Variability in protist grazing and growth on different marine Synechococcus isolates

Abstract

Grazing mortality of the marine phytoplankton Synechococcus is dominated by planktonic protists, yet rates of consumption and factors regulating grazer-Synechococcus interactions are poorly understood. One aspect of predator-prey interactions for which little is known are the mechanisms by which Synechococcus avoids or resists predation and, in turn, how this relates to the ability of Synechococcus to support growth of protist grazer populations. Grazing experiments conducted with the raptorial dinoflagellate Oxyrrhis marina and phylogenetically diverse Synechococcus isolates (strains WH8102, CC9605, CC9311, and CC9902) revealed marked differences in grazing rates-specifically that WH8102 was grazed at significantly lower rates than all other isolates. Additional experiments using the heterotrophic nanoflagellate Goniomonas pacifica and the filter-feeding tintinnid ciliate Eutintinnis sp. revealed that this pattern in grazing susceptibility among the isolates transcended feeding guilds and grazer taxon. Synechococcus cell size, elemental ratios, and motility were not able to explain differences in grazing rates, indicating that other features play a primary role in grazing resistance. Growth of heterotrophic protists was poorly coupled to prey ingestion and was influenced by the strain of Synechococcus being consumed. Although Synechococcus was generally a poor-quality food source, it tended to support higher growth and survival of G. pacifica and O. marina relative to Eutintinnis sp., indicating that suitability of Synechococcus varies among grazer taxa and may be a more suitable food source for the smaller protist grazers. This work has developed tractable model systems for further studies of grazer-Synechococcus interactions in marine microbial food webs.

Fig. 1.

Mean rates (±SE) of ingestion of different Synechococcus isolates recorded for the four grazing experiments conducted with O. marina, G. pacifica, and Eutintinnis sp. Means sharing the same letter are statistically indistinguishable (Tukey-Kramer HSD, α = 0.05).

Fig. 2.

Summary of mean (±SE) carbon-specific ingestion of WH8102 and CC9311 by O. marina, G. pacifica, and Eutintinnis sp. from all four experiments.

Fig. 3.

Ingestion rates (upper panel) and proportion of population feeding (lower panel) (±SE) of O. marina on Synechococcus isolates WH8102 and CC9311 at different stages of growth (i.e., early, mid-, and late exponential).

Fig. 4.

Results from experiments investigating the effect of motility on grazing by comparing ingestion of untreated versus heat-treated Synechococcus isolates WH8102 and CC9311 by O. marina and Eutintinnis sp. Error bars represent 1 standard error.

Fig. 5.

Grazer abundance in growth experiments in which grazers were provided different food sources. Prey treatments supporting grazer growth (i.e., final abundance significantly greater than initial) are indicated by **, while those merely supporting survival (i.e., final abundance significantly greater than starved) are indicated by *. Incubations with O. marina and G. pacifica were 48 h with D. tertiolecta and M. squamata as positive controls (ctrl), respectively, and incubations for Eutintinnis were 24 h with I. galbana as a positive control.

Fig. 6.

Relationship between grazer growth and ingestion associated with each Synechococcus isolate. (A) Log-transformed ingestion rates versus grazer growth for all grazing experiments, except those investigating effects of Synechococcus growth phase and motility; (B) log-transformed carbon-based rates of grazer ingestion versus log-transformed growth rates from those experiments in which positive grazer growth was observed. The hatched line represents the overall mean grazer growth efficiency (GGE, 0.3).