cordes, K.B., 1999. The water hyacinth: an environmental friend or pest? A review. Resour. Environ. Biotechnol. 2, 255281. Portielje, R., Roijackers, R.M.M., 1995. Primary succession of aquatic macrophytes in experimental ditches in relation to nutrient input. Aquat. Bot. 50, 127140. Room, P.M., Kerr, J.D., 1983. Temperatures experienced by the oating weed Salvinia molesta Mitchell and their prediction from meteorological data. Aquat. Bot. 16, 91103. Scheffer, M., Szabo, S., Gragnani, A., van Nes, E.H., Rinaldi, S., Kautsky, N., Norberg, J., Roijackers, R.M.M., Franken, R.J.M., 2003. Floating plant dominance as a stable state. Proc. Natl. Acad. Sci. U.S.A. 100, 4040 4045. Smart, R.M., Barko, J.W., 1985. Laboratory culture of submersed freshwater macrophytes on natural sediments. Aquat. Bot. 21, 251263. Szabo, S., Roijackers, R., Scheffer, M., 2003. A simple method for analysing the effects of algae on the growth of Lemna and preventing algal growth in duckweed bioassays. Arch. Hydrobiol. 157, 567575.