Feeding by the heterotrophic nanoflagellate Katablepharis japonica on red-tide organisms and interactions between the phototrophic dinoflagellate Heterocapsa minima and heterotrophic protists

Abstract

Heterotrophic nanoflagellates are ubiquitous and known to be major predators of bacteria. However, the feeding of free-living heterotrophic nanoflagellates on phytoplankton is poorly understood, although these two components usually co-exist. To investigate the feeding and ecological roles of major heterotrophic nanoflagellates Katablepharis spp., the feeding ability of Katablepharis japonica on bacteria and phytoplankton species and the type of the prey that K. japonica can feed on were explored. Furthermore, the growth of K. japonica and its ingestion rates of the dinoflagellate Akashiwo sanguinea—a suitable algal prey item—heterotrophic bacteria, and the cyanobacteria Synechococcus sp., as a function of prey concentration were determined. Among the prey tested, K. japonica ingested heterotrophic bacteria, Synechococcus sp., the prasinophyte Pyramimonas sp., the cryptophytes Rhodomonas salina and Teleaulax sp., the raphidophytes Heterosigma akashiwo and Chattonella ovata, and the dinoflagellates Heterocapsa rotundata, Amphidinium carterae, Prorocentrum donghaiense, Alexandrium minutum, Cochlodinium polykrikoides, Gymnodinium catenatum, A. sanguinea, Coolia malayensis, and the ciliate Mesodinium rubrum, however, it did not feed on the dinoflagellates Alexandrium catenella, Gambierdiscus caribaeus, Heterocapsa triquetra, Lingulodinium polyedrum, Prorocentrum cordatum, P. micans, and Scrippsiella acuminata and the diatom Skeletonema costatum. Many K. japonica cells attacked and ingested a prey cell together after pecking and rupturing the surface of the prey cell and then uptaking the materials that emerged from the ruptured cell surface. Cell of A. sanguinea supported positive growth of K. japonica, but neither heterotrophic bacteria nor Synechococcus sp. supported growth. The maximum specific growth rate of K. japonica on A. sanguinea was 1.01 d-1. In addition, the maximum ingestion rate of K. japonica for A. sanguinea was 0.13 ng C predator-1d-1 (0.06 cells predator-1d-1). The maximum ingestion rate of K. japonica for heterotrophic bacteria was 0.019 ng C predator-1d-1 (266 bacteria predator-1d-1), and the highest ingestion rate of K. japonica for Synechococcus sp. at the given prey concentrations of up to ca. 107 cells ml-1 was 0.01 ng C predator-1d-1 (48 Synechococcus predator-1d-1). The maximum daily carbon acquisition from A. sanguinea, heterotrophic bacteria, and Synechococcus sp. were 307, 43, and 22%, respectively, of the body carbon of the predator. Thus, low ingestion rates of K. japonica on heterotrophic bacteria and Synechococcus sp. may be responsible for the lack of growth. The results of the present study clearly show that K. japonica is a predator of diverse phytoplankton, including toxic or harmful algae, and may also affect the dynamics of red tides caused by these prey species.

Prior to the present study, the phototrophic dinoflagellate Heterocapsa minima was not reported from Korean waters. I isolated this species from waters of Mijo Port, southern Korea in 2016. The genus Heterocapsa has been well documented as one of the major red-tide or harmful dinoflagellates. To investigate effective protist predators on H. minima, feeding by the engulfment-feeding heterotrophic dinoflagellates (HTDs) Oxyrrhis marina, Gyrodinium dominans, and Polykrikos kofoidii, the peduncle-feeding HTD Pfiesteria piscicida, the pallium-feeding HTD Oblea rotunda, and the naked ciliates Pelagostrobilidium sp. on H. minima was explored. I found that O. marina, G. dominans, P. piscicida, and Pelagostrobilidium sp. were able to feed on H. minima. However, H. minima may not affect growth of predators. These findings suggest that the effect of predation by heterotrophic protists on H. minima might be negligible.