Re-oligotrophication and warming stabilize phytoplankton networks.

Phytoplankton taxa are strongly interconnected as a network, which could show temporal dynamics and non-linear responses to changes in drivers at both seasonal and long-term scale. Using a high quality dataset of 20 Danish lakes (1989-2008), we applied extended Local Similarity Analysis to construct temporal network of phytoplankton communities for each lake, obtained sub-network for each sampling month, and then measured indices of network complexity and stability for each sub-network. We assessed how lake re-oligotrophication, climate warming and grazers influenced the temporal dynamics on network complexity and stability of phytoplankton community covering three aspects: seasonal trends, long-term trends and detrended variability. We found strong seasonality for the complexity and stability of phytoplankton network, an increasing trend for the average degree, modularity, nestedness, persistence and robustness, and a decreasing trend for connectance, negative:positive interactions and vulnerability. Our study revealed a cascading effect of lake re-oligotrophication, climate warming and zooplankton grazers on phytoplankton network stability through changes in network complexity characterizing diversity, interactions and topography. Network stability of phytoplankton increased with average degree, modularity, nestedness and decreased with connectance and negative:positive interactions. Oligotrophication and warming stabilized the phytoplankton network (enhanced robustness, persistence and decreased vulnerability) by enhancing its average degree, modularity, nestedness and by reducing its connectance, while zooplankton richness promoted stability of phytoplankton network through increases in average degree and decreases in negative interactions. Our results further indicate that the stabilization effects might lead to more closed, compartmentalized and nested interconnections especially in the deeper lakes, in the warmer seasons and during bloom periods. From a temporal dynamic network view, our findings highlight stabilization of the phytoplankton community as an adaptive response to lake re-oligotrophication, climate warming and grazers.

Weakened casual feedback loops following intensive restoration efforts and climate changes in a large shallow freshwater lake.

Understanding how phytoplankton interacts with local and regional drivers as well as their feedbacks is a great challenge, and quantitative analyses of the regulating role of human activities and climate changes on these feedback loops are also limited. By using monthly monitoring dataset (2000-2017) from Lake Taihu and empirical dynamic modelling to construct causal networks, we quantified the strengths of causal feedbacks among phytoplankton, local environments, zooplankton, meteorology as well as global climate oscillation. Prevalent bidirectional causal linkages between phytoplankton biomass (chlorophyll a) and the tested drivers were found, providing holistic and quantitative evidence of the ubiquitous feedback loops. Phytoplankton biomass exhibited the highest feedbacks with total inorganic nitrogen and ammonia and the lowest with nitrate. The feedbacks between phytoplankton biomass and environmental factors from 2000 to 2017 could be classified into two groups: the local environments (e.g., nutrients, pH, transparency, zooplankton biomass)-driven enhancement loops promoting the response of the phytoplankton biomass, and the climate (e.g., wind speed)-driven regulatory loops suppressing it. The two counterbalanced groups modified the emergent macroecological patterns. Our findings revealed that the causal feedback networks loosened significantly after 2007 following nutrient loading reduction and unsuccessful biomanipulation restoration attempts by stocking carp. The strength of enhancement loops underwent marked decreases leading to reduced phytoplankton responses to the tested drivers, while the climate (decreasing wind speed, warming winter)-driven regulatory loops increased- like a tug-of-war. To counteract the self-amplifying feedback loops, the present eutrophication mitigation efforts, especially nutrient reduction, should be continued, and introduction of alternative measures to indirectly regulate the critical components (e.g., pH, Secchi depth, zooplankton biomass) of the loops would be beneficial.

How Eutrophication Promotes Exotic Aquatic Plant Invasion in the Lake Littoral Zone?

Eutrophication and exotic species invasion are key drivers of the global loss of biodiversity and ecosystem functions in lakes. We selected two exotic plants (Alternanthera philoxeroides and Myriophyllum aquaticum) and two native plants (Myriophyllum spicatum and Vallisneria spinulosa) to elucidate the effect of eutrophication on exotic plant invasiveness. We found that (1) elevated nutrient favored invasion of exotic species and inhibited growth of native plants. Species combinations and plant densities of native plants had limited effects on the resistance to invasion of the exotics. (2) A. philoxeroides featured the tightest connectivity among traits, which is consistent with its high competitive ability. Although eutrophication caused physiological stress to A. philoxeroides, it could effectively regulate enzyme activity and alleviate the stress. (3) M. aquaticum possessed strong tolerance to habitat disturbance and was highly disruptive to the surrounding plants. Eutrophication will exacerbate the adverse effects of M. aquaticum on the littoral ecosystem. (4) Nutrient enrichment reduced the biomass and relative growth rates of V. spinulosa and lowered phenolics and starch contents of M. spicatum, thereby making them more susceptible to habitat fluctuations. Overall, our study highlights how eutrophication alters the invasiveness of exotic plants and the resistance of native plants in the littoral zone, which is of relevance in a world with intensified human activities.

Floating Mat Formation Makes Zizania latifolia More Competitive under the Conditions of Continuous Significant Water Level Rise.

Water level rise is considered an environmental filter for the growth and reproduction of aquatic plants in lakes. Some emergent macrophytes can form floating mats, enabling them to escape from the negative effects of deep water. However, an understanding of which species can be uprooted and form floating mats easily and what factors affect these tendencies remains greatly elusive. We conducted an experiment to determine whether the monodominance of Zizania latifolia in the emergent vegetation community in Lake Erhai was related to its floating mat formation ability and to try to find the reasons for its floating mat formation ability during the continuous increase in water level over the past few decades. Our results showed that both the frequency and biomass proportion of Z. latifolia were greater among the plants on the floating mats. Furthermore, Z. latifolia was more likely to be uprooted than the other three previously dominant emergent species due to its smaller angle between the plant and the horizontal plane, rather than the root:shoot or volume:mass ratios. The dominance of Z. latifolia in the emergent community in Lake Erhai is due to its easier ability to become uprooted, allowing it to outperform other emergent species and become the single dominant emergent species under the environmental filter of deep water. The ability to uproot and form floating mats may be a competitive survival strategy for emergent species under the conditions of continuous significant water level rise.

Linking trait network to growth performance of submerged macrophytes in response to ammonium pulse.

Extreme precipitation events caused by climate change leads to large variation of nitrogen input to aquatic ecosystems. Our previous study demonstrated the significant effect of different ammonium pulse patterns (differing in magnitude and frequency) on submersed macrophyte growth based on six plant morphological traits. However, how connectivity among plant traits responds to nitrogen pulse changes, which in turn affects plant performance, has not yet been fully elucidated. The response of three common submersed macrophytes (Myriophyllum spicatum, Vallisneria natans and Potamogeton maackianus) to three ammonium pulse patterns was tested using plant trait network (PTN) analysis based on 18 measured physiological and morphological traits. We found that ammonium pulses enhanced trait connectivity in PTN, which may enable plants to assimilate ammonium and/or mitigate ammonium toxicity. Large input pulses with low frequency had stronger effects on PTNs compared to low input pulses with high frequency. Due to the cumulative and time-lagged effect of the plant response to the ammonium pulse, there was a profound and prolonged effect on plant performance after the release of the pulse. The highly connected traits in PTN were those related to biomass allocation (e.g., plant biomass, stem ratio, leaf ratio and ramet number) rather than physiological traits, while phenotype-related traits (e.g., plant height, root length and AB ratio) and energy storage-related traits (e.g., stem starch) were least connected. V. natans showed clear functional divergence among traits, making it more flexible to cope with unfavorable habitats (i.e., high input pulses with low frequencies). M. spicatum with high RGR revealed strong correlations among traits and thus supported nitrogen accumulation from favourable environments (i.e., low input pulses with high frequencies). Our study highlights the responses of PTN for submerged macrophytes to ammonium pulses depends on their intrinsic metabolic rates, the magnitude, frequency and duration of the pulses, and our results contribute to the understanding of the impact of resource pulses on the population dynamics of submersed macrophytes within the context of global climate change.

Linking human activities and global climatic oscillation to phytoplankton dynamics in a subtropical lake.

Human activities and climate change are two major stressors affecting lake ecosystems as well as phytoplankton communities worldwide. However, how the temporal dynamics of phytoplankton are directly or indirectly linked to anthropogenic activities and climatic oscillation remains unclear. We assessed the annual trends (1988-2018) in phytoplankton abundance (PA) in Lake Dongting, China and related it to five groups of variables characterizing human activities, global climate oscillation, water nutrients, hydrology, and meteorology. We found a significant increase in PA, urbanization (Upop), total nitrogen (TN), fertilizer application (FA), number of summer days (SU), and the warm speed duration index (WSDI) and a significant decrease in the water discharge of three inlets (TIWD) and the sediment discharge of three inlets (TISD) and four tributaries (FTSD) and the net sediment deposition (NSD). However, no significant annual trends were observed for the number of rainstorm days (R50mm), the simple precipitation intensity index (SDII) and yearly anomalies of El Niño-Southern oscillation events (ENSOi). Cross-correlation Function analyses demonstrated that the operation of the Three George Dam (TGD) strengthened the effects of hydrology, rainfall patterns and ENSOi on phytoplankton, but strongly weakened the association between water nutrients, human activities and phytoplankton abundance. Path analysis revealed that TP, TN, FA, R50 mm as well as WSDI had a direct positive effect on PA, while a direct negative effect was found for ENSOi, NSD and TISD. Human activities (Upop and FA), warming (WSDI and SU), and rainfall patterns (SDII and R50 mm) exerted indirect controls on phytoplankton through changes in water nutrients and hydrology. Climate change (ENSOi) had a direct effect on PA, but also showed twelve indirect pathways via changes in hydrology and meteorology (both positive and negative effects were found). Overall, meteorology contributed most markedly to the variations of PA (29.3%), followed by hydrology (25.3%), human activities (24%), water nutrients (10.5%), and ENSOi (1.9%). Our results highlight a strongly causal connection between human activities as well as global climate change and phytoplankton and the benefits of considering multiple environmental drivers in determining the temporal dynamics of lake biotic communities.

Abiotic and biotic drivers of temporal dynamics in the spatial heterogeneity of zooplankton communities across lakes in recovery from eutrophication.

Seasonal and annual dynamics of the zooplankton community in lakes are affected by changes in abiotic drivers, trophic interactions (e.g., changes in phytoplankton and fish communities and abundances) and habitat characteristics (e.g. macrophyte abundance and composition). However, little is known about the temporal responses of the zooplankton community to abiotic and biotic drivers across lakes at the regional scale. Using a comprehensive 20-year dataset from 20 Danish lakes in recovery from eutrophication, we assessed the seasonal and annual trends in the spatial heterogeneity of zooplankton community across lakes and related it to abiotic and biotic drivers. We found significant seasonality and inter-annual decreases in spatial zooplankton heterogeneity in both shallow and deep lakes, with the decrease in the spatial turnover dominating the temporal dynamics of the beta diversity. For the inter-annual changes, decreased spatial heterogeneity of phytoplankton, macrophytes and fish were important biotic drivers at the regional scale. Using a series of ordinary least squares regressions and model selection with model averaging approaches, we revealed that both local (e.g., total phosphorus, total nitrogen, pH, Secchi depth, alkalinity, Schmidt stability, water temperature) and regional drivers (e.g., air temperature, solar irradiance) were important variables influencing the spatial zooplankton heterogeneity, although the directions depended on the beta diversity measures and water depth. Our results highlight an important role of bottom-up forces through phytoplankton community as well as macrophytes and top-down forces via fishes in driving the temporal changes in zooplankton community composition patterns at the regional scale.

Seasonal and long-term trends in the spatial heterogeneity of lake phytoplankton communities over two decades of restoration and climate change.

World-wide, reducing the external nutrient loading to lakes has been the primary priority of lake management in the restoration of eutrophic lakes over the past decades, and as expected this has resulted in an increase in the local environmental heterogeneity, and thus biotic heterogeneity, within lakes. However, little is known about how the regional spatial heterogeneity of lake biotic communities changes with restoration across a landscape. Using a long-term monitoring dataset from 20 Danish lakes, we elucidated the seasonal and long-term trends in the spatial heterogeneity of climate, local abiotic variables and phytoplankton communities over two decades of restoration and climate change at landscape level. We found significant seasonality in the spatial heterogeneity of most climatic and local drivers as well as in the total beta diversity (Sørensen coefficient) and its turnover components (Simpson coefficient) of phytoplankton communities among the lakes. The seasonality tended to be less marked in deep than in shallow lakes. We found significant spatial homogenisation of most local drivers (except for alkalinity) and phytoplankton communities after two decades of restoration and that turnover dominated the temporal responses of the total beta diversity of phytoplankton communities. Path analyses showed that the homogenisation of phytoplankton communities was mainly due to a decrease in spatial heterogeneity of total phosphorus and Schmidt stability in shallow lakes and to a decrease in spatial total phosphorus and total nitrogen heterogeneity in deep lakes. However, albeit weakly, the spatial heterogeneity of the phytoplankton communities was affected indirectly by climatic warming in both shallow and deep lakes and directly by wind speed in shallow lakes. We conclude that restoration of eutrophic lakes may lead to an increase in the local heterogeneity of phytoplankton communities at lake scale and an increase in homogeneity at landscape scale.

Effects of ammonium pulse on the growth of three submerged macrophytes.

Ammonium pulse attributed to runoff of urban surface and agriculture following heavy rain is common in inland aquatic systems and can cause profoundly effects on the growth of macrophytes, especially when combined with low light. In this study, three patterns of NH4-N pulse (differing in magnitude and frequency) were applied to examine their effects on the growth of three submersed macrophytes, namely, Myriophyllum spicatum, Potamogeton maackianus, and Vallisneria natans, in terms of biomass, height, branch/ramet number, root length, leaf number, and total branch length under high and low light. Results showed that NH4-N pulse caused negative effects on the biomass of the submerged macrphytes even on the 13th day after releasing NH4-N pulse. The negative effects on M. spicatum were significantly greater than that on V. natans and P. maackianus. The effects of NH4-N pulse on specific species depended on the ammonium loading patterns. The negative effects of NH4-N pulse on P. maackianus were the strongest at high loading with low frequency, and on V. natans at moderate loading with moderate frequency. For M. spicatum, no significant differences were found among the three NH4-N pulse patterns. Low light availability did not significantly aggregate the negative effects of NH4-N pulse on the growth of the submersed macrophytes. Our study contributes to revealing the roles of NH4-N pulse on the growth of aquatic plants and its species specific effects on the dynamics of submerged macrophytes in lakes.

Local and regional drivers of turnover and nestedness components of species and functional beta diversity in lake macrophyte communities in China.

Beta diversity describes the variation in species composition between sites and is often influenced by both local and regional processes. Partitioning beta diversity into turnover (species replacement between sites) and nestedness (richness difference between sites) components may enhance our understanding of the mechanisms behind the local and regional drivers determining species composition across spatial scales. We sampled macrophyte communities in 24 lakes in two regions (Yangtze River basin and Yunnan-Guizhou plateau) of China covering broad climate and nutrient gradients. Based on both species and functional approaches, we calculated multiple-site beta diversity using the Sørensen dissimilarity index and partitioned it into turnover and nestedness coefficients crossed with two nested spatial scales: among depths within transects (transect scale) and among transects within lakes (lake scale). The overall species beta diversity and functional beta diversity (i.e. Sørensen coefficient) were significantly lower and thus more homogeneous at lake scale. Across spatial scales, species beta diversity was mainly explained by turnover patterns (56-61%) and functional beta diversity primarily by nestedness patterns (58-65%). Both local and regional drivers contributed to structuring species and functional beta diversity patterns, largely through changes in species turnover and functional nestedness, respectively. Overall, we observed a significant increase in species beta diversity and its turnover component while a decreasing trend in functional beta diversity and its nestedness component at high altitude. Our results further emphasized that the species beta diversity and its turnover component decreased at high total phosphorus concentration (TP) across the two spatial scales, while the functional beta diversity and its nestedness component decreased at high TP at the transect scale. We conclude that understanding of the relative role of local and regional drivers in determining macrophyte diversity patterns may help managers to select the most appropriate conservation strategies for preservation of biodiversity varying with the scale in focus.

Scale-dependent changes in the functional diversity of macrophytes in subtropical freshwater lakes in south China.

Ecological processes are generally scale-dependent and there is little consensus about the relative importance of deterministic versus stochastic processes in driving patterns of biological diversity. We investigated how the relationship between functional dispersion and environmental gradients changes with spatial scale in subtropical freshwater lakes. The functional alpha and beta dispersions of all the tested traits were significantly under-dispersed across spatial scales and along environmental gradients. Results showed more functional similarity within communities in leaf dry mass content and flowering duration but less functional turnover among communities in all the tested traits at regional scales (Yunnan-Guizhou plateau and the middle and low reaches of the Yangtze River). The strengths and directions of environmental effects on the functional alpha and beta dispersions depended on the selected traits, diversity metrics and spatial scales. Surprisingly, broad-scale factors - elevation and water transparency - decreased the functional turnover for most traits along the gradients, whereas fine-scale factors - water depth - produced the opposite patterns along the gradient, depending on the trait selected. Our study highlights the dominant role of deterministic assembly processes in structuring the local functional composition and governing the spatial functional turnover of macrophyte communities across multiple spatial scales.

Predicting Changes in Macrophyte Community Structure from Functional Traits in a Freshwater Lake: A Test of Maximum Entropy Model.

Trait-based approaches have been widely applied to investigate how community dynamics respond to environmental gradients. In this study, we applied a series of maximum entropy (maxent) models incorporating functional traits to unravel the processes governing macrophyte community structure along water depth gradient in a freshwater lake. We sampled 42 plots and 1513 individual plants, and measured 16 functional traits and abundance of 17 macrophyte species. Study results showed that maxent model can be highly robust (99.8%) in predicting the species relative abundance of macrophytes with observed community-weighted mean (CWM) traits as the constraints, while relative low (about 30%) with CWM traits fitted from water depth gradient as the constraints. The measured traits showed notably distinct importance in predicting species abundances, with lowest for perennial growth form and highest for leaf dry mass content. For tuber and leaf nitrogen content, there were significant shifts in their effects on species relative abundance from positive in shallow water to negative in deep water. This result suggests that macrophyte species with tuber organ and greater leaf nitrogen content would become more abundant in shallow water, but would become less abundant in deep water. Our study highlights how functional traits distributed across gradients provide a robust path towards predictive community ecology.

Functional traits composition predict macrophytes community productivity along a water depth gradient in a freshwater lake.

Functional trait composition of plant communities has been proposed as a helpful key for understanding the mechanisms of biodiversity effects on ecosystem functioning. In this study, we applied a step-wise modeling procedure to test the relative effects of taxonomic diversity, functional identity, and functional diversity on macrophytes community productivity along water depth gradient. We sampled 42 plots and 1513 individual plants and measured 16 functional traits and abundance of 17 macrophyte species. Results showed that there was a significant decrease in taxonomic diversity, functional identity (i.e., stem dry mass content, leaf [C] and leaf [N]), and functional diversity (i.e., floating leaf, mean Julian flowering date and rooting depth) with increasing water depth. For the multiple-trait functional diversity (FD) indices, functional richness decreased, while functional divergence increased with water depth gradient. Macrophyte community productivity was strongly determined by functional trait composition within community, but not significantly affected by taxonomic diversity. Community-weighted means (CWM) showed a two times higher explanatory power relative to FD indices in determining variations in community productivity. For nine of sixteen traits, CWM and FD showed significant correlations with community productivity, although the strength and direction of those relations depended on selected trait. Furthermore, functional composition in a community affected productivity through either additive or opposite effects of CWM and FD, depending on the particular traits being considered. Our results suggested both mechanisms of mass ratio and niche complementarity can operate simultaneously on variations in community productivity, and considering both CWM and FD would lead to a more profound understanding of traits-productivity relationships.

Environmental and ontogenetic effects on intraspecific trait variation of a macrophyte species across five ecological scales.

Although functional trait variability is increasingly used in community ecology, the scale- and size-dependent aspects of trait variation are usually disregarded. Here we quantified the spatial structure of shoot height, branch length, root/shoot ratio and leaf number in a macrophyte species Potamogeton maackianus, and then disentangled the environmental and ontogenetic effects on these traits. Using a hierarchical nested design, we measured the four traits from 681 individuals across five ecological scales: lake, transect, depth stratus, quadrat and individual. A notable high trait variation (coefficient variation: 48-112%) was observed within species. These traits differed in the spatial structure, depending on environmental factors of different scales. Shoot height and branch length were most responsive to lake, transect and depth stratus scales, while root/shoot ratio and leaf number to quadrat and individual scales. The trait variations caused by environment are nearly three times higher than that caused by ontogeny, with ontogenetic variance ranging from 21% (leaf number) to 33% (branch length) of total variance. Remarkably, these traits showed non-negligible ontogenetic variation (0-60%) in each ecological scale, and significant shifts in allometric trajectories at lake and depth stratus scales. Our results highlight that environmental filtering processes can sort individuals within species with traits values adaptive to environmental changes and ontogenetic variation of functional traits was non-negligible across the five ecological scales.

Linking carbon and nitrogen metabolism to depth distribution of submersed macrophytes using high ammonium dosing tests and a lake survey.

Strategies of carbon (C) and nitrogen (N) utilisation are among the factors determining plant distribution. It has been argued that submersed macrophytes adapted to lower light environments are more efficient in maintaining C metabolic homeostasis due to their conservative C strategy and ability to balance C shortage. We studied how depth distributions of 12 submersed macrophytes in Lake Erhai, China, were linked to their C-N metabolic strategies when facing acute [Formula: see text] dosing.[Formula: see text] dosing changed C-N metabolism significantly by decreasing the soluble carbohydrate (SC) content and increasing the [Formula: see text]-N and free amino acid (FAA) content of plant tissues.The proportional changes in SC contents in the leaves and FAA contents in the stems induced by [Formula: see text] dosing were closely correlated (positive for SC and negative for FAA) with the colonising water depths of the plants in Lake Erhai, the plants adapted to lower light regimes being more efficient in maintaining SC and FAA homeostasis.These results indicate that conservative carbohydrate metabolism of submersed macrophytes allowed the plants to colonise greater water depths in eutrophic lakes, where low light availability in the water column diminishes carbohydrate production by the plants.