Effects of harmful algal blooms on competitors: Allelopathic mechanisms of the red tide dinoflagellate Karenia brevis

Because competitive interactions may have led to adaptations enabling bloom-forming phytoplankton to dominate pelagic communities, we explored the allelopathic effects of one red tide dinoflagellate, Karenia brevis, on competing phytoplankton species. Exposure to waterborne compounds from natural K. brevis blooms resulted in growth inhibition or death for four of five co-occurring species tested, whereas compounds exuded by K. brevis cultures suppressed three of these same competitors (the diatoms Asterionellopsis glacialis and Skeletonema costatum and the dinoflagellate Prorocentrum minimum) plus one additional species (the dinoflagellate Akashiwo cf. sanguinea) that was unaffected by bloom exudates. K. brevis exudates lowered photosynthetic efficiency and damaged cell membranes of competing phytoplankton, but had no effect on competitor esterase activity, nor did they limit competitor access to iron. Overall, during blooms, K. brevis exudes potent allelopathic compounds, competitors vary in their susceptibility to K. brevis allelopathy, and K. brevis may achieve nearly monospecific blooms by lowering the photosynthetic efficiency of competitor species and increasing competitor membrane permeability, eventually resulting in competitor growth suppression or death. Because the composition of phytoplankton communities is determined by a wide variety of abiotic and biotic factors, the plankton environment has been used as a model system to understand species interactions and diversity through the lens of disturbance (Hutchinson 1961), predator–prey interactions (Leibold 1989), and resource competition (Tilman 1982). In addition to competing for limiting resources, phytoplankton may exclude each other more directly. The inhibition of competitors by the release of compounds, a process known as allelopathy, may be important in planktonic systems (reviewed in Legrand et al. 2003). Allelopathy has been hypothesized to play a role in species succession (Keating 1977), the formation of harmful algal blooms (Smayda 1997), and the establishment of invasive species (Figueredo et al. 2007). Despite its likely importance, our understanding of allelopathy is still in the early stages. Allelopathy is difficult to conclusively demonstrate in the field, and responsible compounds have rarely been identified. Co-culturing experiments and observations of phytoplankton dynamics in the field have supported the possibility of allelopathy (e.g., Schmidt and Hansen 2001; Vardi et al. 2002), but have not definitively separated its effect from exploitative competition. Although lab experiments using high nutrient concentrations have helped to shed light on the process of allelopathy, their value has often been undermined by the use of whole-cell extracts rather than exudates (Freeburg et al. 1979), which places phytoplankton in contact with a suite of compounds not usually waterborne. We need to simultaneously better understand how allelopathy happens, and what its consequences are in the field (e.g., Fistarol et al. 2003). Although allelopathic compounds remain mostly unidentified, mechanisms for allelopathy have been proposed in some cases. Possible modes of action include oxidative damage, loss of competitor motility, inhibition of photosynthesis, inhibition of enzymes, and membrane damage (reviewed in Legrand et al. 2003). For example, Vardi et al. (2002) found that the presence of the cyanobacterium Microcystis sp. caused a buildup of apoptosis-inducing reactive oxygen species in the competing dinoflagellate Peridinium gatunense. Further, compounds produced by two dinoflagellate species have been reported to cause loss of motility in competitor cells, although there are likely multiple mechanisms. Cell contact with dinoflagellate Heterocapsa sp. was required for a loss of competitor motility (Uchida et al. 1995), whereas cell-free filtrates of the toxic dinoflagellate Alexandrium spp. caused loss of motility in the heterotrophic dinoflagellate Oxyrrhis marina (Tillmann and John 2002). Several studies have indicated that photosystem II (PSII) may be a target for allelopathy. Unknown compounds produced by the cyanobacterium Trichormus doliolum inhibited PSII in other cyanobacteria (Von Elert and Juttner 1997). However, a decrease in photosynthetic efficiency may be a symptom of allelopathy even if PSII is not the target. For example, Sukenik et al. (2002) found that compounds produced by the cyanobacterium Micro1 Corresponding author ( [email protected]). Acknowledgments We thank C. Pirkle for lab assistance and A. Lane, W. Morrison, S. Prince, and two anonymous reviewers for suggestions that improved the manuscript. This research was supported by National Science Foundation (NSF) grants OCE-0134843 and OCE-0726689 to J.K. E.K.P. was supported by an NSF Integrative Graduate Education and Research Traineeship (IGERT) fellowship. Limnol. Oceanogr., 53(2), 2008, 531–541 E 2008, by the American Society of Limnology and Oceanography, Inc.