Phytoplankton can actively diversify their migration strategy in response to turbulent cues

• Published in: Nature (London) Vol. 543; no. 7646; pp. 555 - 558
• Main Authors: Sengupta, Anupam, Carrara, Francesco, Stocker, Roman
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 23.03.2017; Nature Publishing Group
• Subjects: 631/158/856; 631/57/343; 639/301/923/916; 639/766/189; 704/829/826; Acclimatization; Avoidance Learning; Behavior; Cues; Ecosystem; Eddies; Environmental aspects; Gravitation; Humanities and Social Sciences; letter; Locomotion; Marine biology; Microbiological research; multidisciplinary; Nutrient availability; Oceanic turbulence; Oceans and Seas; Phytoplankton; Phytoplankton - physiology; Plankton; Science; Seawater; Stress, Physiological; Subpopulations; Surface water; Swimming; Turbulence; Turbulence (Fluid dynamics); Water Movements
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/nature21415

Here, marine phytoplankton are shown to diversify their migratory strategy in response to turbulent cues through a rapid change in shape, thus challenging a fundamental paradigm in oceanography that phytoplankton are passively at the mercy of ocean turbulence. Phytoplankton evade rough seas Until now, phytoplankton have been considered as passive subjects to ocean turbulence, which can change as suddenly as nutrient and light availability in the dynamic underwater environment. Roman Stocker and colleagues now show that several species of phytoplankton actively respond to turbulent cues by altering their migration routes to avoid layers of strong turbulence. They report that phytoplankton split into two groups, one swimming upward and another downward. This migratory behaviour could affect which species will survive in a changing ocean and will contribute to understanding of how communities respond to a warming climate. Marine phytoplankton inhabit a dynamic environment where turbulence, together with nutrient and light availability, shapes species fitness, succession and selection 1 , 2 . Many species of phytoplankton are motile and undertake diel vertical migrations to gain access to nutrient-rich deeper layers at night and well-lit surface waters during the day 3 , 4 . Disruption of this migratory strategy by turbulence is considered to be an important cause of the succession between motile and non-motile species when conditions turn turbulent 1 , 5 , 6 . However, this classical view neglects the possibility that motile species may actively respond to turbulent cues to avoid layers of strong turbulence 7 . Here we report that phytoplankton, including raphidophytes and dinoflagellates, can actively diversify their migratory strategy in response to hydrodynamic cues characteristic of overturning by Kolmogorov-scale eddies. Upon experiencing repeated overturning with timescales and statistics representative of ocean turbulence, an upward-swimming population rapidly (5–60 min) splits into two subpopulations, one swimming upward and one swimming downward. Quantitative morphological analysis of the harmful-algal-bloom-forming raphidophyte Heterosigma akashiwo together with a model of cell mechanics revealed that this behaviour was accompanied by a modulation of the cells’ fore–aft asymmetry. The minute magnitude of the required modulation, sufficient to invert the preferential swimming direction of the cells, highlights the advanced level of control that phytoplankton can exert on their migratory behaviour. Together with observations of enhanced cellular stress after overturning and the typically deleterious effects of strong turbulence on motile phytoplankton 5 , 8 , these results point to an active adaptation of H. akashiwo to increase the chance of evading turbulent layers by diversifying the direction of migration within the population, in a manner suggestive of evolutionary bet-hedging. This migratory behaviour relaxes the boundaries between the fluid dynamic niches of motile and non-motile phytoplankton, and highlights that rapid responses to hydrodynamic cues are important survival strategies for phytoplankton in the ocean.