Divergent dynamics of microbial components in two temperate shallow lakes with contrasting steady states in the Southern Hemisphere.

Factors that affect abundances of organisms in water bodies are influenced by extrinsic and intrinsic drivers that operate from outside and within a system. A high temporal coherence in the dynamics of abiotic parameters and biological communities among neighboring lakes evidences a strong extrinsic control operating similarly across lakes, and allows for prediction of ecosystems evolution in the context of global change and intensive land use. The Pampa region (Argentina) encompasses many shallow lakes submitted to different degrees of anthropic influence and showing contrasting alternative states. We studied an eutrophic clear and a hypertrophic turbid shallow lake during an annual cycle in order to evaluate whether they responded similarly to extrinsic factors or these were overridden by the effects of the steady state of each lake. Physical and chemical variables were highly coherent between both lakes, but accounted little for the large disparities among abundances and dynamics of microorganisms. While communities from the clear lake responded to a combination of extrinsic and intrinsic factors, the turbid lake showed a state less prone to be affected by climatic effects. We hypothesize that clear lakes would perform better as sentinels of climate change in the Pampa wetland.

The dynamics of picocyanobacteria from a hypereutrophic shallow lake is affected by light-climate and small-bodied zooplankton: a 10-year cytometric time-series analysis.

In aquatic systems, an interplay between bottom-up and top-down processes determines the dynamic of picocyanobacteria (Pcy) abundance and community structure. Here, we analyzed a 10-year time series (sampled fortnightly) from a hypereutrophic turbid shallow lake located within the Pampa Region of South America, generating the first long-term record of freshwater Pcy from the Southern Hemisphere. We used a cytometric approach to study Pcy community, and focused on its relations with nutrient and light conditions (bottom-up) and potential grazers (top-down). A novel Pcy abundance seasonality with winter maximums was observed for years with relatively stable hydrological levels, related with decreased abundance of seasonal rotifers during colder seasons. Pcy showed lower abundance and higher cytometric alpha diversity during summer, probably due to a strong predation exerted by rotifers. In turn, a direct effect of the non-seasonal small cladocerans Bosmina spp. decreased Pcy abundance and induced a shift from single-cell Pcy into aggregated forms. This structuring effect of Bosmina spp. was further confirmed by Pcy cytometric (dis)similarity analyses from the time series and in situ experimental data. Remarkably, Pcy showed acclimatization to underwater light variations, resembling the relevance of light in this turbid system.

Patterns of CO2 concentration and inorganic carbon limitation of phytoplankton biomass in agriculturally eutrophic lakes.

Lake eutrophication is a pervasive problem globally, particularly serious in agricultural and densely populated areas. Whenever nutrients nitrogen and phosphorus do not limit phytoplankton growth directly, high growth rates will rapidly lead to biomass increases causing self-shading and light-limitation, and eventually CO2 depletion. The paradigm of phytoplankton limitation by nutrients and light is so pervasively established, that the lack of nutrient limitation is ordinarily interpreted as sufficient evidence for the condition of light limitation, without considering the possibility of limitation by inorganic carbon. Here, we firstly evaluated how frequently CO2 undersaturation occurs in a set of eutrophic lakes in the Pampa plains. Our results confirm that conditions of CO2 undersaturation develop much more frequently (yearly 34%, summer 44%) in these agriculturally impacted lakes than in deep, temperate lakes in forested watersheds. Secondly, we used Generalized Additive Models to fit trends in CO2 concentration considering three drivers: total incident irradiance, chlorophyll a concentration, and lake depth; in eight multi-year datasets from eutrophic lakes from Europe, North and South America, Asia and New Zealand. CO2 depletion was more often observed at high irradiance levels, and shallow water. CO2 depletion also occurred at high chlorophyll concentration. Finally, we identified occurrences of light- and carbon-limitation at the whole-lake scale. The different responses of chlorophyll a and CO2 allowed us to develop criteria for detecting conditions of CO2 limitation. For the first time, we provided whole-lake evidence of carbon limitation of phytoplankton biomass. CO2 increases and eutrophication represent two major and converging environmental problems that have additive and contrasting effects, promoting phytoplankton, and also leading to carbon depletion. Their interactions deserve further exploration and imaginative approaches to deal with their effects.

Field evidence supports former experimental claims on the stimulatory effect of glyphosate on picocyanobacteria communities.

Glyphosate-based herbicides are the most commonly used herbicide worldwide. Although glyphosate is known to be toxic to aquatic organisms, it can also have stimulatory effects on small-size (ø <2 µm) cyanobacteria (Pcy) able to metabolize and degrade glyphosate and AMPA. Several previous experimental studies in micro- and mesocosms reported increases of Pcy abundance in response to glyphosate additions, but comparable field evidence is presently unavailable. We surveyed a large geographical area in order to collect information on Pcy abundance from lakes within the Pampa region (with over three decades of glyphosate usage) and lakes from Patagonia (with virtually no history of glyphosate usage). Fifty-two Pampean lakes and 24 Patagonian lakes were surveyed. We used three indicators of glyphosate impact: herbicide concentration, the presence of phosphonate metabolism genes (responsible for glyphosate and AMPA degradation) in environmental DNA samples, and descriptors of land use in the surrounding area of each lake. We addressed three questions: (1) is there field evidence of stimulatory effects of glyphosate on picocyanobacteria abundance? (2) is the magnitude of the effects of glyphosate in natural systems comparable to that reported under controlled experimental conditions? and (3), how do the effects of glyphosate compare to the effects of other potential environmental drivers of Pcy biomass? The collected evidence is consistent with the hypothesis that long-term agricultural practices relying on glyphosate-based technologies had important effects on freshwater microbial communities, particularly by promoting increases in picocyanobacteria abundance.

Species-specific phenological trends in shallow Pampean lakes' (Argentina) zooplankton driven by contemporary climate change in the Southern Hemisphere.

The relationship between the timing of recurrent biological events and seasonal climatic patterns (i.e., phenology) is a crucial ecological process. Changes in phenology are increasingly linked to global climate change. However, current evidence of phenological responses to recent climate change is subjected to substantial regional and seasonal biases. Most available evidence on climate-driven phenological changes comes from Northern Hemisphere (NH) ecosystems and typically involves increases in spring and summer temperatures, which translate into earlier onsets of spring population developments. In the Argentine Pampa region, warming has occurred at a much slower pace than in the NH, and trends are mostly restricted to increases in the minimum temperatures. We used zooplankton abundance data from Lake Chascomús (recorded every two weeks from 2005 to 2015) to evaluate potential changes in phenology. We adopted a sequential screening approach to identify taxa displaying phenological trends and evaluated whether such trends could be associated to observe long-term changes in water temperature. Two zooplankton species displayed significant later shifts in phenology metrics (end date of Brachionus havanaensis seasonal distribution: 31 day/decade, onset and end dates of Keratella americana seasonal distribution: 59 day/decade and 82 day/decade, respectively). The timing of the observed shift in B. havanaensis phenology was coincident with a warming trend in the May lake water temperature (4.7°C per decade). Analysis of abundance versus temperature patterns from six additional shallow Pampean lakes, and evaluation of previous experimental results, provided further evidence that the lake water warming trend in May was responsible for the delayed decline of B. havanaensis populations in autumn. This study is the first report of freshwater zooplankton phenology changes in the Southern Hemisphere (SH).

Occurrence and levels of glyphosate and AMPA in shallow lakes from the Pampean and Patagonian regions of Argentina.

Glyphosate (N-(phosphonomethyl)glycine) is a broad-spectrum systemic herbicide used to kill weeds that compete with commercial crops. In Argentina, the use of glyphosate-based herbicides increased dramatically (up to ∼200,000 tons on 2012) since the introduction of glyphosate-resistant crops, such as transgenic soy and resistant corn, and the adoption of non-till practices in the 1990's. Sallow lakes within the Pampa region may be potentially impacted by continuous herbicide usage. We surveyed 52 shallow lakes from the Pampa region (Buenos Aires Province, Argentina) to assess the occurrence and concentrations of glyphosate and its main degradation product (AMPA). For comparison, we also sampled 24 shallow lakes from an area with no agricultural use of glyphosate (Northern Patagonia). Glyphosate and AMPA were analyzed by UPLC-MS/MS ESI (±) in lake water, suspended particulate matter (SPM), and sediment samples. Within the Pampa region, glyphosate residues were detected in >40% of samples. Glyphosate residues were detected more frequently in sediment and surface water than in SPM samples. The mean (maximum) concentrations of glyphosate were 2.11 (4.52) µg l-1 for surface water; 0.10 (0.13) µg l-1 for SPM and 10.47 (20.34) µg kg-1 for sediment samples, respectively. Whereas, mean (maximum) concentrations of AMPA were 0.84 and (0.90) µg l-1 for surface water; 0.07 (0.07) µg l-1 for SPM; and 22.53 (32.89) µg kg-1 for sediment samples. The herbicide was not detected in samples from the Patagonian region. To our knowledge, this is the first study reporting the occurrence and concentrations of the herbicide in freshwater lakes of Argentina.

Rotifer dynamics in three shallow lakes from the Salado river watershed (Argentina): the potential modulating role of incident solar radiation.

In turbid Pampean lakes, incident solar radiation is a major driver of plankton seasonal dynamics. Higher light availability in summer translates into higher primary production, and therefore more food for zooplankton grazers. However, experimental evidence suggests that food produced under the high irradiance conditions prevailing in summer are less suitable to sustain rotifer population growth than that produced under the lower irradiance conditions typical of winter. Here, we analysed time series datasets corresponding to three shallow lakes from the Salado river watershed. This analysis provided evidence for similar seasonal patterns of rotifer relative abundance over a large geographic area. In addition, we performed life table experiments to test the hypothesis that natural seston produced in winter could sustain higher population growth rates than seston produced in summer. We suggest that the natural seasonal changes in temperature and food generate successive time windows, which may be capitalized by the different grazer species, resulting in predictable phenology of grazer populations.

Contrasting patterns of MAAs accumulation in two populations of the copepod Boeckella gracilipes.

The bio-accumulation of mycosporine-like amino acids (MAAs) is common in planktonic copepods that inhabit environments exposed to high levels of solar radiation. MAAs accumulation in copepods can be affected both by extrinsic (environmental) and intrinsic factors (local adaptation, genotype, etc.). Laboratory experiments were performed to study the bio-accumulation of MAAs in two geographically-isolated populations of Boeckella gracilipes from a mountain and a piedmont lake of North Patagonia. We performed two series of 10-day incubations of B. gracilipes from the different lakes applying two radiation conditions (PAR + UVR and darkness), at five different temperatures (5 to 20 °C) and providing a MAA-free flagellate as food. We assumed that differences in final MAAs concentrations between copepod populations should be exclusively due to environmental factors, and that any difference in the patterns of MAAs accumulation should exclusively arise from differences in MAAs concentration at the time of collection. MAAs concentration was three fold higher in B. gracilipes from Lake Verde than in copepods from the Lake Morenito. The MAAs suite was dominated (∼90%) by a combination of porphyra-334 and mycosporine-glycine in copepods from Lake Verde, and porphyra-334 and MAA-332 in those from Lake Morenito. Two exclusive MAA compounds were identified, mycosporine-glycine in copepods from Lake Verde and shinorine in the copepod population from Lake Morenito. Laboratory experiments showed that: (i) exposure to PAR + UVR stimulated the accumulation of MAAs in both copepod populations; (ii) temperature affected the response of MAAs and, remarkably, low temperatures stimulated MAAs accumulation even in dark incubations, (iii) the response to radiation and temperature in MAAs accumulation was more pronounced in the population with low initial MAAs than in the population with high initial MAAs concentrations. The differences in intrinsic factors between B. gracilipes populations, such as local adaptation to contrasting UV and temperature scenarios, among others, appear to play an important role in determining levels and patterns of MAAs accumulation in B. gracilipes.

Alternative states drive the patterns in the bacterioplankton composition in shallow Pampean lakes (Argentina).

We assessed the influence of environmental factors in shaping the free-living bacterial community structure in a set of shallow lakes characterized by contrasting stable state patterns (clear-vegetated, inorganic-turbid and phytoplankton-turbid). Six temperate shallow lakes from the Pampa Plain (Argentina) were sampled over an annual cycle, and two fingerprinting techniques were applied: a 16S rDNA analysis was performed using denaturing gradient gel electrophoresis (DGGE) profiles, and a 16S-23S internally transcribed spacer region analysis was conducted by means of automated ribosomal intergenic spacer analysis (ARISA) profiles. Our results show that the steady state that characterized the different shallow lakes played a major role in structuring the community: the composition of free-living bacteria differed significantly between clear-vegetated, inorganic-turbid and phytoplankton-turbid shallow lakes. The state of the system was more important in determining these patterns than seasonality, geographical location or degree of hydrological connectivity. Moreover, this strong environmental control was particularly evident in the pattern observed in one of the lakes, which shifted from a clear to a turbid state over the course of the study. This lake showed a directional selection of species from a typical clear-like to a turbid-like community. The combined DGGE/ARISA approach revealed not only broad patterns among different alternative steady states, but also more subtle differences within different regimes.

Seasonal variability of optical properties in a highly turbid lake (Laguna Chascomús, Argentina).

We study the underwater light field seasonality in a turbid lake, Laguna Chascomús (Buenos Aires, Argentina). We report (1) relationships between optical properties (OPs) and optically active substances (OASs); (2) relationships between inherent (IOPs) and apparent (AOPs) optical properties; and (3) the seasonal variability in OASs and OPs. Light absorption was dominated by the particulate fraction. The contributions of phytoplankton pigments and unpigmented components were similar. The best predictors of total particulate absorption, unpigmented particulate absorption, turbidity and vertical attenuation coefficient were total suspended solids or their ash content. Many OASs and OPs varied seasonally. The concentrations of OASs were higher during spring and summer, resulting in lower transparency and higher turbidity. However, mass-specific absorption coefficients displayed lower values during spring and summer. Thus, the higher light attenuation observed during spring and summer resulted from higher concentrations of relatively less absorptive OASs. Collectively, these results suggest that: (1) light extinction is enhanced during spring and summer; (2) the enhanced light extinction is due to changes in the particulate fraction; (3) the enhanced light extinction is mostly due to an increase in the amount of particulate material; and (4) the increase of particulate matter also enhanced light extinction through increased scattering.

New evidences of Roundup (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems.

Argentina is the second largest world producer of soybeans (after the USA) and along with the increase in planted surface and production in the country, glyphosate consumption has grown in the same way. We investigated the effects of Roundup (glyphosate formulation) on the periphyton colonization. The experiment was carried out over 42 days in ten outdoor mesocosms of different typology: "clear" waters with aquatic macrophytes and/or metaphyton and "turbid" waters with great occurrence of phytoplankton or suspended inorganic matter. The herbicide was added at 8 mg L(-1) of the active ingredient (glyphosate) in five mesocosms while five were left as controls (without Roundup addition). The estimate of the dissipation rate (k) of glyphosate showed a half-life value of 4.2 days. Total phosphorus significantly increased in treated mesocosms due to Roundup degradation what favored eutrophication process. Roundup produced a clear delay in periphytic colonization in treated mesocosms and values of the periphytic mass variables (dry weight, ash-free dry weight and chlorophyll a) were always higher in control mesocosms. Despite the mortality of algae, mainly diatoms, cyanobacteria was favored in treated mesocosms. It was observed that glyphosate produced a long term shift in the typology of mesocosms, "clear" turning to "turbid", which is consistent with the regional trend in shallow lakes in the Pampa plain of Argentina. Based on our findings it is clear that agricultural practices that involve the use of herbicides such as Roundup affect non-target organisms and the water quality, modifying the structure and functionality of freshwater ecosystems.

Mycosporine-like amino acids in freshwater copepods: potential sources and some factors that affect their bioaccumulation.

Mycosporine-like amino acids (MAAs) are ubiquitous photoprotective compounds in aquatic environments. MAAs are synthesized by a wide variety of organisms (i.e. bacteria, fungi and algae) and their production is photoinducible by ultraviolet radiation (UVR) (280-400 nm) and/or photosynthetically active radiation (400-750 nm). Most animals however, are unable to synthesize MAAs and must acquire these compounds through their diet or from symbiotic organisms. In this paper, we investigate the possible sources of MAAs and factors (temperature and initial MAA concentration) that may affect their bioaccumulation in freshwater copepods. We found that MAA accumulation may occur even if the copepods are cultured on a MAA-free diet. In addition, we found that the bacteriostatic antibiotic, chloramphenicol, inhibits the bioaccumulation of MAAs. These two pieces of evidence suggest that the source of MAAs in these copepods may be prokaryotic organisms in close association with the animals. The two factors investigated in this study, temperature and initial MAA concentrations, were found to affect the rates at which MAAs are accumulated. Temperature had positive effects on both uptake and elimination rates. On the other hand, the rate of uptake decreased at the highest assayed initial MAA concentration, probably because the concentration of MAAs was already close to saturation.

Quality of UVR exposure for different biological systems along a latitudinal gradient.

The exposure of organisms to ultraviolet radiation (UVR) is characterized by the climatology (annual cycle) and the variance (anomalies) of biologically-weighted irradiances at eight geographical locations in austral South America, from 1995-2002. The net effect of UVR on biological systems is a result of the balance of damage and repair which depends on intensity and duration of irradiance and is modulated by its variability. The emphasis in this study is on day-to-day variability, a time scale of importance to adaptive strategies that counteract UVR damage. The irradiances were weighted with DNA- and phytoplankton photosynthesis-action spectra. Low latitude sites show high average UVR. For all sites, the frequency of days with above average irradiances is higher than below average irradiances. Persistence in anomalies is generally low (

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.

UV radiation as a potential driving force for zooplankton community structure in Patagonian lakes.

This article explores the potential role of UV radiation (UVR) as an influence on zooplankton communities. In the first section we provide a general overview of UVR effects on freshwater zooplankton, with an emphasis on Argentine and Chilean environments. In the second section we present the results of a survey involving 53 temperate lakes across a gradient of UVR exposure to determine patterns of species richness and specific diversity. These community characteristics decreased at high potential UVR exposure (i.e. high mean water column irradiance or low lake optical density). A threshold value of mean water column irradiance of approximately 10% of the surface level seems to limit both richness and diversity to minimum values. On the basis of the collected evidence it is not possible to definitely conclude that UVR rather than another covarying factor is responsible for the decrease in specific diversity observed at the lowest end of lake optical depth. However, lakes with values above the previous threshold are likely to exhibit highly depauperate zooplankton communities regardless of the mechanism. As a cautionary note we suggest that changes in the optical characteristics (i.e. changes due to atmospheric conditions, precipitation patterns or vertical displacement of the tree line) may result in sudden shifts in zooplankton community structure.

Mycosporines from freshwater yeasts: a trophic cul-de-sac?

Mycosporine-like amino-acids (MAAs) are found in aquatic bacteria, algae, and animals. A related compound, the mycosporine-glutaminol-glucoside (myc-glu-glu), has recently been reported in freshwater yeasts. Although animals depend on other organisms as their source of MAAs, they can efficiently accumulate them in their tissues. In this work we assessed the potential transfer of the yeast mycosporine myc-glu-glu from the diet into the copepod Boeckella antiqua and the ciliate Paramecium bursaria. For this purpose, we performed experiments to study the feeding of B. antiqua and P. bursaria on the yeast Rhodotorula minuta and their ability to bioaccumulate myc-glu-glu. Bioaccumulation of myc-glu-glu in B. antiqua was assessed through long-term factorial experiments manipulating the diet (Chlamydomonas reinhardii and C. reinhardii + yeasts) and radiation exposure (PAR and PAR + UVR). Shorter term experiments were designed in the case of P. bursaria. The composition and concentration of MAAs in the diet and in the consumers were determined by HPLC analyses. Our results showed that even though both consumers ingested yeast cells, they were unable to accumulate myc-glu-glu. Moreover, when exposed to conditions that stimulated the accumulation of photoprotective compounds (i.e. UVR exposure), an increase in MAAs concentration occurred in copepods fed C. reinhardii plus yeasts as well as in those fed only C. reinhardii. This suggests that the copepods were able to modify their tissue concentrations of MAAs in response to environmental clues but also that the contribution of yeast mycosporines to total MAAs concentration was negligible.

Vertical mixing and ecological effects of ultraviolet radiation in planktonic communities.

We present a mathematical model for a phytoplankton-zooplankton system, based on a predator-prey scheme. The model considers the effects of sinking in the phytoplankton, vertical mixing and attenuation of photosynthetically active radiation (PAR) and ultraviolet radiation (UVR) in the water column. In a first approach, the model was studied under conditions of average PAR irradiance and shows fluctuations and stable equilibrium points. Secondly, we introduced the effects of photoperiod and photoinhibition by UVR and vertical mixing. Under these conditions, the phytoplankton biomass oscillates depending on the combined effects of UVR and mixing. Higher inhibition by UVR and longer mixing periods can induce strong fluctuations in the system but can also produce higher plankton peaks.

Occurrence of photoprotective compounds in yeasts from freshwater ecosystems of northwestern Patagonia (Argentina).

In this paper we present the results of research on the occurrence, induction and role of photoprotective compounds (PPCs) present in native aquatic yeasts from freshwater Patagonian ecosystems. We focus on the effect of UV radiation (UVR) as a factor that controls the level of photoprotection of yeasts, and explore its potential significance in shaping yeast distributional patterns. The research presented here combines field surveys and laboratory work, including the isolation and culture of native yeasts strains, and laboratory assays under different radiation conditions. The results obtained suggest that yeasts are common dwellers of oligotrophic Patagonian water bodies, and provide the first evidence of the distribution of PPC (carotenoid and mycosporine)-producing yeasts in temperate freshwaters. A greater proportion of carotenogenic yeasts were observed in high-elevation lakes. The yeast strains isolated from these environments were found to produce higher amounts of mycosporines (MYCs), and to present higher tolerance to UVB exposure than those from piedmont lakes. Patagonian yeasts have only one type of MYC, mycosporine-glutaminol-glucoside (myc-glu-glu), which seems common to all other yeasts. By analyzing the production of myc-glu-glu in a large number of yeasts belonging to different taxonomic groups, we propose that this compound may have potential use as a chemotaxonomic marker in yeast systematics. Collectively, our work reveals that in Patagonian freshwater yeasts there is an apparent relationship between the ability to produce PPCs, their tolerance to UV exposure and their success in colonizing habitats highly exposed to UVR.

Mycosporines in carotenogenic yeasts.

The ability to produce mycosporines (MYCs) in 157 pigmented yeast strains (eight genera, 25 species) isolated from natural environments of Patagonia (Argentina) was assessed. The strains belong to four taxonomic groups: the Sporidiobolales and Erythrobasidium clade of the class Urediniomycetes, and Cystofilobasidiales and Tremellales of the class Hymenomycetes. Induction of MYCs did not occur in all yeast strains tested and appeared to be an exclusive trait of members of the Erythrobasidium clade and Tremellales. This is the first report on the production of MYCs by pigmented species from the latter group, as well as the first extensive screening of mycosporinogenic yeasts. The consistent occurrence of MYCs in some specific phylogenetic groups suggests this trait bears evolutionary significance and that the presence/absence of MYCs may have potential applications in yeast systematics.

Multichannel radiometer calibration: a new approach.

The error in irradiance measured with Sun-calibrated multichannel radiometers may be large when the solar zenith angle (SZA) increases. This could be particularly detrimental in radiometers installed at mid and high latitudes, where SZAs at noon are larger than 50 degrees during part of the year. When a multiregressive methodology, including the total ozone column and SZA, was applied in the calculation of the calibration constant, an important improvement was observed. By combining two different equations, an improvement was obtained at almost all the SZAs in the calibration. An independent test that compared the irradiance of a multichannel instrument and a spectroradiometer installed in Ushuaia, Argentina, was used to confirm the results.