Flow extremes and benthic organic matter shape the metabolism of a headwater Mediterranean stream

Headwater streams are key sites of nutrient and organic matter processing and retention, but little is known about temporal variability in gross primary production (GPP) and ecosystem respiration (ER) rates as a result of the short duration of most metabolism measurements in lotic ecosystems. We examined temporal variability and controls on ecosystem metabolism by measuring daily rates continuously for 2 years in Walker Branch, a first-order deciduous forest stream. Four important scales of temporal variability in ecosystem metabolism rates were identified: (1) seasonal, (2) day-to-day, (3) episodic (storm-related), and (4) inter-annual. Seasonal patterns were largely controlled by the leaf phenology and productivity of the deciduous riparian forest. Walker Branch was strongly net heterotrophic throughout the year with the exception of the open-canopy spring when GPP and ER rates were co-equal. Day-to-day variability in weather conditions influenced light reaching the streambed, resulting in high day-to-day variability in GPP particularly during spring (daily light levels explained 84% of the variance in daily GPP in April). Episodic storms depressed GPP for several days in spring, but increased GPP in autumn by removing leaves shading the streambed. Storms depressed ER initially, but then stimulated ER to 2–3 times pre-storm levels for several days. Walker Branch was strongly net heterotrophic in both years of the study, with annual GPP being similar (488 and 519 g O2 m−2 y−1 or 183 and 195 g C m−2 y−1) but annual ER being higher in 2004 than 2005 (−1,645 vs. −1,292 g O2 m−2 y−1 or −617 and −485 g C m−2 y−1). Inter-annual variability in ecosystem metabolism (assessed by comparing 2004 and 2005 rates with previous measurements) was the result of the storm frequency and timing and the size of the spring macroalgal bloom. Changes in local climate can have substantial impacts on stream ecosystem metabolism rates and ultimately influence the carbon source and sink properties of these important ecosystems.

Summary1. Rates of whole‐system metabolism (production and respiration) are fundamental indicators of ecosystem structure and function. Although first‐order, proximal controls are well understood, assessments of the interactions between proximal controls and distal controls, such as land use and geographic region, are lacking. Thus, the influence of land use on stream metabolism across geographic regions is unknown. Further, there is limited understanding of how land use may alter variability in ecosystem metabolism across regions.2. Stream metabolism was measured in nine streams in each of eight regions (n = 72) across the United States and Puerto Rico. In each region, three streams were selected from a range of three land uses: agriculturally influenced, urban‐influenced, and reference streams. Stream metabolism was estimated from diel changes in dissolved oxygen concentrations in each stream reach with correction for reaeration and groundwater input.3. Gross primary production (GPP) was highest in regions with little riparian vegetation (sagebrush steppe in Wyoming, desert shrub in Arizona/New Mexico) and lowest in forested regions (North Carolina, Oregon). In contrast, ecosystem respiration (ER) varied both within and among regions. Reference streams had significantly lower rates of GPP than urban or agriculturally influenced streams.4. GPP was positively correlated with photosynthetically active radiation and autotrophic biomass. Multiple regression models compared using Akaike’s information criterion (AIC) indicated GPP increased with water column ammonium and the fraction of the catchment in urban and reference land‐use categories. Multiple regression models also identified velocity, temperature, nitrate, ammonium, dissolved organic carbon, GPP, coarse benthic organic matter, fine benthic organic matter and the fraction of all land‐use categories in the catchment as regulators of ER.5. Structural equation modelling indicated significant distal as well as proximal control pathways including a direct effect of land‐use on GPP as well as SRP, DIN, and PAR effects on GPP; GPP effects on autotrophic biomass, organic matter, and ER; and organic matter effects on ER.6. Overall, consideration of the data separated by land‐use categories showed reduced inter‐regional variability in rates of metabolism, indicating that the influence of agricultural and urban land use can obscure regional differences in stream metabolism.

Large-Scale Trends for Stream Benthic Respiration

1. We studied whole‐ecosystem metabolism in eight streams from several biomes in North America to identify controls on the rate of stream metabolism over a large geographic range. The streams studied had climates ranging from tropical to cool‐temperate and from humid to arid and were all relatively uninfluenced by human disturbances.2. Rates of gross primary production (GPP), ecosystem respiration (R) and net ecosystem production (NEP) were determined using the open‐system, two‐station diurnal oxygen change method.3. Three general patterns in metabolism were evident among streams: (1) relatively high GPP with positive NEP (i.e. net oxygen production) in early afternoon, (2) moderate primary production with a distinct peak in GPP during daylight but negative NEP at all times and (3) little or no evidence of GPP during daylight and a relatively constant and negative NEP over the entire day.4. Gross primary production was most strongly correlated with photosynthetically active radiation (PAR). A multiple regression model that included log PAR and stream water soluble reactive phosphorus (SRP) concentration explained 90% of the variation in log GPP.5. Ecosystem respiration was significantly correlated with SRP concentration and size of the transient storage zone and, together, these factors explained 73% of the variation in R. The rate of R was poorly correlated with the rate of GPP.6. Net ecosystem production was significantly correlated only with PAR, with 53% of the variation in log NEP explained by log PAR. Only Sycamore Creek, a desert stream in Arizona, had positive NEP (GPP: R > 1), supporting the idea that streams are generally net sinks rather than net sources of organic matter.7. Our results suggest that light, phosphorus concentration and channel hydraulics are important controls on the rate of ecosystem metabolism in streams over very extensive geographic areas.

Carbon exchange of forest plantations: global patterns and biophysical drivers

This study reports the annual carbon balance of a drained riparian fen under two‐cut or three‐cut managements of festulolium and tall fescue. CO2 fluxes measured with closed chambers were partitioned into gross primary production (GPP) and ecosystem respiration (ER) for modelling according to environmental factors (light and temperature) and canopy reflectance (ratio vegetation index, RVI). Methodological assessments were made of (i) GPP models with or without temperature functions (Ft) to adjust GPP constraints imposed by low temperature (<10 °C) and (ii) ER models with RVI or GPP parameters as biomass proxies. The sensitivity of the models was also tested on partial datasets including only alternate measurement campaigns and on datasets only from the crop growing period. Use of Ft in GPP models effectively corrected GPP overestimation in cold periods, and this approach was used throughout. Annual fluxes obtained with ER models including RVI or GPP parameters were similar, and also annual GPP and ER fluxes obtained with full and partial datasets were similar. Annual CO2 fluxes and biomass yield were not significantly different in the crop/management combinations although the individual collars (n = 12) showed some variations in GPP (−1818 to −2409 g CO2‐C m−2), ER (1071 to 1738 g CO2‐C m−2), net ecosystem exchange (NEE, −669 to −949 g CO2‐C m−2) and biomass yield (556 to 1044 g CO2‐C m−2). Net ecosystem carbon balance (NECB), as the sum of NEE and biomass carbon export, was only slightly negative to positive in all crop/management combinations. NECBs, interpreted as emission factors, tended to favour the least biomass producing systems as the best management options in relation to climate saving carbon balances. Yet, considering the down‐stream advantages of biomass for fossil fuel replacement, yield‐scaled carbon fluxes are suggested to be given additional considerations for comparison of management options in terms of atmospheric impact.

The biological processes of carbon (C) uptake via plant photosynthesis (gross primary productivity, GPP) and carbon loss by autotrophic and heterotrophic respiration (ecosystem respiration, Reco) each constitute a C flux of approx. 130 Gt C per year, equal to 1/7 of the atmospheric C pool. Still, because the biological processes driving GPP and Reco are both active during daytime, they are intrinsically difficult to measure directly. The eddy covariance technique, which is effectively the gold standard for measuring net ecosystem exchange (NEE), relies on partitioning models of NEE to estimate GPP and Reco, but these methods remain debated because other processes, such as inhibition of leaf-level respiration during daytime, are not accounted for.   In ecosystems with short-stature vegetation like grasslands, shrublands, tundra, and many agricultural systems, light and dark closed chamber measurements at the ecosystem scale enable direct daytime measurements of NEE (under light conditions) and Reco (under dark conditions) while GPP can be directly estimated as NEE - Reco. Long-term data series of automated light and dark chamber measurements are, however, very rare. Here, we present data of > 50,000 measurements over six years from a novel, automated light and dark gas exchange measurement chamber that was tested in heathland, wetland, and agricultural vegetation types. In the heathland, we applied standard eddy covariance gap-filling methods to estimate annual NEE across the six years of observations. The results show annual NEE rates ranging from -96 (net uptake) to 21 (net release) g C m-2y-1 over the different years. We further applied standard eddy covariance nighttime and daytime methods to partition the observed NEE measurements into GPP and Reco. Using the nighttime method, GPP ranged from 966 to 1355 g C m-2y-1 while Reco ranged from 867 to 1372 g C m-2y-1. On average, this was only 0-4% higher than observed rates from the chamber measurements. In comparison, the daytime method yielded GPP and Reco rates that were approximately 11-30% higher than observed rates. The slightly to moderately lower direct measurements with the automatic light and dark chamber could indicate that the chamber observations are able to account at least partially for the daytime leaf-level inhibition of respiration and thus may provide a sound method for measuring the actual rates of GPP and Reco. While potential biases cannot be ruled out and will be discussed, our results indicate that automated light and dark chambers may provide an additional and highly useful tool for estimating rates of GPP and Reco in short-stature vegetation and may further serve to help constrain methods for partitioning NEE fluxes observed with other techniques, such as the eddy covariance methodology.

In many lowland streams, macrophytes are highly abundant and play a key role in ecosystem structure and function. However, no studies on annual stream metabolism have been conducted in streams with significant macrophyte abundance, despite the well-known effect on both gross primary production (GPP) and ecosystem respiration (ER). Macrophyte abundance in temperate streams is strongly seasonal, with highest biomass during summer and lowest during winter. We expected that this phenological pattern would drive annual fluctuations in GPP and ER. We measured daily metabolism for one year in two stream reaches, one with and one without macrophytes. Our results demonstrated that annual, aggregated GPP and ER were 2.2 and 1.3 times higher in the macrophyte reach. Furthermore, while daily GPP was the same between the two reaches during winter where biomass was negligible, GPP was higher during spring, summer and fall for the macrophyte reach. The range in daily ER was more constrained during summer, but more variable during fall and winter in the macrophyte reach relative to the non-macrophyte reach. Macrophyte abundance and chlorophyll-a controlled 80% of the variation in annual GPP for the macrophyte reach. Similarly, 63% of the variation in annual ER was controlled by macrophyte abundance together with discharge in the macrophyte reach. Although macrophytes enhanced GPP on an annual and seasonal time scale in agricultural lowland streams, both reaches were heterotrophic (i.e., GPP < ER) reflecting high organic matter supply from the landscape and in-stream retention and decomposition of organic matter within the macrophyte beds.

Stream metabolism provides insight into the functional processes that regulate trophic status, biomass, and nutrient cycling in streams. Comparative (spatial) analyses of streams generally do not account for shifting at‐site controls on stream metabolism over time and, thus, may not identify the primary controls on cross‐site differences in trophic status, biomass, and nutrient cycling over longer time scales. The spatial component included assessing environmental factors controlling stream metabolism (daily values) during a summer low‐flow period (August) at 17 wadable stream sites in four regions of the United States. Explanatory variables for the spatial analysis included discrete nutrients and physical parameters. The temporal component included assessing 12 of the 17 sites with more than 90 days of stream metabolism values, and continuous nitrate, photosynthetically active radiation (PAR), turbidity, maximum water temperature (°C) and stream stage (water surface elevation). Spatial analysis at the 17 sites during August (31 days) found that average gross primary production (GPP) ranged from 0.1 to 4 g O2 m−2 day−1 and ecosystem respiration (ER) from 0.37 to 6.4 g O2 m−2 day−1. Sites were primarily heterotrophic; however, some sites varied from autotrophic to heterotrophic daily. Multiple regression indicated that GPP was a function of orthophosphate, percent canopy cover, and the number of days since a high flow (R2 = 0.51), whereas ER was primarily a function of GPP (R2 = 0.40). Temporal patterns in daily stream metabolism were evaluated using at‐site autoregressive models at 12 streams with relatively complete, continuous records. PAR, nitrate and maximum water temperature were the dominant variables influencing GPP, and water depth and nitrate were the most common explanatory variables for ER models. The autoregressive components (i.e., GPP or ER for the previous day) had a strong influence on both GPP and ER except after spates, indicating that biomass may be the dominant control on metabolism rather than variability in environmental factors during stable‐flow periods. We found two dominant temporal metabolism regimes: a seasonal pattern with elevated spring metabolism followed by low stable summer metabolism and a temporally disturbed pattern which tended to occur in streams with frequent spates. These patterns were not indicated by differences in metabolism among streams during stable low‐flow conditions. Because streams are generally heterotrophic with only limited periods when production may be high, comparative analyses must estimate stream metabolism over a time scale representing at‐site spatial variability and account for controls on periods of high production to adequately characterise differences between streams.

Streams play a key role in the global biogeochemical cycles, processing material from adjacent terrestrial systems and transporting it downstream. However, the drivers of stream metabolism, especially those acting at broad spatial scales, are still not well understood. Moreover, stream metabolism can be affected by hydrological changes associated with seasonality, and thus, assessing the temporality of metabolic rates is a key question to understand stream function. This study aims to analyse the geographical and temporal patterns in stream metabolism and to identify the main drivers regulating the wholeecosystem metabolic rates at local and regional scales. Using a coordinated distributed experiment, we studied ten headwaters streams located across five European ecoregions during summer and fall 2014. We characterized the magnitude and variability of gross primary production (GPP) and ecosystem respiration (ER) with the open-channel method. Moreover, we examined several climatic, geographical, hydrological, morphological, and physicochemical variables that can potentially control stream metabolic rates. Daily rates of stream metabolism varied considerately across streams, with GPP and ER ranging from 0.06 to 4.33 g O 2 m -2 d -1 and from 0.72 to 14.20 g O 2 m -2 d -1 , respectively. All streams were highly heterotrophic (P/R < 1), except the southernmost one. We found that the drier climates tended to have the highest GPP, while humid regions presented the highest ER. Between the sampling periods no statistical differences were found. Partial-least squares models (PLS) explained 80% of the variance in GPP and ER rates across headwater streams and included both local and regional variables. Rates of GPP varied primarily in response to the local variables, such as streambed substrate and stream water temperature. In contrast, regional variables, such as the mean annual temperature or the land use of the catchment, had more relevance to explain ER. Overall, our results highlight that stream metabolism depends on both local and regional drivers and show the positive experience of a young network of researchers to assess scientific challenges across large-scale geographic areas.

1. In unshaded, nutrient‐rich streams, prolific growth of stream macrophytes often results in flows that over‐top the banks and in high primary production and respiration that may result in extreme diel variations in dissolved oxygen. Consequently, water protection authorities commonly remove macrophytes periodically. 2. We investigated the effect of plant removal on stream metabolism and oxygen balance in two Swiss streams with a high macrophyte biomass. We monitored the concentration of dissolved oxygen before and after macrophytes were removed by cutting and dredging, and calculated rates of gross primary production and ecosystem respiration by means of diel oxygen curves. 3. The removal of plants, which had reached a dry biomass of 320–420 g m−2 immediately before plant removal, had a different impact on stream metabolism in the two streams. In the first (plants removed in May), neither primary production nor ecosystem respiration were significantly affected. In the second (plants removed in late July), gross primary production and ecosystem respiration were reduced by about 70%. In this latter stream gross primary production increased in the first 2 weeks after plant removal but never recovered to pre‐disturbance levels. 4. The removal of plants coincided with only a moderate increase in nocturnal oxygen concentration (+1 mg L−1). This, and the rapid partial recovery of stream metabolism in the second stream, suggests that an increase in the oxygen concentration after plant cutting is transient in unshaded, nutrient‐rich streams.

We present a comprehensive data set of gross primary production (GPP) and ecosystem respiration (ER) in open‐canopy, nutrient‐rich streams draining row‐crop agriculture in the midwestern United States. We used two approaches to characterize temporal and spatial variation in whole‐stream metabolism: continuous measurements in one agricultural stream for 1 yr, and periodic daily measurements in six agricultural streams on six dates spanning summer, autumn, and winter. Continuous measurements revealed high rates of GPP (range: 0.1 to 22.0 g O2 m−2 d−1) and ER (range: −0.9 to −34.8 g O2 m−2 d−1) that varied seasonally with light availability and temperature. GPP and ER were correlated during periods of high autotrophic production, suggesting that autotrophic respiration comprised a large portion of ER; however, the GPP : ER ratio exceeded 1 for only 4% of the year. While there were distinct temporal patterns in metabolism in one agricultural stream, rates of GPP and ER were similar among six streams when assessed via periodic daily measurements, and 26% of all periodic daily measurements were autotrophic with GPP : ER &gt; 1. However, these periodic measurements were collected under baseflow conditions and may have overestimated the extent of autotrophy in agricultural streams. Overall, the open canopy and elevated nutrients of agricultural streams resulted in higher rates of GPP and ER compared with more pristine systems. Estimates of metabolism are needed from underrepresented systems to accurately quantify carbon fluxes from fluvial ecosystems.

Summary Stream ecosystem metabolism integrates production and respiration of organic matter and plays a fundamental role in the global carbon (C) cycle. Several studies have identified distal and proximal physical controls, for example, land use and transient storage, or the effects of water chemistry, that is, organic matter and nutrient availability, on stream metabolism. In parallel, research on organic matter quality has identified conspicuous gradients of chemical composition, yet mostly without demonstrating any functional implications. We hypothesise that organic matter holds a key position in a more comprehensive causal framework of stream ecosystem metabolism, and that a concurrent study can improve mechanistic understanding. Specifically, we here postulate that dissolved organic matter (DOM) quality, that is, its chemical composition, acts as a control of ecosystem respiration (ER) as much as it is a result of gross primary production (GPP). As such, DOM quality likely forms a central link between land use and stream metabolism, besides known physical controls including transient storage and light availability. To examine these hypotheses, we studied 33 streams in north‐eastern Austria, a region with diverse land use ranging from semi‐natural, forested areas to agricultural areas and settlements. We analysed DOM composition by absorbance and fluorescence spectroscopy, including modelling excitation–emission matrices with parallel factor analysis. We then opposed these data to GPP and ER estimated by fitting a metabolism model to single‐station diurnal oxygen records. Structural equation modelling revealed land use as a control on light conditions, DOM composition and concentration and nutrient concentrations, which together ultimately shaped GPP and ER. In particular, humified, coloured and aromatic DOM of predominantly terrestrial origin was prevalent in coniferous forest catchments and increased stream ER. Agricultural and urban areas enriched streams with phosphorous and nitrogen, which increased ER and GPP. Besides nutrients, GPP seemed to be weakly correlated with light availability and – in contrast to our hypothesis – left only a weak imprint on DOM composition. Land‐use change is rated as the most pervasive human influence on natural ecosystems and our results highlight its impact on aquatic GPP and ER in streams. To understand the role of inland waters in the global C cycle will require mechanistic understanding of ecosystem metabolism, which notably includes organic matter quality as a hitherto underappreciated key player.

Stream metabolism is affected by both natural and human-induced processes. While metabolism has multiple implications for ecological processes, relatively little is known about how metabolic rates are influenced by land use in tropical streams. In this study, we assessed the metabolic characteristics and related environmental factors of six streams located in a transition area from Cerrado to Atlantic Forest (São Carlos/Brazil). Three streams were relatively preserved, while three were flowing through more agriculturally and/or urban impacted watersheds. Surface water samples were analyzed for biological and physico-chemical parameters as well as discharge and percentage of canopy cover. Metabolism was determined through the single-station method to estimate gross primary production (GPP), ecosystem respiration (ER) and net ecosystem production (NEP) with BAyesian Single-station Estimation (BASE). Nutrient concentrations tended to be higher in impacted versus preserved streams (e.g., average total phosphorus between 0.028-0.042 mg L-1 and 0.009-0.038 mg L-1, respectively). Average canopy cover varied between 58 and 77%, with no significant spatial or seasonal variation. All streams were net heterotrophic (ER exceeded GPP) in all sampling periods. GPP rates were always lower than 0.7 gO2 m-2 d-1 in all streams and ER varied from 0.6 to 42.1 gO2 m-2 d-1. Linear Mixed-Effect models showed that depth, discharge, velocity and total phosphorus are the most important predictors for GPP. For ER, depth, velocity and canopy cover are significant potential predictors. Canopy cover was the main light limiting factor and influenced stream metabolism. Our findings reinforced the concepts that shifts in the shading effect provided by vegetation (e.g., through deforestation) or changes in discharge (e.g., through land use conversion or water abstractions) can impact freshwater metabolism. Our study suggests that human activities in low latitude areas can alter tropical streams’ water quality, ecosystem function, and the degree of riparian influence. Our data showed that tropical streams can be especially responsive to increases of organic matter inputs leading to high respiration rates and net heterotrophy, and this should be considered to support management and restoration efforts.

Headwater streams influence the biogeochemical characteristics of large rivers and play important roles in regional and global carbon budgets. The combined effects of seasonality and land use change on the biogeochemistry of headwater streams, however, are not well understood. In this study we assessed the influence of catchment land use and seasonality on the composition of dissolved organic matter (DOM) and ecosystem metabolism in headwater streams of a Kenyan river. Fifty sites in 34 streams draining a gradient of catchment land use from 100% natural forest to 100% agriculture were sampled to determine temporal and spatial variation in DOM composition. Gross primary production (GPP) and ecosystem respiration (ER) were determined in 10 streams draining primarily forest or agricultural catchments. Absorbance and fluorescence spectrophotometry of DOM reflected notable shifts in composition along the land use gradient and with season. During the dry season, forest streams contained higher molecular weight and terrestrially derived DOM, whereas agricultural streams were dominated by autochthonous production and low molecular weight DOM. During the rainy season, aromaticity and high molecular weight DOM increased in agricultural streams, coinciding with seasonal erosion of soils and inputs of organic matter from farmlands. Most of the streams were heterotrophic. However, GPP and ER were generally greater in agricultural streams, driven by higher dissolved nutrient (mainly TDN) concentrations, light availability (open canopy) and temperature compared with forest streams. There were correlations between freshly and autochthonously produced DOM, GPP and ER during both the dry and wet seasons. This is one of the few studies to link land-use with organic carbon dynamics and DOM composition. Measures of ecosystem metabolism in these streams help to affirm the role of tropical streams and rivers as important components of the global carbon cycle and demonstrate that even semi-intensive, smallholder agriculture can have measurable effects on riverine ecosystem functioning.