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).