Feast or flee: bioelectrical regulation of feeding and predator evasion behaviors in the planktonic alveolate Favella sp. (Spirotrichia).

Alveolate (ciliates and dinoflagellates) grazers are integral components of the marine food web and must therefore be able to sense a range of mechanical and chemical signals produced by prey and predators, integrating them via signal transduction mechanisms to respond with effective prey capture and predator evasion behaviors. However, the sensory biology of alveolate grazers is poorly understood. Using novel techniques that combine electrophysiological measurements and high-speed videomicroscopy, we investigated the sensory biology of Favella sp., a model alveolate grazer, in the context of its trophic ecology. Favella sp. produced frequent rhythmic depolarizations (∼500 ms long) that caused backward swimming and are responsible for endogenous swimming patterns relevant to foraging. Contact of both prey cells and non-prey polystyrene microspheres at the cilia produced immediate mechanostimulated depolarizations (∼500 ms long) that caused backward swimming, and likely underlie aggregative swimming patterns of Favella sp. in response to patches of prey. Contact of particles at the peristomal cavity that were not suitable for ingestion resulted in depolarizations after a lag of ∼600 ms, allowing time for particles to be processed before rejection. Ingestion of preferred prey particles was accompanied by transient hyperpolarizations (∼1 s) that likely regulate this step of the feeding process. Predation attempts by the copepod Acartia tonsa elicited fast (∼20 ms) animal-like action potentials accompanied by rapid contraction of the cell to avoid predation. We have shown that the sensory mechanisms of Favella sp. are finely tuned to the type, location, and intensity of stimuli from prey and predators.

Mesozooplankton community responses to a large-scale harmful algal bloom induced by the non-indigenous dinoflagellate Lingulodinium polyedra.

Our understanding of how zooplankton community composition varies in relation to harmful algal blooms remains limited, particularly in ecosystems where toxin-producing algae may have been introduced through anthropogenic activities. Harmful algal blooms (HABs) naturally occur on the coast of southern Africa, where they are predominantly associated with the cold Benguela region. In the warm-temperate waters east of Cape Agulhas, HABs occur rarely and red tides are mostly associated with the non-toxin producing dinoflagellate Noctiluca scintillans. Blooms of N. scintillans may cause water discolouration, but this is generally short-lived with limited impact on the ecosystem. However, in December 2013 the eastern Agulhas region experienced an extensive HAB, which persisted for ca. 4 months and affected >500 km of coastline, from Wilderness to East London. This unprecedented event was caused by the non-indigenous toxin-producing dinoflagellate, Lingulodinium polyedra. The impact on the coastal seas was widespread and severe, with instances of low dissolved O2 levels and fish kills being reported at the time in the broader Algoa Bay area. This study investigated the impact of the L. polyedra bloom on the mesozooplankton of Algoa Bay and reports the successive changes in zooplankton community composition and biomass observed from July 2013 to July 2014. The bloom impacted species diversity and richness, with a marked shift in dominance from a calanoid copepod dominated community to one dominated by microzooplankton (specifically cyclopoid copepods, tintinnids and cladocerans), over the period November 2013-March 2014. Calanoid copepod abundance was significantly reduced throughout Algoa Bay with the progression of the bloom, and this significantly impacted the total zooplankton biomass of the region. The results of the study suggest that harmful algal blooms have a negative impact on zooplankton communities, with notable implications for the higher trophic levels of the coastal pelagic ecosystem.

Connecting alveolate cell biology with trophic ecology in the marine plankton using the ciliate Favella as a model.

Planktonic alveolates (ciliates and dinoflagellates), key trophic links in marine planktonic communities, exhibit complex behaviors that are underappreciated by microbiologists and ecologists. Furthermore, the physiological mechanisms underlying these behaviors are still poorly understood except in a few freshwater model ciliates, which are significantly different in cell structure and behavior than marine planktonic species. Here, we argue for an interdisciplinary research approach to connect physiological mechanisms with population-level outcomes of behaviors. Presenting the tintinnid ciliate Favella as a model alveolate, we review its population ecology, behavior, and cellular/molecular biology in the context of sensory biology and synthesize past research and current findings to construct a conceptual model describing the sensory biology of Favella. We discuss how emerging genomic information and new technical methods for integrating research across different levels of biological organization are paving the way for rapid advance. These research approaches will yield a deeper understanding of the role that planktonic alveolates may play in biogeochemical cycles, and how they may respond to future ocean conditions.