Nutrient enrichment homogenizes taxonomic and functional diversity of benthic macroinvertebrate assemblages in shallow lakes

Abstract

Eutrophication alters the trophic dynamics in lakes and may result in biotic homogenization. How nutrient enrichment drives patterns of taxonomic and functional (i.e. trait-based) homogenization of macroinvertebrate assemblages at within-lake (local) and among-lake (regional) scales is, however, not well understood. Taxonomic and functional compositions of macroinvertebrate assemblages in 41 lakes of the middle and lower reaches of the Yangtze River and Huaihe River were analyzed at within-lake and among-lake scales. Our results indicated that there was a significant difference in macroinvertebrate assemblages among lakes under different trophic status, and that total phosphorus was the major environmental factor that regulated both taxonomic and functional beta diversity of macroinvertebrate assemblages. That the abundances of pollution-tolerant species (e.g. Limnodrilus hoffmeisteri and Microchironomus tabarui) increased with trophic state contributed the most to among-lake dissimilarity. Functional beta diversity was significantly positively correlated with taxonomic beta diversity, while functional beta diversity was on average lower than taxonomic beta diversity. A combination of univariate and multivariate techniques revealed that nutrient enrichment homogenized taxonomic and functional diversity of benthic macroinvertebrate assemblages in shallow lakes at within-lake and amonglake scales, and that there was an overall trend towards taxonomic homogenization that exceeded the trend of functional homogenization. Thus, taxonomic and functional compositions should be considered simultaneously to improve understanding of the response of aquatic communities to anthropogenic disturbance, as the loss and gain of species may be influenced by species-specific features, and functional composition may exhibit a relatively high correspondence with changes in environmental conditions. Introduction Focusing on species composition is the traditional approach to describe ecological communities, and it treats all species as functionally equivalent and phylogenetically independent (Petchey and Gaston 2006). The variation in species composition may thus sometimes fall short in providing a comprehensive picture of community assembly (Carmona et al. 2016; Devictor et al. 2010). Current research emphasizes that multiple facets of biodiversity (i.e., taxonomic, functional, and phylogenetic diversity) should be considered to provide a clearer picture of spatial patterning of ecological communities (Cai et al. 2018; Devictor et al. 2010). Functional (or trait-based) approaches can provide a more mechanistic perspective of the community-environment relationships and functioning of ecosystems in comparison to purely taxonomic approaches (Cadotte et al. 2011). This is because species primarily react to the environmental gradients through the specific functional traits and roles they play in an ecosystem (Carmona et al. 2016). Species composition may also be affected by dispersal and other stochastic forces (Heino et al. 2015b), while traits may be phylogenetically conserved, with closely-related species being adapted to similar environmental conditions and having equivalent traits and being affected by environmental filtering (Heino and Tolonen 2017). Moreover, functional composition may exhibit a relatively high correspondence with changes in environmental conditions, reflecting resilience of ecosystems (Göthe et al. 2017; Laliberté et al. 2010). Biodiversity can be divided into alpha, gamma and beta diversity (Whittaker 1960), of which beta diversity has gained increasing interest in recent years (Anderson et al. 2011). Beta diversity is a function of the compositional dissimilarity of biotic assemblages among sites or along environmental gradients (Donohue et al. 2009). The reduction in beta diversity leads to biotic homogenization, which is considered to be one of the most widespread forms of biotic impoverishment on the earth (Menezes et al. 2015). Biotic homogenization is the process by which biological differences of regional biotas in any organizational level decrease over time, in terms of genetic, taxonomic or functional features. It is a multifaceted process which involves environmental alterations, species invasions and extinctions (Petsch 2016; Olden and Rooney 2006). Homogenization of environmental conditions resulting from anthropogenic activities could contribute to biotic homogenization (Zorzalalmeida et al. 2017). Nevertheless, biotic homogenization is not random because the loss and gain of species may be influenced by species-specific features (Brice et al. 2017; McKinney et al. 1999). More sensitive species may be replaced by more tolerant species following environmental change, leading to increase of the similarity in species features, i.e. functional homogenization (Olden and Rooney 2006; McKinney et al. 1999). Although functional and taxonomic homogenization may occur simultaneously, patterns in these two processes might differ. Previous research indicated that functional homogenization exceeded taxonomic homogenization among European freshwater fish assemblages (Villéger et al. 2014), while Su et al. (2015) reported that taxonomic homogenization exceeded functional homogenization of fish assemblages in Yunnan, China. The relationship between taxonomic and functional homogenization varies greatly, depending on the initial habitat conditions and species composition (Su et al. 2015). If species of the original ecosystem status share similar traits, a decrease in species richness or a slight taxonomic homogenization may have no effect on the functional composition and subsequently on ecosystem function (Sonnier et al. 2014). Different responses of taxonomic and functional homogenization to environmental changes should thus be assessed to better understand biotic homogenization. Eutrophication resulting from nutrient enrichment, mainly driven by nitrogen and phosphorus, comprises a globally important anthropogenic threat to aquatic ecosystems (Heisler et al. 2008). The negative effects of nutrient enrichment on the ecosystem may be expected, wherever nutrient enrichment increases environmental degradation and decreases oxygen availability and habitat structural complexity (Wengrat et al. 2017; Donohue et al. 2009). Anthropogenic nutrient enrichment can alter community structure of aquatic organisms (Carvalho et al. 2006), e.g. through increase of phytoplankton biomass and algal blooms, and degradation of macrophyte cover, which would lead to consequent changes in the ecological functioning of lakes, e.g. energy flows, nutrient cycling and ecosystem services they provide to humans (Heisler et al. 2008; Schindler 2006). Many studies have focused on the impacts of eutrophication on species-based beta diversity and species richness (Zorzalalmeida et al. 2017; Dawson et al. 2016; Bini et al. 2014). For example, Donohue et al. (2009) found that nutrient enrichment led to taxonomic homogenization of lake benthic assemblages at both within-lake and among-lake scales. Menezes et al. (2015) found that fish species richness and diversity converged with progressive eutrophication, and eutrophication homogenized fish community composition in the littoral zone. However, current understanding of its effects on aquatic organisms has almost entirely focused on the change in taxonomic similarity between assemblages, whereas knowledge on functional diversity remains poor. This study was based on surveys of benthic macroinvertebrates of 41 subtropical shallow lakes across the middle and lower reaches of the Yangtze River and Huaihe River system in China, for which eutrophication is one of the major environmental problems. In this study, we hypothesized that nutrient enrichment would lead to taxonomic and functional (i.e. inferred from static trait-based information) homogenization of lake benthic assemblages at both local (within-lake) and regional (among-lake) scales (Su et al. 2015; Villéger et al. 2014). Furthermore, we expected that taxonomic homogenization would be larger than functional homogenization since functional redundancy of some species exists (Baiser and Lockwood 2011). Specifically, the loss of some functions due to species loss in a community may be supplemented by the remaining species. Materials and Methods Study area and lakes The middle and lower reaches of the Yangtze River and Huaihe River (MLYH) belong to the warm temperate monsoon and sub-humid climate region, with high density of freshwater lakes. This region is highly developed, with relatively high levels of urban and agricultural development. The middle and lower reaches of the Yangtze River and Huaihe River cover an area of 1,051,000 km 2 , with a mean annual rainfall of above 1,000 mm, and contains approximately 655 (surface area > 1 km 2 ) freshwater lakes, with a total water area of 20,529 km 2 (Jiang et al. 2009). Many lakes in MLYH have experienced dramatic environmental degradation over the past three decades, due to the influence of human activities (Le et al. 2010). The sediments of these lakes were mainly composed of fine sediment, with relatively high background nutrient concentrations (Yang et al. 2010). In this study, 41 shallow lakes were investigated within this region, and six sampling sites of each lake were sampled, making up a total of 246 samples (Fig. 1, Table S1). Generally, the six sampling sites were randomly distributed in sublittoral zones since all the studied lakes were very shallow and without profundal zone (max water depth < 8.2 m, mean water depth < 5.2 m) (Table S1). Field sampling and laboratory analyses Macroinvertebrate samples were collected during April to June in 2012. Sampling was conducted with 1/16 m 2 modified Peterson grab, with six grabs comprising a sample. All materials collected from a site were pooled and rinsed in the field to remove fine sediments, and all remaining materials were fixed with a 7% buffer