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Snail herbivory on submerged macrophytes and nutrient release: Implications for macrophyte management
e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 1664–1667
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/ecoleng
Snail herbivory on submerged macrophytes and nutrient release: Implications for macrophyte management Kuan-Yi Li a,d , Zheng-Wen Liu a,b,∗ , Yao-Hui Hu a , Hong-Wei Yang c,a a
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, 210008, China b Jinan University, Guangzhou 510630, China c Nanjing University, Nanjing 210081, China d Graduate School of Chinese Academy of Sciences, Beijing, 100039, China
a r t i c l e
i n f o
a b s t r a c t
Article history:
Radix swinhoei (H. Adams) is a freshwater snail commonly found in shallow regions of Lake
Received 11 March 2007
Taihu. This research estimated, based on experiments, the consumption rates of R. swin-
Received in revised form
hoei on three young submerged plants (Vallisneria spiralis, Hydrilla verticillata and Potamogeton
20 April 2008
malaianus) and its rates of nutrient release. Results showed that the snails consumed V.
Accepted 2 May 2008
spiralis at the highest rate (23.34 mg g−1 d−1 ), P. malaianus at a lower rate (11.97 mg g−1 d−1 ), and H. verticillata at the lowest rate (7.04 mg g−1 d−1 ). The consumption rates on V. spiralis varied significantly, with snail size, ranging from 13.63 mg g−1 d−1 for large-size snails to
Keywords:
143.42 mg g−1 d−1 for small-size ones. The average nutrient release rates of snails grazing on different macrophytes were 45.93 g
Snail Grazing
PO4 -P and 0.58 mg NH4 -N g−1 d−1 . The food species had a significant effect on NH4 -N release
Nutrient release
rates but not on PO4 -P. However, the snail size had a significant effect on PO4 -P release
Submerged plants
rates and not on NH4 -N. The present study indicates that through selective grazing and nutrient release, snails may impose a significant impact on the macrophyte community, which should be considered in managing the macrophytes of a lake. © 2008 Elsevier B.V. All rights reserved.
1.
Introduction
Submerged macrophytes play important roles in freshwater ecosystems (Scheffer et al., 1993; Rai et al., 1995; Jeppesen et al., 1998; Kemp et al., 2000). Their growth can be affected by both biotic and abiotic factors, such as herbivory and nutrients (Carpenter and Lodge, 1986). Snails are common invertebrates ´ in aquatic ecosystems (Lodge, 1985; Pieczynska et al., 1999; Lewis, 2005). Their herbivory can directly affect aquatic plant ´ growth (Pieczynska, 2003; Elger and Lemoine, 2005; Carlsson and Lacoursière, 2005; Li et al., 2005). Selective grazing and associated nutrient regeneration can affect the taxonomic
∗
Corresponding author. Tel.: +86 25 86882103; fax: +86 25 57714759. E-mail address: [email protected] (Z.-W. Liu). 0925-8574/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2008.05.009
composition of aquatic macrophytes in lakes (Underwood, 1991; Pinowska, 2002). Radix swinhoei (H. Adams) is a freshwater snail commonly found in Lake Taihu (31◦ 30 N, 120◦ 30 E), a eutrophic shallow lake in China. There are several dense macrophyte beds in the lake. R. swinhoei is associated with aquatic plants (e.g. Hydrilla verticillata, Potamogeton malaianus, Vallisneria spiralis, and Elodea nuttallii). However, there is no information available on the interaction between R. swinhoei and macrophytes in Lake Taihu. In this study, laboratory experiments were designed to (1) measure R. swinhoei consumption rates on three dominant submerged plants in Lake Taihu and (2) measure phosphorus and nitrogen release rates of R. swinhoei in rela-
1665
e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 1664–1667
tion to macrophyte species grazed and snail size. This study will contribute to our understanding of the role of R. swinhoei in freshwater ecosystems.
2.
Materials and methods
The snail R. swinhoei and macrophytes H. verticillata, P. malaianus and V. spiralis used in the experiments were collected from the littoral zone of Lake Taihu. Macrophytes were cultivated and snails were fostered in different outdoor tanks with lake sediments for 1 month before experiments began. Experiments were conducted in laboratory under natural light conditions and water temperature was 26–30 ◦ C.
2.1.
Snail consumption experiments
All macrophytes chosen for our experiments were young, bright green in color, and without apparent damage. After being rinsed to remove epiphytic flora and marl coverage, all plants were placed on bibulous paper for 90 s and weighed. Snails were kept without food for 48 h prior to experiments. Before being introduced into experimental tanks, experimental snails were washed carefully and air-dried for 2 min and fresh weight was determined. The snail consumption rates were estimated from the difference in the initial and final weights of plants exposed to snails in the experiments. Each of the plant leaves (V. spiralis and P. malaianus) or shoots (H. verticillata) was exposed to snails for 36 h in 500 ml of water. There were four replicates of each treatment. To determine whether the snail size affects their consumption rates, V. spiralis leaves were exposed to three sizes of snails (large size: 0.94 g/ind; middle size: 0.38 g/ind; small size: 0.13 g/ind) for 36 h in 500 ml of water. There were three replicates of each treatment.
2.2.
Snail nutrient release experiments
The release rates of orthophosphate phosphorus (PO4 -P) and ammonia nitrogen (NH4 -N) by snails were determined as the difference between the final nutrient concentrations in a beaker with snails and a control beaker without snails. To investigate the effect of macrophyte species grazing on nutrient release, the snails which just had grazed three submerged plants in the consumption experiment were placed in a beaker with 500 ml of distilled water for 3 h, and then the concentration of nutrients of water in the beaker was analyzed. To determine the effect of snail size on their nutrient releases, the various sizes of snails which just had grazed on V. spiralis in the consumption experiments were also placed into a beaker with 500 ml of distilled water for 3 h, and then the nutrient concentration of the water in the beaker was analyzed. There were three replicates and three controls in each experiment. The PO4 -P and NH4 -N were analyzed colorimetrically (Huang et al., 1999).
2.3.
Statistical analyses
All statistical procedures were performed using SPSS software (version 11.5). A t-test was used to analyze differences in snail
Table 1 – Radix swinhoei consumption rates on young macrophytes (p < 0.05, ANOVA) Macrophytes
Snail size (g/ind)
Hydrilla verticillata Potamogeton malaianus Vallisneria spiralis
0.47 ± 0.02 0.49 ± 0.03 0.48 ± 0.05
Consumption rates (mg g−1 d−1 ) 7.04 ± 2.84 11.97 ± 4.61 23.34 ± 9.63
No significant difference in snail size (p > 0.05, t-test). Values are mean ± S.D.
size in each experiment. Data on snail consumption rates and nutrient release rates were analyzed with ANOVA.
3.
Results
3.1.
Snail consumption experiments
V. spiralis was consumed by snails at the highest rate (23.34 mg g−1 d−1 ), followed by P. malaianus (11.97 mg g−1 d−1 ), and H. verticillata (7.04 mg g−1 d−1 ) (Table 1). The consumption rates on V. spiralis varied significantly with snail size, ranging from 13.63 mg g−1 d−1 for large-size snails to 143.42 mg g−1 d−1 for small-size ones (Table 2). There was a negative correlation between the consumption rates and snail size (r2 = 0.70, p < 0.01).
3.2.
Snail nutrient release experiments
Nutrient release rate was highest for snails grazed on V. spiralis (49.77 g PO4 -P and 0.66 mg NH4 -N g−1 d−1 ), intermediate on P. malaianus (45.50 g PO4 -P and 0.55 mg NH4 -N g−1 d−1 ), and lowest on H. verticillata (42.41 g PO4 -P and 0.53 mg NH4 -N g−1 d−1 ) (Table 3). Statistical analyses showed that plant species had a significant effect on NH4 -N release rates (p < 0.05, ANOVA) and no significant effect on PO4 -P release rates (p > 0.05, ANOVA). The size of snail which had fed on V. spiralis had a significant effect on PO4 -P release rates (p < 0.05, ANOVA) and no significant effect on NH4 -N release rates (p > 0.05, ANOVA) (Table 4).
4.
Discussion
The results of this study are in agreement with other studies (Sheldon, 1987; Elger and Lemoine, 2005) showing that living macrophytes can be eaten by snails. In our preliminary experiments, the snail R. swinhoei was observed to consume many
Table 2 – Radix swinhoei consumption rates on Vallisneria spiralis (p < 0.001, ANOVA) Snail size (g/ind) 0.94 ± 0.05 0.38 ± 0.00 0.13 ± 0.01
Consumption rates (mg g−1 d−1 ) 13.63 ± 1.94 39.26 ± 2.64 143.42 ± 18.56
Significant difference in snail size (p < 0.05, t-test). Values are mean ± S.D.
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e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 1664–1667
Table 3 – Nutrient release rates of large-size snail Radix swinhoei (H. Adams) after consuming three plants (NH4 -N, p < 0.05, ANOVA; PO4 -P, p > 0.05, ANOVA) Food species
Snail size (g/ind)
Nutrient release rates NH4 -N
0.94 ± 0.06 0.91 ± 0.05 0.94 ± 0.06
H. verticillata P. malaianus V. spiralis
(mg g−1
d−1 )
0.53 ± 0.02 0.55 ± 0.07 0.66 ± 0.13
PO4 -P (g g−1 d−1 ) 42.41 ± 5.03 45.50 ± 11.29 49.77 ± 1.04
No significant difference in snail size (p > 0.05, t-test). Values are mean ± S.D.
plant species, such as V. spiralis, P. malaianus, P. maackianus, H. verticillata, N. peltatum, T. bispinosa, and can be considered a generalist grazer (Li et al., 2005). Elger and Lemoine (2005) found that the consumption rate of Lymnaea stagnalis varied considerably across eleven macrophyte species, ranging from 11.3 mg g−1 d−1 to 149.4 mg g−1 d−1 . The snail Lymnaea turricula consumed Cladophora sp. at the highest rate (45 mg g−1 d−1 ) and C. demersum at the lowest rate (2 mg g−1 d−1 ) (Pinowska, 2002). In our experiments, the consumption rate of the largesize snail R. swinhoei on three submerged plants ranged from 7.04 mg g−1 d−1 to 23.34 mg g−1 d−1 , but the consumption rate of small-size ones exceeded 180 mg g−1 d−1 . Therefore, the consumption rates were significantly affected by snail size: smaller snails fed more than larger individuals. These results are consistent with Levri and Lively (1996). With selective removal of plant biomass, herbivory of snails might affect plant species composition and diversity. Sheldon (1987) demonstrated that herbivorous snails strongly affected the structure of submerged macrophytes in North American lakes and resulted in the dominance by C. demersum. Carlsson and Lacoursière (2005) found the golden apple snail (Pomacea canaliculata) had a strong negative effect on duckweed (Lemna minor) and water hyacinth (Eichhornia crassipes) growth in field enclosures and mediated a shift from clear water and macrophyte dominance to turbid water and phytoplankton dominance. Our study showed that snail R. swinhoei could graze on aquatic macrophytes from Lake Taihu. However, the herbivorous effect of snails on the freshwater macrophyte communities in Lake Taihu needs further research. The average nutrient release rates of R. swinhoei were 45.93 g PO4 -P and 0.58 mg NH4 -N g−1 d−1 , and these release rates were higher than the rates observed by other authors (Pinowska, 2002; Underwood, 1991) for L. turricula (24.2 g PO4 P and 48.9 g NH4 -N g−1 d−1 ) and Planorbis planorbis (2.9 g PO4 -P and 8.7 g NH4 -N g−1 d−1 ). Snail species, nutrient con-
Table 4 – Nutrient release rates of the various sizes of snail Radix swinhoei (H. Adams) after consuming Vallisneria spiralis (NH4 -N, p > 0.05, ANOVA; PO4 -P, p < 0.05, ANOVA) Snail size (g/ind)
Nutrient release rates NH4 -N (mg g−1 d−1 )
0.94 ± 0.06 0.38 ± 0.00 0.13 ± 0.01
0.66 ± 0.13 0.66 ± 0.15 0.58 ± 0.04
PO4 -P (g g−1 d−1 ) 49.72 ± 1.04 50.41 ± 3.57 68.57 ± 8.39
Significant difference in snail size (p < 0.05, t-test). Values are mean ± S.D.
tent of plant species and environmental conditions (e.g. water temperature) in the experiments might affect nutrient release rates (Underwood, 1991; Brendelberger, 1997; Pinowska, 2002). The snails grazing on V. spiralis had a much higher NH4 -N release rate than those grazing on H. verticillata and P. malaianus, because of the higher consumption rate of V. spiralis, but their PO4 -P release rates were similar. It is puzzling for the low snail consumption rate but similar to PO4 -P release rates for snails grazing on P. malaianus and V. spiralis. It could be that consumed foods might have different nitrogen and phosphorus content (Irons et al., 1988) and the limited ability of snails to break down often refractory food substances can affect the amount of phosphorus assimilated and released (Brendelberger, 1997). In the present experiments, snail size significantly affected the PO4 -P release rates. The small-size snails showed the highest release rate and the large-size ones displayed the lowest release rate. This result is consistent with Pinowska (2002) and can be explained by the snail consumption rates. In fact, the consumption rate on V. spiralis was significantly correlated to the PO4 -P release rate (Tables 2 and 4). On the contrary, the smaller snails showed the lower NH4 -N release rate than the larger ones. This may be related to the nitrogen metabolism of snails, for the excretion of ammonia nitrogen may be regarded as the rate of protein and amino acid catabolism (Widdows, 1978) and invertebrate herbivores are strongly nitrogen-limited (Mattson, 1980). This implies that young snails utilize more nitrogen-rich compounds for their growth than adult ones. Furthermore, diffusion is the principal mode of ammonia excretion in invertebrates since its concentration in the body fluids is considered to be higher than that in the ambient environment (Kinne, 1976). The higher rate of nutrient release in larger individuals could be attributed to the larger surface area for diffusion as compared to the smaller ones (Clarke et al., 1994). Our study indicates that through selective grazing and nutrient release, snails may impose a significant impact on macrophyte community, which should be considered for managing the macrophytes of a lake.
Acknowledgements This research was supported jointly by the National High Technology Research and Development Program (2006AA06Z337) and the Key Project of Chinese Academy of Sciences (KZCX1SW-12). The authors appreciate the constructive suggestions given by Wu Qinglong of Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences.
e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 1664–1667
references
Brendelberger, H., 1997. Determination of digestive enzyme kinetics: a new method to define trophic niches in freshwater snails. Oecologia 109, 34–40. Carlsson, N.O.L., Lacoursière, J.O., 2005. Herbivory on aquatic vascular plants by the introduced golden apple snail (Pomacea canaliculata) in Lao PDR. Biol. Invas. 7, 233–241. Carpenter, S.R., Lodge, D.M., 1986. Effects of submersed macrophytes on ecosystem processes. Aquat. Bot. 26, 341–370. Clarke, A., Thomas, E.P., Whitehouse, M.J., 1994. Nitrogen excretion in the Antarctic limpet Nacella concinna (Strebel, 1908). J. Moll. Stud. 60, 141–147. Elger, A., Lemoine, D., 2005. Determinants of macrophyte palatability to the pond snail Lymnaea stagnalis. Freshwater Biol. 50, 86–95. Huang, X.F., Cheng, W.M., Cai, Q.M., 1999. Survey, Observation and Analysis of Lake Ecology. Standards Press of China. Irons, I.I.I.J.G., Oswood, M.W., Bryant, P.J., 1988. Consumption of leaf detritus by a stream shredder: influence of tree species and nutrient status. Hydrobiologia 160, 53–61. Jeppesen, E., Søndergaard, M., Christoffersen, K. (Eds.), 1998. The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York, p. 423. Kemp, J.L., Harper, D.M., Crosa, G.A., 2000. The habitat-scale ecohydraulics of rivers. Ecol. Eng. 16, 17–29. Kinne, O., 1976. Cultivation of marine organisms. Water quality management and technology. In: Kinne, O. (Ed.), Marine Ecology, vol. III, Part 1. Wiley–Interscience, New York, pp. 79–300. Levri, E.P., Lively, C.M., 1996. The effects of size, reproductive condition, and parasitism on foraging behavior in a freshwater snail, Potamopyrgus antipodarum. Anim. Behav. 51, 891–901.
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Lewis, R.R., 2005. Ecological engineering for successful management and restoration of mangrove forests. Ecol. Eng. 24, 403–418. Li, Y.K., Yu, D., Xu, X.W., Xie, Y.H., 2005. Light intensity increases the susceptibility of Vallisneria natans to snail herbivory. Aquat. Bot. 81, 265–275. Lodge, D.M., 1985. Macrophyte-gastropod associations: observations and experiments on macrophyte choice by gastropods. Freshwater Biol. 15, 695–708. Mattson, W.J., 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11, 119–161. ´ Pieczynska, E., 2003. Effect of damage by the snail Lymnaea (Lymnaea) stagnalis (L.) on the growth of Elodea canadensis Michx. Aquat. Bot. 75, 137–145. ´ Pieczynska, E., Kołodziejczyk, A., Rybak, J.I., 1999. The responses of littoral invertebrates to eutrophication-linked changes in plant communities. Hydrobiologia 391, 9–21. Pinowska, A., 2002. Effects of snail grazing and nutrient release on growth of the macrophytes Ceratophyllum demersum and Elodea canadensis and the filamentous green alga Cladophora sp. Hydrobiologia 479, 83–94. Rai, U.N., Sinha, S., Tripathi, R.D., Chandra, P., 1995. Wastewater treatability potential of some aquatic macrophytes: removal of heavy metals. Ecol. Eng. 5, 5–12. Scheffer, M., Hosper, S.H., Meijer, M.-L., et al., 1993. Alternative equilibria in shallow lakes. Trends Ecol. Evol. 8, 275–279. Sheldon, S.P., 1987. The effects of herbivorous snails on submerged macrophyte communities in Minnesota lakes. Ecology 68, 1920–1931. Underwood, G.J.C., 1991. Growth enhancement of the macrophyte Ceratophyllum demersum in the presence of the snail Planorbis planorbis: the effect of grazing and chemical conditioning. Freshwater Biol. 26, 325–334. Widdows, J., 1978. Physiological indices of stress in Mytilus edulis. J. Mar. Biol. Asso. U. K. 58, 125–142.
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/ecoleng
Snail herbivory on submerged macrophytes and nutrient release: Implications for macrophyte management Kuan-Yi Li a,d , Zheng-Wen Liu a,b,∗ , Yao-Hui Hu a , Hong-Wei Yang c,a a
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, 210008, China b Jinan University, Guangzhou 510630, China c Nanjing University, Nanjing 210081, China d Graduate School of Chinese Academy of Sciences, Beijing, 100039, China
a r t i c l e
i n f o
a b s t r a c t
Article history:
Radix swinhoei (H. Adams) is a freshwater snail commonly found in shallow regions of Lake
Received 11 March 2007
Taihu. This research estimated, based on experiments, the consumption rates of R. swin-
Received in revised form
hoei on three young submerged plants (Vallisneria spiralis, Hydrilla verticillata and Potamogeton
20 April 2008
malaianus) and its rates of nutrient release. Results showed that the snails consumed V.
Accepted 2 May 2008
spiralis at the highest rate (23.34 mg g−1 d−1 ), P. malaianus at a lower rate (11.97 mg g−1 d−1 ), and H. verticillata at the lowest rate (7.04 mg g−1 d−1 ). The consumption rates on V. spiralis varied significantly, with snail size, ranging from 13.63 mg g−1 d−1 for large-size snails to
Keywords:
143.42 mg g−1 d−1 for small-size ones. The average nutrient release rates of snails grazing on different macrophytes were 45.93 g
Snail Grazing
PO4 -P and 0.58 mg NH4 -N g−1 d−1 . The food species had a significant effect on NH4 -N release
Nutrient release
rates but not on PO4 -P. However, the snail size had a significant effect on PO4 -P release
Submerged plants
rates and not on NH4 -N. The present study indicates that through selective grazing and nutrient release, snails may impose a significant impact on the macrophyte community, which should be considered in managing the macrophytes of a lake. © 2008 Elsevier B.V. All rights reserved.
1.
Introduction
Submerged macrophytes play important roles in freshwater ecosystems (Scheffer et al., 1993; Rai et al., 1995; Jeppesen et al., 1998; Kemp et al., 2000). Their growth can be affected by both biotic and abiotic factors, such as herbivory and nutrients (Carpenter and Lodge, 1986). Snails are common invertebrates ´ in aquatic ecosystems (Lodge, 1985; Pieczynska et al., 1999; Lewis, 2005). Their herbivory can directly affect aquatic plant ´ growth (Pieczynska, 2003; Elger and Lemoine, 2005; Carlsson and Lacoursière, 2005; Li et al., 2005). Selective grazing and associated nutrient regeneration can affect the taxonomic
∗
Corresponding author. Tel.: +86 25 86882103; fax: +86 25 57714759. E-mail address: [email protected] (Z.-W. Liu). 0925-8574/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2008.05.009
composition of aquatic macrophytes in lakes (Underwood, 1991; Pinowska, 2002). Radix swinhoei (H. Adams) is a freshwater snail commonly found in Lake Taihu (31◦ 30 N, 120◦ 30 E), a eutrophic shallow lake in China. There are several dense macrophyte beds in the lake. R. swinhoei is associated with aquatic plants (e.g. Hydrilla verticillata, Potamogeton malaianus, Vallisneria spiralis, and Elodea nuttallii). However, there is no information available on the interaction between R. swinhoei and macrophytes in Lake Taihu. In this study, laboratory experiments were designed to (1) measure R. swinhoei consumption rates on three dominant submerged plants in Lake Taihu and (2) measure phosphorus and nitrogen release rates of R. swinhoei in rela-
1665
e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 1664–1667
tion to macrophyte species grazed and snail size. This study will contribute to our understanding of the role of R. swinhoei in freshwater ecosystems.
2.
Materials and methods
The snail R. swinhoei and macrophytes H. verticillata, P. malaianus and V. spiralis used in the experiments were collected from the littoral zone of Lake Taihu. Macrophytes were cultivated and snails were fostered in different outdoor tanks with lake sediments for 1 month before experiments began. Experiments were conducted in laboratory under natural light conditions and water temperature was 26–30 ◦ C.
2.1.
Snail consumption experiments
All macrophytes chosen for our experiments were young, bright green in color, and without apparent damage. After being rinsed to remove epiphytic flora and marl coverage, all plants were placed on bibulous paper for 90 s and weighed. Snails were kept without food for 48 h prior to experiments. Before being introduced into experimental tanks, experimental snails were washed carefully and air-dried for 2 min and fresh weight was determined. The snail consumption rates were estimated from the difference in the initial and final weights of plants exposed to snails in the experiments. Each of the plant leaves (V. spiralis and P. malaianus) or shoots (H. verticillata) was exposed to snails for 36 h in 500 ml of water. There were four replicates of each treatment. To determine whether the snail size affects their consumption rates, V. spiralis leaves were exposed to three sizes of snails (large size: 0.94 g/ind; middle size: 0.38 g/ind; small size: 0.13 g/ind) for 36 h in 500 ml of water. There were three replicates of each treatment.
2.2.
Snail nutrient release experiments
The release rates of orthophosphate phosphorus (PO4 -P) and ammonia nitrogen (NH4 -N) by snails were determined as the difference between the final nutrient concentrations in a beaker with snails and a control beaker without snails. To investigate the effect of macrophyte species grazing on nutrient release, the snails which just had grazed three submerged plants in the consumption experiment were placed in a beaker with 500 ml of distilled water for 3 h, and then the concentration of nutrients of water in the beaker was analyzed. To determine the effect of snail size on their nutrient releases, the various sizes of snails which just had grazed on V. spiralis in the consumption experiments were also placed into a beaker with 500 ml of distilled water for 3 h, and then the nutrient concentration of the water in the beaker was analyzed. There were three replicates and three controls in each experiment. The PO4 -P and NH4 -N were analyzed colorimetrically (Huang et al., 1999).
2.3.
Statistical analyses
All statistical procedures were performed using SPSS software (version 11.5). A t-test was used to analyze differences in snail
Table 1 – Radix swinhoei consumption rates on young macrophytes (p < 0.05, ANOVA) Macrophytes
Snail size (g/ind)
Hydrilla verticillata Potamogeton malaianus Vallisneria spiralis
0.47 ± 0.02 0.49 ± 0.03 0.48 ± 0.05
Consumption rates (mg g−1 d−1 ) 7.04 ± 2.84 11.97 ± 4.61 23.34 ± 9.63
No significant difference in snail size (p > 0.05, t-test). Values are mean ± S.D.
size in each experiment. Data on snail consumption rates and nutrient release rates were analyzed with ANOVA.
3.
Results
3.1.
Snail consumption experiments
V. spiralis was consumed by snails at the highest rate (23.34 mg g−1 d−1 ), followed by P. malaianus (11.97 mg g−1 d−1 ), and H. verticillata (7.04 mg g−1 d−1 ) (Table 1). The consumption rates on V. spiralis varied significantly with snail size, ranging from 13.63 mg g−1 d−1 for large-size snails to 143.42 mg g−1 d−1 for small-size ones (Table 2). There was a negative correlation between the consumption rates and snail size (r2 = 0.70, p < 0.01).
3.2.
Snail nutrient release experiments
Nutrient release rate was highest for snails grazed on V. spiralis (49.77 g PO4 -P and 0.66 mg NH4 -N g−1 d−1 ), intermediate on P. malaianus (45.50 g PO4 -P and 0.55 mg NH4 -N g−1 d−1 ), and lowest on H. verticillata (42.41 g PO4 -P and 0.53 mg NH4 -N g−1 d−1 ) (Table 3). Statistical analyses showed that plant species had a significant effect on NH4 -N release rates (p < 0.05, ANOVA) and no significant effect on PO4 -P release rates (p > 0.05, ANOVA). The size of snail which had fed on V. spiralis had a significant effect on PO4 -P release rates (p < 0.05, ANOVA) and no significant effect on NH4 -N release rates (p > 0.05, ANOVA) (Table 4).
4.
Discussion
The results of this study are in agreement with other studies (Sheldon, 1987; Elger and Lemoine, 2005) showing that living macrophytes can be eaten by snails. In our preliminary experiments, the snail R. swinhoei was observed to consume many
Table 2 – Radix swinhoei consumption rates on Vallisneria spiralis (p < 0.001, ANOVA) Snail size (g/ind) 0.94 ± 0.05 0.38 ± 0.00 0.13 ± 0.01
Consumption rates (mg g−1 d−1 ) 13.63 ± 1.94 39.26 ± 2.64 143.42 ± 18.56
Significant difference in snail size (p < 0.05, t-test). Values are mean ± S.D.
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e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 1664–1667
Table 3 – Nutrient release rates of large-size snail Radix swinhoei (H. Adams) after consuming three plants (NH4 -N, p < 0.05, ANOVA; PO4 -P, p > 0.05, ANOVA) Food species
Snail size (g/ind)
Nutrient release rates NH4 -N
0.94 ± 0.06 0.91 ± 0.05 0.94 ± 0.06
H. verticillata P. malaianus V. spiralis
(mg g−1
d−1 )
0.53 ± 0.02 0.55 ± 0.07 0.66 ± 0.13
PO4 -P (g g−1 d−1 ) 42.41 ± 5.03 45.50 ± 11.29 49.77 ± 1.04
No significant difference in snail size (p > 0.05, t-test). Values are mean ± S.D.
plant species, such as V. spiralis, P. malaianus, P. maackianus, H. verticillata, N. peltatum, T. bispinosa, and can be considered a generalist grazer (Li et al., 2005). Elger and Lemoine (2005) found that the consumption rate of Lymnaea stagnalis varied considerably across eleven macrophyte species, ranging from 11.3 mg g−1 d−1 to 149.4 mg g−1 d−1 . The snail Lymnaea turricula consumed Cladophora sp. at the highest rate (45 mg g−1 d−1 ) and C. demersum at the lowest rate (2 mg g−1 d−1 ) (Pinowska, 2002). In our experiments, the consumption rate of the largesize snail R. swinhoei on three submerged plants ranged from 7.04 mg g−1 d−1 to 23.34 mg g−1 d−1 , but the consumption rate of small-size ones exceeded 180 mg g−1 d−1 . Therefore, the consumption rates were significantly affected by snail size: smaller snails fed more than larger individuals. These results are consistent with Levri and Lively (1996). With selective removal of plant biomass, herbivory of snails might affect plant species composition and diversity. Sheldon (1987) demonstrated that herbivorous snails strongly affected the structure of submerged macrophytes in North American lakes and resulted in the dominance by C. demersum. Carlsson and Lacoursière (2005) found the golden apple snail (Pomacea canaliculata) had a strong negative effect on duckweed (Lemna minor) and water hyacinth (Eichhornia crassipes) growth in field enclosures and mediated a shift from clear water and macrophyte dominance to turbid water and phytoplankton dominance. Our study showed that snail R. swinhoei could graze on aquatic macrophytes from Lake Taihu. However, the herbivorous effect of snails on the freshwater macrophyte communities in Lake Taihu needs further research. The average nutrient release rates of R. swinhoei were 45.93 g PO4 -P and 0.58 mg NH4 -N g−1 d−1 , and these release rates were higher than the rates observed by other authors (Pinowska, 2002; Underwood, 1991) for L. turricula (24.2 g PO4 P and 48.9 g NH4 -N g−1 d−1 ) and Planorbis planorbis (2.9 g PO4 -P and 8.7 g NH4 -N g−1 d−1 ). Snail species, nutrient con-
Table 4 – Nutrient release rates of the various sizes of snail Radix swinhoei (H. Adams) after consuming Vallisneria spiralis (NH4 -N, p > 0.05, ANOVA; PO4 -P, p < 0.05, ANOVA) Snail size (g/ind)
Nutrient release rates NH4 -N (mg g−1 d−1 )
0.94 ± 0.06 0.38 ± 0.00 0.13 ± 0.01
0.66 ± 0.13 0.66 ± 0.15 0.58 ± 0.04
PO4 -P (g g−1 d−1 ) 49.72 ± 1.04 50.41 ± 3.57 68.57 ± 8.39
Significant difference in snail size (p < 0.05, t-test). Values are mean ± S.D.
tent of plant species and environmental conditions (e.g. water temperature) in the experiments might affect nutrient release rates (Underwood, 1991; Brendelberger, 1997; Pinowska, 2002). The snails grazing on V. spiralis had a much higher NH4 -N release rate than those grazing on H. verticillata and P. malaianus, because of the higher consumption rate of V. spiralis, but their PO4 -P release rates were similar. It is puzzling for the low snail consumption rate but similar to PO4 -P release rates for snails grazing on P. malaianus and V. spiralis. It could be that consumed foods might have different nitrogen and phosphorus content (Irons et al., 1988) and the limited ability of snails to break down often refractory food substances can affect the amount of phosphorus assimilated and released (Brendelberger, 1997). In the present experiments, snail size significantly affected the PO4 -P release rates. The small-size snails showed the highest release rate and the large-size ones displayed the lowest release rate. This result is consistent with Pinowska (2002) and can be explained by the snail consumption rates. In fact, the consumption rate on V. spiralis was significantly correlated to the PO4 -P release rate (Tables 2 and 4). On the contrary, the smaller snails showed the lower NH4 -N release rate than the larger ones. This may be related to the nitrogen metabolism of snails, for the excretion of ammonia nitrogen may be regarded as the rate of protein and amino acid catabolism (Widdows, 1978) and invertebrate herbivores are strongly nitrogen-limited (Mattson, 1980). This implies that young snails utilize more nitrogen-rich compounds for their growth than adult ones. Furthermore, diffusion is the principal mode of ammonia excretion in invertebrates since its concentration in the body fluids is considered to be higher than that in the ambient environment (Kinne, 1976). The higher rate of nutrient release in larger individuals could be attributed to the larger surface area for diffusion as compared to the smaller ones (Clarke et al., 1994). Our study indicates that through selective grazing and nutrient release, snails may impose a significant impact on macrophyte community, which should be considered for managing the macrophytes of a lake.
Acknowledgements This research was supported jointly by the National High Technology Research and Development Program (2006AA06Z337) and the Key Project of Chinese Academy of Sciences (KZCX1SW-12). The authors appreciate the constructive suggestions given by Wu Qinglong of Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences.
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