Modelling epilithic biofilms combining hydrodynamics,invertebrate grazing and algal traits

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Temporal Dynamics of River Biofilm in Constant Flows: A Case Study in a Riverside Laboratory Flume

A 15‐week experiment was performed in a riverside laboratory flume (with diverted river water) to check variations of river biofilm structure (biomass, algal and bacterial compositions) and function (community gross primary production GPP and respiration) under constant flow while water quality went through natural temporal variations. One major suspended matter pulse coinciding with one river flood was recorded after 10 weeks of experiment. Epilithic biofilm first exhibited a 10‐week typical pattern of biomass accrual reaching 33 g ash‐free dry matter (AFDM) m^–2 and 487 mg chlorophyll‐a m^–2 and then, experienced a shift to dominance of loss processes (loss of 60% AFDM and 80% chlorophyll‐a) coinciding with the main suspended matter pulse. Algal diversity remained low and constant during the experiment: Fragilaria capucina and Encyonema minutum always contribute over 80% of cell counts. DGGE banding patterns discriminated between two groups that corresponded to samples before and after biomass loss, indicating major changes in the bacterial community composition. GPP/R remained high during the experiment, suggesting that photoautotrophic metabolism prevailed and detachment was not autogenic (i.e., due to algal senescence or driven by heterotrophic processes within the biofilm). Observational results suggested that silt deposition into the biofilm matrix could have triggered biomass loss. (© 2010 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Top‐down effects of a lytic bacteriophage and protozoa on bacteria in aqueous and biofilm phases

Lytic bacteriophages and protozoan predators are the major causes of bacterial mortality in natural microbial communities, which also makes them potential candidates for biological control of bacterial pathogens. However, little is known about the relative impact of bacteriophages and protozoa on the dynamics of bacterial biomass in aqueous and biofilm phases. Here, we studied the temporal and spatial dynamics of bacterial biomass in a microcosm experiment where opportunistic pathogenic bacteria Serratia marcescens was exposed to particle‐feeding ciliates, surface‐feeding amoebas, and lytic bacteriophages for 8 weeks, ca. 1300 generations. We found that ciliates were the most efficient enemy type in reducing bacterial biomass in the open water, but least efficient in reducing the biofilm biomass. Biofilm was rather resistant against bacterivores, but amoebae had a significant long‐term negative effect on bacterial biomass both in the open‐water phase and biofilm. Bacteriophages had only a minor long‐term effect on bacterial biomass in open‐water and biofilm phases. However, separate short‐term experiments with the ancestral bacteriophages and bacteria revealed that bacteriophages crash the bacterial biomass dramatically in the open‐water phase within the first 24 h. Thereafter, the bacteria evolve phage‐resistance that largely prevents top‐down effects. The combination of all three enemy types was most effective in reducing biofilm biomass, whereas in the open‐water phase the ciliates dominated the trophic effects. Our results highlight the importance of enemy feeding mode on determining the spatial distribution and abundance of bacterial biomass. Moreover, the enemy type can be crucially important predictor of whether the rapid defense evolution can significantly affect top‐down regulation of bacteria.     

Discharge,legacy effects and nutrient availability as determinants of temporal patterns in biofilm metabolism and accrual in an arctic river

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Permeability of a growing biofilm in a porous media fluid flow analyzed by magnetic resonance displacement‐relaxation correlations

Biofilm growth in porous media is difficult to study non‐invasively due to the opaqueness and heterogeneity of the systems. Magnetic resonance is utilized to non‐invasively study water dynamics within porous media. Displacement‐relaxation correlation experiments were performed on fluid flow during biofilm growth in a model porous media of mono‐dispersed polystyrene beads. The spin–spin T₂ magnetic relaxation distinguishes between the biofilm phase and bulk fluid phase due to water–biopolymer interactions present in the biofilm, and the flow dynamics are measured using PGSE NMR experiments. By correlating these two measurements, the effects of biofilm growth on the fluid dynamics can be separated into a detailed analysis of both the biofilm phase and the fluid phase simultaneously within the same experiment. Within the displacement resolution of these experiments, no convective flow was measured through the biomass. An increased amount of longitudinal hydrodynamic dispersion indicates increased hydrodynamic mixing due to fluid channeling caused by biofilm growth. The effect of different biofilm growth conditions was measured by varying the strength of the bacterial growth medium. Biotechnol. Bioeng. 2013; 110: 1366–1375. © 2012 Wiley Periodicals, Inc.     

Plankton relationships under small water level fluctuations in a subtropical reservoir

In reservoirs, variations in water level may affect plankton biomass and species composition. Studies on the effect of water-level fluctuations are scarce and restricted to Europe and Australia. In the Río Tercero Reservoir (Argentina), the management policies of a nuclear-power plant require a minimum depth of 650 m. During periods of excessive rainfall, however, the input is such that the excess passes over the spillway, thus causing a high turnover of water. Phytoplankton, zooplankton, and physicochemical variables were monitored over 2 years at three sampling stations during a period with annual precipitation higher than the historical annual mean. Different hydrological situations occurred based on precipitation, spillway outflow, and water-renewal rate. At high renewal rates, phyto- and zoo-plankton diversities peaked. During high outflow periods phytoplankton biomass peaked through the contribution of Ceratium hirundinella. Once the spillway outflow ceased, stable conditions (low renewal rates) were achieved, thus allowing the onset of biological interactions. Maximum phytoplankton density (mainly Actinocyclus normanii) was reached at such times, and efficient grazers (Daphnia laevis) with long life cycles dominated in terms of biomass. The structure and dynamics of the plankton community could be altered by changes in hydrological conditions (renewal rate and spillway outflow) that act to compromise the apparent stability imposed by steady water levels. These variables must be considered to identify disturbance conditions and improve knowledge of reservoir environments, so as to implement appropriate management practices.     

Movers and shakers: nutrient subsidies and benthic disturbance predict biofilm biomass and stable isotope signatures in coastal streams

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New penis characters to distinguish between two American Artemia species

Biofilms are an ensemble of autotrophs and heterotrophs, which are highly efficient in removing inorganic and organic compounds, as well as other chemicals, from river water. They are, therefore, key elements in the self-purification processes which occur in rivers. Biofilm function is related to several environmental factors that govern river ecosystems: physical (light, temperature, water current), chemical (nutrient availability, toxicant effects), but also biological. Among the biological factors, community composition (algae, bacteria and fungi), biofilm structure (layer arrangement and biomass accumulation), and the presence of grazers determine variations in the efficiency of the self-depuration function of biofilms in rivers. Algae and bacteria show specific abilities for nutrients and other organic and inorganic compounds, but biofilm thickness may affect these abilities, both through a decrease in diffusion and by enhancing recycling within the biofilm. Nutrient uptake and consequently the capacity of biofilm to ameliorate water quality decreases with biomass. Moreover, biofilm thickness determines the effect of toxicants, since biomass prevents their diffusion through the biofilm. Grazing interferes in the relative efficiency of biofilms, by simplifying the composition of the biofilm community and by decreasing the amount of sorption and uptake of the biofilm. Closer attention should be paid to these aspects, since they unambiguously interfere with the performance of biofilms in the amelioration of the quality of river water.     

Biofilm Structure and Function and Possible Implications for Riverine DOC Dynamics

Biofilms are major sites of carbon cycling in streams and rivers. Here we elucidate the relationship between biofilm structure and function and river DOC dynamics. Metabolism (extracellular enzymatic activity) and structure (algae, bacteria, C/N content) of light-grown (in an open channel) and dark-grown (in a dark pipe) biofilms were studied over a year, and variations in dissolved organic carbon (DOC) and biodegradable DOC (BDOC) were also recorded. A laboratory experiment on ¹⁴C-glucose uptake and DOC dynamics was also performed by incubating natural biofilms in microcosms. On the basis of our field (annual DOC budget) and laboratory results, we conclude that light-grown biofilm is, on annual average, a net DOC consumer. This biofilm showed a high monthly variability in DOC uptake/release rates, but, on average, the annual uptake rate was greater than that of the dark-grown biofilm. The higher algal biomass and greater structure of the light-grown biofilm may enhance the development of the bacterial community (bacterial biomass and activity) and microbial heterotrophic activity. In addition, the light-grown biofilm may promote abiotic adsorption because of the development of a polysaccharide matrix. In contrast, the dark-grown biofilm is highly dependent on the amount and quality of organic matter that enters the system and is more efficient in the uptake of labile molecules (higher ¹⁴C-glucose uptake rate per mgC). The positive relationships between the extracellular enzymatic activity of biofilm and DOC and BDOC content in flowing water indicate that biofilm metabolism contributes to DOC dynamics in fluvial systems. Our results show that short-term fluvial DOC dynamics is mainly due to the use and recycling of the more labile molecules. At the river ecosystem level, the potential surface area for biofilm formation and the quantity and quality of available organic carbon might determine the effects of biofilm function on DOC dynamics.     

The effect of agriculture on the seasonal dynamics and functional diversity of benthic biofilm in tropical headwater streams

Tropical streams are one of the most endangered ecosystems in the world due to the constant pressures from human activities. Among these activities, agriculture represents a land use that is crucial for human development but also a key driver of stream degradation and biodiversity decline in the tropics. Against this background, we investigated indirect effects of agriculture (alterations in stream flow and nutrient availability) and climate characteristics (water temperature) on benthic biofilm communities in tropical streams (São Paulo State, Brazil). Three first‐order streams draining catchments dominated by agricultural land use (sugarcane for bioenergy production, pasture) with some remaining riparian forest were studied for 1 year. We focused on the relationships of benthic biofilm biomass, algal biomass, diatom community, and functional structure with streamflow dynamics, nitrate concentrations, and water temperature. Our results indicate that these biological responses were mainly mediated by flow and water temperature and not by resource availability in the studied headwater streams. This result could be explained by the heavy rains and elevated runoff generation in these tropical catchments under agricultural influence, which might override the known effects of nutrient enrichment on benthic biofilm communities. Considering forecast climate and land‐use changes in tropical streams, our findings may suggest potential shifts in benthic biofilm communities, with functional consequences for aquatic food webs in these environments. Abstract in Brazilian Portuguese is available with online material.     

Warming alters coupled carbon and nutrient cycles in experimental streams

Although much effort has been devoted to quantifying how warming alters carbon cycling across diverse ecosystems, less is known about how these changes are linked to the cycling of bioavailable nitrogen and phosphorus. In freshwater ecosystems, benthic biofilms (i.e. thin films of algae, bacteria, fungi, and detrital matter) act as biogeochemical hotspots by controlling important fluxes of energy and material. Understanding how biofilms respond to warming is thus critical for predicting responses of coupled elemental cycles in freshwater systems. We developed biofilm communities in experimental streamside channels along a gradient of mean water temperatures (7.5–23.6 °C), while closely maintaining natural diel and seasonal temperature variation with a common water and propagule source. Both structural (i.e. biomass, stoichiometry, assemblage structure) and functional (i.e. metabolism, N₂‐fixation, nutrient uptake) attributes of biofilms were measured on multiple dates to link changes in carbon flow explicitly to the dynamics of nitrogen and phosphorus. Temperature had strong positive effects on biofilm biomass (2.8‐ to 24‐fold variation) and net ecosystem productivity (44‐ to 317‐fold variation), despite extremely low concentrations of limiting dissolved nitrogen. Temperature had surprisingly minimal effects on biofilm stoichiometry: carbon:nitrogen (C:N) ratios were temperature‐invariant, while carbon:phosphorus (C:P) ratios declined slightly with increasing temperature. Biofilm communities were dominated by cyanobacteria at all temperatures (>91% of total biovolume) and N₂‐fixation rates increased up to 120‐fold between the coldest and warmest treatments. Although ammonium‐N uptake increased with temperature (2.8‐ to 6.8‐fold variation), the much higher N₂‐fixation rates supplied the majority of N to the ecosystem at higher temperatures. Our results demonstrate that temperature can alter how carbon is cycled and coupled to nitrogen and phosphorus. The uncoupling of C fixation from dissolved inorganic nitrogen supply produced large unexpected changes in biofilm development, elemental cycling, and likely downstream exports of nutrients and organic matter.     

Bacterial Community Succession in Natural River Biofilm Assemblages

Temporal bacterial community changes in river biofilms were studied using 16S rRNA gene-based polymerase chain reaction–denaturing gradient gel electrophoresis (DGGE) followed by sequence analysis. Naturally occurring biofilms were sampled in 2001 during an undisturbed 7-month low-water period in the River Garonne (SW France). During the sampling period epilithic biomass exhibited a particular pattern: two 3-month periods of accumulation that resulted in two peaks in summer and fall, each at about 25 g ash-free dry mass per square meter. Bacterial community DGGE profiles differed between the summer and fall biomass peaks and shared only 30% common operational taxonomic units (OTUs), suggesting the influence of seasonal factors on these communities. During the second biomass accrual phase, bacterial richness and the appearance of new OTUs fitted a conceptual model of bacterial biofilm succession. During succession, five OTUs (corresponding to Dechloromonas sp., Nitrospira sp., and three different Spirosoma spp.) exhibited particular patterns and were present only during clearly defined successional stages, suggesting differences in life-history strategies for epilithic bacteria. Co-inertia analysis of DGGE banding patterns and physical–chemical data showed a significant relationship between community structure and environmental conditions suggesting that bacterial communities were mainly influenced by seasonal changes (temperature, light) and hydrodynamic stability. Within the periods of stability, analysis of environmental variables and community patterns showed the dominant influence of time and maturation on bacterial community structure. Thus, succession in these naturally occurring epilithic biofilm assemblages appears to occur through a combination of allogenic (seasonal) and autogenic changes.     

Production and population ecology ofPhyllospadix iwatensis Makino. I. Leaf growth and biomass in an intertidal zone

In an intertidal zone on Choshi coast, Japan,Phyllospadix iwatensis Makino emerges at daytime in spring and summer, while at night time in winter. The plants therefore experience seasonally different stresses caused by emergence, for example, intense light, ultraviolet rays, extreme temperature and desiccation, all of which the plants are unable to avoid during daytime emergence. Seasonal changes in the biomass and LAI suggest that the optimum periods for growth ofP. iwatensis would be in March when the emergent period is short or nil and light availability is high while water temperature is not too low. Dense foliage and low canopy height ofP. iwatensis in the intertidal zone relieve the plant from the stresses in emergent periods and from the disturbance caused by strong water movement in some coastal areas with active wave action.     

Variations in resistance to canopy disturbances and their interactions with the spatial structure of major species in a cool‐temperate forest

Question: How does typhoon‐related disturbance (more specifically, disturbance in the understorey due to tree‐fall and branch‐fall) affect different species mortality rates in a vertically well‐structured forest community? Location: Cool‐temperate, old‐growth forest in the Daisen Forest Reserve, Japan. Methods: We investigated the canopy dynamics and mortality rate trends of trees ≥5 cm diameter at breast height in a 4‐ha study plot, and analysed the effects of tree diameter and spatial structure on the mortality risks for major tree species in the understorey. Results: Significant differences were found in the mortality rates and proportions of injured dead stems between census periods, which were more pronounced in the understorey than in the canopy. Acer micranthum, which showed increased mortality during typhoon disturbance periods, had a clumped distribution. In contrast, Acer japonicum and Viburnum furcatum, which showed similar mortality rates between census periods, had a loosely clumped spatial distribution and a negative association with canopy trees, respectively. In the understorey stems of Acanthopanax sciadophylloides and Fagus crenata, whose spatial distribution patterns depended on canopy gaps, significant increases in mortality rates were observed only during severe typhoon‐related disturbance periods. Conclusions: The sensitivity of trees to typhoon‐related canopy disturbance is more pronounced in the lower layers of vertically structured forest communities. Differences in mortality patterns generated through the combined effects of spatial variation in disturbance regime and species‐specific spatial distribution patterns (spatial aggregation, association with canopy trees, and canopy gap dependency) contribute to the co‐existence of understorey species in forest communities that are subject to typhoon‐related disturbance.     

Influence of drought on algal biofilms and meiofaunal assemblages of temperate reservoirs and rivers

The role of hydrological droughts in shaping meiofauna abundance through alterations in biofilm biomass and composition was investigated. In January 2005, continental Portugal was under a moderate to severe drought resulting from a 40% to 60% decrease in rainfall during the previous 12 months relative to the long-term average (1961–1990). Reservoir capacity was reduced by 30–50% relative to average values and the width of streams was reduced by 20–80% in the Zêzere River Basin (central Portugal). Algal biomass and algal class composition of biofilms was assessed through quantification of algal pigments in three reservoir and six river locations. During drought, habitat alterations are expected to be sharp in rivers while, in the absence of water quality deterioration, the habitat characteristics of reservoirs are expected to remain fairly unaffected. Chlorophylls and carotenoid pigments were extracted from biofilm samples and analysed using high performance liquid chromatography (HPLC). In the winter of 2003, during the period of average rainfall, biofilm biomass did not exceed 5 μg chlorophyll a cm⁻² at any location. River biofilm biomass was roughly half of that measured in the reservoirs. In the winter of 2005 (drought), biofilm biomass increased by more than 5-fold in river locations and remained low or decreased in the reservoirs. Algal biofilms were either dominated by Bacillariophyceae or by Chlorophyceae regardless of the existence of drought. The relative contribution of Bacillariophyceae to total biofilm biomass was higher during the drought than under average hydrological conditions. The abundance of harpacticoids, cladocerans and ostracods was favoured by the drought only in the reservoirs where an increase in diatom proportion in biofilms was observed. The increase in the abundance of cyclopoid copepods, turbellarians, nematodes and chironomids in rivers during the drought could be explained by algal class composition and biomass of biofilms and environmental variables (organic matter sediment content, phosphorus availability content and sediment granulometry). The hydrological drought appears to regulate meiofauna abundance only in river locations, possibly through the promotion of the growth of biofilms and the availability of organic matter deposited in rivers during the drought. Handling editor: D. Ryder     

Responses of phytoplankton diversity to physical disturbance under manual operation in a large reservoir, China

In aquatic ecosystems, physical disturbances have been suggested to be one of the main factors influencing phytoplankton structure and diversity. To elucidate whether large-scale artificial operation of a hydroelectric reservoir has potential impacts on phytoplankton diversity, the impact on phytoplankton biodiversity of physical disturbances under artificial operation from May 2007 to April 2008 in tributaries of the Three Gorges Reservoir (TGR), China, was analysed. Two disturbance parameters, i.e. the absolute incremental rates of discharge (R _d,i ) and precipitation (R _p,i ), were created in this study for evaluating physical disturbance intensities during low and high water level periods of the TGR. Results showed that river discharge seemed to be the main factor controlling the phytoplankton diversity in low water level periods (≤151 m), and that precipitation was a potential promoter of the physical disturbance. During the 156-m impoundment process, the species diversity clearly decreased due to the high dilution effect on the phytoplankton communities. At high water level periods (>151 m), the low levels of disturbance eventually allowed the phytoplankton community to approach competitive exclusion in late February 2008. Sharply declining diversity values appeared when the Dinophyta blooms occurred in late March and late April 2008 (Peridinium and Ceratium, respectively).     

Models of underlying autotrophic biomass dynamics fit to daily river ecosystem productivity estimates improve understanding of ecosystem disturbance and resilience

Directly observing autotrophic biomass at ecologically relevant frequencies is difficult in many ecosystems, hampering our ability to predict productivity through time. Since disturbances can impart distinct reductions in river productivity through time by modifying underlying standing stocks of biomass, mechanistic models fit to productivity time series can infer underlying biomass dynamics. We incorporated biomass dynamics into a river ecosystem productivity model for six rivers to identify disturbance flow thresholds and understand the resilience of primary producers. The magnitude of flood necessary to disturb biomass and thereby reduce ecosystem productivity was consistently lower than the more commonly used disturbance flow threshold of the flood magnitude necessary to mobilize river bed sediment. The estimated daily maximum percent increase in biomass (a proxy for resilience) ranged from 5% to 42% across rivers. Our latent biomass model improves understanding of disturbance thresholds and recovery patterns of autotrophic biomass within river ecosystems.     

Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high‐resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown‐of‐thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km², predicting a mean annual coral loss of ?0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner‐shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no‐take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.     

River otter and mink occupancy dynamics in riparian systems

Semi-aquatic mammals are dependent upon streams and riparian areas, which are a product of the landscapes they drain. Both local stream morphology and surrounding land use are likely to have important influences on current occupancy of semi-aquatic mammals and potentially affect future geographic distributions. We identified aspects of the riparian system and stream structure at multiple scales that relate to the presence of river otter (Lontra canadensis) and mink (Neovison vison) to better understand how changing landscapes affect occupancy dynamics of these semi-aquatic mammals and to facilitate future monitoring and management. We estimated multi-season occupancy using 103 sites sampled over 6 seasonal sampling periods in southern Illinois, USA (44,526 km²) during 2012–2014. We hypothesized river otter and mink occupancy were related to multiple aspects of landscape and local habitat attributes including land cover, water availability, human disturbance, and stream characteristics. Occupancy of river otter was predicted by large stream size, less developed area near the stream site, and proximity to areas with reintroduced or remnant populations of river otter. Mink were more likely to occupy sites with small streams and decreased water availability near the site. However, top models for both species had low weights and high uncertainty for multiple variables. Habitat-based models may not be the best predictors of occupancy for these carnivores because they are more likely to respond to prey diversity or availability, but landscape changes that decrease natural water availability and increase human disturbance to the stream at the local scale are likely to negatively affect river otter. © 2019 The Authors. The Journal of Wildlife Management published by Wiley Periodicals, Inc. on behalf of The Wildlife Society.     

SELF‐THINNING AND SIZE INEQUALITY DYNAMICS IN A CLONAL SEAWEED (SARGASSUM LAPAZEANUM,PHAEOPHYCEAE)1

Fronds of clonal seaweeds with extensive holdfasts relative to frond size are known not to self‐thin during growth, even in crowded stands. We tested whether frond self‐thinning would occur for such a seaweed since these traits are more similar to those of unitary seaweeds, which do self‐thin in crowded conditions. We used Sargassum lapazeanum Setch. et N. L. Gardner (Fucales, Phaeophyceae) from the Pacific coast of Mexico, for which we first confirmed its clonal nature by performing a regeneration experiment in culture tanks. During the growth season (winter to late spring), S. lapazeanum stand biomass increased, while frond density and size inequality (Gini coefficient for frond biomass) decreased. These results indicate that self‐thinning occurred at the frond level. We propose a conceptual model for frond dynamics for clonal seaweeds in general. In stands of clonal species with small fronds and relatively extensive holdfasts (particularly when holdfasts are perennial), frond dynamics would be determined mostly by intraclonal regulation, which seems to prevent excessive crowding from occurring. Such species display a positive biomass–density relationship during the growth season. On the contrary, in stands of clonal species with large fronds relative to holdfast size, frond dynamics would be determined mostly by interactions among genets. For such species, self‐thinning may be detected at the frond level in crowded stands, resulting in a negative biomass–density relationship during growth.