Lluís Camarero

Seasonal ecosystem variability in remote mountain lakes: implications for detecting climatic signals in sediment records.

Weather variation and climate fluctuations are the main sources of ecosystem variability in remote mountain lakes. Here we describe the main patterns of seasonal variability in the ecosystems of nine lakes in Europe, and discuss the implications for recording climatic features in their sediments. Despite the diversity in latitude and size, the lakes showed a number of common features. They were ice-covered between 5–9 months, and all but one were dimictic. This particular lake was long and shallow, and wind action episodically mixed the water column throughout the ice-free period. All lakes showed characteristic oxygen depletion during the ice-covered-period, which was greater in the most productive lakes. Two types of lakes were distinguished according to the number of production peaks during the ice-free season. Lakes with longer summer stratification tended to have two productive periods: one at the onset of stratification, and the other during the autumn overturn. Lakes with shorter stratification had a single peak during the ice-free period. All lakes presented deep chlorophyll maxima during summer stratification, and subsurface chlorophyll maxima beneath the ice. Phosphorus limitation was common to all lakes, since nitrogen compounds were significantly more abundant than the requirements for the primary production observed. The major chemical components present in the lakes showed a short but extreme dilution during thawing. Certain lake features may favour the recording of particular climatic fluctuations, for instance: lakes with two distinct productive periods, climatic fluctuations in spring or autumn (e.g., through chrysophycean cysts); lakes with higher oxygen consumption, climatic factors affecting the duration of the ice-cover (e.g., through low-oxygen tolerant chironomids); lakes with higher water retention time; changes in atmospheric deposition (e.g., through carbon or pigment burial); lakes with longer stratification, air temperature changes during summer and autumn (e.g., through all epilimnetic species).

Viability and potential for immigration of airborne bacteria from Africa that reach high mountain lakes in Europe

We have analysed the diversity of the bacteria, which grow after addition of concentrated airborne particles and desert dust in different microcosms combinations with water samples from oligotrophic alpine lakes. We used, on the one hand, airborne bacteria transported by an African dust plume and collected in a high mountain area in the central Pyrenees (Spain). On the other hand, we collected desert dust in Mauritania (c. 3000 km distance, and a few days estimated airborne journey), a known source region for dust storms in West Africa, which originates many of the dust plumes landing on Europe. In all the dust-amended treatments we consistently observed bacterial growth of common phyla usually found in freshwater ecosystems, i.e. Alpha-, Beta- and Gammaproteobacteria, Actinobacteria, and a few Bacteroidetes, but with different composition based on lake water pretreatment and dust type. Overall, we tentatively split the bacterial community in (i) typical freshwater non-airborne bacteria, (ii) cosmopolitan long-distance airborne bacteria, (iii) non-freshwater low-distance airborne bacteria, (iv) non-freshwater long-distance airborne soil bacteria and (v) freshwater non-soil airborne bacteria. We identified viable long-distance airborne bacteria as immigrants in alpine lakes (e.g. Sphingomonas-like) but also viable putative airborne pathogens with the potential to grow in remote alpine areas (Acinetobacter-like and Arthrobacter-like). Generation of atmospheric aerosols and remote dust deposition is a global process, largely enhanced by perturbations linked to the global change, and high mountain lakes are very convenient worldwide model systems for monitoring global-scale bacterial dispersion and pathogens entries in remote pristine environments.

Lake Redó ecosystem response to an increasing warming in the Pyrennees during the twentieth century.

The ecosystem response of Lake Redó (Central Pyrenees) to fluctuations in seasonal air temperature during the last two centuries was investigated by comparison of reconstructed air temperatures with the sediment record. Fine slicing allowed a resolution of 3–6 years according to the 210Pb dating, although it was still difficult to easily investigate the response to air temperature forcing, since extreme fluctuations in temperature occur on interannual time-scales. However, the resolution was sufficient to show responses on decadal and century scales. An overall tendency to warming in mean annual temperature in the Central Pyrenees has been caused by summer and in particular by autumn increases. Many of the measured sediment variables apparently responded to these long term trends, but the significance of the relationships was highly conditioned by the structure of the data. The variables responding most on the finer time scales were the microfossils. For diatoms, chironomids and chrysophytes the main variability correlated to summer and to autumn temperatures. For two planktonic species, Fragilaria nanana and Cyclotella pseudostelligera, we found a link of their variability with temperature fluctuations in their growing months (September and October, respectively). This relationship appeared at a certain point during a general warming trend, indicating a threshold in the response. On the other hand, no significant changes in the dominant species could be linked to temperature, nor in any significant subgroup of the 180 diatom species present in the core. In contrast, for most chironomids (particularly Paratanytarsus austriacus, Heterotrissocladius marcidus and Micropsectra radialis) a negative relationship with summer temperature extended throughout the studied period. This response of the whole group gives chironomids a more robust role as indicators for recording temperature changes on long time-scales (e.g., through the Holocene) and for lake signal inter-comparison. Finally, our results indicated that, in all cases, there was a significant resilience to high frequency changes and hysteresis despite extreme fluctuations. Although we were dealing with organisms with one or many generations per year, their populations seemed to follow the decadal trends in air temperature.

Global change revealed by palaeolimnological records from remote lakes: a review

Over recent decades, palaeolimnological records from remote sites have provided convincing evidence for the onset and development of several facets of global environmental change. Remote lakes, defined here as those occurring in high latitude or high altitude regions, have the advantage of not being overprinted by local anthropogenic processes. As such, many of these sites record broad-scale environmental changes, frequently driven by regime shifts in the Earth system. Here, we review a selection of studies from North America and Europe and discuss their broader implications. The history of investigation has evolved synchronously with the scope and awareness of environmental problems. An initial focus on acid deposition switched to metal and other types of pollutants, then climate change and eventually to atmospheric deposition-fertilising effects. However, none of these topics is independent of the other, and all of them affect ecosystem function and biodiversity in profound ways. Currently, remote lake palaeolimnology is developing unique datasets for each region investigated that benchmark current trends with respect to past, purely natural variability in lake systems. Fostering conceptual and methodological bridges with other environmental disciplines will upturn contribution of remote lake palaeolimnology in solving existing and emerging questions in global change science and planetary stewardship.

Dust inputs and bacteria influence dissolved organic matter in clear alpine lakes.

Remote lakes are usually unaffected by direct human influence, yet they receive inputs of atmospheric pollutants, dust, and other aerosols, both inorganic and organic. In remote, alpine lakes, these atmospheric inputs may influence the pool of dissolved organic matter, a critical constituent for the biogeochemical functioning of aquatic ecosystems. Here, to assess this influence, we evaluate factors related to aerosol deposition, climate, catchment properties, and microbial constituents in a global dataset of 86 alpine and polar lakes. We show significant latitudinal trends in dissolved organic matter quantity and quality, and uncover new evidence that this geographic pattern is influenced by dust deposition, flux of incident ultraviolet radiation, and bacterial processing. Our results suggest that changes in land use and climate that result in increasing dust flux, ultraviolet radiation, and air temperature may act to shift the optical quality of dissolved organic matter in clear, alpine lakes.

Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes

ABSTRACT The annual changes in the composition and abundance of ammonia-oxidizing archaea (AOA) were analyzed monthly in surface waters of three high mountain lakes within the Limnological Observatory of the Pyrenees (LOOP; northeast Spain) using both 16S rRNA and functional (ammonia monooxygenase gene, amoA) gene sequencing as well as quantitative PCR amplification. The set of biological data was related to changes in nitrogen species and to other relevant environmental variables. The whole archaeal assemblage was dominated by phylotypes closely related to the crenarchaeal 1.1a group (58% ± 18% of total 16S rRNA gene sequences), and consistent structural changes were detected during the study. Water temperature was the environmental variable that better explained spring, summer, and winter (ice-covered lakes) archaeal assemblage structure. The amoA gene was detected year round, and seasonal changes in amoA gene composition were well correlated with changes in the archaeal 16S rRNA gene pool. In addition, copy numbers of both the specific 1.1a group 16 rRNA and archaeal amoA genes were well correlated, suggesting that most freshwater 1.1a Crenarchaeota had the potential to carry out ammonia oxidation. Seasonal changes in the diversity and abundance of AOA (i.e., amoA) were better explained by temporal changes in ammonium, the substrate for nitrification, and mostly nitrite, the product of ammonia oxidation. Lacustrine amoA gene sequences grouped in coherent freshwater phylogenetic clusters, suggesting that freshwater habitats harbor typical amoA-containing ecotypes, which is different from soils and seas. We observed within the freshwater amoA gene sequence pool a high genetic divergence (translating to up to 32% amino acid divergence) between the spring and the remaining AOA assemblages. This suggests that different AOA ecotypes are adapted to different temporal ecological niches in these lakes.

Chemistry of bulk precipitation in the central and eastern Pyrenees, northeast Spain

Bulk precipitation samples from four locations in the Pyrenees were analysed for major ions and nutrients. The chemical composition of precipitation was related to the origin of storms. Rains coming from the Mediterranean Sea (south-southeast) were alkaline, while those from the Atlantic (northwest) were more acidic. The situation and particular orography of each sampling point determine the amount of precipitation received from each direction and, therefore, the chemical features of rain at each location. We detected differences in the acid loading among the four sampling sites. Bulk precipitation in the Pyrenees is more alkaline than precipitation in central Europe (Alps), owing to the higher Ca2+ concentrations and the lower acid pollutant levels (SO42− and NO3−) found in the Pyrenees.

Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake

Freshwater habitats have been identified as one of the largest reservoirs of archaeal genetic diversity, with specific lineages of ammonia-oxidizing archaea (AOA) populations different from soils and seas. The ecology and biology of lacustrine AOA is, however, poorly known. In the present study, vertical changes in archaeal abundance by CARD-FISH, quantitative PCR (qPCR) analyses and identity by clone libraries were correlated with environmental parameters in the deep glacial high-altitude Lake Redon. The lake is located in the central Spanish Pyrenees where atmospheric depositions are the main source of reactive nitrogen. Strong correlations were found between abundance of thaumarchaeotal 16S rRNA gene, archaeal amoA gene and nitrite concentrations, indicating an ammonium oxidation potential by these microorganisms. The bacterial amoA gene was not detected. Three depths with potential ammonia-oxidation activity were unveiled along the vertical gradient, (i) on the top of the lake in winter–spring (that is, the 0 oC slush layers above the ice-covered sheet), (ii) at the thermocline and (iii) the bottom waters in summer—autumn. Overall, up to 90% of the 16S rRNA gene sequences matched Thaumarchaeota, mostly from both the Marine Group (MG) 1.1a (Nitrosoarchaeum-like) and the sister clade SAGMGC−1 (Nitrosotalea-like). Clone-libraries analysis showed the two clades changed their relative abundances with water depth being higher in surface and lower in depth for SAGMGC−1 than for MG 1.1a, reflecting a vertical phylogenetic segregation. Overall, the relative abundance and recurrent appearance of SAGMGC−1 suggests a significant environmental role of this clade in alpine lakes. These results expand the set of ecological and thermal conditions where Thaumarchaeota are distributed, unveiling vertical positioning in the water column as a key factor to understand the ecology of different thaumarchaeotal clades in lacustrine environments.

Chemical composition of disturbed and undisturbed high-mountain lakes in the Pyrenees: A reference for acidified sites

102 lakes distributed along the Catalan Pyrenees (from 0°41′ E to 1°48′ E) were sampled during summer in 1987. The alkalinity of the lakes was low (<300 μequiv l−1) but there was no regional acidification. Most chemical variance was related to the nature of the bedrock. Lakes on Devonian, Cambro-Ordovician, Silurian or granodioritic batholites were easily distinguished. Even between different batholites, there were significant differences. There was no clear distinction either in the chemistry or in trophic status between disturbed and undisturbed lakes, except for certain extreme cases. Pasture is the most important source of eutrophication, but is restricted to small, very shallow and usually endorreic lakes.

Atmospheric phosphorus deposition may cause lakes to revert from phosphorus limitation back to nitrogen limitation

Recent findings indicate that increased atmospheric deposition of nitrogen of human origin has caused changes in the pattern of ecological nutrient limitation in lakes in the northern hemisphere. An increase in the nitrogen to phosphorus ratio, and hence a shift from pristine nitrogen limitation to human-induced phosphorus limitation of phytoplankton growth, seems to have been driven by deposition of atmospheric nitrogen. These findings challenge the classical paradigm of lake phytoplankton productivity being naturally limited by phosphorus availability. However, atmospheric phosphorus deposition may also be highly relevant. Here we show how dissolved inorganic nitrogen concentration has decreased in the Pyrenean lake district over recent decades, despite there being an increase in deposition of atmospheric nitrogen. This is related to an increased atmospheric phosphorus load in the lake water, as a result of higher atmospheric inputs. These changes are causing phytoplankton to revert from being phosphorus-limited to being nitrogen-limited.