A global agenda for advancing freshwater biodiversity research.

Global freshwater biodiversity is declining dramatically, and meeting the challenges of this crisis requires bold goals and the mobilisation of substantial resources. While the reasons are varied, investments in both research and conservation of freshwater biodiversity lag far behind those in the terrestrial and marine realms. Inspired by a global consultation, we identify 15 pressing priority needs, grouped into five research areas, in an effort to support informed stewardship of freshwater biodiversity. The proposed agenda aims to advance freshwater biodiversity research globally as a critical step in improving coordinated actions towards its sustainable management and conservation.

Phytoplankton and cyanobacteria abundances in mid-21st century lakes depend strongly on future land use and climate projections.

Land use and climate change are anticipated to affect phytoplankton of lakes worldwide. The effects will depend on the magnitude of projected land use and climate changes and lake sensitivity to these factors. We used random forests fit with long-term (1971-2016) phytoplankton and cyanobacteria abundance time series, climate observations (1971-2016), and upstream catchment land use (global Clumondo models for the year 2000) data from 14 European and 15 North American lakes basins. We projected future phytoplankton and cyanobacteria abundance in the 29 focal lake basins and 1567 lakes across focal regions based on three land use (sustainability, middle of the road, and regional rivalry) and two climate (RCP 2.6 and 8.5) scenarios to mid-21st century. On average, lakes are expected to have higher phytoplankton and cyanobacteria due to increases in both urban land use and temperature, and decreases in forest habitat. However, the relative importance of land use and climate effects varied substantially among regions and lakes. Accounting for land use and climate changes in a combined way based on extensive data allowed us to identify urbanization as the major driver of phytoplankton development in lakes located in urban areas, and climate as major driver in lakes located in remote areas where past and future land use changes were minimal. For approximately one-third of the studied lakes, both drivers were relatively important. The results of this large scale study suggest the best approaches for mitigating the effects of human activity on lake phytoplankton and cyanobacteria will depend strongly on lake sensitivity to long-term change and the magnitude of projected land use and climate changes at a given location. Our quantitative analyses suggest local management measures should focus on retaining nutrients in urban landscapes to prevent nutrient pollution from exacerbating ongoing changes to lake ecosystems from climate change.

Earlier winter/spring runoff and snowmelt during warmer winters lead to lower summer chlorophyll-a in north temperate lakes.

Winter conditions, such as ice cover and snow accumulation, are changing rapidly at northern latitudes and can have important implications for lake processes. For example, snowmelt in the watershed-a defining feature of lake hydrology because it delivers a large portion of annual nutrient inputs-is becoming earlier. Consequently, earlier and a shorter duration of snowmelt are expected to affect annual phytoplankton biomass. To test this hypothesis, we developed an index of runoff timing based on the date when 50% of cumulative runoff between January 1 and May 31 had occurred. The runoff index was computed using stream discharge for inflows, outflows, or for flows from nearby streams for 41 lakes in Europe and North America. The runoff index was then compared with summer chlorophyll-a (Chl-a) concentration (a proxy for phytoplankton biomass) across 5-53 years for each lake. Earlier runoff generally corresponded to lower summer Chl-a. Furthermore, years with earlier runoff also had lower winter/spring runoff magnitude, more protracted runoff, and earlier ice-out. We examined several lake characteristics that may regulate the strength of the relationship between runoff timing and summer Chl-a concentrations; however, our tested covariates had little effect on the relationship. Date of ice-out was not clearly related to summer Chl-a concentrations. Our results indicate that ongoing changes in winter conditions may have important consequences for summer phytoplankton biomass and production.

Long-term warming destabilizes aquatic ecosystems through weakening biodiversity-mediated causal networks.

Understanding how ecosystems will respond to climate changes requires unravelling the network of functional responses and feedbacks among biodiversity, physicochemical environments, and productivity. These ecosystem components not only change over time but also interact with each other. Therefore, investigation of individual relationships may give limited insights into their interdependencies and limit ability to predict future ecosystem states. We address this problem by analyzing long-term (16-39 years) time series data from 10 aquatic ecosystems and using convergent cross mapping (CCM) to quantify the causal networks linking phytoplankton species richness, biomass, and physicochemical factors. We determined that individual quantities (e.g., total species richness or nutrients) were not significant predictors of ecosystem stability (quantified as long-term fluctuation of phytoplankton biomass); rather, the integrated causal pathway in the ecosystem network, composed of the interactions among species richness, nutrient cycling, and phytoplankton biomass, was the best predictor of stability. Furthermore, systems that experienced stronger warming over time had both weakened causal interactions and larger fluctuations. Thus, rather than thinking in terms of separate factors, a more holistic network view, that causally links species richness and the other ecosystem components, is required to understand and predict climate impacts on the temporal stability of aquatic ecosystems.

Storm impacts on phytoplankton community dynamics in lakes.

In many regions across the globe, extreme weather events such as storms have increased in frequency, intensity, and duration due to climate change. Ecological theory predicts that such extreme events should have large impacts on ecosystem structure and function. High winds and precipitation associated with storms can affect lakes via short-term runoff events from watersheds and physical mixing of the water column. In addition, lakes connected to rivers and streams will also experience flushing due to high flow rates. Although we have a well-developed understanding of how wind and precipitation events can alter lake physical processes and some aspects of biogeochemical cycling, our mechanistic understanding of the emergent responses of phytoplankton communities is poor. Here we provide a comprehensive synthesis that identifies how storms interact with lake and watershed attributes and their antecedent conditions to generate changes in lake physical and chemical environments. Such changes can restructure phytoplankton communities and their dynamics, as well as result in altered ecological function (e.g., carbon, nutrient and energy cycling) in the short- and long-term. We summarize the current understanding of storm-induced phytoplankton dynamics, identify knowledge gaps with a systematic review of the literature, and suggest future research directions across a gradient of lake types and environmental conditions.

Evaluating early-warning indicators of critical transitions in natural aquatic ecosystems.

Ecosystems can show sudden and persistent changes in state despite only incremental changes in drivers. Such critical transitions are difficult to predict, because the state of the system often shows little change before the transition. Early-warning indicators (EWIs) are hypothesized to signal the loss of system resilience and have been shown to precede critical transitions in theoretical models, paleo-climate time series, and in laboratory as well as whole lake experiments. The generalizability of EWIs for detecting critical transitions in empirical time series of natural aquatic ecosystems remains largely untested, however. Here we assessed four commonly used EWIs on long-term datasets of five freshwater ecosystems that have experienced sudden, persistent transitions and for which the relevant ecological mechanisms and drivers are well understood. These case studies were categorized by three mechanisms that can generate critical transitions between alternative states: competition, trophic cascade, and intraguild predation. Although EWIs could be detected in most of the case studies, agreement among the four indicators was low. In some cases, EWIs were detected considerably ahead of the transition. Nonetheless, our results show that at present, EWIs do not provide reliable and consistent signals of impending critical transitions despite using some of the best routinely monitored freshwater ecosystems. Our analysis strongly suggests that a priori knowledge of the underlying mechanisms driving ecosystem transitions is necessary to identify relevant state variables for successfully monitoring EWIs.

Ecology under lake ice.

Winter conditions are rapidly changing in temperate ecosystems, particularly for those that experience periods of snow and ice cover. Relatively little is known of winter ecology in these systems, due to a historical research focus on summer 'growing seasons'. We executed the first global quantitative synthesis on under-ice lake ecology, including 36 abiotic and biotic variables from 42 research groups and 101 lakes, examining seasonal differences and connections as well as how seasonal differences vary with geophysical factors. Plankton were more abundant under ice than expected; mean winter values were 43.2% of summer values for chlorophyll a, 15.8% of summer phytoplankton biovolume and 25.3% of summer zooplankton density. Dissolved nitrogen concentrations were typically higher during winter, and these differences were exaggerated in smaller lakes. Lake size also influenced winter-summer patterns for dissolved organic carbon (DOC), with higher winter DOC in smaller lakes. At coarse levels of taxonomic aggregation, phytoplankton and zooplankton community composition showed few systematic differences between seasons, although literature suggests that seasonal differences are frequently lake-specific, species-specific, or occur at the level of functional group. Within the subset of lakes that had longer time series, winter influenced the subsequent summer for some nutrient variables and zooplankton biomass.

Winter severity determines functional trait composition of phytoplankton in seasonally ice-covered lakes.

How climate change will affect the community dynamics and functionality of lake ecosystems during winter is still little understood. This is also true for phytoplankton in seasonally ice-covered temperate lakes which are particularly vulnerable to the presence or absence of ice. We examined changes in pelagic phytoplankton winter community structure in a north temperate lake (Müggelsee, Germany), covering 18 winters between 1995 and 2013. We tested how phytoplankton taxa composition varied along a winter-severity gradient and to what extent winter severity shaped the functional trait composition of overwintering phytoplankton communities using multivariate statistical analyses and a functional trait-based approach. We hypothesized that overwintering phytoplankton communities are dominated by taxa with trait combinations corresponding to the prevailing winter water column conditions, using ice thickness measurements as a winter-severity indicator. Winter severity had little effect on univariate diversity indicators (taxon richness and evenness), but a strong relationship was found between the phytoplankton community structure and winter severity when taxon trait identity was taken into account. Species responses to winter severity were mediated by the key functional traits: motility, nutritional mode, and the ability to form resting stages. Accordingly, one or the other of two functional groups dominated the phytoplankton biomass during mild winters (i.e., thin or no ice cover; phototrophic taxa) or severe winters (i.e., thick ice cover; exclusively motile taxa). Based on predicted milder winters for temperate regions and a reduction in ice-cover durations, phytoplankton communities during winter can be expected to comprise taxa that have a relative advantage when the water column is well mixed (i.e., need not be motile) and light is less limiting (i.e., need not be mixotrophic). A potential implication of this result is that winter severity promotes different communities at the vernal equinox, which may have different nutritional quality for the next trophic level and ecosystem-scale effects.

Global impacts of the 1980s regime shift.

Despite evidence from a number of Earth systems that abrupt temporal changes known as regime shifts are important, their nature, scale and mechanisms remain poorly documented and understood. Applying principal component analysis, change-point analysis and a sequential t-test analysis of regime shifts to 72 time series, we confirm that the 1980s regime shift represented a major change in the Earth's biophysical systems from the upper atmosphere to the depths of the ocean and from the Arctic to the Antarctic, and occurred at slightly different times around the world. Using historical climate model simulations from the Coupled Model Intercomparison Project Phase 5 (CMIP5) and statistical modelling of historical temperatures, we then demonstrate that this event was triggered by rapid global warming from anthropogenic plus natural forcing, the latter associated with the recovery from the El Chichón volcanic eruption. The shift in temperature that occurred at this time is hypothesized as the main forcing for a cascade of abrupt environmental changes. Within the context of the last century or more, the 1980s event was unique in terms of its global scope and scale; our observed consequences imply that if unavoidable natural events such as major volcanic eruptions interact with anthropogenic warming unforeseen multiplier effects may occur.

Synchronous dynamics of zooplankton competitors prevail in temperate lake ecosystems.

Although competing species are expected to exhibit compensatory dynamics (negative temporal covariation), empirical work has demonstrated that competitive communities often exhibit synchronous dynamics (positive temporal covariation). This has led to the suggestion that environmental forcing dominates species dynamics; however, synchronous and compensatory dynamics may appear at different length scales and/or at different times, making it challenging to identify their relative importance. We compiled 58 long-term datasets of zooplankton abundance in north-temperate and sub-tropical lakes and used wavelet analysis to quantify general patterns in the times and scales at which synchronous/compensatory dynamics dominated zooplankton communities in different regions and across the entire dataset. Synchronous dynamics were far more prevalent at all scales and times and were ubiquitous at the annual scale. Although we found compensatory dynamics in approximately 14% of all combinations of time period/scale/lake, there were no consistent scales or time periods during which compensatory dynamics were apparent across different regions. Our results suggest that the processes driving compensatory dynamics may be local in their extent, while those generating synchronous dynamics operate at much larger scales. This highlights an important gap in our understanding of the interaction between environmental and biotic forces that structure communities.

To bloom or not to bloom: contrasting responses of cyanobacteria to recent heat waves explained by critical thresholds of abiotic drivers.

Past heat waves are considered harbingers of future climate change. In this study, we have evaluated the effects of two recent Central European summer heat waves (2003 and 2006) on cyanobacterial blooms in a eutrophic, shallow lake. While a bloom of cyanobacteria developed in 2006, consistent with our expectations, cyanobacterial biomass surprisingly remained at a record-low during the entire summer of 2003. Critical thresholds of abiotic drivers extracted from the long-term (1993-2007) data set of the studied lake using classification tree analysis (CTA) proved suitable to explain these observations. We found that cyanobacterial blooms were especially favoured in 2006 because thermal stratification was critically intense (Schmidt stability >44 g cm cm(-2)) and long-lasting (>3 weeks). Our results also suggest that some cyanobacterial species (Anabaena sp.) benefitted directly from the stable water column, whereas other species (Planktothrix sp.) took advantage of stratification-induced internal nutrient loading. In 2003, conditions were less favourable for cyanobacteria due to a spell of lower temperatures and stronger winds in mid-summer; as a result, the identified thresholds of thermal stratification were hardly ever reached. Overall, our study shows that extracting critical thresholds of environmental drivers from long-term records is a promising avenue for predicting ecosystem responses to future climate warming. Specifically, our results emphasize that not average temperature increase but changes in short-term meteorological variability will determine whether cyanobacteria will bloom more often in a warmer world.

Phytoplankton responses to repeated pulse perturbations imposed on a trend of increasing eutrophication.

While eutrophication remains one of the main pressures acting on freshwater ecosystems, the prevalence of anthropogenic and nature-induced stochastic pulse perturbations is predicted to increase due to climate change. Despite all our knowledge on the effects of eutrophication and stochastic events operating in isolation, we know little about how eutrophication may affect the response and recovery of aquatic ecosystems to pulse perturbations. There are multiple ways in which eutrophication and pulse perturbations may interact to induce potentially synergic changes in the system, for instance, by increasing the amount of nutrients released after a pulse perturbation. Here, we performed a controlled press and pulse perturbation experiment using mesocosms filled with natural lake water to address how eutrophication modulates the phytoplankton response to sequential mortality pulse perturbations; and what is the combined effect of press and pulse perturbations on the resistance and resilience of the phytoplankton community. Our experiment showed that eutrophication increased the absolute scale of the chlorophyll-a response to pulse perturbations but did not change the proportion of the response relative to its pre-event condition (resistance). Moreover, the capacity of the community to recover from pulse perturbations was significantly affected by the cumulative effect of sequential pulse perturbations but not by eutrophication itself. By the end of the experiment, some mesocosms could not recover from pulse perturbations, irrespective of the trophic state induced by the press perturbation. While not resisting or recovering any less from pulse perturbations, phytoplankton communities from eutrophying systems showed chlorophyll-a levels much higher than non-eutrophying ones. This implies that the higher absolute response to stochastic pulse perturbations in a eutrophying system may increase the already significant risks for water quality (e.g., algal blooms in drinking water supplies), even if the relative scale of the response to pulse perturbations between eutrophying and non-eutrophying systems remains the same.

Causal networks of phytoplankton diversity and biomass are modulated by environmental context.

Untangling causal links and feedbacks among biodiversity, ecosystem functioning, and environmental factors is challenging due to their complex and context-dependent interactions (e.g., a nutrient-dependent relationship between diversity and biomass). Consequently, studies that only consider separable, unidirectional effects can produce divergent conclusions and equivocal ecological implications. To address this complexity, we use empirical dynamic modeling to assemble causal networks for 19 natural aquatic ecosystems (N24◦~N58◦) and quantified strengths of feedbacks among phytoplankton diversity, phytoplankton biomass, and environmental factors. Through a cross-system comparison, we identify macroecological patterns; in more diverse, oligotrophic ecosystems, biodiversity effects are more important than environmental effects (nutrients and temperature) as drivers of biomass. Furthermore, feedback strengths vary with productivity. In warm, productive systems, strong nitrate-mediated feedbacks usually prevail, whereas there are strong, phosphate-mediated feedbacks in cold, less productive systems. Our findings, based on recovered feedbacks, highlight the importance of a network view in future ecosystem management.

Global data set of long-term summertime vertical temperature profiles in 153 lakes.

Climate change and other anthropogenic stressors have led to long-term changes in the thermal structure, including surface temperatures, deepwater temperatures, and vertical thermal gradients, in many lakes around the world. Though many studies highlight warming of surface water temperatures in lakes worldwide, less is known about long-term trends in full vertical thermal structure and deepwater temperatures, which have been changing less consistently in both direction and magnitude. Here, we present a globally-expansive data set of summertime in-situ vertical temperature profiles from 153 lakes, with one time series beginning as early as 1894. We also compiled lake geographic, morphometric, and water quality variables that can influence vertical thermal structure through a variety of potential mechanisms in these lakes. These long-term time series of vertical temperature profiles and corresponding lake characteristics serve as valuable data to help understand changes and drivers of lake thermal structure in a time of rapid global and ecological change.

Environmental stability and lake zooplankton diversity - contrasting effects of chemical and thermal variability.

Environmental variability in space and time is a primary mechanism allowing species that share resources to coexist. Fluctuating conditions are a double edged sword for diversity, either promoting coexistence through temporal niche partitioning or excluding species by stochastic extinctions. The net effect of environmental variation on diversity is largely unknown. We examined the association between zooplankton species richness in lakes and environmental variability on interannual, seasonal and shorter time scales, as well as long-term average conditions. We analyzed data on physical, chemical and biological limnology in 53 temperate zone lakes in North America and Europe sampled over a combined 1042 years. Large fluctuations in pH, phosphorus and dissolved organic carbon concentration on different time scales were associated with reduced zooplankton species richness. More species were found in lakes that showed greater temperature variation on all time scales. Environmental variability on different time scales showed similar or, in some cases, stronger associations with zooplankton species richness compared with long-term average conditions. Our results suggest that temporal fluctuations in the chemical environment tend to exclude zooplankton species while temperature variability promotes greater richness. The results indicate that anthropogenic increases in temporal variability of future climates may have profound effects on biodiversity.

Meta-analysis of multidecadal biodiversity trends in Europe.

Local biodiversity trends over time are likely to be decoupled from global trends, as local processes may compensate or counteract global change. We analyze 161 long-term biological time series (15-91 years) collected across Europe, using a comprehensive dataset comprising ~6,200 marine, freshwater and terrestrial taxa. We test whether (i) local long-term biodiversity trends are consistent among biogeoregions, realms and taxonomic groups, and (ii) changes in biodiversity correlate with regional climate and local conditions. Our results reveal that local trends of abundance, richness and diversity differ among biogeoregions, realms and taxonomic groups, demonstrating that biodiversity changes at local scale are often complex and cannot be easily generalized. However, we find increases in richness and abundance with increasing temperature and naturalness as well as a clear spatial pattern in changes in community composition (i.e. temporal taxonomic turnover) in most biogeoregions of Northern and Eastern Europe.

Deeper waters are changing less consistently than surface waters in a global analysis of 102 lakes.

Globally, lake surface water temperatures have warmed rapidly relative to air temperatures, but changes in deepwater temperatures and vertical thermal structure are still largely unknown. We have compiled the most comprehensive data set to date of long-term (1970-2009) summertime vertical temperature profiles in lakes across the world to examine trends and drivers of whole-lake vertical thermal structure. We found significant increases in surface water temperatures across lakes at an average rate of + 0.37 °C decade-1, comparable to changes reported previously for other lakes, and similarly consistent trends of increasing water column stability (+ 0.08 kg m-3 decade-1). In contrast, however, deepwater temperature trends showed little change on average (+ 0.06 °C decade-1), but had high variability across lakes, with trends in individual lakes ranging from - 0.68 °C decade-1 to + 0.65 °C decade-1. The variability in deepwater temperature trends was not explained by trends in either surface water temperatures or thermal stability within lakes, and only 8.4% was explained by lake thermal region or local lake characteristics in a random forest analysis. These findings suggest that external drivers beyond our tested lake characteristics are important in explaining long-term trends in thermal structure, such as local to regional climate patterns or additional external anthropogenic influences.

Lakes as sentinels of climate change.

While there is a general sense that lakes can act as sentinels of climate change, their efficacy has not been thoroughly analyzed. We identified the key response variables within a lake that act as indicators of the effects of climate change on both the lake and the catchment. These variables reflect a wide range of physical, chemical, and biological responses to climate. However, the efficacy of the different indicators is affected by regional response to climate change, characteristics of the catchment, and lake mixing regimes. Thus, particular indicators or combinations of indicators are more effective for different lake types and geographic regions. The extraction of climate signals can be further complicated by the influence of other environmental changes, such as eutrophication or acidification, and the equivalent reverse phenomena, in addition to other land-use influences. In many cases, however, confounding factors can be addressed through analytical tools such as detrending or filtering. Lakes are effective sentinels for climate change because they are sensitive to climate, respond rapidly to change, and integrate information about changes in the catchment.

Energetic equivalence underpins the size structure of tree and phytoplankton communities.

The size structure of autotroph communities - the relative abundance of small vs. large individuals - shapes the functioning of ecosystems. Whether common mechanisms underpin the size structure of unicellular and multicellular autotrophs is, however, unknown. Using a global data compilation, we show that individual body masses in tree and phytoplankton communities follow power-law distributions and that the average exponents of these individual size distributions (ISD) differ. Phytoplankton communities are characterized by an average ISD exponent consistent with three-quarter-power scaling of metabolism with body mass and equivalence in energy use among mass classes. Tree communities deviate from this pattern in a manner consistent with equivalence in energy use among diameter size classes. Our findings suggest that whilst universal metabolic constraints ultimately underlie the emergent size structure of autotroph communities, divergent aspects of body size (volumetric vs. linear dimensions) shape the ecological outcome of metabolic scaling in forest vs. pelagic ecosystems.