Short-term effects of elevated CO2 on periphyton community in an artificially constructed channel
© The Author(s) 2016
Received: 3 March 2016
Accepted: 1 July 2016
Published: 24 October 2016
Direct impact of inorganic carbon (i.e., carbon dioxide (CO2)) on the periphyton community is important to understand how and to what extent atmospheric conditions can affect the structure and dynamics of these communities in lotic systems. We investigated the influence of elevated CO2 concentration on the periphyton community in the artificially constructed channels during the winter period. The channels made of acrylic paneling were continuously supplied with surface water discharged from a small reservoir, which was supported with ground water, at a flow rate of 5 L/min, and water temperature ranging 4–5 °C. The effects of elevated CO2 concentrations (790 ppm) were evaluated in comparison with the control (395 ppm CO2) by analyzing pH, water carbon content and nutrients in water, periphyton composition and biomass, chlorophyll-a, ash-free dry-matter at 2-day intervals for 10 days.
After the addition of CO2, significant decreases of pH, NH3-N, and PO4-P (p < 0.05) and increases of chlorophyll-a, ash-free dry-matter, and the cell density of periphyton (p < 0.01) were observed, whereas the species composition of periphyton and water carbon content did not change.
These results suggest that elevated CO2 in flowing water system with low temperature could facilitate the growth of periphyton resulting in biomass increase, which could further influence water quality and the consumers throughout the food web.
Carbon dioxide (CO2) is a major greenhouse gas with the greatest potential to influence global climate change since the industrial revolution, while the CO2 emission into the atmosphere has been increasing, and its concentration will reportedly double in the next 50–100 years (Houghton et al. 2001). Atmospheric CO2 concentrations have risen from 295 parts per million (ppm) to 380 ppm over the last 100 years and have contributed substantially to global warming, climate change, and resultant biological extinctions (Lewis and Nocera 2006; Battisti and Naylor 2008). CO2 emissions vary with seasonal photosynthesis, respiration of plants, and the amount of fossil fuels consumed (IPCC 2007). In particular, the atmospheric CO2 concentration during the winter season typically increases due to the reduction of photosynthesis of plants and an increase in active consumption of fossil fuels (Lewis and Nocera 2006; Sayre 2010). Low water temperature during the winter increases CO2 solubility (Tortell et al. 2008), which may be expected to affect aquatic ecosystems.
CO2 gas dissociates into HCO3 −, CO3 2−, and H+ ions in water and may enhance algal growth and production. In general, benthic and planktonic algae use bicarbonate (HCO3 −) and carbonate (CO3 2−) as carbon sources (Falkowski and Raven 2007; Giordano et al. 2005). Almost all studies on algal biomass variations with increased CO2 have been conducted in marine water in response to a volcanic eruption (Hall-Spencer et al. 2008; Johnson et al. 2011). In contrast, few studies have been performed regarding the impact of increased CO2 on periphyton structure and function in freshwater ecosystems. One exception is a study that assessed these variables on the fish community (Ross et al. 2001). In the freshwater system, the amount of organic carbon supply frequently exceeds inorganic carbon, particularly at high altitudes, because streams receive carbon as particulate organic matter such as dead leaves. These leaves are processed by fungi, bacteria, and benthic macroinvertebrates (Biggs et al. 1998; Tuchman et al. 2002).
Studies considering the direct impact of inorganic carbon (i.e., CO2) on the periphyton community are important to understand how and to what extent atmospheric conditions can affect the structure and dynamics of these communities. Particularly, in a flowing water system, the periphyton community relies on various physicochemical factors as well as other aquatic organisms. Thus, even a small disturbance in CO2 can considerably affect the abundance and species composition of periphyton (Hillebrand and Sommer 2000; Villeneuve et al. 2010).
The present study aimed to elucidate the impact of elevated CO2 concentrations on biomass and species composition of periphyton in an aquatic environment with low temperature, high solubility of CO2, and low photosynthesis.
The experiment was conducted in the artificial channel for 3 weeks in December when the water temperature was 4–5 °C (2012). The experimental water was transported by an electric pump from a small reservoir to a tank in the laboratory (2 t). The reservoir was located near the laboratory at Konkuk University (36° 00′ N, 140° 02′ E). It was 55,661 m2 in volume with depths of 1.5–2.5 m. This reservoir was ice-covered during the study. For the study, we used the running water from the discharging point of the reservoir. Water was supplied to two buckets (150 L) where CO2 was injected and pumped into the inlets of each artificial channel. The water flow was controlled at 5 L/min. The atmospheric CO2 concentration (control group) was automatically measured with a portable meter (Model CGP-1: DKK-TOA, Tokyo, Japan) near the laboratory, and was approximately 395 ppm during the experimental period. For the treatment group, CO2 was injected to yield a twofold higher concentration—790 ppm. CO2 gas was purchased from a domestic company (Donghwa Industrial Gas Co. Ltd., Seoul, Korea). Cool-white fluorescent lamps were installed 1 m above the upper part of the artificial channel to deliver a light intensity of 50 μmol/m2/s and a 10-h light and 14-h dark photo-period.
During the experiment, water quality factors including water temperature, electric conductivity, pH, suspended solids (SS), total carbon, total inorganic carbon, total organic carbon (TOC), chlorophyll (Chl)-a, nutrient contents (nitrogen and phosphorus), ash-free dry-matter (AFDM), and periphyton (biomass and species composition) were examined to compare the differences between the control and treatment groups after exposure to CO2.
Analysis of water quality
Sampling and analysis were performed at 2-day intervals for 10 days and, thus, six times total including day 0. Water temperature, pH, and electric conductivity were measured with a multi-probe detector (YSI 600QS-O-M, YSI Inc., Yellow Springs, OH, USA) at the buckets located at the outlets of each artificial channel. Total carbon, total inorganic carbon, and TOC were measured with a TOC analyzer (Shimazu, Kyoto, Japan) after injecting CO2. Chl-a, suspended solids, and nutrients were also analyzed. To analyze Chl-a concentrations, a water sample was filtered through Whatman GF/F filter paper (Whatman International Ltd., Maidstone, UK) and extracted in the dark at 4 °C for 24 h with 10 mL of 90 % acetone. Then, the sample was centrifuged for 20 min at 1650 rpm (VS-5000 N, Vision Scientific, Seoul, Korea) (APHA 2005) and the supernatant was measured with a spectrophotometer (Optizen 2010 UZ, MECASYS Inc., Seoul, Korea). Suspended solids were measured by first filtering 200 mL of experimental water that had passed through the artificial channel (APHA 2005). The difference was measured between the initial weight (A) and final weight (B) of the filter dried in an oven at 105 °C for 24 h (OF-11, JEIO Tech Inc. Seoul, Korea). The final weight of the filter was measured with the GF/C filter. Nutrients were analyzed by following methods: NO2-N and NO3-N by the ultra-violet visible spectrophotometry method, NH3-N by the indophenol method, total nitrogen (TN) by the absorption metric method, and PO4-P and total phosphorous (TP) by the ascorbic acid method (APHA 2005).
Analysis of periphyton
The periphyton were sampled by brushing the complete surface of the substrates in each artificial channel. Parts of the sample were used to analyze Chl-a and AFDM, and the others were fixed in Lugol solution to identify the species. Chl-a formed in the substrate was analyzed by applying the same methods as mentioned previously. The amount of AFDM was obtained from the measured weight difference between A1 (the weight of the sample filtered through the GF/F filter bed and dried in an oven at 105 °C for 24 h) and A2 (the weight of the filter GF/F bed burnt for 2 h in a furnace). Species identification of periphyton were conducted with a ×400–1000 light microscope (Zeiss, Zena, Germany). The abundances of periphyton were expressed as cell number per area (cells/cm2). As representative references, Patrick and Reimer (1966), Krammer and Lange-Bertalot (1991a, 1991b, 2007a, 2007b), and Chung (1993) were used to identify the periphyton species.
Student’s t test was used to compare differences in water quality variables, relative abundance of periphyton, and species composition between control (without CO2 addition) and treatment (with CO2 addition) groups (SPSS v. 18.0.0; SPSS Inc., Chicago, IL, USA) at a p < 0.05 significance level.
Results and discussion
Mean values of experimental parameters in the artificial laboratory stream with control (2 × 6) and treatment groups (2 × 6)
4.8 ± 0.2
4.8 ± 0.2
9.18 ± 0.06
9.02 ± 0.03
Electric conductivity (μS/cm)
267.8 ± 2.7
268.0 ± 2.8
85.12 ± 11.42
88.99 ± 11.56
Suspended solid (mg/L)
23.33 ± 1.22
23.08 ± 3.53
51.00 ± 0.40
50.00 ± 0.20
2.60 ± 0.05
2.58 ± 0.05
10.00 ± 0.20
8.00 ± 0.20
Total nitrogen (mg/L)
3.45 ± 0.07
3.43 ± 0.06
1.30 ± 0.90
0.80 ± 0.30
Total phosphorus (μg/L)
51.00 ± 0.20
49.00 ± 0.30
Total organic carbon (mg/L)
5.34 ± 0.34
5.68 ± 0.19
Inorganic carbon (mg/L)
14.66 ± 0.64
13.49 ± 0.64
Total carbon (mg/L)
20.00 ± 0.65
19.17 ± 0.52
Periphyton chlorophyll-a (μg/cm2)
5.28 ± 1.29
6.75 ± 1.35
Periphyton ash-free dry-matter (mg/cm2)
1.09 ± 0.15
1.29 ± 0.15
Periphyton density (106 cells/cm2)
4.2 ± 0.7
5.6 ± 0.9
Fragilaria capucina var. gracilis (106 cells/cm2)
3.2 ± 0.5
4.3 ± 0.7
Fragilaria capucina (106 cells/cm2)
0.8 ± 0.2
1.0 ± 0.3
Cryptomonas ovata (104 cells/cm2)
5.9 ± 0.5
7.9 ± 0.8
Scenedesmus quadricauda (104 cells/cm2)
5.3 ± 0.7
5.0 ± 0.8
Aulacoseira ambigua (104 cells/cm2)
3.2 ± 0.6
4.2 ± 0.8
The present study indicates that the biomass of periphyton slightly increased with a twofold increase in CO2, but no apparent change was observed in species composition. A recent study demonstrated that a twofold increase in atmospheric CO2 doubled primary productivity (Schippers et al. 2004). Additionally, Levitan et al. (2007) found a 1.5–3-fold increase in cyanobacteria biomass with a twofold increase in CO2 from 250 to 500 ppm under constant respiration and photosynthesis. Other studies also showed an increase in algal density including diatoms with an increase in CO2 concentrations (Biswas et al. 2011). Johnson et al. (2011) also observed an increase in the amount of pennate diatoms up to sevenfold at 592 and 1611 μatm compared to 419 μatm of CO2. According to Tortell et al. (2008), Chaetoceros spp., which has large cells and forms chains, became dominant and the density of the small-celled Pseudo-nitzschia subcurvata decreased rapidly when the CO2 concentration was increased to 800 ppm.
In contrast, increased CO2 did not affect algae growth in other studies (Goldman 1999; Tortell et al. 2000, Suffrian et al. 2008). Hargrave et al. (2009) studied the impact of increased CO2 on periphyton in streams and reported a temporary yet significant difference in primary productivity between 360 and 720 ppm CO2. However, they did not see significant changes in biomass or community composition of periphyton. Fu et al. (2007) also reported that Synechococcus is sensitive at 380 and 750 ppm CO2 and appeared stagnant. In the present study, it was presumed that changes in algal biomass were observed due to changes in CO2. The effects could have been indirect because the winter leads to low levels of nutrients and low light availability, but these effects are also associated with a rise in CO2 solubility (Hein and Sand-Jensen 1997).
Differences in carbon acquisition efficiency during carbon fixation by algal species influences interspecific competition; thus, increased CO2 might cause a change in the composition of the algal community (Rost et al. 2003; Fu et al. 2007; Trimborn et al. 2009). The cell membranes of diatoms have high CO2 permeability, and CO2 diffusive exchange between cells and the external environment is very high (Hopkinson et al. 2011). Biswas et al. (2011) reported that the algal growth rate doubled when CO2 pressure increased from 225 to 646–1860 μatm, and the dominant species shifted from diatoms to cyanobacteria. In this study, no changes were observed in periphyton species composition, perhaps due to the use of cold water with low species richness.
The experimental water in the present study was essentially lake water, not stream water, because the ambient water used was discharged from an outlet of a small reservoir. Also, in this study, we extended the commonly used lake-river hybrid systems or systems of rivers fed by lentic systems. Thus, our results could be useful to understand the dynamics of periphyton or meroplanktonic algae in such aquatic ecosystems. The increased CO2 could increase the amount of dissolved inorganic carbon in stream water, facilitate the growth of periphyton, and thereby further influence biomass and community composition of macroinvertebrates and fish throughout the food web. Periphyton can also raise the relative rate of carbon assimilation compared to nutrient uptake, which could reduce the nutritional quality of algae for other organisms. This, in turn, can influence the community composition of macroinvertebrate consumers (Hargrave et al. 2009).
Our results clearly showed that the increased CO2 in low-temperature running water enhanced periphyton development (i.e., biomass, Chl-a, and AFDM), but did not shift species composition. In addition, water contents of ammonia and phosphate decreased after addition of CO2, perhaps due to the increase in the periphyton biomass. However, it remains unknown how CO2 concentrations may affect the periphyton community in high-temperature conditions. Thus, more research is needed to generalize the impact of CO2 on various running water systems, including streams with different dimensions and localities (Finlay et al. 1999; Finlay 2003, 2004).
- Chl-a :
Intergovernmental Panel on Climate Change
Total organic carbon
This study was supported by “The Environmental Basic Survey of the Han River” (1333-406-260). The authors are grateful to the reviewers for their constructive comments for the improvement of the earlier version of the manuscript.
This study was funded by National Institute of Environmental Research, Republic of Korea, in the project name of “The Environmental Basic Survey of the Han River” (1333-406-260).
Availability of data and materials
The data in our work will not be shared with a reason that there are no any particular data base and material to uniquely support the work; data and supporting materials are straightforward.
HJP performed the experiment and wrote the manuscript. DRK assisted in the experiment and the data analysis. BHK constructed the experimental channel and assisted in the experimental design and the manuscript preparation. SJH supervised the research and assisted in the data interpretation and the manuscript preparation and revision. All authors read and approved the final manuscript
The authors declare that they have no competing interests.
Consent for publication
Ethic approval and consent to participate
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