Snail–periphyton interactions in a prairie lacustrine wetland

This study examined the effects of nutrients and macrophytes on snail grazers and periphyton in a prairie wetland food web. Snails (Gyraulus circumstriatus) and periphyton in large enclosures in a lacustrine wetland, Delta Marsh, MB, Canada were subjected to two experimental treatments, nutrient addition (nitrogen, phosphorus) and macrophyte exclusion (using a porous geotextile carpet) during July and August. Snail biomass and periphyton biomass (on both artificial substrata and submerged macrophytes) increased over time in all treatments, representing seasonal growth. Snail biomass was three times higher on macrophytes than on artificial substrata. In response to nutrient addition, snail biomass was significantly elevated over time on macrophytes but not on artificial substrata. Conversely, periphyton biomass was higher on artificial substrata but not on macrophytes in response to nutrient addition. Snail biomass and periphyton biomass on artificial substrata showed no response to macrophyte exclusion. Snail biomass on all substrata was inversely correlated with turbidity, whereas periphyton biomass showed no relationship with turbidity. Timing of nutrient additions to wetlands may influence whether the response occurs primarily in phytoplankton or in periphyton and macrophytes.     

不同初始螺类密度对沉水植物刺苦草Vallisneria spinulosa Yan及其附着藻类的影响

大型水生植物及其附着藻类是浅水湖泊中的重要初级生产者。淡水螺类作为重要的初级消费者,其密度对沉水植物及其附着藻类的影响存在争议。本研究设置4种初始螺类密度（0、40、80、240 ind·m^-2）,研究淡水螺类（椭圆萝卜螺Radix swinhoei H.Adams）对刺苦草（Vallisneria spinulosa Yan）及其附着藻类的直接牧食作用和螺类种群的变化。结果显示,在添加螺处理中,刺苦草和人工基质表面附着藻类的生物量显著降低,同时沉水植物的生长显著增加,在较高初始密度螺类处理中刺苦草产生更多的分株。到实验结束时,螺类的死亡率较高,但3个有螺处理间螺类鲜重无显著差异,而高初始密度螺类条件下的最终密度仍较高,同时个体重量（均重）也较小。在中富营养条件下淡水螺类可以直接牧食沉水植物叶片,但对植物生长的抑制作用不显著,有可能是因为沉水植物并不能作为唯一的食物来源维持螺类种群,同时螺类的种群结构受到水体营养水平等因素的制约。     

Density-dependent effects of snail grazing on the growth of a submerged macrophyte,Vallisneria spiralis

In order to better understand the role of herbivorous snails in freshwater ecosystems, we conducted experiments investigating food preference of the snail Radix swinhoei on leaves of the submerged plant Vallisneria spiralis with and without periphyton coverage. The effects of snail grazing on the growth of V. spiralis were assessed in a no-snail control and at three snail densities (80, 160, 240 individuals m^?2). Results showed that the snails chose preferentially leaves covered by periphyton. Grazing activity at low snail density (80 individuals m^?2) was found to stimulate V. spiralis growth, but at higher snail density (240 individuals m^?2), plant growth was apparently suppressed. An increase observed in nutrient concentrations in water column with increasing snail density may be attributed to nutrient release by snails. This study suggests that the nature of the relationship between herbivorous snails and macrophytes in freshwater ecosystems depends on the abundance of the snails. At low snail density, the relationship may be a mutualistic one, but at high density snail herbivory may impact negatively on macrophyte biomass in lakes.     

蓝藻堆积和螺类牧食对苦草生长的影响

设计了双因素四组处理(对照组,加螺组,加藻组,螺藻组)的室外受控实验,模拟湖泊沿岸带水华蓝藻的堆积以及底栖螺类的牧食活动对沉水植物苦草生长的影响。结果表明:蓝藻堆积(水体叶绿素a浓度为220μg/L)对苦草的生长具有明显的抑制作用,和对照组以及加螺组相比,加藻组和螺藻组中苦草的相对生长率分别下降了40.9%和36.4%,分株数也分别下降了56.4%和64.1%,分析认为蓝藻在水体表层堆积所产生的遮光可能是抑制底层苦草生长的主要原因。然而,环棱螺能在一定程度上促进苦草的生长,加螺组和螺藻组中苦草的相对生长率和分株数分别要明显高于对照组和加藻组,这可能要归因于螺类的牧食去除了沉水植物表面附着生物。实验中蓝藻堆积和螺类牧食对苦草的各项生长指标均无显著的交互作用,但蓝藻对苦草生长的抑制作用要远大于螺类对植物生长的促进作用。研究证实了在富营养浅水湖泊中,水华蓝藻在湖泊沿岸带的堆积会严重胁迫沉水植物的生长,而底栖螺类的牧食活动则能在一定程度上提高植物在不良环境下的生存能力。     

Periphytic food and predatory crayfish: relative roles in determining snail distribution

Summary In the laboratory and field, we examined how periphyton (food of snails) and predatory crayfish influenced snail distribution in Trout Lake, a permanent, northern Wisconsin lake. Laboratory experiments (with no crayfish) tested the importance of periphyton biomass in determining snail preference among rocks, and among rock, sand, and macrophyte substrates. Among rocks with four different amounts of periphyton, periphyton biomass and the number of Lymnaea emarginata, Physa spp., and Amnicola spp. were positively related. A similar, but non-significant, trend occurred for Helisoma anceps. A field experiment at a site in Trout Lake where predation risk was low confirmed the preference by snails for periphyton covered rocks; more snails colonized rocks with periphyton than rocks without. When given a choice of rock, sand, and macrophytes in the laboratory, L. emarginata preferred high periphyton biomass and rock. Laboratory and field results contrasted with the distribution of snails in Trout Lake; no snails occurred in areas with abundant periphyton-covered rocks, but snails were abundant nearby on scattered rocks with little periphyton. However, where snails were absent, crayfish were abundant (14.5 crayfish-trap^–1-day^–1), and where snails were abundant, crayfish were rare (3.2 crayfish-trap^–1-day^–1), suggesting that crayfish predation reduced snails. The hypothesis that the negative association between snail and periphyton biomass resulted from snail grazing was supported by the results of a field snail enclosure-exclosure experiment (1 m² cages; n=3). All experiments and observations therefore suggest that: 1) crayfish predation is more important than a preference for high periphyton biomass in determining snail distribution in Trout Lake; 2) periphyton biomass is negtively related to snail grazing; and 3) crayfish had a positive indirect effect on periphyton by preying on grazing snails.     

Plant community dynamics in a chain of lakes: principal factors in the decline of rooted macrophytes with eutrophication

Shoe Lake and East Graham Lake, part of a small chain of lakes in southeastern Michigan, USA, differ in nutrient loading and in the structure and productivity of their aquatic plant communities. A comparative study of species frequency and biomass distributions, nutrient contents, and responses to experimental nutrient enrichment and shading, was conducted to determine the principal factors controlling the macrophyte dynamics. A central objective was to address the question of why rooted macrophyte growth declines with eutrophication, and to test existing models designed to explain this phenomenon. In the more eutrophic Shoe Lake, diversity and productivity of rooted macrophytes were relatively low, restricted primarily by combined shading of phytoplankton, periphyton, and non-rooted macrophytes (principally Ceratophyllum demersum, along with Utricularia vulgaris and Cladophora fracta). In the less eutrophic East Graham Lake, lower nitrogen availability restricted the growth of all of these shading components, resulting in clearer water and higher productivity and diversity of rooted macrophytes. The macrophytes did not allelopathically suppress the phytoplankton in East Graham Lake. The results supported a direct relationship between nutrient loading, increasing growth of phytoplankton, periphyton and non-rooted macrophytes, and decline of rooted macrophytes.     

Wave exposure related growth of epiphyton: implications for the distribution of submerged macrophytes in eutrophic lakes

The distribution of submerged macrophytes in eutrophic lakes has been found to be skewed towards sites with intermediate exposure to waves. Low submerged macrophyte biomass at exposed sites has been explained by, for instance, physical damage from waves. The aim of this study was to investigate if lower biomass at sheltered sites compared to sites with intermediate exposure to waves can be caused by competition from epiphyton.Investigations were performed in eutrophic lakes in southern Sweden. Samples of submerged macrophytes and epiphytic algae on the macrophytes were taken along a wave exposure gradient. The amount of epiphyton (AFDW) per macrophyte biomass decreased with increased exposure. Biomass of submerged macrophytes, on the other hand, increased with increased exposure until a relatively abrupt disappearance of submerged vegetation occurred at high exposures. Production of epiphytic algae was monitored on artificial substrates from June to September at a sheltered and an exposed site in three lakes. It was higher at sheltered sites compared with exposed sites.We suggest that epiphytic algae may be an important factor in limiting the distribution of submerged macrophytes at sheltered sites in eutrophic lakes.     

Indirect effects of fish on macrophytes in Bays Mountain Lake: evidence for a littoral trophic cascade

Summary We began this experiment to test specific hypotheses regarding direct and indirect effects of fish predation on the littoral macroinvertebrate community of Bays Mountain Lake, Tennessee. We used 24 m² enclosures in which we manipulated the presence and absence of large redear sunfish (Lepomis microlophus>150 mm SL), and small sunfish (L. macrochirus and L. microlophus <50 mm SL) over a 16-mo period. Here we report on effects of fish predation on gastropod grazers that appear to cascade to periphyton and macrophytes.Both large redear sunfish and small sunfish maintained low snail biomass, but snails in fish-free controls increased significantly during the first 2-mo of the experiment. By late summer of the first year of the experiment, the difference in biomass between enclosures with and without fish had increased dramatically (>10×). Midway through the second summer of the experiment, we noted apparent differences in the abundance of periphyton between enclosures containing fish and those that did not. We also noted differences in the macrophyte distribution among enclosures. To document these responses, we estimated periphyton cover, biovolume and cell size frequencies as well as macrophyte distributions among enclosures at the end of the experiment. When fish were absent, periphyton percent cover was significantly reduced compared to when fish were present. Periphyton cell-size distributions in enclosures without fish were skewed toward small cells (only 12% were greater than 200 m³), which is consistent with intense snail grazing. The macrophyte Najas flexilis had more than 60 x higher biomass in the fish-free enclosures than in enclosures containing fish; Potamogeton diversifolius was found only in fish-free enclosures. These results suggest a chain of strong interactions (i.e. from fish to snails to periphyton to macrophytes) that may be important in lake littoral systems. This contrasts sharply with earlier predictions based on cascading trophic interactions that propose that fish predation on snails would enhance macrophyte biomass.     

“螺-草”的互利关系

水生态系统中存在螺-草互利现象。然而,植食性螺类与水生植物之间是否存在这种互利关系目前尚无定论。椭圆萝卜螺（肺螺亚纲）与铜锈环棱螺（前腮亚纲）是常见的淡水螺类,其中,椭圆萝卜螺能牧食多种水生植物的活体。通过室外实验,研究了这两种螺类在不同密度条件下对沉水植物（苦草）生长的影响。实验结果表明,低密度的椭圆萝卜螺促进了苦草的生长,螺、草之间存在明显的互利关系,高密度时螺类对苦草植株本身的大量牧食则显著限制了植物的生长。对铜锈环棱螺而言,不同密度的螺类均明显促进了受附生生物胁迫的苦草的生长,螺-草互利关系成立。分析认为,螺-草互利关系的存在是有其限制条件的,对植食性螺类而言,只有在较低的螺类密度条件下才存在这种互利关系。     

Community structure and diel migration of zooplankton in shallow brackish lakes: role of salinity and predators

Diel horizontal migration (DHM), where zooplankton moves towards macrophytes during daytime to avoid planktivorous fish, has been reported as a common migration pattern of zooplankton in shallow temperate freshwater lakes. However, in shallow eutrophic brackish lakes, macrophytes seem not to have the same refuge effect, as these lakes may remain turbid even at relatively high macrophyte abundances. To investigate the extent to which macrophytes serve as a refuge for zooplankton at different salinities, we introduced artificial plants mimicking submerged macrophytes in the littoral zone of four shallow lakes, with salinities ranging from almost freshwater (0.3) to oligohaline waters (3.8). Furthermore, we examined the effects of different salinities on the community structure. Diel samples of zooplankton were taken from artificial plants, from areas where macrophytes had been removed (intermediate areas) and, in two of the lakes, also in open water. Fish and macroinvertebrates were sampled amongst the artificial plants and in intermediate areas to investigate their influence on zooplankton migration. Our results indicated that diel vertical migration (DVM) was the most frequent migration pattern of zooplankton groups, suggesting that submerged macrophytes were a poor refuge against predation at all salinities under study. Presumably, this pattern was the result of the relatively high densities of small planktivorous fish and macroinvertebrate predators within the submerged plants. In addition, we found major differences in the composition of zooplankton, fish and macroinvertebrate communities at the different salinities and species richness and diversity of zooplankton decreased with increasing salinity. At low salinities both planktonic/free-swimming and benthic/plant-associated cladocerans occurred, whilst only benthic ones occurred at the highest salinity. The low zooplankton biomass and overall smaller-bodied zooplankton specimens may result in a lower grazing capacity on phytoplankton, and enhance the turbid state in nutrient rich shallow brackish lakes.     

The response of periphyton and submerged macrophytes to nitrogen and phosphorus loading in shallow warm lakes: a mesocosm experiment

1. Recent experimental and field studies on temperate shallow lakes indicate that nitrogen may play a greater role in their functioning than previously thought. Several studies document that abundance and richness of submerged macrophytes, both central in shallow lake ecology, may decrease with increasing nitrogen loading, especially at high phosphorus levels. However, the role of nitrogen in warm lakes with fluctuating water regimes remains to be described in detail. 2. The effect of increasing nitrate and phosphate concentrations on submerged macrophyte growth was examined in a 3‐month mesocosm experiment conducted in summer in a shallow freshwater lake on the north western coast of Turkey with a Mediterranean climate. Twenty four field mesocosms, open to the sediment and atmosphere, were stocked with Myriophyllum spicatum shoots and small cyprinid fish. Three nitrate loadings in combination with two phosphate loadings were applied in a fourfold replicated design. 3. Mean ± SD nutrient concentrations maintained throughout the experiment were 0.55 ± 0.17, 2.2 ± 0.97, 9.2 ± 5.45 mg L^?1 total nitrogen and 55 ± 19.2, 73 ± 22.9 μg L^?1 total phosphorus. Mean periphyton biomass increased with increasing nutrient concentrations and peaked at the highest nitrogen and phosphorus loadings, while the mean phytoplankton biomass remained relatively low in all treatments. 4. Percent volume inhabited (% PVI) by macrophytes throughout the experiment and total macrophyte biomass at the end of the experiment did not differ among treatments. In addition to stocked M. spicatum, Ceratophyllum demersum and Potamogeton crispus appeared in the majority of the mesocosms. The plants grew continuously up to 50% PVI throughout the experiment and remained resilient to shading provided by periphyton and phytoplankton. 5. The mean summer air temperature in 2007 was 2.2 °C higher than the average of the last 32 years, which resulted in a water level decrease of 0.3 m in the mesocosms over three months. This might have counteracted the shading of submerged macrophytes provided by phytoplankton and periphyton. The results of the experiment are consistent with observations of higher macrophyte resilience to nutrient loading in Mediterranean lakes compared with northern temperate lakes.     

Size-dependent effects of an invasive herbivorous snail (Pomacea canaliculata) on macrophytes and periphyton in Asian wetlands

1. The invasive golden apple snail (Pomacea canaliculata), native to South America, is a serious pest on rice seedlings in south‐east Asia and has also been shown to consume large amounts of macrophytes in natural wetlands, with large effects on ecosystem functioning. Earlier studies suggest that the snail undergoes an ontogenetic diet shift, feeding on algae and detritus as juveniles and shifting to aquatic macrophytes as adults. 2. Here, we study the effects of snail populations with a size‐structure typical of either populations at an invasive front or the size‐structure of established populations. In an enclosure experiment performed in a wetland in Laos, we compared treatments with small snails only (3 mm; invasive treatment) to treatments with small, medium sized (10 mm) and adult (>25 mm) snails (established treatment). The effects of snail grazing on three aquatic macrophyte species and periphytic algae were quantified. 3. We found that snails of all sizes had a strong negative effect on the biomass of all macrophyte species and periphytic algae. There was no evidence of an ontogenetic diet change, i.e. snails in both the invasive and established treatments affected macrophyte biomass. Foraging was size‐dependent in that small snails had higher relative foraging capacity (g plant consumed per g of snail) compared with medium and adult snails. Small snails, therefore, depressed growth of medium snails at increasing densities through exploitative competition for preferred resources, while adult snails did not grow at all in the presence of small snails. 4. Density dependence is common in freshwater invertebrates, including gastropod populations, but differences in size dependent foraging‐ and competitive‐ability have rarely been demonstrated in this group of organisms. Knowledge about intra‐specific differences in ecological performance may, however, both deepen our understanding of the processes that underlie population dynamics in invertebrates such as gastropods, and help develop control strategies for invasive golden apple snails.     

Submerged Macrophytes Mitigate Direct and Indirect Insecticide Effects in Freshwater Communities

Understanding how ecological interactions mitigate the impacts of perturbations such as pesticides in biological communities is an important basic and applied question for ecologists. In aquatic ecosystems, new evidence from microcosm experiments suggests that submerged macrophytes can buffer cladocerans from pulse exposures to the widely used insecticide malathion, and that mitigation increases with macrophyte density. However, whether these results scale up to more complex aquatic communities where ecological interactions such as competition can alter toxicity is unknown. Further, macrophyte abilities to mitigate different insecticide exposure scenarios (i.e. single versus repeated pulses) have never been tested. To address these gaps, we performed a factorial mesocosm experiment examining the influence of four macrophyte treatments (0, 10, 50, or 100 Elodea Canadensis shoots planted per mesocosm) crossed with three malathion exposure scenarios (no insecticide, single pulse, repeated pulses) on aquatic communities containing zooplankton, phytoplankton, periphyton, two snail species, and larval amphibians. In the absence of macrophytes, single malathion pulses caused short-term declines in cladoceran abundance followed by their rapid recovery, which precluded any indirect effects (i.e. trophic cascades). However, repeated malathion pulses caused cladoceran extinctions, resulting in persistent phytoplankton blooms and reduced abundance of one snail species. In contrast, with macrophytes present, even at low density, malathion had no effect on any taxa. We also discovered novel effects of macrophytes on the benthic food web. In the two highest macrophyte treatments, we observed trends of reduced periphyton biomass, decreased abundance of one snail species, and decreased amphibian time to and mass at metamorphosis. To our knowledge, this is the first evidence of negative submerged macrophyte effects on amphibians, a taxa of global conservation concern. Our findings suggest that facilitating macrophytes could be an important strategy for buffering freshwater communities from insecticides, though consideration of their impacts on animal species is necessary.     

Snail communities increase submerged macrophyte growth by grazing epiphytic algae and phytoplankton in a mesocosm experiment

The relationships between producers (e.g., macrophytes, phytoplankton and epiphytic algae) and snails play an important role in maintaining the function and stability of shallow ecosystems. Complex relationships exist among macrophytes, epiphytic algae, phytoplankton, and snails. We studied the effects of snail communities (consisting of Radix swinhoei, Hippeutis cantori, Bellamya aeruginosa, and Parafossarulus striatulus) on the biomass of phytoplankton and epiphytic algae as well as on the growth of three species of submerged macrophytes (Hydrilla verticillata, Vallisneria natans, and one exotic submerged plant, Elodea nuttallii) in a 90‐day outdoor mesocosm experiment conducted on the shore of subtropical Lake Liangzihu, China. A structural equation model showed that the snail communities affected the submerged macrophytes by grazing phytoplankton and epiphytic algae (reduction in phytoplankton Chl‐a and epiphytic algal abundance), enhancing the biomass of submerged macrophytes. Highly branched macrophytes with high surfaces and morphologies and many microhabitats supported the most snails and epiphytic algae (the biomass of the snail communities and epiphytic algae on H. verticillata was greater than that on V. natans), and snails preferred to feed on native plants. Competition drove the snails to change their grazing preferences to achieve coexistence.     

Interactions between neighboring algae and snail grazing in structuring microdistribution patterns of periphyton

The micro-distribution of periphyton (filamentous algae) on homogeneous substrates was examined in experimental tanks with and without the pressure of grazing snails. The growth of periphyton attached to artificial substrate was estimated at a small spatial scale (9.3 mm×9.3 mm cells) by varying the number of grazers (0, 5, or 10 snails per tank), using image processing analysis without removing the periphyton. The results suggest that periphyton growth within a cell was negatively affected by the biomass of periphyton in the cell but was positively affected by the biomass of periphyton in neighboring cells. A semivariogram analysis indicated that spatial heterogeneity increased with increasing grazing pressure. The size of patches was not clearly related to the number of snails, but there was a tendency for relative patch size to increase with snail density. Computer simulations were also conducted to examine factors affecting the degree of spatial heterogeneity. The simulation studies indicated that snails should graze a site that was previously grazed in order to produce the observed spatial heterogeneity of periphyton. The results also indicated that the positive effects of neighboring periphyton on the growth of algae might create patches. The interactions among neighboring algae and snail grazing might be an important factor creating the spatial heterogeneity of periphyton even on homogeneous substrates.     

Invertebrate grazing during the regenerative phase affects the ultimate structure of macrophyte communities

1. Although the biomass of freshwater macrophytes consumed by invertebrate herbivores (excluding crayfish) is usually low, there is growing evidence that invertebrates do exert a structuring effect on macrophyte communities. To explain this, we postulated that the effect of invertebrates may be concentrated on macrophytes during their regenerative phase.
2. We tested this hypothesis by means of a mesocosm-based experiment, in which we investigated the effects of different densities of pond snails [ Lymnaea stagnalis (L.)] on macrophytes regenerating from the natural sediment propagule bank.
3. After 2 months, a diverse macrophyte community had established in the absence of snails, mainly from sexual propagules. Under moderate snail grazing (4 individuals m⁻²), the ultimate biomass of macrophytes was similar, but its species composition differed dramatically. Only a few unpalatable taxa, such as Ceratophyllum demersum and Nymphaeaceae, persisted. Moreover, the relative success of macrophytes regenerating from vegetative rather than sexual propagules improved. Under higher snail grazing (20 m⁻²), all macrophytes disappeared before the end of the experiment.
4. These results confirm that snails at natural densities can have a strong effect on the ultimate structure of macrophyte communities by selectively consuming some species at a juvenile stage. Therefore, the regenerative phase can be seen as a window of opportunity for invertebrate grazers, which can have a qualitative effect on communities that is disproportionate to the biomass consumed.     

Competition and facilitation within and between a snail and a mayfly larva and the effect on the grazing process

We studied the competitive effects within and between two taxonomically distant freshwater herbivores, a snail and a mayfly, common in Swedish lakes, Lymnaea peregra and Cloeon dipterum, respectively, and their effect on grazing in a laboratory experiment. The experimental set-up consisted of 2-l aquaria, each containing a periphyton covered tile. Intra- and interspecific effects were tested by increasing the density of one species at a time in four different treatments, (1) snails (intraspecific treatment), (2) mayflies (intraspecific treatment), (3) mixed-snails (interspecific treatments, snails kept constant) and (4) mixed-mayflies (interspecific treatments, mayflies kept constant). Intraspecific competition affected both snails and mayflies negatively, i.e. increasing mortality with increasing con-specific density. Furthermore, there was a decrease in snail growth with increasing snail density. In the mixed-species treatments both species changed their microhabitat use indicating interspecific competition. Despite this, we also found a positive effect of mayfly density on snail growth, most likely due to indirect commensalism. No density-dependent effect of grazing on periphyton was found, probably due to interference competition between grazers. However, there was a significant difference in periphyton biomass, due to species composition of grazers. Irrespective of their densities, if they co-existed, the two grazer species decreased the periphyton biomass significantly compared with both single-species treatments. We considered this as a joint action of facilitation and interaction. Our results suggest that competition can be an important structuring factor in macroinvertebrate communities and that species composition can be significant for ecosystem processes within lentic environments.     

Responses of four submerged macrophytes to freshwater snail density (Radix swinhoei) under clear‐water conditions: A mesocosm study

Macrophytes play a key role in stabilizing clear‐water conditions in shallow freshwater ecosystems. Their populations are maintained by a balance between plant grazing and plant growth. As a freshwater snail commonly found in shallow lakes, Radix swinhoei can affect the growth of submerged macrophytes by removing epiphyton from the surface of aquatic plants and by grazing directly on macrophyte organs. Thus, we conducted a long‐term (11‐month) experiment to explore the effects of snail density on macrophytes with distinctive structures in an outdoor clear‐water mesocosm system (with relatively low total nitrogen (TN, 0.66 ± 0.27 mg/L) and total phosphorus (TP, 36 ± 20 μg/L) and a phytoplankton chlorophyll a (Chla) range of 14.8 ± 4.9 μg/L) based on two different snail densities (low and high) and four macrophyte species treatments (Myriophyllum spicatum, Potamogeton wrightii, P. crispus, and P. oxyphyllus). In the high‐density treatment, snail biomass and abundance (36.5 ± 16.5 g/m² and 169 ± 92 ind/m², respectively) were approximately twice that observed in the low‐density treatment, resulting in lower total and aboveground biomass and ramet number in the macrophytes. In addition, plant height and plant volume inhabited (PVI) showed species‐specific responses to snail densities, that is, the height of P. oxyphyllus and PVI of M. spicatum were both higher under low‐density treatment. Thus, compared with low‐density treatment, the inhibitory effects of long‐term high snail density on macrophytes by direct feeding may be greater than the positive effects resulting from epiphyton clearance when under clear‐water conditions with low epiphyton biomass. Thus, under clear‐water conditions, the growth and community composition of submerged macrophytes could be potentially modified by the manual addition of invertebrates (i.e., snails) to lakes if the inhibitory effects from predatory fish are minor.     

Synergy between shading and herbivory triggers macrophyte loss and regime shifts in aquatic systems

Macrophytes play a keystone role in shallow aquatic ecosystems. In lakes, macrophytes stabilize clear‐water conditions with high biodiversity and their decline can cause a shift to a turbid state with lower biodiversity. Various mechanisms have been suggested as triggers of macrophyte collapse. Herbivory by waterfowl and fish seems to be one of the obvious factors, but the response of macrophytes to herbivory is ambiguous. We hypothesized that herbivory alone does not typically cause macrophyte collapse, but that shading from periphyton can enhance the effect of herbivores. Shading of macrophytes is supposed to increase with eutrophication due to changes in the top–down control cascading from fish via macroinvertebrates to periphyton. We elaborated on this idea by fitting a macrophyte growth model with different herbivore grazing and periphyton shading scenarios. In addition, we performed a meta‐analysis on existing experimental herbivore exclosure studies with respect to periphyton growth. The model supported our proposed hypothesis and the reviewed field studies appeared to point in the same direction. We suggest that a significant herbivore impact may indicate a reduced resilience of vegetation to eutrophication, making it an early warning signal for an imminent macrophyte collapse leading to a sudden shift of the system to turbid conditions.