A Game of Russian Roulette for a Generalist Dinoflagellate Parasitoid: Host Susceptibility Is the Key to Success

Abstract

Marine microbial interactions involving eukaryotes and their parasites play an important role in shaping the structure of phytoplankton communities. These interactions may alter population densities of the main host, which in turn may have consequences for the other concurrent species. The effect generalist parasitoids exert on a community is strongly dependent on the degree of host specificity. Parvilucifera sinerae is a generalist parasitoid able to infect a wide range of dinoflagellates, including toxic-bloom-forming species. A density-dependent chemical cue has been identified as the trigger for the activation of the infective stage. Together these traits make Parvilucifera-dinoflagellate hosts a good model to investigate the degree of specificity of a generalist parasitoid, and the potential effects that it could have at the community level. Here, we present for the first time, the strategy by which a generalist dinoflagellate parasitoid seeks out its host and determine whether it exhibits host preferences, highlighting key factors in determining infection. Our results demonstrate that in its infective stage, P. sinerae is able to sense potential hosts, but does not actively select among them. Instead, the parasitoids contact the host at random, governed by the encounter probability rate and once encountered, the chance to penetrate inside the host cell and develop the infection strongly depends on the degree of host susceptibility. As such, their strategy for persistence is more of a game of Russian roulette, where the chance of survival is dependent on the susceptibility of the host. Our study identifies P. sinerae as a potential key player in community ecology, where in mixed dinoflagellate communities consisting of hosts that are highly susceptible to infection, parasitoid preferences may mediate coexistence between host species, reducing the dominance of the superior competitor. Alternatively, it may increase competition, leading to species exclusion. If, however, highly susceptible hosts are absent from the community, the parasitoid population could suffer a dilution effect maintaining a lower parasitoid density. Therefore, both host community structure and host susceptibility will determine infectivity in the field.

Keywords: Parvilucifera; dinoflagellates; host–parasite interactions; perkinsids; prevalence; specificity.

FIGURE 1

Optical micrographs of the different life-cycle stages of Parvilucifera sinerae infecting five dinoflagellate hosts. Scale bar = 20 μm.

FIGURE 2

Parvilucifera sinerae generations in Alexandrium minutum(A), Scrippsiella trochoidea(B), Heterocapsa niei(C), Protoceratium reticulatum(D), and Gymnodinium catenatum(E). Y-axis is the concentration of parasitoid sporangia (cells mL^-1). X-axis is the time since parasitoid inoculation in days. Red dots are the observed concentration of sporangia. Black line is the fitted curve of sporangia concentration observed through the time. Blue dashed line is the peak of each generation predicted by the model. Note difference in y-axis scale in (E) which is two orders of magnitude lower.

FIGURE 3

Parasitoid zoospore chemotaxis for two chemical cues (A) and three dinoflagellate species (B). Ic is the chemotaxis index, defined as the proportion of zoospores that enter the syringe relative to the control (L1 medium). Data are expressed as mean ± SD.

FIGURE 4

Parasitoid prevalence (%) in each of the five host species mixed in an artificial community during the 3 days after parasitoid inoculation. Data are expressed as mean ± SD.

FIGURE 5

Parasitoid prevalence as a function of inoculum size for P. sinerae infecting A. minutum(A), S. trochoidea(B), H. niei(C), P. reticulatum(D), and G. catenatum(E). Host density was maintained at 5 × 10³ cells mL^-1, with zoospore density varied to yield zoospore:host ratios of 1:1 to 120:1. Data are expressed as mean ± SD.

FIGURE 6

Effect of host abundance in host infection in System A: a mixed culture of A. minutum and S. trochoidea(A–C), and in System B: a mixed culture of A. minutum and H. niei(D–F). (A,D) Initial host density of both host was the same 10³ cells mL^-1; (B,E) S. trochoidea and H. niei were at 10⁴ cells mL^-1 and A. minutum was at 10³ cells mL^-1. (C,F) A. minutum was at initial density of 10⁴ cells mL^-1, and S. trochoidea and H. niei at 10³ cells mL^-1. Data are expressed as mean ± SD.

FIGURE 7

Potential effects of P. sinerae (adapted from Figure 1 of Hatcher et al., 2012). Arrows depict positive (+) and negative (–) direct effects (numerical effects) on population density resulting from the impact of a consumer or the resources; arrow thickness indicates strength of interaction; red arrows indicate key interactions, leading to the following patterns: (A) Parasitoid-mediated coexistence: regulation of a superior competitor by the parasitoid, i.e., A. minutum, enables S. trochoidea, less harmed by the parasitoid, to persist. (B) Apparent competition: higher densities of A. minutum host result in higher parasitoid population densities, which have a detrimental effect on H. niei host: thus, A. minutum acts as a reservoir of infection to H. niei.