INTRODUCTION
The rich diversity of organisms’ movement behavior has long invoked curiosity. Plants may passively adapt their inclining positions to alleviate competition for light (1,2), while most animals and many microorganisms can actively move from one place to another to seek forage, to mate with partners (3,4), or to escape from predators (5,6). A comprehensive understanding of the drivers, patterns and mechanisms of organismal movement is central to elucidating its ecological and evolutionary significance (7-10). In the extensive body of movement behavioral ecology, particular interest has been paid to foraging, being a fundamental activity providing energy throughout an organism’s life cycle (5,8). In spite of diverse modes of foraging movement among life forms (1,8,9), their intrinsic spatiotemporal patterns may converge to maximize biological fitness of individual foragers as it is predicted by the optimal foraging theory (OFT) (11, 12).
So far, perhaps the most convincing evidence supporting this prediction is provided by theoretical and experimental studies on movement patterns of a range of microorganisms (e.g. swimming bacteria, microalgae and multi-cellular planktons) in strictly controlled microcosm environments (13-16). In these systems with low information availability, microorganisms having weak resource detection capabilities usually perform random-like movements during the process of foraging. It has been repeatedly observed that intermittent locomotion (also known as stop-and-go movement or pause-travel locomotion, Fig. 1A) is common in these cases, and is characterized by discontinuous movements interwoven with significant punctuations and reorientations. A prevalent idea is that foraging efficiency can be maximized by certain statistical properties provided by their movement patterns. For example, the probability distributions of time intervals or spatial displacements between reorientations have been found to fit Brownian type or Lévy type walks, which are theoretically regarded to be optimal solutions of the random search problems under specific conditions (13,17-23).
The suggestion that the optimal foraging principle underpins diverse movement forms is indeed appealing. However, the universality of this strikingly simple principle remains controversial. It has been argued that there are exceptions in real-world ecosystems that are more complex deviating theoretical hypothesis (14,24,25), for instance, some individuals switching between Lévy and Brownian movement patterns as they traverse different habitat types (26,27). So far, optimal foraging is typically referred to as a hypothesis because it has not been established that the assumptions underlying these theories indeed hold. Furthermore, it remains elusive to which extent the optimal foraging principle can be verified to a range of newly discovered movement forms in microorganisms. Apart from the classical ‘run-and-tumble’ movement pattern (characterized by almost straight runs that are interrupted by tumbles) that have been extensively studied since the seminal work onEscherichia coli in the 1970s (10,28), recent studies discovered a variety of different movement modes (14,16,29), such as the ‘run-and-stop’ and ‘run-reverse-flick’ patterns (Fig. 1A) in the soil bacteria Pseudomonas putida (30), Myxococcus xanthus(31,32), and the marine bacteria Vibrio alginoticus (24). Very recently, one of the most intriguing movement patterns was found in pennate raphid diatoms, a species-rich and ecologically important group of microalgae mostly inhabiting benthic habitats in marine and freshwater environments. They move in a gliding manner, forming trajectories that highly resemble circular arcs (16). This unique movement pattern (termed as ‘circular run-and-reversal’, see Fig. 1A, results and discussion for detailed descriptions) is distinct from those of previously documented model organisms (28), whose trajectories typically consist of line segments in contrast with circular arcs. Our understanding of the statistical properties of these movement patterns is still rudimentary. In particular, it remains unknown if this type of movement conforms to optimal foraging behavior.
Here, we performed a systematic study on the novel ‘circular run-and-reversal’ behavior in the marine biofilm-inhabiting diatomNavicula arenaria var. rostellata . By combining experimental data and theoretical analyses, we demonstrate that the circular run-and-reversal behavior plays a crucial role in optimizing searching strategies. Our results suggest that in a silicon-limited environment, the diatoms can maximize their foraging efficiency by adapting the key parameters including reversal rate and rotational diffusivity and they can change the behavior strategy in a silicon-rich environment (Fig.1B).