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Response of a Microbial Food Web to Prolonged Seasonal Hypoxia in a Boreal Lake

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Response of a Microbial Food Web to Prolonged Seasonal Hypoxia in a Boreal Lake Vol. 14: 105–120, 2012 AQUATIC BIOLOGY Published online January 4 doi: 10.3354/ab00379 Aquat Biol OPEN ACCESS FEATURE ARTICLE Response of a microbial food web to prolonged seasonal hypoxia in a boreal lake Grazyna· Bre˛ k-Laitinen*, Jessica López Bellido, Anne Ojala Department of Environmental Sciences, University of Helsinki, 15140 Lahti, Finland ABSTRACT: The clearwater boreal Lake Vesijärvi ex- periences annual periods of hypolimnetic hypoxia with unknown consequences for the microbial food web. We quantified the abundance of heterotrophic bacteria, autotrophic picoplankton (APP), nanoflagel- lates (NF) and ciliates in Lake Vesijärvi throughout the water column and vegetation season and deter- mined how these varied with changes in environ - mental conditions, including dissolved oxygen con- centrations. The abundance and diversity of ciliates increased significantly throughout the water column with the development of thermal stratification and the onset of hypoxia leading to distinct ciliate communi- ties in the oxic epilimnion and hypoxic hypolimnion. Hypoxia strongly influences the microbial community of Bacterivorous taxa dominated in the hypoxic zone, Lake Vesijärvi, Finland. Inset: epifluorescence micrograph while in the epilimnion, bacterivorous, algivorous and of APP cells (red), and DAPI signals of DNA containing cells predatory taxa feeding on other protozoa were pre- (blue); scale bar = 10 μm. sent. Seasonal changes in oxygen and temperature Photos: G. Bre˛ k-Laitinen explained nearly 80% of variance in ciliate community composition. Changes in total ciliate numbers corre- lated with seasonal dynamics of bacteria, but not with the dynamics of NF. In the epilimnion, NF were abun- dant in early spring and their numbers were positively INTRODUCTION correlated to numbers of prostomatids and haptorids, but not to APP or bacteria. In the hypolimnion, a sig- Low oxygen content in the hypolimnion has be - nificant correlation was found between NF and bacte- come a widespread phenomenon in lacustrine as ria, but not NF and ciliates. Significant positive corre- well as marine ecosystems worldwide (Diaz 2001). lations between ciliates and bacteria suggest that Hypoxia, defined as dissolved oxygen concentrations concentrations of food resources are important in de- <2 mg l−1, typically arises from water column stra - termining the abundance of ciliates in the plankton. tification, biological processes and nutrient inputs Moreover, we recorded close coupling between sea- (Rabalais et al. 2007). While <4 mg O l−1 is consid- sonal dynamics of bacteria and productivity of phyto- 2 ered stressful for fish, concentrations <2 mg O l−1 are plankton, including APP. 2 stressful for most organisms. Specifically, low oxygen KEY WORDS: Autotrophic picoplankton · Bacteria · concentration is a stressor of benthic communities Nanoflagellates · Ciliates · Anoxia · Hypoxia and can cause major alterations in energy flow (Diaz & Rosenberg 2008). However, although the effects of Resale or republication not permitted without written consent of the publisher hypoxia and anoxia on the benthos are quite well *Email: [email protected] © Inter-Research 2012 · www.int-res.com 106 Aquat Biol 14: 105–120, 2012 known, the consequences for microorganisms and respond to oxygen in accordance with the needs of ecosystem functioning further up in the water col- their endo- or ectosymbiotic organisms. Many aero- umn are poorly defined (Eby et al. 2005). bic ciliates harbour oxygenic algal symbionts, which Total anoxia also initiates major changes in the bio- allow them to thrive even in very low oxygen concen- geochemistry of lakes (Finlay et al. 1997). Some trations (Finlay & Esteban 1998). While ciliate com- energy is processed by benthic animals under persis- munities in the epilimnion display various feeding tent hypoxia and anoxia, but organic matter is mostly modes attributed to the vast array of food choices, processed through microbes (Diaz & Rosenberg in the hypoxic zone, herbivory is disrupted and bac- 2008). A series of electron acceptors other than oxy- terivory dominates (Gobler et al. 2008). gen are used by functional microbial groups, i.e. Here we present the distribution patterns and nitrate reduction is followed by reduction of man- seasonal trends of key components of the microbial ganese, iron and sulphate, and finally methanogene- food web in relation to hypoxia and anoxia in a meso- sis takes over, resulting in fluxes of methane (Finlay eutrophic, anthropogenically affected clearwater lake et al. 1997). Methanogenic Archaea become domi- in southern Finland. Due to the lake morphometry nant decomposers in anoxic freshwaters with ele- and eutrophication, the hypolimnion in one of the vated hypolimnetic temperatures (Glissmann et al. major basins regularly experiences an extended, per- 2004). Enhanced epilimnetic primary production, a sistent period of hypoxia in summer, when the lake is result of internal loading through the release of phos- stratified (Kairesalo & Vakkilainen 2004). The impli- phorous contained in lake sediment, leads to an cations of this phenomenon are numerous, including accumulation of particulate organic matter, which an impact on fishery yields and recruitment. Previous further encourages microbial activity. In low oxygen investigations of the lake have focused on the chemi- conditions, zooplankton grazing is suspended and cal and physical environment, larger phytoplankton, protozoa such as nanoflagellates (NF) and ciliates zooplankton and fish stocks in relation to biomanipu- appear as the main grazers (Marcus 2001). lation (Horppila et al. 1996). To date no studies have NF and ciliates are key components of the so-called been conducted on the microbial and protozoan com- microbial loop, which is a crucial part of pelagic food munity in this lake and, in general, the knowledge of webs (Azam et al. 1983). Autotrophic picoplankton microbial food webs in non-humic boreal lakes is (APP; size <2.0 μm) is an important source of organic fragmentary. We particularly intended to gain insight carbon for other microorganisms, hence the concept into the dynamic nature of the ciliate community in of a microbial food web instead of a microbial loop relation to the development of seasonal hypoxia. We (Sherr & Sherr 2000). NF, which have high growth expected to find clear spatial patterns in community efficiencies, may effectively control communities of composition, which in turn affect abundance of other APP in the euphotic zone as well as heterotrophic components of the microbial food web, namely APP, picoplankton (i.e. bacteria) and their abundance is bacteria and NF. Based on previous grazing experi- usually 1 to 2 orders of magnitude higher than that of ments (Bre˛ k-Laitinen & Ojala 2011), we hypothesised ciliates (Šimek et al. 1997). NF reside in the water that, among microconsumers, NF are significantly column throughout the oxygen gradient (Gobler et coupled with picoplankton throughout the water col- al. 2008) and their grazing efficiency is more affected umn and growing season, whereas the ciliate com- by temperature than by decreases in oxygen concen- munity with dynamic vertical patterns imposes a tem- trations (Park & Cho 2002). Ciliates are more sensi- porary pressure only on certain components of the tive to changes in oxygen and show dramatic re - microbial food web. As the development of hypoxia sponses in community composition (Finlay & Esteban may decrease the number of habitat niches and food 1998), with their abundance and growth rates often diversity in anoxic parts of the water column (Guhl et declining in the hypoxic zone (Guhl et al. 1994). The al. 1994), we also expected to find a lower diversity of oxygen gradient separates ciliate taxonomic compo- ciliated protozoa during thermal stratification. sition and creates a characteristic spatial organisa- tion with vertical distribution patterns. Epilimnetic aerobic ciliates do not cross the oxycline, while micro- MATERIALS AND METHODS aerophiles, due to a narrow preference range for oxy- gen pressure, are found mainly around the oxycline, Study site where they form clear bands (Fenchel & Finlay 2008). Anaerobic ciliates are intolerant to oxygen and stay Lake Vesijärvi is a large glacial drift lake in the in the hypolimnion, below the oxycline. Some ciliates Kymijoki River basin in southern Finland, with a Bre˛ k-Laitinen et al.: Microbial food web in a hypoxic lake 107 length of 25 km, a total area of 111 km2 and a catch- were transferred to 150 ml dark glass bottles and ment to lake-surface ratio of approximately 4.6. In fixed immediately with acid Lugol’s iodine solution to contrast to most lakes in Finland, which have brown a final concentration of 1% (Throndsen 1978). Sam- water, Lake Vesijärvi is a clearwater lake with a ples for APP were taken with the same tube sampler, colour value of 30 mg Pt l−1 (Kansanen et al. 1991). starting from the surface down to a depth of 15 m at The epilimnetic dissolved organic (DOC) and inor- 1 m intervals and collected with the same type of bot- ganic (DIC) carbon concentrations during the grow- tles as described in the previous sentence. Unpre- ing season both average 7.3 mg C l−1, without sea- served APP samples were placed in crushed ice and sonal patterns or depth profiles. The low colour value counted within 2 h. Before summer stratification, the in contrast to high DOC concentration indicates that APP samples were taken only from a depth of 0 to autochthonous colourless DOC is abundant in Lake 6 m, which
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