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The role of terrestrial and phytoplankton-derived organic matter in planktonic food webs
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Lakes are important global ecosystems and many of them are nutrient-poor (unproductive). Especially in northern boreal latitudes, lakes may be heavily subsidized by terrestrial organic material (t-OM) from peat layers in the catchment. Thus, in addition to heterotrophic bacteria and phytoplankton, zooplankton may also use the particulate fraction of peat layer t-OM (t-POM) as a potential food source in those systems. Inputs of t-OM in northern latitudes are anticipated to increase in the future due to increasing precipitation and temperature. As t-OM is a good substrate for bacterial growth and as bacteria can often outcompete phytoplankton for inorganic nutrients, the proportions of heterotrophic bacteria and phytoplankton are expected to change in unproductive lakes. This may have pronounced impacts on zooplankton population dynamics.

The aim of my thesis was to investigate how changes in food quality and quantity will affect metazoan zooplankton performance in unproductive lakes. Three laboratory studies assessed the quality of specific food components (phytoplankton, bacteria and peat layer t-POM) and their effects on Daphnia survival, growth and reproduction. Further, a mesocosm study with a full natural plankton community tested the predictions of the Light:Nutrient-Hypothesis in an unproductive clear water lake in situ by adding carbon and inorganic nutrients and changing light availability.

I found that pure bacterial (Pseudomonas sp.) or t-POM diets could not sustain Daphnia populations, even though both were readily ingested. Daphnids needed at least 10-20% phytoplankton (Rhodomonas) in the diet to survive and even higher proportions (≥ 50%) were necessary for the production of viable offspring. Further, I showed that the dilution of non-limiting concentrations of Rhodomonas with increasing proportions of Pseudomonas or t-POM led to decreased Daphnia performance. Both Pseudomonas and t-POM lack essential biochemicals (fatty acids and sterols). In contrast, mineral nutrient limitation only occurred on t-POM-dominated diets as evidenced by a labeling experiment that showed Daphnia can incorporate carbon and phosphorus from Rhodomonas and Pseudomonas with similar efficiencies. Thus, peat layer t-POM was a lower quality food than Pseudomonas. This was corroborated by the finding that intermediate additions of Pseudomonas to limiting amounts of Rhodomonas supported increased Daphnia survival, growth and reproduction while t-POM additions had no beneficial effect.

My results suggest that high terrestrial stable isotope signals in metazoan zooplankton are most likely derived from t-OM that is channeled tohigher trophic levels via the microbial loop (i.e. heterotrophic bacteria and/or bacterivorous protozoa) but not from direct metazoan feeding on t-POM. Furthermore, bacteria may serve as an important supplement to zooplankton diets when phytoplankton abundance is low. However, a sufficient proportion of high quality phytoplankton is always necessary to fulfil mineral and especially biochemical requirements of zooplankton in unproductive aquatic systems.

The results of the mesocosm study showed that the Light:Nutrient-Hypothesis is not applicable to unproductive clear water systems in which the phytoplankton community is dominated by mixotrophs. In the face of the theoretical predictions, low light levels led to decreased zooplankton biomass. This was most likely caused by a shift in the algal community composition towards less edible taxa. Another reason may have been a weakening of the microbial loop. This is in line with the results of the laboratory studies that point out the importance of the microbial food web for zooplankton nutrition in unproductive lakes.

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2012. , 33 p.
Keyword [en]
Daphnia, phytoplankton, heterotrophic bacteria, terrestrial particulate organic material, food quality, food quantity, fatty acids, oligotrophic, Light:Nutrient-Hypothesis
National Category
Ecology
Research subject
Limnology
Identifiers
URN: urn:nbn:se:umu:diva-62287ISBN: 978-91-7459-512-3 (print)OAI: oai:DiVA.org:umu-62287DiVA: diva2:577031
Public defence
2013-01-25, KBC-Huset, Lilla Hörsalen (KB3A9), Umeå Universitet, Umeå, 10:15 (English)
Opponent
Supervisors
Available from: 2012-12-20 Created: 2012-12-14 Last updated: 2012-12-17Bibliographically approved
List of papers
1. Survival, growth and reproduction of Daphnia galeata feeding on single and mixed Pseudomonas and Rhodomonas diets
Open this publication in new window or tab >>Survival, growth and reproduction of Daphnia galeata feeding on single and mixed Pseudomonas and Rhodomonas diets
2012 (English)In: Freshwater Biology, ISSN 0046-5070, E-ISSN 1365-2427, Vol. 57, no 4, 835-846 p.Article in journal (Refereed) Published
Abstract [en]

1. Bacteria can be an important resource for zooplankton production in aquatic food webs, although the degree to which bacteria sustain zooplankton growth and reproduction is not clear. We performed a growth experiment with Daphnia galeata feeding on different ratios of P-replete Pseudomonas and Rhodomonas, ranging from a 100% bacterial to a 100% algal diet. 2. A pure bacterial diet did not support survival, growth or reproduction of D. galeata. While a 20% share of Rhodomonas in the food allowed survival of daphniids, the occurrence of offspring on a 50% algal diet indicated that the threshold for successful reproduction was between those two proportions of algal food. Increasing the proportion of the alga further increased growth and reproductive output, indicating that Rhodomonas was a higher-quality food than Pseudomonas. 3. A subsequent labelling experiment demonstrated that D. galeata incorporated phosphorus from Pseudomonas and Rhodomonas with similar efficiency, whereas carbon was incorporated more efficiently from Pseudomonas than from Rhodomonas. 4. Hence, we hypothesise that inadequate levels of essential biochemicals in pure bacterial diets led to decreased Daphnia performance. Concentrations of fatty acids in general, and especially of polyunsaturated fatty acids, were much lower in Pseudomonas than in Rhodomonas. This difference could explain the different growth and reproduction responses, although limitation by other essential biochemicals (e.g. sterols) cannot be ruled out. 5. Hence, where they dominate, bacteria may provide a significant part of the elemental flux to species feeding higher in the food web on the short term. However, the performance of consumers may be constrained by essential biochemicals.

Keyword
assimilation efficiency, heterotrophic bacteria, phytoplankton, polyunsaturated fatty acids, sterols
National Category
Natural Sciences
Identifiers
urn:nbn:se:umu:diva-55352 (URN)10.1111/j.1365-2427.2012.02751.x (DOI)000301227000018 ()
Available from: 2012-05-15 Created: 2012-05-14 Last updated: 2017-12-07Bibliographically approved
2. Poor direct exploitation of terrestrial particulate organic material from peat layers by Daphnia galeata.
Open this publication in new window or tab >>Poor direct exploitation of terrestrial particulate organic material from peat layers by Daphnia galeata.
2012 (English)In: Canadian Journal of Fisheries and Aquatic Sciences, ISSN 0706-652X, E-ISSN 1205-7533, Vol. 69, no 11, 1870-1880 p.Article in journal (Refereed) Published
Abstract [en]

Terrestrial organic material (t-OM) can subsidize lake food webs indirectly via incorporation of dissolved t-OM by bacteria and subsequent transfer to higher trophic levels or directly through metazoan consumption of particulate t-OM (t-POM). We tested the effects of peat layer t-POM on Daphnia galeata performance. A pure t-POM diet could not sustain survival, growth, and reproduction of D. galeata. Mixtures of heterotrophic bacteria (Pseudomonas sp.) and phytoplankton (Rhodomonas lacustris) gave higher survival, growth, and reproduction than mixtures of t-POM and Rhodomonas. Daphnids performed best when feeding on pure Rhodomonas diets. Quantification of phosphorus (P) and essential biochemicals (i.e., fatty acids) revealed that Rhodomonas had the highest amounts of all these components. Pseudomonas, while rich in P, contained few essential fatty acids, and t-POM had low concentrations of both P and fatty acids. We therefore suggest that the poor food quality of t-POM in our experiment was due to its suboptimal mineral and biochemical composition and that a substantial proportion of high-quality phytoplankton is necessary to sustain zooplankton biomass.

National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-62258 (URN)10.1139/f2012-110 (DOI)
Available from: 2012-12-13 Created: 2012-12-13 Last updated: 2017-12-06Bibliographically approved
3. Daphnia galeata performance along food quantity gradients of mixed Rhodomonas, Pseudomonas and terrestrial particulate organic material
Open this publication in new window or tab >>Daphnia galeata performance along food quantity gradients of mixed Rhodomonas, Pseudomonas and terrestrial particulate organic material
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Unproductive lakes are often characterized by high inputs of allochthonous dissolved and particulate organic carbon compared to autochthonous carbon, resulting in low phytoplankton abundances and high heterotrophic bacterial biomass. Thus, metazooplankton in these lakes feed on a mixture of phytoplankton, bacteria and terrestrial particulate organic material (t-POM) where the proportions of these components can be highly variable. As the nutritional value of the different food components varies, the dilution of phytoplankton (high-quality food) with high proportions of bacteria and/or t-POM (low-quality food) is expected to affect the performance of unselective filter feeders such as Daphnia. We tested how different combinations of constant concentrations of phytoplankton and increasing additions of bacterioplankton or t-POM affect zooplankton performance. We found that increasing the concentrations of both the bacterium Pseudomonas and t-POM relative to phytoplankton (Rhodomonas) negatively affected Daphnia survival, growth and reproduction when Rhodomonas was available at non-limiting concentrations (0.37 and 0.55 mgC L-1). When Rhodomonas quantity was low (0.22 mgC L-1), the addition of Pseudomonas led to better Daphnia performance except at very high concentrations of the bacterium relative to Rhodomonas. In contrast, the addition of t-POM was detrimental for overall Daphnia performance at low Rhodomonas quantity. These results imply that the ability of zooplankton to use low-quality food is affected by the availability of high-quality food. Further, food sources that do not fulfil dietary requirements of grazers may still provide nutritional benefits as long as other complimentary food components are available in sufficient quantities to compensate for mineral and/or biochemical deficiencies.

Keyword
heterotrophic bacteria, phytoplankton, food quality, allochthonous, autochthonous, zooplankton
National Category
Ecology
Research subject
Limnology
Identifiers
urn:nbn:se:umu:diva-62277 (URN)
Funder
FormasSwedish Research Council, 2007-5523
Available from: 2012-12-14 Created: 2012-12-14 Last updated: 2012-12-17
4. Testing the light: nutrient hypothesis in an oligotrophic boreal lake
Open this publication in new window or tab >>Testing the light: nutrient hypothesis in an oligotrophic boreal lake
2011 (English)In: Ecosphere, ISSN 2150-8925, Vol. 2, no 11, 123- p.Article in journal (Refereed) Published
Abstract [en]

Anthropogenic changes in the nitrogen (N), phosphorus (P), and carbon (C) cycles have altered nutrient concentrations and the light climate in freshwaters globally. These factors affect phytoplankton (PPr) and bacterial production (BP), which constitute the basal energy resource for higher trophic levels in the pelagic zone of lakes. The light:nutrient hypothesis (LNH) predicts that although basal production decreases at low light, seston C:nutrient ratios also decrease, thus increasing food quality for crustacean zooplankton and potentially offsetting the negative effects of reduced food availability. We tested the LNH in an oligotrophic boreal lake by manipulating N, P, C and reducing light, and measuring PPr, BP, seston C:nutrient ratios and zooplankton biomass in 32 mesocosms. Low light strongly reduced zooplankton biomass in contrast to LNH predictions. PPr did not decrease with low light as predicted by the LNH, however, the phytoplankton community shifted towards low light adapted, but potentially less edible phytoplankton species, such as colony forming Dinobryon (Chrysophyta) and gymnoid (Dinoflagellata) taxa, which were negatively correlated with zooplankton biomass. Seston C:nutrient ratios did not decrease with reduced light, possibly due to the high abundance of mixotrophic phytoplankton across treatments. BP decreased with low light and correlations between BP, bacterial biomass, ciliates and zooplankton suggest that bacteria may be coupled with zooplankton biomass. Thus, the LNH was inadequate when predicting changes in crustacean zooplankton biomass in this typical oligotrophic boreal system, where Daphnia is rare and mixotrophic phytoplankton are abundant. Instead, alternative explanations, such as changes in phytoplankton edibility and energy transferred through the microbial food chain may need investigation to explain reduced zooplankton biomass in low light treatments.

Place, publisher, year, edition, pages
Ecological Society of America, 2011
Keyword
bacterial production, food web, light : nutrient hypothesis, mesocosm, phytoplankton primary production, stoichiometry
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-50231 (URN)10.1890/ES11-00223.1 (DOI)
Available from: 2011-12-01 Created: 2011-12-01 Last updated: 2016-05-23Bibliographically approved

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