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The mode of nutrition of mixotrophic flagellates determines the food quality for their consumers
(2007)
In this pilot study, we describe a high-pressure incubation system allowing multiple subsampling of a pressurized culture without decompression. The system was tested using one piezophilic (Photobacterium profundum), one piezotolerant (Colwellia maris) bacterial strain and a decompressed sample from the Mediterranean deep sea (3044 m) determining bacterial community composition, protein production (BPP) and cell multiplication rates (BCM) up to 27 MPa. The results showed elevation of BPP at high pressure was by a factor of 1.5 +/- 1.4 and 3.9 +/- 2.3 for P. profundum and C. maris, respectively, compared to ambient-pressure treatments and by a factor of 6.9 +/- 3.8 fold in the field samples. In P. profundum and C. maris, BCM at high pressure was elevated (3.1 +/- 1.5 and 2.9 +/- 1.7 fold, respectively) compared to the ambient-pressure treatments. After 3 days of incubation at 27 MPa, the natural bacterial deep-sea community was dominated by one phylum of the genus Exiguobacterium, indicating the rapid selection of piezotolerant bacteria. In future studies, our novel incubation system could be part of an isopiestic pressure chain, allowing more accurate measurement of bacterial activity rates which is important both for modeling and for predicting the efficiency of the oceanic carbon pump.
The nutrition of animal consumers is an important regulator of ecological processes due to its effects on their physiology, life-history and behaviour. Understanding the ecological effects of poor nutrition depends on correctly diagnosing the nature and strength of nutritional limitation. Despite the need to assess nutritional limitation, current approaches to delineating nutritional constraints can be non-specific and imprecise. Here, we consider the need and potential to develop new complementary approaches to the study of nutritional constraints on animal consumers by studying and using a suite of established and emerging biochemical and molecular responses. These nutritional indicators include gene expression, transcript regulators, protein profiling and activity, and gross biochemical and elemental composition. The potential applications of nutritional indicators to ecological studies are highlighted to demonstrate the value that this approach would have to future studies in community and ecosystem ecology.
Carbon assimilation mode in mixotrophs and the fatty acid composition of their rotifer consumers
(2009)
P>1. We examined an important ecophysiological link between the mixotrophic flagellate Chlamydomonas acidophila and its consumers, the rotifers Elosa worallii, Cephalodella sp. and Brachionus sericus, by comparing their fatty acid profiles. 2. The mixotrophic flagellate was grown under either exclusively autotrophic conditions in the light, under exclusively heterotrophic conditions in the dark with an organic carbon source (glucose), or in the light plus the organic carbon sources (=mixotrophic). 3. Under heterotrophic growth conditions, C. acidophila strongly reduced its content of the n-3 polyunsaturated fatty acid (PUFA) alpha-linolenic acid (ALA, C18:3n-3) compared with auto- and mixotrophic growth conditions. Although PUFAs with more than 18 carbon atoms were not detected in C. acidophila, significant amounts of eicosatetraenoic (ETA, 20:4n-3) and eicosapentaenoic acid (EPA, 20:5n-3) were found in three rotifer consumers. 4. Species-specific differences in the fatty acid profiles with respect to ETA, EPA and the precursor ALA were found in the rotifers: Brachionus and Cephalodella fed on the heterotrophic diets synthesised less EPA. In Elosa, smaller amounts of ALA were detected but were converted efficiently to a constant content of EPA and to an exceptionally high content of ETA. 5. Since in nature the mode of carbon assimilation among mixotrophic organisms differs, and their fatty acid composition varies depending on their mode of carbon assimilation, the availability of ALA might be critical for their consumers. An insufficient dietary supply of this precursor for the synthesis of ETA and EPA can prevent consumers from regulating their content of ETA and EPA. Therefore, observed differences in values of the latter might underly species-specific differences in the competitive capability of consumers.
The factors that determine the efficiency of energy transfer in aquatic food webs have been investigated for many decades. The plant-animal interface is the most variable and least predictable of all levels in the food web. In order to study determinants of food quality in a large lake and to test the recently proposed central importance of the long-chained eicosapentaenoic acid (EPA) at the pelagic producer-grazer interface, we tested the importance of polyunsaturated fatty acids (PUFAs) at the pelagic producerconsumer interface by correlating sestonic food parameters with somatic growth rates of a clone of Daphnia galeata. Daphnia growth rates were obtained from standardized laboratory experiments spanning one season with Daphnia feeding on natural seston from Lake Constance, a large pre-alpine lake. Somatic growth rates were fitted to sestonic parameters by using a saturation function. A moderate amount of variation was explained when the model included the elemental parameters carbon (r2 = 0.6) and nitrogen (r2 = 0.71). A tighter fit was obtained when sestonic phosphorus was incorporated (r2 = 0.86). The nonlinear regression with EPA was relatively weak (r2 = 0.77), whereas the highest degree of variance was explained by three C18-PUFAs. The best (r2 = 0.95), and only significant, correlation of Daphnia's growth was found with the C18-PUFA α-linolenic acid (α-LA; C18:3n-3). This correlation was weakest in late August when C:P values increased to 300, suggesting that mineral and PUFA-limitation of Daphnia's growth changed seasonally. Sestonic phosphorus and some PUFAs showed not only tight correlations with growth, but also with sestonic α-LA content. We computed Monte Carlo simulations to test whether the observed effects of α-LA on growth could be accounted for by EPA, phosphorus, or one of the two C18-PUFAs, stearidonic acid (C18:4n-3) and linoleic acid (C18:2n-6). With >99 % probability, the correlation of growth with α-LA could not be explained by any of these parameters. In order to test for EPA limitation of Daphnia's growth, in parallel with experiments on pure seston, growth was determined on seston supplemented with chemostat-grown, P-limited Stephanodiscus hantzschii, which is rich in EPA. Although supplementation increased the EPA content 80-800x, no significant changes in the nonlinear regression of the growth rates with α-LA were found, indicating that growth of Daphnia on pure seston was not EPA limited. This indicates that the two fatty acids, EPA and α-LA, were not mutually substitutable biochemical resources and points to different physiological functions of these two PUFAs. These results support the PUFA-limitation hypothesis for sestonic C:P < 300 but are contrary to the hypothesis of a general importance of EPA, since no evidence for EPA limitation was found. It is suggested that the resource ratios of EPA and α-LA rather than the absolute concentrations determine which of the two resources is limiting growth.
Significant seasonal variation in size at settlement has been observed in newly settled larvae of Dreissena polymorpha in Lake Constance. Diet quality, which varies temporally and spatially in freshwater habitats, has been suggested as a significant factor influencing life history and development of freshwater invertebrates. Accordingly, experiments were conducted with field-collected larvae to test the hypothesis that diet quality can determine planktonic larval growth rates, size at settlement and subsequent post-metamorphic growth rates. Larvae were fed one of two diets or starved. One diet was composed of cyanobacterial cells which are deficient in polyunsaturated fatty acids (PUFAs), and the other was a mixed diet rich in PUFAs. Freshly metamorphosed animals from the starvation treatment had a carbon content per individual 70% lower than that of larvae fed the mixed diet. This apparent exhaustion of larval internal reserves resulted in a 50% reduction of the postmetamorphic growth rates. Growth was also reduced in animals previously fed the cyanobacterial diet. Hence, low food quantity or low food quality during the larval stage of D. polymorpha lead to irreversible effects for postmetamorphic animals, and is related to inferior competitive abilities.
Species such as Dreissena polymorpha sometimes contribute substantially in the transfer of primary to secondary production. During the ontogenetic cycle, the reproductive investment of adult mussels is one of the main parameters that affect recruitment success. We studied how food quality and temperature affect the reproductive investment in term of egg mass of D. polymorpha in a lake by sampling mussels monthly from 4 m and 15 m depths. Temperature affected reproduction directly and also indirectly through the food. To assess whether temperature and/or food conditions led to the differences observed in mussels sampled from the two depths, mussels were reared in the laboratory under two different temperature regimes for 3 months, simulating the temperature of the lake at 4 m and 15 m depth. Possible effects of food quality were tested at each temperature using four diets differing in fatty acid composition. Temperature played an important role as a trigger for spawning, and the type of diet clearly affected the reproductive investment. When the heterokont chromophyte alga Nannochloropsis limnetica, which is rich in polyunsaturated fatty acids (PUFAs) and long-chained PUFAs (>C18), was fed to mussels, an increased egg mass was obtained. This result was in contrast to that found when the green alga Scenedesmus obliquus and the cyanobacterium Aphanothece sp., both of which are deficient in long-chained PUFAs, were offered as food to the mussels. Such a PUFA-dependent food quality may affect reproduction in lakes. Food quality effects vary seasonally in a lake and may be most important in summer, when low-food- quality green algae and cyanobacteria are abundant. The low biochemical quality of these blooms may affect at least the later period of gametogenesis of D. polymorpha, which reproduces from June to August.
Food quality controls egg quality of the zebra mussel Dreissena polymorpha : The role of fatty acids
(2004)
We investigated the investment of adult Dreissena polymorpha to the eggs by sampling mussels monthly from 4- and 15-m water depth. The fatty acid composition of eggs differed significantly between depths and over time. To assess whether temperature and food conditions led to the differences observed for mussels sampled from the two depths, mussels were reared in the laboratory under two different 3-month temperature regimes, simulating the temperature of the lake at 4- and 15-m depth. Possible effects of food quality were tested in each simulation using four diets differing in fatty acid composition: Cryptomonas erosa, Nannochloropsis limnetica [rich in polyunsaturated fatty acids (PUFAs) and long- chained PUFAs (.C18)], Scenedesmus obliquus, and the cyanobacterium Aphanothece sp. (deficient in long-chained PUFAs). In newly released eggs, specific (n-3) and (n-6) long-chained PUFAs increased when these fatty acids were available in the natural seston or in the laboratory diets. Mussels fed organisms deficient in long-chained PUFAs were still able to allocate arachidonic acid, eicosapentaenoic acid, and docosahexaenoic acid into eggs, which suggests that minimum levels of particular fatty acids were maintained in eggs by transfer from internal reserves of the female mussels to oocytes. In contrast to the diet, there were no effects of the temperature on the fatty acid composition of eggs.
Settlement on suitable substrata under favourable environmental conditions is an important factor for a successful recruitment of adult populations of Dreissena polymorpha. Therefore, the pattern of settlement of zebra mussel (Dreissena polymorpha) larvae at different depths was studied in Lake Constance. Maximum densities of larvae and newly settled juvenile mussels were observed at 4m depth, while only single settlement episodes were recorded at greater depths (15 m and 30 m). Temperature fluctuation was used as a surrogate parameter for internal seiches. Biotic and abiotic parameters were subjected to a principal component analysis (PCA). The tight coupling of the internal seiches, larval abundance and settlement at 4-m depth vs. the lack of coupling of the latter two variables at greater depths indicated that water currents transported settling larvae to the substrata at greater depth. Our data suggest that physical factors, such as boundary mixing and internal seiches, should be considered as sources of variability in settlement.
The factors that determine the efficiency of energy transfer in aquatic food webs have been investigated for many decades. The plant-animal interface is the most variable and least predictable of all levels in the food web. In order to study determinants of food quality in a large lake and to test the recently proposed central importance of the long-chained eicosapentaenoic acid (EPA) at the pelagic producer-grazer interface, we tested the importance of polyunsaturated fatty acids (PUFAs) at the pelagic producer-consumer interface by correlating sestonic food parameters with somatic growth rates of a clone of Daphnia galeata. Daphnia growth rates were obtained from standardized laboratory experiments spanning one season with Daphnia feeding on natural seston from Lake Constance, a large pre-alpine lake. Somatic growth rates were fitted to sestonic parameters by using a saturation function. A moderate amount of variation was explained when the model included the elemental parameters carbon (r2 = 0.6) and nitrogen (r2 = 0.71). A tighter fit was obtained when sestonic phosphorus was incorporated (r2 = 0.86). The nonlinear regression with EPA was relatively weak (r2 = 0.77), whereas the highest degree of variance was explained by three C18-PUFAs. The best (r2 = 0.95), and only significant, correlation of Daphnia's growth was found with the C18-PUFA a-linolenic acid (a-LA; C18:3n-3). This correlation was weakest in late August when C:P values increased to 300, suggesting that mineral and PUFA- limitation of Daphnia's growth changed seasonally. Sestonic phosphorus and some PUFAs showed not only tight correlations with growth, but also with sestonic alpha-LA content. We computed Monte Carlo simulations to test whether the observed effects of alpha-LA on growth could be accounted for by EPA, phosphorus, or one of the two C18-PUFAs, stearidonic acid (C18:4n-3) and linoleic acid (C18:2n-6). With >99% probability, the correlation of growth with alpha-LA could not be explained by any of these parameters. In order to test for EPA limitation of Daphnia's growth, in parallel with experiments on pure seston, growth was determined on seston supplemented with chemostat-grown, Plimited Stephanodiscus hantzschii, which is rich in EPA. Although supplementation increased the EPA content 80-800x, no significant changes in the nonlinear regression of the growth rates with alpha-LA were found, indicating that growth of Daphnia on pure seston was not EPA limited. This indicates that the two fatty acids, EPA and alpha-LA, were not mutually substitutable biochemical resources and points to different physiological functions of these two PUFAs. These results support the PUFA-limitation hypothesis for sestonic C:P < 300 but are contrary to the hypothesis of a general importance of EPA, since no evidence for EPA limitation was found. It is suggested that the resource ratios of EPA and alpha-LA rather than the absolute concentrations determine which of the two resources is limiting growth.