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Intensive agriculture with high reliance on pesticides and fertilizers constitutes a major strategy for 'feeding the world'. However, such conventional intensification is linked to diminishing returns and can result in 'intensification traps'-production declines triggered by the negative feedback of biodiversity loss at high input levels. Here we developed a novel framework that accounts for biodiversity feedback on crop yields to evaluate the risk and magnitude of intensification traps. Simulations grounded in systematic literature reviews showed that intensification traps emerge in most landscape types, but to a lesser extent in major cereal production systems. Furthermore, small reductions in maximal production (5-10%) could be frequently transmitted into substantial biodiversity gains, resulting in small-loss large-gain trade-offs prevailing across landscape types. However, sensitivity analyses revealed a strong context dependence of trap emergence, inducing substantial uncertainty in the identification of optimal management at the field scale. Hence, we recommend the development of case-specific safety margins for intensification preventing double losses in biodiversity and food security associated with intensification traps.
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Conservación de los Recursos Naturales , Plaguicidas , Retroalimentación , Conservación de los Recursos Naturales/métodos , Biodiversidad , Agricultura/métodosRESUMEN
Ratios between viruses, heterotrophic prokaryotes and chlorophyll a are key indicators of microbial food structure and both virus-prokaryote and prokaryote-chlorophyll ratios have been proposed to decrease with system productivity. However, the mechanisms underlying these responses are still insufficiently resolved and their consistency across aquatic ecosystem types requires critical evaluation. We assessed microbial community ratios in highly productive African soda-lakes and used our data from naturally hypereutrophic systems which are largely underrepresented in literature, to complement earlier across-system meta-analyses. In contrast to marine and freshwater systems, prokaryote-chlorophyll ratios in African soda-lakes did not decrease along productivity gradients. High-resolution time series from two soda-lakes indicated that this lack of response could be driven by a weakened top-down control of heterotrophic prokaryotes. Our analysis of virus-prokaryote relationships, revealed a reduction of virus-prokaryote ratios by high suspended particle concentrations in soda-lakes. This effect, likely driven by the adsorption of free-living viruses, was also found in three out of four additionally analysed marine datasets. However, the decrease of virus-prokaryote ratios previously reported in highly productive marine systems, was neither detectable in soda-lakes nor freshwaters. Hence, our study demonstrates that system-specific analyses can reveal the diversity of mechanisms that structure microbial food-webs and shape their response to productivity increases.
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Microbiota , Virus , Ecosistema , Clorofila A , Células Procariotas , Cadena Alimentaria , Clorofila , Lagos/químicaRESUMEN
Locomotion in benthic invertebrates can strongly affect habitat selection and ecosystem nutrient cycling. In the case of freshwater mussels, the drivers of locomotion are largely unresolved. Our aim was to assess the influence of light presence and intensity on the locomotory behaviour of freshwater mussels in controlled laboratory experiments. The species investigated in our study were Anodonta anatina and Unio pictorum, two widely distributed mussels in European lentic and lotic inland waters. At low algal concentrations, known to be associated with more frequent locomotory activities, we found that both species moved primarily in the absence of light (72.7% of all movements across experiments). However, the movements of both species were directed towards the light source, resembling a net-positive 'phototactic' response but in the absence of light. The distance to the light source, which was negatively correlated to light intensity, had a positive effect on the distance covered in locomotory activities by A. anatina but not by U. pictorum. Intraspecific variation in shell size had no impact on movement distance, indicating that the energetic costs of movement were not a limiting factor. We suggest that the observed movement towards brighter locations helps to enhance food quantity and quality, whilst movement in darkness mitigates predation risks.
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Bivalvos , Unionidae , Animales , Ecosistema , Locomoción , AlimentosRESUMEN
The coastline of Sub-Saharan Africa hosts highly diverse fish communities of great conservation value, which are also key resources for local livelihoods. However, many costal ecosystems are threatened by overexploitation and their conservation state is frequently unknown due to their vast spatial extent and limited monitoring budgets. Here, we evaluated the potential of citizen science-based eDNA surveys to alleviate such chronic data deficiencies and assessed fish communities in Mozambique using two 12S metabarcoding primer sets. Samples were either collected by scientific personnel or trained community members and results from the two metabarcoding primers were combined using a new data merging approach. Irrespective of the background of sampling personnel, a high average fish species richness was recorded (38 ± 20 OTUs per sample). Individual sections of the coastline largely differed in the occurrence of threatened and commercially important species, highlighting the need for regionally differentiated management strategies. A detailed comparison of the two applied primer sets revealed an important trade-off in primer choice with MiFish primers amplifying a higher number of species but Riaz primers performing better in the detection of threatened fish species. This trade-off could be partly resolved by applying our new data-merging approach, which was especially designed to increase the robustness of multiprimer assessments in regions with poor reference libraries. Overall, our study provides encouraging results but also highlights that eDNA-based monitoring will require further improvements of, for example, reference databases and local analytical infrastructure to facilitate routine applications in Sub-Saharan Africa.
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Ciencia Ciudadana , ADN Ambiental , Animales , Ecosistema , Código de Barras del ADN Taxonómico/métodos , Biodiversidad , Monitoreo del Ambiente/métodos , Peces/genética , Especies en Peligro de ExtinciónRESUMEN
Protozoan predators form an essential component of activated sludge communities that is tightly linked to wastewater treatment efficiency. Nonetheless, very little is known how protozoan predation is channelled via bacterial communities to affect ecosystem functioning. Therefore, we experimentally manipulated protozoan predation pressure in activated-sludge communities to determine its impacts on microbial diversity, composition and putative functionality. Different components of bacterial diversity such as taxa richness, evenness, genetic diversity and beta diversity all responded strongly and positively to high protozoan predation pressure. These responses were non-linear and levelled off at higher levels of predation pressure, supporting predictions of hump-shaped relationships between predation pressure and prey diversity. In contrast to predation intensity, the impact of predator diversity had both positive (taxa richness) and negative (evenness and phylogenetic distinctiveness) effects on bacterial diversity. Furthermore, predation shaped the structure of bacterial communities. Reduction in top-down control negatively affected the majority of taxa that are generally associated with increased treatment efficiency, compromising particularly the potential for nitrogen removal. Consequently, our findings highlight responses of bacterial diversity and community composition as two distinct mechanisms linking protozoan predation with ecosystem functioning in activated sludge communities.
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Ecosistema , Conducta Predatoria , Animales , Bacterias/genética , Filogenia , Aguas del AlcantarilladoRESUMEN
BACKGROUND: Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change-including eutrophication-that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. METHODS: Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. RESULTS: C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont's DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. CONCLUSION: Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation-a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract.
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Antozoos , Cnidarios , Dinoflagelados , Animales , Eutrofización , Nitrógeno , Filogenia , SimbiosisRESUMEN
In recent years, eDNA-based assessments have evolved as valuable tools for research and conservation. Most eDNA-based applications rely on comparisons across time or space. However, temporal, and spatial dynamics of eDNA concentrations are shaped by various drivers that can affect the reliability of such comparative approaches. Here, we assessed (i) seasonal variability, (ii) degradation rates and (iii) micro-habitat heterogeneity of eDNA concentrations as key factors likely to inflict uncertainty in across site and time comparisons. In a controlled mesocosm experiment, using the white-clawed crayfish as a model organism, we found detection probabilities of technical replicates to vary substantially and range from as little as 20 to upwards of 80% between seasons. Further, degradation rates of crayfish eDNA were low and target eDNA was still detectable 14-21 days after the removal of crayfish. Finally, we recorded substantial small-scale in-situ heterogeneity and large variability among sampling sites in a single pond of merely 1000m2 in size. Consequently, all three tested drivers of spatial and temporal variation have the potential to severely impact the reliability of eDNA-based site comparisons and need to be accounted for in sampling design and data analysis of field-based applications.
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ADN , Ecosistema , Animales , Astacoidea/genética , Reproducibilidad de los Resultados , Estaciones del AñoRESUMEN
Global declines in biodiversity highlight the need to effectively monitor the density and distribution of threatened species. In recent years, molecular survey methods detecting DNA released by target-species into their environment (eDNA) have been rapidly on the rise. Despite providing new, cost-effective tools for conservation, eDNA-based methods are prone to errors. Best field and laboratory practices can mitigate some, but the risks of errors cannot be eliminated and need to be accounted for. Here, we synthesize recent advances in data processing tools that increase the reliability of interpretations drawn from eDNA data. We review advances in occupancy models to consider spatial data-structures and simultaneously assess rates of false positive and negative results. Further, we introduce process-based models and the integration of metabarcoding data as complementing approaches to increase the reliability of target-species assessments. These tools will be most effective when capitalizing on multi-source data sets collating eDNA with classical survey and citizen-science approaches, paving the way for more robust decision-making processes in conservation planning.
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Biodiversidad , Código de Barras del ADN Taxonómico , ADN Ambiental/análisis , Conservación de los Recursos Naturales , Monitoreo del Ambiente , Reproducibilidad de los ResultadosRESUMEN
'One World - One Health' is a developing concept which aims to explicitly incorporate linkages between the environment and human society into wildlife and human health care. Past work in the field has concentrated on aspects of disease, particularly emerging zoonoses, and focused on terrestrial systems. Here, we argue that marine environments are crucial components of the 'One World - One Health' framework, and that coral reefs are the epitome of its underlying philosophy. That is, they provide vast contributions to a wide range of ecosystem services with strong and direct links to human well-being. Further, the sensitivity of corals to climate change, and the current emergence of a wide range of diseases, make coral reefs ideal study systems to assess links, impacts, and feedback mechanisms that can affect human and ecosystem health. There are well established protocols for monitoring corals, as well as global networks of coral researchers, but there remain substantial challenges to understanding these complex systems, their health and links to provisioning of ecosystem services. We explore these challenges and conclude with a look at how developing technology offers potential ways of addressing them. We argue that a greater integration of coral reef research into the 'One World - One Health' framework will enrich our understanding of the many links within, and between, ecosystems and human society. This will ultimately support the development of measures for improving the health of both humans and the environment.
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Antozoos/fisiología , Cambio Climático , Arrecifes de Coral , Ecosistema , Salud Única , Animales , Océanos y MaresRESUMEN
eDNA-based methods represent non-invasive and cost-effective approaches for species monitoring and their application as a conservation tool has rapidly increased within the last decade. Currently, they are primarily used to determine the presence/absence of invasive, endangered or commercially important species, but they also hold potential to contribute to an improved understanding of the ecological interactions that drive species distributions. However, this next step of eDNA-based applications requires a thorough method development. We developed an eDNA assay for the white-clawed crayfish (Austropotamobius pallipes), a flagship species of conservation in the UK and Western Europe. Multiple subsequent in-situ and ex-situ validation tests aimed at improving method performance allowed us to apply eDNA-based surveys to evaluate interactions between white-clawed crayfish, crayfish plague and invasive signal crayfish. The assay performed well in terms of specificity (no detection of non-target DNA) and sensitivity, which was higher compared to traditional methods (in this case torching). The eDNA-based quantification of species biomass was, however, less reliable. Comparison of eDNA sampling methods (precipitation vs. various filtration approaches) revealed that optimal sampling method differed across environments and might depend on inhibitor concentrations. Finally, we applied our methodology together with established assays for crayfish plague and the invasive signal crayfish, demonstrating their significant interactions in a UK river system. Our analysis highlights the importance of thorough methodological development of eDNA-based assays. Only a critical evaluation of methodological strengths and weaknesses will allow us to capitalise on the full potential of eDNA-based methods and use them as decision support tools in environmental monitoring and conservation practice.
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Astacoidea , Ríos , Animales , Astacoidea/genética , ADN , Monitoreo del Ambiente , Europa (Continente)RESUMEN
Compound-specific isotope analyses (CSIA) of fatty acids (FA) constitute a promising tool for tracing energy flows in food-webs. However, past applications of FA-specific carbon isotope analyses have been restricted to a relatively coarse food-source separation and mainly quantified dietary contributions from different habitats. Our aim was to evaluate the potential of FA-CSIA to provide high-resolution data on within-system energy flows using algae and zooplankton as model organisms. First, we investigated the power of FA-CSIA to distinguish among four different algae groups, namely cyanobacteria, chlorophytes, haptophytes and diatoms. We found substantial within-group variation but also demonstrated that δ13C of several FA (e.g. 18:3ω3 or 18:4ω3) differed among taxa, resulting in group-specific isotopic fingerprints. Second, we assessed changes in FA isotope ratios with trophic transfer. Isotope fractionation was highly variable in daphnids and rotifers exposed to different food sources. Only δ13C of nutritionally valuable poly-unsaturated FA remained relatively constant, highlighting their potential as dietary tracers. The variability in fractionation was partly driven by the identity of food sources. Such systematic effects likely reflect the impact of dietary quality on consumers' metabolism and suggest that FA isotopes could be useful nutritional indicators in the field. Overall, our results reveal that the variability of FA isotope ratios provides a substantial challenge, but that FA-CSIA nevertheless have several promising applications in food-web ecology. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.
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Organismos Acuáticos/química , Isótopos de Carbono/análisis , Ácidos Grasos/análisis , Cadena Alimentaria , Animales , Chlorophyta/química , Copépodos/química , Cianobacterias/química , Diatomeas/química , Haptophyta/química , Rotíferos/químicaRESUMEN
BACKGROUND: Coral reefs face unprecedented declines in diversity and cover, a development largely attributed to climate change-induced bleaching and subsequent disease outbreaks. Coral-associated microbiomes may strongly influence the fitness of their hosts and alter heat tolerance and disease susceptibility of coral colonies. Here, we describe a new coral disease found in Micronesia and present a detailed assessment of infection-driven changes in the coral microbiome. RESULTS: Combining field monitoring and histological, microscopic and next-generation barcoding assessments, we demonstrate that the outbreak of the disease, named 'grey-patch disease', is associated with the establishment of cyanobacterial biofilm overgrowing coral tissue. The disease is characterised by slow progression rates, with coral tissue sometimes growing back over the GPD biofilm. Network analysis of the corals' microbiome highlighted the clustering of specific microbes which appeared to benefit from the onset of disease, resulting in the formation of 'infection clusters' in the microbiomes of apparently healthy corals. CONCLUSIONS: Our results appear to be in contrast to the recently proposed Anna-Karenina principle, which states that disturbances (such as disease) trigger chaotic dynamics in microbial communities and increase ß-diversity. Here, we show significantly higher community similarity (compositional homogeneity) in the pathobiome of diseased corals, compared to the microbiome associated with apparently healthy tissue. A possible explanation for this pattern is strong competition between the pathogenic community and those associated with the 'healthy' coral holobiont, homogenising the composition of the pathobiome. Further, one of our key findings is that multiple agents appear to be involved in degrading the corals' defences causing the onset of this disease. This supports recent findings indicating a need for a shift from the one-pathogen-one-disease paradigm to exploring the importance of multiple pathogenic players in any given disease.
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Antozoos , Bacterias/patogenicidad , Arrecifes de Coral , Interacciones Microbianas/fisiología , Microbiota/fisiología , Simbiosis/fisiología , Animales , Antozoos/microbiología , Antozoos/fisiología , MicronesiaRESUMEN
Environmental DNA (eDNA) barcoding has a high potential to increase the cost-efficiency of species detection and monitoring in aquatic habitats. However, despite vast developments in the field, many published assays often lack detailed validation and there is little to no commonly (agreed upon) standardization of protocols. In this study, we evaluated the reliability of eDNA detection and quantification using published primers and assays targeting the Freshwater Pearl Mussel as a model organism. We first assessed limits of detection for two different target genes (COI and 16S) following the MIQE guidelines, and then tested the reliability of quantification in a double-blind mesocosm experiment. Our results reveal that different methodological indicators, namely accuracy, repeatability and detection probability affected the reliability of eDNA measurement at the different levels tested. The selection of the optimal analytical method was mainly determined by detection probability. Both the COI and 16S assays were highly specific for the targeted organism and showed similar accuracy and repeatability, whilst the limit of detection was clearly lower for the COI based approach. In contrast, the reliability of eDNA quantification hinged on repeatability, reflected by the scattering (r2 = 0.87) around the relationship between eDNA and mussel density in mesocosms. A bootstrapping approach, which allowed for the assignment of measures associated with repeatability of samples, revealed that variability between natural replicates (i.e. accuracy) strongly influenced the number of replicates required for a reliable species detection and quantification in the field.
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Organismos Acuáticos/clasificación , Organismos Acuáticos/genética , Código de Barras del ADN Taxonómico/métodos , ADN Ambiental/análisis , Metagenómica/métodos , Complejo IV de Transporte de Electrones/genética , ARN Ribosómico 16S/genética , Reproducibilidad de los Resultados , Sensibilidad y EspecificidadRESUMEN
A recent study concluded that omnivorous plankton will shift from predatory to herbivorous feeding with climate warming, as consumers require increased carbon:phosphorous in their food. Although this is an appealing hypothesis, we suggest the conclusion is unfounded, based on the data presented, which seem in places questionable and poorly interpreted.
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Copépodos/fisiología , Conducta Alimentaria/fisiología , Cadena Alimentaria , Calor , Animales , Cambio Climático , Preferencias AlimentariasRESUMEN
Zooplankton blooms are a frequent phenomenon in tropical systems. However, drivers of bloom formation and the contribution of emerging resting eggs are largely unexplored. We investigated the dynamics and the triggers of rotifer blooms in African soda-lakes and assessed their impact on other trophic levels. A meta-analysis of rotifer peak densities including abundances of up to 6 × 105 individuals L-1 demonstrated that rotifer bloom formation was uncoupled from the food environment and the seasonality of climatic conditions. A time series with weekly sampling intervals from Lake Nakuru (Kenya) revealed that intrinsic growth factors (food quality and the physicochemical environment) significantly affected rotifer population fluctuations, but were of minor importance for bloom formation. Instead, rotifer bloom formation was linked to sediment resuspension, a prerequisite for hatching of resting-eggs. Population growth rates exceed pelagic birth rates and simulations of rotifer dynamics confirmed the quantitative importance of rotifer emergence from the sediment egg-bank and signifying a decoupling of bloom formation from pelagic reproduction. Rotifer blooms led to a top-down control of small-sized algae and facilitated a switch to more grazing-resistant, filamentous cyanobacteria. This shift in phytoplankton composition cascaded up the food chain and triggered the return of filter-feeding flamingos. Calculations of consequent changes in the lake's energy budget and export of aquatic primary production to terrestrial ecosystems demonstrated the large potential impact of nonseasonal disturbances on the functioning of shallow tropical lakes.
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ß-N-Methylamino-L-alanine (BMAA), a neurotoxin reportedly produced by cyanobacteria, diatoms and dinoflagellates, is proposed to be linked to the development of neurological diseases. BMAA has been found in aquatic and terrestrial ecosystems worldwide, both in its phytoplankton producers and in several invertebrate and vertebrate organisms that bioaccumulate it. LC-MS/MS is the most frequently used analytical technique in BMAA research due to its high selectivity, though consensus is lacking as to the best extraction method to apply. This study accordingly surveys the efficiency of three extraction methods regularly used in BMAA research to extract BMAA from cyanobacteria samples. The results obtained provide insights into possible reasons for the BMAA concentration discrepancies in previous publications. In addition and according to the method validation guidelines for analysing cyanotoxins, the TCA protein precipitation method, followed by AQC derivatization and LC-MS/MS analysis, is now validated for extracting protein-bound (after protein hydrolysis) and free BMAA from cyanobacteria matrix. BMAA biological variability was also tested through the extraction of diatom and cyanobacteria species, revealing a high variance in BMAA levels (0.0080-2.5797 µg g(-1) DW).
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Aminoácidos Diaminos/aislamiento & purificación , Métodos Analíticos de la Preparación de la Muestra/métodos , Cianobacterias/química , Neurotoxinas/aislamiento & purificación , Aminoácidos Diaminos/química , Aminoácidos Diaminos/metabolismo , Cianobacterias/metabolismo , Toxinas de Cianobacterias , Neurotoxinas/química , Neurotoxinas/metabolismo , Espectrometría de Masas en TándemRESUMEN
1. The analysis of functional groups with a resolution to the individual species level is a basic requirement to better understand complex interactions in aquatic food webs. Species-specific stable isotope analyses are currently applied to analyse the trophic role of large zooplankton or fish species, but technical constraints complicate their application to smaller-sized plankton. 2. We investigated rotifer food assimilation during a short-term microzooplankton bloom in the East African soda lake Nakuru by developing a method for species-specific sampling of rotifers. 3. The two dominant rotifers, Brachionus plicatilis and Brachionus dimidiatus, were separated to single-species samples (purity >95%) and significantly differed in their isotopic values (4.1 in δ13C and 1.5 in δ15N). Bayesian mixing models indicated that isotopic differences were caused by different assimilation of filamentous cyanobacteria and particles <2 µm and underlined the importance of species-specific sampling of smaller plankton compartments. 4. A main difference was that the filamentous cyanobacterium Arthrospira fusiformis, which frequently forms blooms in African soda lakes, was an important food source for the larger-sized B. plicatilis (48%), whereas it was hardly ingested by B. dimidiatus. Overall, A. fusiformis was, relative to its biomass, assimilated to small extents, demonstrating a high grazing resistance of this species. 5. In combination with high population densities, these results demonstrate a strong potential of rotifer blooms to shape phytoplankton communities and are the first in situ demonstration of a quantitatively important direct trophic link between rotifers and filamentous cyanobacteria.
RESUMEN
The filamentous spirally coiled cyanoprokaryote Arthrospira fusiformis is found in extremely high densities in tropical soda lakes acting as driving force of the food web. We studied pronounced temporal morphological changes of Arthrospira in Kenyan soda lakes, Nakuru and Bogoria, and identified underlying key factors. Cell (diameter and height) and filament (height of coil, coil diameter, and number) dimensions were measured from weekly samples collected over a period of 16 months. In both lakes, medium-sized cells and large, widely coiled filaments prevailed most. Percentage of large, widely coiled filaments was promoted by elevated levels of soluble reactive phosphorus, wind speed, temperature and conductivity and the opposite for small filaments. Large, narrow-coiled filaments were associated with an increase in mainly Arthrospira-grazing zooplankton and cyanophage infections. Widely coiled spirals were promoted by increased turbulences. Based on fluorescence measurements, we found widely coiled filaments representing high vitality. From this study we were able to demonstrate for the first time morphological patterns of Arthrospira in nature. Arthrospira morphotypes are suitable for indicating the biological status in soda lakes as they are subjective and therefore reflective of what is happening in its habitat. Additionally, this outcome might be also of interest for commercial 'Spirulina' farms in enhancing high-quality production.