Swimming and feeding of
Julia Dölger1, Lasse Tor Nielsen2, Thomas Kiørboe2 & Anders Andersen1
Many unicellular flagellates are mixotrophic and access resources through both photosynthesis and
prey capture. Their fitness depends on those processes as well as on swimming and predator avoidance.
How does the flagellar arrangement and beat pattern of the flagellate affect swimming speed,
predation risk due to flow-sensing predators, and prey capture? Here, we describe measured flows
around two species of mixotrophic, biflagellated haptophytes with qualitatively different flagellar
arrangements and beat patterns. We model the near cell flows using two symmetrically arranged point
forces with variable position next to a no-slip sphere. Utilizing the observations and the model we find
that puller force arrangements favour feeding, whereas equatorial force arrangements favour fast and
quiet swimming. We determine the capture rates of both passive and motile prey, and we show that the
flow facilitates transport of captured prey along the haptonema structure. We argue that prey capture
alone cannot fulfil the energy needs of the observed species, and that the mixotrophic life strategy is
essential for survival.
Small plankton form an essential part of the marine ecosystem. Such organisms face the challenge of living in a
light- and nutrient-limited environment, while being exposed to flow-sensing predators. Many unicellular flagellates
in the size range from 2 to 50 micrometer are mixotrophic and use a combination of photosynthesis,
dissolved nutrient uptake, and prey capture to access resources1,2. Despite the increase in predation risk due to
the induced flow disturbances, they must swim to reach light and food and create feeding currents that enhance
prey capture and nutrient uptake. They do so by means of cilia and flagella in different numbers and with different
positions, lengths, and dynamics3–5. This diversity in flagellar arrangements suggests different strategies with
trade-offs, since not all functions can be optimized simultaneously. Biflagellates with two left-right symmetrically
arranged flagella, such as the well-studied algae Chlamydomonas reinhardtii, are an abundant and successful
flagellate form4,6. By tuning the flagellar arrangement and beat pattern, biflagellates can arrange the thrust forces
in front of the cell (puller), equatorially (neutral), or behind the cell (pusher)7. What are the advantages and disadvantages
of different flagellar arrangements and beat patterns in mixotrophic biflagellates, and to what extent are
these archetypical, multi-functional organisms optimized for swimming, predator avoidance, and prey capture?
To answer these questions we focus on two mixotrophic, biflagellated species of haptophytes with different
morphologies, kinematics, and feeding strategies (Methods, Fig. 1, and Supplementary Videos S1 and S2).
Prymnesium polylepis has long flagella that move in an undulatory fashion and it feeds on small prey captured
on the long and slender haptonema that emerges from the cell front. The feeding process involves capture, transport
along the haptonema, and delivery of prey to the ingestion site at the opposite end of the cell8 (Fig. 1c–f).
Prymnesium parvum feeds on much larger food items, and even performs micropredation on fish using toxins9,10.
Organisms of this species do not have an apparent use of the haptonema and exhibit a short haptonema and short
flagella moving with a ciliary beat.
The flow around an organism produced by its flagellar motion is important for all essential functions3. It
reveals information about swimming, power consumption, feeding currents, and exposure to flow-sensing predators11–
13. Idealized viscous flow models can be used to examine the hydrodynamics around a microswimmer3,14.
Models representing a swimmer just by a few point forces on the fluid are able to describe the flow far from the
organism11,15,16, whereas the flow close to the organism is poorly represented since such models fail to describe
the boundary conditions at the cell surface. Examples of models suited for the description of near cell flows are
the squirmer model used for ciliates17,18 and the Oseen model used for copepods and uniflagellates12,19–21. The
effect of different flagellar arrangements and beat patterns in biflagellates has previously been investigated with
1Technical University of Denmark, Department of Physics and Centre for Ocean Life, DK-2800 Kgs. Lyngby,
Denmark. 2Technical University of Denmark, National Institute of Aquatic Resources and Centre for Ocean Life, DK-
2920 Charlottenlund, Denmark. Correspondence and requests for materials should be addressed to T.K. (email: tk@
aqua.dtu.dk) or A.A. (email: email@example.com).
received: 05 August 2016
accepted: 29 November 2016
Published: 05 January 2017
Scientific Reports | 7:39892 | DOI: 10.1038/srep39892 1