Mesocosm experiment reveals a strong positive effect of snail presence on macrophyte growth, resulting from control of epiphyton and nuisance filamentous algae: Implications for shallow lake management

Highlights

• Nutrient loading increased phytoplankton, epiphyton and filamentous algae, decreased biomass of submerged macrophytes.

• Snails reduced phytoplankton, epiphyton and filamentous algae, increased submerged macrophytes.

• Snails are able to reduce the effect of eutrophication in shallow waters.

Abstract

Increased nutrient loading has adverse effects on the growth of submerged macrophytes in eutrophic shallow lakes. Where growth of phytoplankton, epiphyton and filamentous algae is excessive, all may contribute to shading that limits macrophyte growth. However, when abundant, herbivorous snails may dampen this effect by reducing the biomass of epiphyton, and perhaps also of nuisance filamentous algae, both which have the potential to become more abundant in a future warmer world. We studied the effects of herbivorous snails (Radix swinhoei) on the biomass of phytoplankton, epiphyton and filamentous algae as well as the growth of the submerged macrophyte, Vallisneria denseserrulata, under contrasting nutrient loadings (low, nitrogen (N) 113 μg L⁻¹·d⁻¹ and phosphorus (P) 10 μg L⁻¹·d⁻¹; high, N 339 μg L⁻¹·d⁻¹ and P 30 μg L⁻¹·d⁻¹) in a 30 day outdoor mesocosm experiment, conducted on the shore of subtropical Lake Taihu, China. We found significant interactive effects of nutrient loading and snail presence on biomasses of epiphyton and filamentous algae and on the biomass and relative growth rate of submerged macrophytes. When snails were absent, the biomass of epiphyton and the biomass and coverage of filamentous algae all increased markedly, while the biomass, density and relative growth rate of V. denseserrulata decreased significantly with increased nutrient loading. When snails were present, biomasses of epiphyton, phytoplankton and filamentous algae were significantly reduced and growth of V. denseserrulata significantly increased under both high and low nutrient loading scenarios, and the effect was most pronounced in the nutrient-rich treatment. The present study suggests that in shallow aquatic ecosystems, herbivorous snails reduce the negative impact of nutrient loading on submerged macrophyte growth, by controlling both epiphyton and nuisance filamentous algae. How best to protect snails from fish predation in order to realize this potential under natural conditions is a matter that warrants further studies.

Introduction

Eutrophication resulting from the excessive input of nutrients from human activities is a serious problem impacting shallow lakes worldwide. The effects include declines in submerged macrophyte biomass and coverage, which in shallow systems can lead to a shift from clear to turbid water conditions (Moss, 1990; Jeppesen et al., 1998; Liu et al., 2018). One of the mechanisms behind macrophyte decline is increased shading caused by an increase in the biomass of phytoplankton in the water and by the growth of epiphyton on the surface of the macrophytes (Brönmark, 1985; Jones and Sayer, 2003; Arthaud et al., 2012; Olsen et al., 2015; Zhang et al., 2015). This shading effect can be exacerbated by the development of floating clusters of filamentous algae and the effect increases with eutrophication (Phillips et al., 1978; Ozimek et al., 1991; Olsen et al., 2015). In eutrophic shallow lakes it has been well documented that increased fish predation reduces the abundance of large zooplankton and the effect of grazing on phytoplankton (Jeppesen et al., 2011). This has been cited as a cause of increased phytoplankton growth leading to a reduction or loss of submerged macrophytes in eutrophic shallow lakes (Scheffer, 1997; Jeppesen et al., 2011).

Shallow eutrophic lakes are often seen to become dominated by filamentous algae during warm periods (Irfanullah and Moss, 2004, Irfanullah and Moss, 2005) or in the period after ecological restoration before submerged plants become well-established (Ruley and Rusch, 2002, Ruley and Rusch, 2004). It may be that filamentous algae and epiphyton collectively exert more serious inhibitory effect on submerged macrophyte growth than phytoplankton. Jones and Sayer (2003) reported that the epiphyton density (determined by chlorophyll a content) exerted a stronger negative effect on plant biomass in 17 plant-dominated shallow lakes in the UK than phytoplankton. Similarly, Sand-Jensen and Søndergaard (1981) found that the shading effect of epiphyton on submerged macrophytes was greater than that associated with phytoplankton. Further, studies by Jones et al. (1998) suggest that filamentous flocs may be more damaging to macrophyte growth than epiphyton, and in a study of a shallow Chinese lake Olsen et al. (2015) showed seasonal variation in the effects of phytoplankton, epiphyton and filamentous algae on macrophytes, with filamentous algae becoming a dominant factor in winter while phytoplankton and epiphyton were more significant in summer.

Multiple studies have shown that grazing of epiphyton by herbivorous invertebrates such as crayfish, shrimps, oligochaetes, mayflies and chironomids results in less shading and greater macrophyte growth (Botts, 1993; Jeppesen et al., 1998; Wellnitz and Ward, 1998; Asaeda et al., 2004; Bayley et al., 2007; Ye et al., 2019). Many species of herbivorous snails, including Radix spp., are highly efficient in removing epiphyton (Brönmark, 1985, Brönmark, 1989; Cao et al., 2014; Li et al., 2019). Grazing may also alter successional processes and help to maintain an algal community at an early seral stage (Brönmark and Vermaat, 1998). A study by Li et al. (2008) suggests that the persistence of clear water state in the East Bay area of Lake Taihu despite increased nutrient loading was related to the grazing of epiphyton by the snail Bellamya aeruginosa. Recently, Mormul et al. (2018) found that the snail R. balthica had a strong positive effect on submerged macrophyte growth, and attributed this to the grazing of epiphyton.

Previous studies have found fish and crayfish, rather than small-sized herbivores such as snails, to be the dominant grazers of filamentous algae (Lodge et al., 1998). In a field experiment performed in a freshwater pond in Hong Kong, Fang et al. (2010) showed that the large apple snail Pomacea canaliculata was able to control the biomass of filamentous algae. Pinowska (2002) showed that high densities of the snail Lymnaea (Galba) turricula were able to consume the biomass of the filamentous algae Cladophora sp. under experimental conditions.

Other studies also show that certain palatable macrophytes will be consumed by some species of herbivorous snails when the availability of other food items is insufficient (Sheldon, 1987, Sheldon, 1990; Elger et al., 2002, Elger et al., 2007; Li et al., 2009a, Li et al., 2009b). In a laboratory experiment, Sheldon, 1987, Sheldon, 1990 found that grazing by the freshwater snails Physa gyrina and Amnicola limosa had a significant effect on macrophyte communities early in the season before epiphytes formed an extensive cover.

Radix swinhoei is the dominant snail in lakes of the Yangtze basin (Wang et al., 2006), especially in macrophyte-dominated areas. Although experiments have shown that Radix species are able to consume epiphytes and thus benefit submerged macrophytes in eutrophic waters (Li et al., 2009a; Mormul et al., 2018), it is also evident that Radix sp. can feed directly on submerged macrophytes, especially when they are present in high densities (Li et al., 2009a, Li et al., 2009b). Meanwhile, nutrient release by snails may enhance the growth of both phytoplankton and submerged macrophytes. It is unclear to what extent small snail species like R. swinhoei can control filamentous algae in eutrophic lakes. Evidence of the role of snails is important as they may have important implications for the management of eutrophic shallow systems in which submerged macrophytes are vital in maintaining or restoring clear water states (Jeppesen et al., 1998; Liu et al., 2018).

We hypothesized that snail grazing controls both epiphytic and filamentous algae and potentially benefits the growth of submerged macrophytes by reducing the shading effect. We further hypothesized that this effect would be more pronounced at higher nutrient loadings/concentrations which, otherwise, would result in a stronger negative pressure on submerged macrophytes. In order to test our hypotheses, we conducted an outdoor mesocosm experiment to elucidate the effects of snails (R. swinhoei) on aquatic ecosystems under contrasting nutrient loading scenarios.