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Pelagic respiration in the coastal zone of the southern Baltic Sea
Ecohydrology & Hydrobiology 15 (2015) 215–219
Contents lists available at ScienceDirect
Ecohydrology & Hydrobiology journal homepage: www.elsevier.com/locate/ecohyd
Short Communication
Pelagic respiration in the coastal zone of the southern Baltic Sea Krzysztof Rychert *, Magdalena Wielgat-Rychert, Marta Wołoszynek, Gracjan Sojda Department of Ecology, Pomeranian University in Słupsk, ul. Arciszewskiego 22b, 76-200 Słupsk, Poland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 December 2014 Accepted 3 June 2015 Available online 17 June 2015
Respiration measurements were carried out year round at two stations located in the coastal zone of the southern Baltic Sea. Study sites differed with their characteristics: first one was located in the coastal zone of the Gulf of Gdan´sk near the town of Sopot (548270 N, 188350 E), second one was located in the coastal waters of the southern Baltic Sea near the town of Ustka (548350 N, 168500 E). The study reports a range of respiration rates and mean annual values, which are useful for development and parameterization of biogeochemical models. Respiration was estimated as the decrease in oxygen concentration in water confined in glass bottles. The mean annual respiration rate was 0.37 mgO2 l1 d1 at the study site in Sopot and 0.18 mgO2 l1 d1 at the study site in Ustka. In Ustka, respiration rates depended on temperature (R2 = 0.77, p = 0.0008), whereas in Sopot there was no such statistically significant dependence. At both study sites, there was no significant relationship between respiration rates and bacterial abundance. Diel oxygen consumption was compared with that measured during prolonged, five-day incubation period to detect excess resources capable of maintaining respiration rates. In Sopot respiration rates decreased during the five-day incubation period, whereas at study site in Ustka, they were generally stable during such incubation, what suggested that utilization of excess resources was prevented by top–down control of grazers. ß 2015 European Regional Centre for Ecohydrology of the Polish Academy of Sciences. Published by Elsevier Sp. z o.o. All rights reserved.
Keywords: Oxygen consumption Temperature Bacteria Organic matter Grazers
1. Introduction Ecosystem metabolism comprises two main processes: primary production and organic matter degradation. In aquatic environments, the latter is most often approximated by respiration (=oxygen consumption) and is less thoroughly studied than primary production (Holtappels et al., 2014; Jahnke and Craven, 1995; Robinson et al., 2002; Wiliams and del Giorgio, 2005). This particularly concerns the regulation of respiration rates by different
* Corresponding author. Tel.: +48 598405421. E-mail address: [email protected] (K. Rychert).
factors (Wiliams and del Giorgio, 2005). Ecosystem metabolism is often affected by eutrophication, which is defined as an increase in nutrient supply resulting in an increase in primary production. Especially sensitive to eutrophication process are semi-enclosed and relatively small water bodies, such as the Baltic Sea, that are surrounded by highly industrialized countries (Gustafsson et al., 2012; Larsson et al., 1985; Wulff et al., 1990), particularly along their coastal zones (Cederwall and Elmgren, 1990; Łysiak-Pastuszak et al., 2004; Rosenberg et al., 1990). The eutrophication of the Baltic has resulted in increased primary production that has caused changes in the food-web structure affecting not only unicellular organisms (Wasmund et al., 2008; Piwosz and Pernthaler,
http://dx.doi.org/10.1016/j.ecohyd.2015.06.001 1642-3593/ß 2015 European Regional Centre for Ecohydrology of the Polish Academy of Sciences. Published by Elsevier Sp. z o.o. All rights reserved.
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K. Rychert et al. / Ecohydrology & Hydrobiology 15 (2015) 215–219
2010), but probably even fish species that are important to commercial fisheries (Elmgren, 1989; Hansson and Rudstam, 1990; Jansson and Dahlberg, 1999). The results of the latest studies indicate that the trophic status in most Baltic Sea areas has not been reduced despite measures implemented to reduce external inputs of nitrogen and phosphorus. More research is needed to understand the impact of eutrophication on the marine environment (Funkey et al., 2014; Gustafsson et al., 2012; HELCOM, 2014; Stigebrandt et al., 2014) and to understand paths of organic matter decomposition in the Baltic Sea ecosystem. In the present study, we observed seasonal changes in respiration rates at two study sites located in the coastal zone of the southern Baltic Sea and checked their dependence on temperature and bacterial abundance. The study sites differed in characteristics: the first site in Sopot was located in the coastal zone of the Gulf of Gdan´sk, whereas the second site in Ustka was located in the coastal zone of open waters of the southern Baltic Sea. The study reports a range of respiration rates and mean annual values. A second aim of the study was to evaluate whether respiration rates were bottom–up or top–down controlled. Bottom–up control means that respiration rates depend on the availability of biodegradable organic matter (Andersson et al., 2006; Gonza´lez et al., 2003), whereas top–down control means that standing stocks of the smallest picoplanktonic and nanoplanktonic organisms, which account for the bulk of respiration (Jahnke and Craven, 1995; Robinson and Williams, 2005), are restricted by the grazing pressure of larger organisms. The type of control decides whether organic matter is broken down at the study site or it is exported toward offshore waters. The type of control exerted on respiration was assessed based on decreases in respiration rates during extended dark incubations. We assumed that stable respiration rates during a five-day incubation period indicated excess resources, the utilization of which was prevented by the top–down control of the respiring organisms. 2. Materials and methods The studies were carried out at two study sites: in Sopot and in Ustka (Fig. 1). Measurements were carried out at the Sopot site (548270 N, 188350 E) between April 2003 and March 2004 (12 data points), and water for the experiments was taken from the end of 450-m wooden pier. Measurements at the Ustka site (548350 N, 168500 E) were conducted between October 2007 and September 2008 (10 data points). Water was collected from the end of a 70-m concrete pier. Both study sites were of comparable depth (6.0–6.5 m), and water was taken from the wellmixed part of the water column. Respiration measurements were always accompanied by water temperature and salinity measurements and also counts of bacterial abundance. At the Sopot site water temperature and salinity was measured with portable STD probe (Sensordata). At the Ustka site water temperature was measured with mercurial thermometer and water salinity with portable salinometer (Elmetron). At both study sites, bacterial counts were performed under an epifluorescence microscope after staining with acridine orange (Hobbie et al., 1977).
Fig. 1. Location of two study sites in the coastal zone of the southern Baltic Sea.
Respiration was estimated as the decrease in oxygen concentration in water confined in glass bottles, i.e., the difference between oxygen concentration before and after dark incubation at in situ temperatures. Before each experiment, the equipment was acid-washed and rinsed with deionized water. The water, taken from study sites, was siphoned through a gas-tight tubing into Winkler flasks (about 120 ml) to measure the initial oxygen concentrations, and into four 1000-ml-bottles (Sopot) or eight Winkler flasks (Ustka), in which the water was incubated for 24 h (two 1000-ml-bottles in Sopot and three Winkler flasks in Ustka) and five days (two 1000-mlbottles in Sopot and five Winkler flasks in Ustka). As mentioned above, all incubations were carried out in the dark and at in situ temperatures. After incubations, the final oxygen concentrations were measured. In Sopot, prior to measurements of oxygen concentration, water from each 1000-ml-bottle was siphoned through a gas-tight tubing into three Winkler flasks. All oxygen measurements were carried out with the Winkler method using piston titrators: Metrohm Titrino 702SM for Sopot and Schott Titroline Basic for Ustka. Metrohm Titrino was combined with potentiometric electrode (Metrohm Pt Titrode), which allows automatic detection of the end-point of titration. In Ustka, where Shott Titroline titrator was used, end-point was detected with a standard starch indicator. A single oxygen concentration measurement was the average of at least three separate titrations. The differences in oxygen concentrations were expressed in mgO2 l1 per day or five days, depending on the incubation type. 3. Results and discussion 3.1. Environmental parameters and bacterial abundance Water temperature ranged from 1 8C to 21 8C in Sopot and from 3 8C to 20 8C in Ustka (Fig. 2). Water salinity at both study sites was slightly lower than that observed in
K. Rychert et al. / Ecohydrology & Hydrobiology 15 (2015) 215–219
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2001), in the coastal zone of the Gulf of Gdan´sk (up to 1.28 mgO2 l1 d1; York et al., 2001), and in offshore waters of the Gulf of Gdan´sk and close to the Vistula River mouth (up to 1.00 mgO2 l1 d1; Witek et al., 1999). Mean annual respiration rates (Sopot: 0.37 mgO2 l1 d1; Ustka: 0.18 mgO2 l1 d1) flanked mean values for coastal waters (0.24 mgO2 l1 d1; Robinson and Williams, 2005). 3.3. Factors affecting respiration rates
Fig. 2. Seasonal changes in respiration rates and temperature observed in pelagic water at both study sites.
the surface waters of the southern Baltic Sea (7.5%; Mattha¨us et al., 2008). The mean salinity in Sopot was 7.1%, and it changed during the study regularly from the lowest value recorded in April (6.4%) to the highest in February (7.4%). Mean water salinity at the Ustka study site was lower (6.7%, range: 4.6–7.7%), and it fluctuated irregularly because of the variable impact of fresh water from the mouth of the Słupia River located just 1.3 km to the east. In general, changes in environmental conditions at the Sopot study site were gentle, whereas those in Ustka changed irregularly. Bacterial abundance in Sopot ranged from low values in winter (4–5 109 cells l1) to high values observed during spring bloom (11.7 109 cells l1) and during summer (up to 17 109 cells l1). In Ustka, bacterial abundance ranged from low values during winter (about 1.5 109 cells l1) to high values in summer (5–6 109 cells l1) and in autumn (up to 8 109 cells l1). 3.2. Seasonal changes in respiration rates Respiration rates at the Sopot site ranged from 0.14 to 0.66 mgO2 l1 d1, and those in Ustka were comparable (0.00–0.64 mgO2 l1 d1, Fig. 2). The highest respiration rates in Ustka were observed during summer, whereas in Sopot two respiration rate peaks were observed: the first during the spring phytoplankton blooms (for details see Rychert et al., 2013) and the second during summer. Similar respiration rate ranges but with higher maximal values were observed in the southern Baltic Sea before: in the Pomeranian Bay (up to 0.81 mgO2 l1 d1; Witek et al.,
The highest respiration rates at the Ustka study site were observed during summer, and respiration depended on temperature (R2 = 0.77, p = 0.0008). There was no distinct spring bloom (see also Rychert et al., 2013). In Sopot, the highest respiration rates were observed during spring phytoplankton blooms when the temperature was lower than in summer (Fig. 2). Consequently, the relationship between temperature and respiration rates at the Sopot site was insignificant. A statistically significant but moderate relationship between temperature and respiration rates was also observed in marine waters by Fourqurean et al. (1997), Sampou and Kemp (1994), and Witek et al. (1999). High respiration rates during spring blooms, as noted at the Sopot study site, were also reported by Kuparinen (1987) in the Gulf of Finland (northern Baltic Sea). According to the literature, the dependence between bacterial abundance and community respiration is typically weak or even insignificant (e.g., Chen et al., 2003; Fourqurean et al., 1997; but see Robinson et al., 2002). In this study, correlations between bacterial abundances and respiration rates were insignificant at both stations studied. Bacteria are the main oxygen consumers in aquatic environments (Wiliams and del Giorgio, 2005), and weak or insignificant dependencies between them and respiration rates are typically explained by the fact that only some of the bacteria, the so-called active fraction of bacterioplankton, are metabolically active (Sherr et al., 1999; Smith, 1998; Vaque´ et al., 2001). During general counts of bacteria, as performed in this study, both active and inactive bacteria are counted together and both fractions cannot be differentiated. 3.4. Bottom–up versus top–down control of respiration rates The type of control exerted on respiration was assessed on the basis of decreases in respiration rates during dark incubation, which permitted detecting excess resources capable of maintaining respiration rates. To do this, we compared diel oxygen consumptions (=respirations) with oxygen consumptions measured during five-day incubation. In Sopot diel oxygen consumption was 35 10% (mean and standard deviation) of the oxygen consumption measured during the five-day incubation period (12 comparisons). This indicated that respiration rates decreased during the five-day incubation period (generally one-third of overall oxygen consumption occurred during the first day of incubation and two-thirds during the remaining four days). In Ustka diel oxygen consumption was 20 10% (mean and standard deviation) of the oxygen consumption measured during the five-day incubation period (10 comparisons). The
K. Rychert et al. / Ecohydrology & Hydrobiology 15 (2015) 215–219
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Table 1 Mean annual abundances of bacteria and biomasses of protozoa at two study sites calculated on the basis of year-round studies (Rychert et al., 2013). Please note a relatively high biomass of heterotrophic flagellates in comparison to the occurrence of bacteria and other protozoa at the Ustka study site. Sopot
Group 1
Bacteria (cells l ) Heterotrophic flagellates (mgC l1) Heterotrophic ciliates (mgC l1) Heterotrophic dinoflagellates (mgC l1)
References
Ustka 9
8.16 10 9.7 20.5 13.0
statutory activities of the Pomeranian University in Słupsk (Poland), project number 11.6.14 (studies performed at the study site in Ustka, preparation of the manuscript).
9
4.55 10 20.5 13.3 4.8
mean value of this ratio observed in Ustka (20%) meant that the respiration rate was typically stable over a five-day incubation period indicating excess resources that were not utilized at this station. The diel to five-day oxygen consumption ratios at both study sites were significantly different (t-test for independent samples, p = 0.004). Dark incubation leads to decline in organic matter production by primary producers (Nagata, 2000), therefore it was not definitely demonstrated that respiration rates at Sopot study site were bottom–up controlled. However, the excess of resources detected at Ustka study site demonstrated that respiration rates at this site were prevailingly top–down controlled. In conclusion, organic matter from the Ustka study site can be exported toward offshore waters. Separate study on protozoan communities at both study sites (Rychert et al., 2013) also suggests that at the Ustka study site picoplankton, which accounts for the bulk of respiration (e.g., Wiliams and del Giorgio, 2005), is top–down controlled. Heterotrophic nanoflagellates, that are the main grazers of picoplankton (Azam et al., 1983; Sherr and Sherr, 2002), reached there a relatively high biomass in comparison to the occurrence of bacteria and other protozoa (Table 1). It was most probably the result of strong, wind-induced benthic resuspension, because water was sampled closer to the shore than in Sopot (Rychert and Wielgat-Rychert, 2008; Rychert et al., 2013). A similar situation, that is, relatively high flagellate abundance, was observed by Garstecki et al. (2000) at a sampling site in Kirrbucht (the southern Baltic Sea). Conflict of interest None declared. Financial disclosure None. Ethical statement Authors state that the research was conducted according to ethical standards. Acknowledgments The study was supported by the Polish Ministry of Science and Higher Education – grant No. 2 P04F 074 27 (studies performed at the study site in Sopot) and as
Andersson, A., Samuelsson, K., Haecky, P., Albertsson, J., 2006. Changes in the pelagic microbial food web due to artificial eutrophication. Aquat. Ecol. 40, 299–313. Azam, F., Fenchel, T., Field, J.D., Gray, J.S., Meyer-Reil, L.A., Thingstad, F., 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263. Cederwall, H., Elmgren, R., 1990. Biological effects of eutrophication in the Baltic Sea, particularly the coastal zone. Ambio 19, 109–112. Chen, C.C., Shiah, F.K., Gong, G.C., Chiang, K.P., 2003. Planktonic community respiration in the East China Sea: importance of microbial consumption of organic carbon. Deep Sea Res. II 50, 1311–1325. Elmgren, R., 1989. Man’s impact on the ecosystem of the Baltic Sea: energy flows today and at the turn of the century. Ambio 18, 326–332. Fourqurean, J.W., Webb, K.L., Hollibaugh, J.T., Smith, S.V., 1997. Contributions of the plankton community to ecosystem respiration, Tomales Bay, California. Estuar. Coast. Shelf Sci. 44, 493–505. Funkey, C.P., Conley, D.J., Reuss, N.S., Humborg, C., Jilbert, T., Slomp, C.P., 2014. Hypoxia sustains cyanobacteria blooms in the Baltic Sea. Environ. Sci. Technol. 48, 2598–2602. Garstecki, T., Verhoeven, R., Wickham, S.A., Arndt, H., 2000. Benthicpelagic coupling: a comparison of the community structure of benthic and planktonic heterotrophic protists in shallow inlets of the southern Baltic. Fresh. Biol. 45, 147–167. Gonza´lez, N., Anado´n, R., Viesca, L., 2003. Carbon flux through the microbial community in a temperate sea during summer: role of bacterial metabolism. Aquat. Microb. Ecol. 33, 117–126. Gustafsson, B.G., Schenk, F., Blenckner, T., Eilola, K., Meier, H.E.M., Mu¨llerKarulis, B., Neumann, T., Ruoho-Airola, T., Savchuk, O.P., Zorita, E., 2012. Reconstructing the development of Baltic Sea Eutrophication 1850–2006. Ambio 41, 534–548. Hansson, S., Rudstam, L.G., 1990. Eutrophication and Baltic fish communities. Ambio 19, 123–125. HELCOM, 2014. Eutrophication status of the Baltic Sea 2007–2011 – a concise thematic assessment. In: Baltic Sea Environment Proceedings 143. Helsinki Commission, Helsinki. Hobbie, J.E., Daley, R.J., Jasper, S., 1977. Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33, 1225–1228. Holtappels, M., Tiano, L., Kalvelage, T., Lavik, G., Revsbech, N.P., Kuypers, M.M.M., 2014. Aquatic respiration rate measurements at low oxygen concentrations. PLoS ONE 9 (2), e89369. Jahnke, R.A., Craven, D.B., 1995. Quantifying the role of heterotrophic bacteria in the carbon cycle: a need for respiration rate measurements. Limnol. Oceanogr. 40, 436–441. Jansson, B.-O., Dahlberg, K., 1999. The environmental status of the Baltic sea in the 1940, today and in the future. Ambio 28, 312–319. Kuparinen, J., 1987. Production and respiration of overall plankton and ultraplankton communities at the entrance to the Gulf of Finland in the Baltic Sea. Mar. Biol. 93, 591–607. Larsson, U., Elmgren, R., Wulff, F., 1985. Eutrophication and the Baltic Sea: causes and consequences. Ambio 14, 9–14. Łysiak-Pastuszak, E., Drgas, N., Pia˛tkowska, Z., 2004. Eutrophication in the Polish coastal zone: the past, present status and future scenarios. Mar. Pollut. Bull. 49, 186–195. Mattha¨us, W., Nehring, D., Feistel, R., Nausch, G., Mohrholz, V., Lass, H.-U., 2008. The inflow of highly saline water in the Baltic Sea. In: Feistel, R., Nausch, G., Wasmund, N. (Eds.), State and Evolution of the Baltic Sea. Wiley & Sons, Hoboken, pp. 265–309. Nagata, T., 2000. Production mechanisms of dissolved organic matter. In: Kirchman, D.L. (Ed.), Microbial Ecology of the Oceans. Wiley-Liss, New York, pp. 121–152. Piwosz, K., Pernthaler, J., 2010. Seasonal population dynamics and trophic role of planktonic nanoflagellates in coastal surface waters of the Southern Baltic Sea. Environ. Microbiol. 12, 364–377. Robinson, C., Serret, P., Tilstone, G., Teira, E., Zubkov, M.V., Rees, A.P., Woodward, E.M.S., 2002. Plankton respiration in the Eastern Atlantic Ocean. Deep Sea Res. I 49, 787–813. Robinson, C., Williams, P.J.B., 2005. Respiration and its measurement in the surface waters. In: del Giorgio, P.A., Williams, P.J.B. (Eds.), Respiration in Aquatic Ecosystems. Oxford University Press, New York, pp. 147–180.
K. Rychert et al. / Ecohydrology & Hydrobiology 15 (2015) 215–219 Rosenberg, R., Elmgren, R., Fleischer, S., Jonsson, P., Persson, G., Dahlin, H., 1990. Marine eutrophication case studies in Sweden. Ambio 19, 102–108. Rychert, K., Spich, K., Laskus, K., Pa˛czkowska, M., Wielgat-Rychert, M., Sojda, G., 2013. Composition of protozoan communities at two sites in the coastal zone of the southern Baltic Sea. Oceanol. Hydrobiol. Stud. 42, 268–276. Rychert, K., Wielgat-Rychert, M., 2008. Biodegradable organic matter in the coastal waters of Central Pomerania (Ustka) and the Gulf of Gdan´sk (Sopot). In: Bajkiewicz-Grabowska, E., Borowiak, D. (Eds.), Anthropogenic and Natural Transformations of Lakes, 2. KLUG-PTLim, Gdan´sk, pp. 179–182. Sampou, P., Kemp, W.M., 1994. Factors regulating plankton community respiration in Chesapeake Bay. Mar. Ecol. Prog. Ser. 110, 249–258. Sherr, B.F., del Giorgio, P.A., Sherr, E.B., 1999. Estimating the abundance and single-cell characteristics of respiring bacteria via redox dye CTC. Aquat. Microb. Ecol. 18, 117–131. Sherr, E.B., Sherr, B.F., 2002. Significance of predation by protists in aquatic microbial food webs. Antonie Leeuwenhoek 81, 293–308. Smith, E.M., 1998. Coherence of microbial respiration rate and cellspecific bacterial activity in a coastal planktonic community. Aquat. Microb. Ecol. 16, 27–35. ¨ dalen, M., Hall, P.O.J., Liljebladh, Stigebrandt, A., Rahm, L., Viktorsson, L., O B., 2014. A new phosphorus paradigm for the Baltic Proper. Ambio 43, 634–643.
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Vaque´, D., Casamayor, E.O., Gasol, J.M., 2001. Dynamics of whole community bacterial production and grazing losses in seawater incubations as related to the changes in the proportions of bacteria with different DNA content. Aquat. Microb. Ecol. 25, 163–177. Wasmund, N., Go¨bel, J., von Bodungen, B., 2008. 100-years-changes in the phytoplankton community of Kiel Bight (Baltic Sea). J. Mar. Syst. 73, 300–322. Wiliams, P.J.B., del Giorgio, P.A., 2005. Respiration in aquatic ecosystems: history and background. In: del Giorgio, P.A., Williams, P.J.B. (Eds.), Respiration in Aquatic Environments. Oxford University Press, New York, pp. 1–17. Witek, Z., Drgas, A., Ameryk, A., Ochocki, S., 2001. Production and mineralization of organic matter in the Pomeranian Bay. Bull. Sea Fish. Inst. 3, 49–69. Witek, Z., Ochocki, S., Nakonieczny, J., Podgo´rska, B., Drgas, A., 1999. Primary production and decomposition of organic matter in the epipelagic zone of the Gulf of Gdan´sk, an estuary of the Vistula. ICES J. Mar. Sci. 56 (Suppl.), 3–14. Wulff, F., Stigebrandt, A., Rahm, L., 1990. Nutrient dynamics of the Baltic Sea. Ambio 19, 126–133. York, J.K., Witek, Z., Labudda, S., Ochocki, S., 2001. Comparison of primary production and pelagic community respiration rates in the coastal zone of the Gulf of Gdan´sk. Oceanologia 43, 365–370.
Contents lists available at ScienceDirect
Ecohydrology & Hydrobiology journal homepage: www.elsevier.com/locate/ecohyd
Short Communication
Pelagic respiration in the coastal zone of the southern Baltic Sea Krzysztof Rychert *, Magdalena Wielgat-Rychert, Marta Wołoszynek, Gracjan Sojda Department of Ecology, Pomeranian University in Słupsk, ul. Arciszewskiego 22b, 76-200 Słupsk, Poland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 December 2014 Accepted 3 June 2015 Available online 17 June 2015
Respiration measurements were carried out year round at two stations located in the coastal zone of the southern Baltic Sea. Study sites differed with their characteristics: first one was located in the coastal zone of the Gulf of Gdan´sk near the town of Sopot (548270 N, 188350 E), second one was located in the coastal waters of the southern Baltic Sea near the town of Ustka (548350 N, 168500 E). The study reports a range of respiration rates and mean annual values, which are useful for development and parameterization of biogeochemical models. Respiration was estimated as the decrease in oxygen concentration in water confined in glass bottles. The mean annual respiration rate was 0.37 mgO2 l1 d1 at the study site in Sopot and 0.18 mgO2 l1 d1 at the study site in Ustka. In Ustka, respiration rates depended on temperature (R2 = 0.77, p = 0.0008), whereas in Sopot there was no such statistically significant dependence. At both study sites, there was no significant relationship between respiration rates and bacterial abundance. Diel oxygen consumption was compared with that measured during prolonged, five-day incubation period to detect excess resources capable of maintaining respiration rates. In Sopot respiration rates decreased during the five-day incubation period, whereas at study site in Ustka, they were generally stable during such incubation, what suggested that utilization of excess resources was prevented by top–down control of grazers. ß 2015 European Regional Centre for Ecohydrology of the Polish Academy of Sciences. Published by Elsevier Sp. z o.o. All rights reserved.
Keywords: Oxygen consumption Temperature Bacteria Organic matter Grazers
1. Introduction Ecosystem metabolism comprises two main processes: primary production and organic matter degradation. In aquatic environments, the latter is most often approximated by respiration (=oxygen consumption) and is less thoroughly studied than primary production (Holtappels et al., 2014; Jahnke and Craven, 1995; Robinson et al., 2002; Wiliams and del Giorgio, 2005). This particularly concerns the regulation of respiration rates by different
* Corresponding author. Tel.: +48 598405421. E-mail address: [email protected] (K. Rychert).
factors (Wiliams and del Giorgio, 2005). Ecosystem metabolism is often affected by eutrophication, which is defined as an increase in nutrient supply resulting in an increase in primary production. Especially sensitive to eutrophication process are semi-enclosed and relatively small water bodies, such as the Baltic Sea, that are surrounded by highly industrialized countries (Gustafsson et al., 2012; Larsson et al., 1985; Wulff et al., 1990), particularly along their coastal zones (Cederwall and Elmgren, 1990; Łysiak-Pastuszak et al., 2004; Rosenberg et al., 1990). The eutrophication of the Baltic has resulted in increased primary production that has caused changes in the food-web structure affecting not only unicellular organisms (Wasmund et al., 2008; Piwosz and Pernthaler,
http://dx.doi.org/10.1016/j.ecohyd.2015.06.001 1642-3593/ß 2015 European Regional Centre for Ecohydrology of the Polish Academy of Sciences. Published by Elsevier Sp. z o.o. All rights reserved.
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K. Rychert et al. / Ecohydrology & Hydrobiology 15 (2015) 215–219
2010), but probably even fish species that are important to commercial fisheries (Elmgren, 1989; Hansson and Rudstam, 1990; Jansson and Dahlberg, 1999). The results of the latest studies indicate that the trophic status in most Baltic Sea areas has not been reduced despite measures implemented to reduce external inputs of nitrogen and phosphorus. More research is needed to understand the impact of eutrophication on the marine environment (Funkey et al., 2014; Gustafsson et al., 2012; HELCOM, 2014; Stigebrandt et al., 2014) and to understand paths of organic matter decomposition in the Baltic Sea ecosystem. In the present study, we observed seasonal changes in respiration rates at two study sites located in the coastal zone of the southern Baltic Sea and checked their dependence on temperature and bacterial abundance. The study sites differed in characteristics: the first site in Sopot was located in the coastal zone of the Gulf of Gdan´sk, whereas the second site in Ustka was located in the coastal zone of open waters of the southern Baltic Sea. The study reports a range of respiration rates and mean annual values. A second aim of the study was to evaluate whether respiration rates were bottom–up or top–down controlled. Bottom–up control means that respiration rates depend on the availability of biodegradable organic matter (Andersson et al., 2006; Gonza´lez et al., 2003), whereas top–down control means that standing stocks of the smallest picoplanktonic and nanoplanktonic organisms, which account for the bulk of respiration (Jahnke and Craven, 1995; Robinson and Williams, 2005), are restricted by the grazing pressure of larger organisms. The type of control decides whether organic matter is broken down at the study site or it is exported toward offshore waters. The type of control exerted on respiration was assessed based on decreases in respiration rates during extended dark incubations. We assumed that stable respiration rates during a five-day incubation period indicated excess resources, the utilization of which was prevented by the top–down control of the respiring organisms. 2. Materials and methods The studies were carried out at two study sites: in Sopot and in Ustka (Fig. 1). Measurements were carried out at the Sopot site (548270 N, 188350 E) between April 2003 and March 2004 (12 data points), and water for the experiments was taken from the end of 450-m wooden pier. Measurements at the Ustka site (548350 N, 168500 E) were conducted between October 2007 and September 2008 (10 data points). Water was collected from the end of a 70-m concrete pier. Both study sites were of comparable depth (6.0–6.5 m), and water was taken from the wellmixed part of the water column. Respiration measurements were always accompanied by water temperature and salinity measurements and also counts of bacterial abundance. At the Sopot site water temperature and salinity was measured with portable STD probe (Sensordata). At the Ustka site water temperature was measured with mercurial thermometer and water salinity with portable salinometer (Elmetron). At both study sites, bacterial counts were performed under an epifluorescence microscope after staining with acridine orange (Hobbie et al., 1977).
Fig. 1. Location of two study sites in the coastal zone of the southern Baltic Sea.
Respiration was estimated as the decrease in oxygen concentration in water confined in glass bottles, i.e., the difference between oxygen concentration before and after dark incubation at in situ temperatures. Before each experiment, the equipment was acid-washed and rinsed with deionized water. The water, taken from study sites, was siphoned through a gas-tight tubing into Winkler flasks (about 120 ml) to measure the initial oxygen concentrations, and into four 1000-ml-bottles (Sopot) or eight Winkler flasks (Ustka), in which the water was incubated for 24 h (two 1000-ml-bottles in Sopot and three Winkler flasks in Ustka) and five days (two 1000-mlbottles in Sopot and five Winkler flasks in Ustka). As mentioned above, all incubations were carried out in the dark and at in situ temperatures. After incubations, the final oxygen concentrations were measured. In Sopot, prior to measurements of oxygen concentration, water from each 1000-ml-bottle was siphoned through a gas-tight tubing into three Winkler flasks. All oxygen measurements were carried out with the Winkler method using piston titrators: Metrohm Titrino 702SM for Sopot and Schott Titroline Basic for Ustka. Metrohm Titrino was combined with potentiometric electrode (Metrohm Pt Titrode), which allows automatic detection of the end-point of titration. In Ustka, where Shott Titroline titrator was used, end-point was detected with a standard starch indicator. A single oxygen concentration measurement was the average of at least three separate titrations. The differences in oxygen concentrations were expressed in mgO2 l1 per day or five days, depending on the incubation type. 3. Results and discussion 3.1. Environmental parameters and bacterial abundance Water temperature ranged from 1 8C to 21 8C in Sopot and from 3 8C to 20 8C in Ustka (Fig. 2). Water salinity at both study sites was slightly lower than that observed in
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2001), in the coastal zone of the Gulf of Gdan´sk (up to 1.28 mgO2 l1 d1; York et al., 2001), and in offshore waters of the Gulf of Gdan´sk and close to the Vistula River mouth (up to 1.00 mgO2 l1 d1; Witek et al., 1999). Mean annual respiration rates (Sopot: 0.37 mgO2 l1 d1; Ustka: 0.18 mgO2 l1 d1) flanked mean values for coastal waters (0.24 mgO2 l1 d1; Robinson and Williams, 2005). 3.3. Factors affecting respiration rates
Fig. 2. Seasonal changes in respiration rates and temperature observed in pelagic water at both study sites.
the surface waters of the southern Baltic Sea (7.5%; Mattha¨us et al., 2008). The mean salinity in Sopot was 7.1%, and it changed during the study regularly from the lowest value recorded in April (6.4%) to the highest in February (7.4%). Mean water salinity at the Ustka study site was lower (6.7%, range: 4.6–7.7%), and it fluctuated irregularly because of the variable impact of fresh water from the mouth of the Słupia River located just 1.3 km to the east. In general, changes in environmental conditions at the Sopot study site were gentle, whereas those in Ustka changed irregularly. Bacterial abundance in Sopot ranged from low values in winter (4–5 109 cells l1) to high values observed during spring bloom (11.7 109 cells l1) and during summer (up to 17 109 cells l1). In Ustka, bacterial abundance ranged from low values during winter (about 1.5 109 cells l1) to high values in summer (5–6 109 cells l1) and in autumn (up to 8 109 cells l1). 3.2. Seasonal changes in respiration rates Respiration rates at the Sopot site ranged from 0.14 to 0.66 mgO2 l1 d1, and those in Ustka were comparable (0.00–0.64 mgO2 l1 d1, Fig. 2). The highest respiration rates in Ustka were observed during summer, whereas in Sopot two respiration rate peaks were observed: the first during the spring phytoplankton blooms (for details see Rychert et al., 2013) and the second during summer. Similar respiration rate ranges but with higher maximal values were observed in the southern Baltic Sea before: in the Pomeranian Bay (up to 0.81 mgO2 l1 d1; Witek et al.,
The highest respiration rates at the Ustka study site were observed during summer, and respiration depended on temperature (R2 = 0.77, p = 0.0008). There was no distinct spring bloom (see also Rychert et al., 2013). In Sopot, the highest respiration rates were observed during spring phytoplankton blooms when the temperature was lower than in summer (Fig. 2). Consequently, the relationship between temperature and respiration rates at the Sopot site was insignificant. A statistically significant but moderate relationship between temperature and respiration rates was also observed in marine waters by Fourqurean et al. (1997), Sampou and Kemp (1994), and Witek et al. (1999). High respiration rates during spring blooms, as noted at the Sopot study site, were also reported by Kuparinen (1987) in the Gulf of Finland (northern Baltic Sea). According to the literature, the dependence between bacterial abundance and community respiration is typically weak or even insignificant (e.g., Chen et al., 2003; Fourqurean et al., 1997; but see Robinson et al., 2002). In this study, correlations between bacterial abundances and respiration rates were insignificant at both stations studied. Bacteria are the main oxygen consumers in aquatic environments (Wiliams and del Giorgio, 2005), and weak or insignificant dependencies between them and respiration rates are typically explained by the fact that only some of the bacteria, the so-called active fraction of bacterioplankton, are metabolically active (Sherr et al., 1999; Smith, 1998; Vaque´ et al., 2001). During general counts of bacteria, as performed in this study, both active and inactive bacteria are counted together and both fractions cannot be differentiated. 3.4. Bottom–up versus top–down control of respiration rates The type of control exerted on respiration was assessed on the basis of decreases in respiration rates during dark incubation, which permitted detecting excess resources capable of maintaining respiration rates. To do this, we compared diel oxygen consumptions (=respirations) with oxygen consumptions measured during five-day incubation. In Sopot diel oxygen consumption was 35 10% (mean and standard deviation) of the oxygen consumption measured during the five-day incubation period (12 comparisons). This indicated that respiration rates decreased during the five-day incubation period (generally one-third of overall oxygen consumption occurred during the first day of incubation and two-thirds during the remaining four days). In Ustka diel oxygen consumption was 20 10% (mean and standard deviation) of the oxygen consumption measured during the five-day incubation period (10 comparisons). The
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Table 1 Mean annual abundances of bacteria and biomasses of protozoa at two study sites calculated on the basis of year-round studies (Rychert et al., 2013). Please note a relatively high biomass of heterotrophic flagellates in comparison to the occurrence of bacteria and other protozoa at the Ustka study site. Sopot
Group 1
Bacteria (cells l ) Heterotrophic flagellates (mgC l1) Heterotrophic ciliates (mgC l1) Heterotrophic dinoflagellates (mgC l1)
References
Ustka 9
8.16 10 9.7 20.5 13.0
statutory activities of the Pomeranian University in Słupsk (Poland), project number 11.6.14 (studies performed at the study site in Ustka, preparation of the manuscript).
9
4.55 10 20.5 13.3 4.8
mean value of this ratio observed in Ustka (20%) meant that the respiration rate was typically stable over a five-day incubation period indicating excess resources that were not utilized at this station. The diel to five-day oxygen consumption ratios at both study sites were significantly different (t-test for independent samples, p = 0.004). Dark incubation leads to decline in organic matter production by primary producers (Nagata, 2000), therefore it was not definitely demonstrated that respiration rates at Sopot study site were bottom–up controlled. However, the excess of resources detected at Ustka study site demonstrated that respiration rates at this site were prevailingly top–down controlled. In conclusion, organic matter from the Ustka study site can be exported toward offshore waters. Separate study on protozoan communities at both study sites (Rychert et al., 2013) also suggests that at the Ustka study site picoplankton, which accounts for the bulk of respiration (e.g., Wiliams and del Giorgio, 2005), is top–down controlled. Heterotrophic nanoflagellates, that are the main grazers of picoplankton (Azam et al., 1983; Sherr and Sherr, 2002), reached there a relatively high biomass in comparison to the occurrence of bacteria and other protozoa (Table 1). It was most probably the result of strong, wind-induced benthic resuspension, because water was sampled closer to the shore than in Sopot (Rychert and Wielgat-Rychert, 2008; Rychert et al., 2013). A similar situation, that is, relatively high flagellate abundance, was observed by Garstecki et al. (2000) at a sampling site in Kirrbucht (the southern Baltic Sea). Conflict of interest None declared. Financial disclosure None. Ethical statement Authors state that the research was conducted according to ethical standards. Acknowledgments The study was supported by the Polish Ministry of Science and Higher Education – grant No. 2 P04F 074 27 (studies performed at the study site in Sopot) and as
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