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Trophic complexity of zooplankton–cyanobacteria interactions in the Baltic Sea: Insights from molecular diet analysis
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.ORCID iD: 0000-0002-4587-8541
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Blooms of nitrogen fixing cyanobacteria (NFC) occur in many freshwater and marine systems, including the Baltic Sea. By fixing dissolved nitrogen, they circumvent general summer nitrogen limitation, while also generating a supply of novel bioavailable nitrogen for non-diazotrophic primary producers and ultimately supporting secondary production. Elucidating trophic links between primary consumers and NFC is essential for understanding role of these blooms for secondary production. However, until recently, there was no reliable method to quantify individual prey species for zooplankter feeding in situ. The development of PCR-based methods to detect prey-specific DNA in the diet of consumers, including microscopic animals, allows identification and quantification of trophic linkages in the field.

Using molecular diet analysis in combination with egg production measurements, biochemical markers of growth and condition; and stable isotope approach, we explored a possibility to determine (1) whether cyanobacteria are grazed and assimilated by mesozooplankters (Papers I and II), (2) which species/groups are particularly efficient consumers of cyanobacteria (Papers II and III), and (3) how feeding on cyanobacteria affects zooplankton growth and development (Paper I and III). Taken together, these laboratory and field observations, provided evidence that NFC contribute to feeding and reproduction of zooplankton during summer and create a favorable growth environment for the copepod nauplii (Paper I). The favorable growth conditions for juvenile copepods observed during NFC blooms were hypothesized to be mediated by picoplankton that take up bioavailable nitrogen exuded from cyanobacterial cells. This hypothesis found support in Paper II that provided quantitative estimates for the direct picocyanobacteria → mesozooplankton pathway, with highest weight-specific consumption observed in nauplii. Further, using field observations on zooplankton and phytoplankton development during a growth season in the northern Baltic proper, we found that NFC nitrogen is assimilated and transferred to zooplankton via both direct grazing and indirectly through grazing on small-sized phyto- and bacterioplankton (Paper III). Finally, these and other findings emphasizing the importance of NFC for Baltic Sea secondary production during growth season were synthesized to show that diazotrophic nitrogen enters food webs already at bloom initiation (Paper III) and is transferred via multiple pathways to pelagic and benthic food webs and, ultimately, to fish (Paper IV).

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2015. , 42 p.
Keyword [en]
bloom-forming filamentous cyanobacteria, diazotrophs, picocyanobacteria, zooplankton, grazing, molecular diet analysis, stable isotopes, biochemical indices
National Category
Biological Sciences Ecology
Research subject
Marine Ecology
Identifiers
URN: urn:nbn:se:su:diva-116219ISBN: 978-91-7649-118-8 (print)OAI: oai:DiVA.org:su-116219DiVA: diva2:805207
Public defence
2015-05-22, Stora föreläsningssalen, Institutionen för ekologi, miljö och botanik, Lilla Frescativägen 5, Stockholm, 13:00 (English)
Opponent
Supervisors
Funder
Baltic Ecosystem Adaptive Management (BEAM)Swedish Research Council Formas
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Accepted.

Available from: 2015-04-28 Created: 2015-04-14 Last updated: 2015-10-26Bibliographically approved
List of papers
1. Bloom-Forming Cyanobacteria Support Copepod Reproduction and Development in the Baltic Sea
Open this publication in new window or tab >>Bloom-Forming Cyanobacteria Support Copepod Reproduction and Development in the Baltic Sea
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2014 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 11, e112692Article in journal (Refereed) Published
Abstract [en]

It is commonly accepted that summer cyanobacterial blooms cannot be efficiently utilized by grazers due to low nutritional quality and production of toxins; however the evidence for such effects in situ is often contradictory. Using field and experimental observations on Baltic copepods and bloom-forming diazotrophic filamentous cyanobacteria, we show that cyanobacteria may in fact support zooplankton production during summer. To highlight this side of zooplankton-cyanobacteria interactions, we conducted: (1) a field survey investigating linkages between cyanobacteria, reproduction and growth indices in the copepod Acartia tonsa; (2) an experiment testing relationships between ingestion of the cyanobacterium Nodularia spumigena (measured by molecular diet analysis) and organismal responses (oxidative balance, reproduction and development) in the copepod A. bifilosa; and (3) an analysis of long term (1999-2009) data testing relationships between cyanobacteria and growth indices in nauplii of the copepods, Acartia spp. and Eurytemora affinis, in a coastal area of the northern Baltic proper. In the field survey, N. spumigena had positive effects on copepod egg production and egg viability, effectively increasing their viable egg production. By contrast, Aphanizomenon sp. showed a negative relationship with egg viability yet no significant effect on the viable egg production. In the experiment, ingestion of N. spumigena mixed with green algae Brachiomonas submarina had significant positive effects on copepod oxidative balance, egg viability and development of early nauplial stages, whereas egg production was negatively affected. Finally, the long term data analysis identified cyanobacteria as a significant positive predictor for the nauplial growth in Acartia spp. and E. affinis. Taken together, these results suggest that bloom forming diazotrophic cyanobacteria contribute to feeding and reproduction of zooplankton during summer and create a favorable growth environment for the copepod nauplii.

National Category
Biological Sciences Earth and Related Environmental Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-111918 (URN)10.1371/journal.pone.0112692 (DOI)000345533200032 ()
Note

AuthorCount:9;

Available from: 2015-01-09 Created: 2015-01-08 Last updated: 2017-12-05Bibliographically approved
2. Mesozooplankton Grazing on Picocyanobacteria in the Baltic Sea as Inferred from Molecular Diet Analysis
Open this publication in new window or tab >>Mesozooplankton Grazing on Picocyanobacteria in the Baltic Sea as Inferred from Molecular Diet Analysis
2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 11, e79230Article in journal (Refereed) Published
Abstract [en]

Our current knowledge on the microbial component of zooplankton diet is limited, and it is generally assumed that bacteria-sized prey is not directly consumed by most mesozooplankton grazers in the marine food webs. We questioned this assumption and conducted field and laboratory studies to examine picocyanobacteria contribution to the diets of Baltic Sea zooplankton, including copepods. First, qPCR targeting ITS-1 rDNA sequence of the picocyanobacteria Synechococcus spp. was used to examine picocyanobacterial DNA occurrence in the guts of Baltic zooplankton (copepods, cladocerans and rotifers). All field-collected zooplankton were found to consume picocyanobacteria in substantial quantities. In terms of Synechococcus quantity, the individual gut content was highest in cladocerans, whereas biomass-specific gut content was highest in rotifers and copepod nauplii. Moreover, the gut content in copepods was positively related to the picocyanobacteria abundance and negatively to the total phytoplankton abundance in the water column at the time of sampling. This indicates that increased availability of picocyanobacteria resulted in the increased intake of this prey and that copepods may rely more on picoplankton when food in the preferred size range declines. Second, a feeding experiments with a laboratory reared copepod Acartia tonsa fed a mixture of the picocyanobacterium Synechococcus bacillaris and microalga Rhodomonas salina confirmed that copepods ingested Synechococcus, even when the alternative food was plentiful. Finally, palatability of the picocyanobacteria for A. tonsa was demonstrated using uptake of C-13 by the copepods as a proxy for carbon uptake in feeding experiment with C-13-labeled S. bacillaris. These findings suggest that, if abundant, picoplankton may become an important component of mesozooplankton diet, which needs to be accounted for in food web models and productivity assessments.

National Category
Biological Sciences Environmental Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-98306 (URN)10.1371/journal.pone.0079230 (DOI)000327308500038 ()
Note

AuthorCount:2;

Available from: 2014-01-07 Created: 2014-01-03 Last updated: 2017-12-06Bibliographically approved
3. Grazing on nitrogen-fixing filamentous cyanobacteria and transfer of diazotrophic nitrogen to zooplankton grazers in the open Baltic Sea
Open this publication in new window or tab >>Grazing on nitrogen-fixing filamentous cyanobacteria and transfer of diazotrophic nitrogen to zooplankton grazers in the open Baltic Sea
(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-116220 (URN)
External cooperation:
Available from: 2015-04-14 Created: 2015-04-14 Last updated: 2016-08-30Bibliographically approved
4. Nitrogen fixation by cyanobacteria stimulates production in Baltic food webs
Open this publication in new window or tab >>Nitrogen fixation by cyanobacteria stimulates production in Baltic food webs
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2015 (English)In: Ambio, ISSN 0044-7447, E-ISSN 1654-7209, Vol. 44, 413-426 p.Article in journal (Refereed) Published
Abstract [en]

Filamentous, nitrogen-fixing cyanobacteria form extensive summer blooms in the Baltic Sea. Their ability to fix dissolved N-2 allows cyanobacteria to circumvent the general summer nitrogen limitation, while also generating a supply of novel bioavailable nitrogen for the food web. However, the fate of the nitrogen fixed by cyanobacteria remains unresolved, as does its importance for secondary production in the Baltic Sea. Here, we synthesize recent experimental and field studies providing strong empirical evidence that cyanobacterial nitrogen is efficiently assimilated and transferred in Baltic food webs via two major pathways: directly by grazing on fresh or decaying cyanobacteria and indirectly through the uptake by other phytoplankton and microbes of bioavailable nitrogen exuded from cyanobacterial cells. This information is an essential step toward guiding nutrient management to minimize noxious blooms without overly reducing secondary production, and ultimately most probably fish production in the Baltic Sea.

Keyword
Diazotrophic cyanobacteria, Food webs, Zooplankton grazing, Secondary production, Fish
National Category
Environmental Engineering Earth and Related Environmental Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-122130 (URN)10.1007/s13280-015-0660-x (DOI)000362290800009 ()
Available from: 2015-10-26 Created: 2015-10-26 Last updated: 2017-12-01Bibliographically approved

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