Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production

Abstract

Terrestrial organic matter inputs have long been thought to play an important role in aquatic food web dynamics. Results from recent whole lake (13)C addition experiments suggest terrestrial particulate organic carbon (t-POC) inputs account for a disproportionate portion of zooplankton production. For example, several studies concluded that although t-POC only represented approximately 20% of the flux of particulate carbon available to herbivorous zooplankton, this food source accounted for approximately 50% of the C incorporated by zooplankton. We tested the direct dietary impact of t-POC (from the leaves of riparian vegetation) and various phytoplankton on Daphnia magna somatic growth, reproduction, growth efficiency, and lipid composition. By itself, t-POC was a very poor quality resource compared to cryptophytes, diatoms, and chlorophytes, but t-POC had similar food quality compared to cyanobacteria. Small additions of high quality Cryptomonas ozolinii to t-POC-dominated diets greatly increased Daphnia growth and reproduction. When offered alone, t-POC resulted in a Daphnia growth efficiency of 5 +/- 1%, whereas 100% Cryptomonas and Scenedesmus obliquus diets resulted in growth efficiencies of 46 +/- 8% (+/- SD) and 36 +/- 3%, respectively. When offered in a 50:50 mixed diet with Cryptomonas or Scenedesmus, the t-POC fraction resulted in a partial growth efficiency of 22 +/- 9% and 15 +/- 6%, respectively. Daphnia that obtained 80% of their available food from t-POC assimilated 84% of their fatty acids from the phytoplankton component of their diet. Overall, our results suggest Daphnia selectively allocate phytoplankton-derived POC and lipids to enhance somatic growth and reproduction, while t-POC makes a minor contribution to zooplankton production.

Fig. 1.

The reproductive and size responses to the t-POC and Cryptomonas diets in the first two life table experiments. (A) Cumulative reproduction (mean ± 1 SD) for the first life table experiment. (B) Age at first reproduction for the second life table experiment (the age of reproduction for the 100% t-POC treatment was taken from the first experiment). (C) Cumulative reproduction during 14 days for the second experiment. (D) Mean Daphnia dry weight at age 14 days from the second life table.

Fig. 2.

Cumulative production (mean ± 1 SD) for the batch experiment. A represents the results for the Cryptomonas treatments and B represents the Scenedesmus treatments. The 100% t-POC treatment (shown in both panels for comparison) was terminated 1 week early so that there would be sufficient Daphnia biomass for fatty acid biomaker determinations. The outcome for the Microcystis treatment is not depicted in this Figure, but this treatment had a cumulative production of 4.7 ± 1.3 mg D.W. L⁻¹, which was 31% less than the 100% t-POC treatment.

Fig. 3.

The reproductive and size responses to t-POC and phytoplankton diets in a validation life table experiment. This experiment was designed to test whether t-POC is generally much lower food quality that phytoplankton, or was just lower food quality than the phytoplankton we used for our first two experiments. For this experiment, we selected representatives of cryptophytes, diatoms, green algae, and cyanobacteria which were from different genera than those used in previous experiments; that is, Rhodomonas lacustris (Rhod), Fragilaria crotonensis (Frag), Chlamydomonas reinhardti (Chlam), and Anabaena flos-aquae (Anab). We also used a new t-POC source that was derived from equal dry weights of red alder, black cottonwood, big leaf maple, and willow, which were subsequently milled and sieved together. In this experiment Daphnia magna fed Rhodomonas, Fragilaria, and Chlamydomonas were significantly larger and more fecund (P < 0.05 for individual t tests after Bonferroni correction) than Daphnia fed mixed t-POC, however, Daphnia fed Anabaena had similar outcomes compared to mixed t-POC. The fecundity results accounted for mortality differences, whereas the size differences were only for surviving individuals.

Fig. 4.

Daphnia magna fatty acid composition for the second life table experiment. The dominant fatty acids (EPA, SDA, 16:0, 16:1ω7, 18:1ω9, and 18:2ω6) are expressed on the left-hand y axis and the ω3:ω6 fatty acid ratio is expressed on the right-hand y axis.

Fig. 5.

A principal component analysis (PCA) of fatty acid composition for the diet and Daphnia samples from the third life table experiment (see Table S1). The first principal component (PC), see x axis of A and B, explained 30.7% of the overall variability and was positively correlated with the SAFA stearic acid (18:0) as well as the sum of long chain (i.e., C₂₀, C₂₂, and C₂₄) SAFAs (r = 0.83 and 0.88, respectively), and negatively correlated with C₁₆ PUFAs (r = −0.93). The second PC, see y axis of A, explained 27.6% of the variability and was positively correlated with EPA (r = 0.93) and negatively correlated with C₁₈ ω6 PUFAs (r = −0.84). The third PC, see y axis of B, explained an additional 20.3% of variability and was positively correlated with C₁₆ MUFAs (r = 0.94) and negatively correlated with C₁₈ ω3 PUFAs (r = −0.94). In the legend for this figure, In_t-POC represents the initial mixed t-POC, aged_t-POC represents the mixed t-POC that accumulated within the feeding vials during this experiment, Anab represents Anabaena, Chlam represents Chlamydomonas, Frag represents Fragilaria, Rhod represents Rhodomonas, and Dph represents Daphnia. For example, Rhod represents the FA composition of Rhodomonas and Dph_Rhod represents the FA composition of Daphnia fed Rhodomonas. All values are based on duplicate samples, except for the Daphnia consuming aged mixed t-POC and Fragilaria diet samples where one replicate was lost due to contamination.