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European Journal of Protistology 59 (2017) 65–74

Motile behaviour of the free-living planktonic ciliate
Zoothamnium pelagicum (Ciliophora, Peritrichia)
Fernando Gómez
Carmen Campos Panisse 3, E-11500 Puerto de Santa María, Spain

Received 12 December 2016; received in revised form 15 March 2017; accepted 17 March 2017
Available online 23 March 2017

Abstract
Zoothamnium pelagicum is the only free-floating species among ∼1000 peritrich ciliates that develops its complete life cycle
in the open ocean. In the NW Mediterranean Sea, Z. pelagicum was usually associated with ectobiotic bacteria, while in the
South Atlantic Ocean was sometimes fouled by the diatom Licmophora. Each colony constituted a radial branch that joined
at its base with other colonies to form a lens-shaped pseudocolony of up to 400 zooids. The cilia beat slowly, propelling the
expanded pseudocolony in the direction of the concave face. Contraction was triggered by external stimuli (threat) or occurred
spontaneously. Frame-by-frame analyses of high-speed camera sequences revealed that during contraction the pseudocolony
reduced its diameter 70–75% in 3–3.2 ms with peak velocity up to 350 mm s−1 . The contraction induced a forward jump of
1–2 mm that attained a peak speed of 110 mm s−1 (∼250 pseudocolony lengths s−1 ) in 5 ms after onset. This medusa-like
locomotion at low Reynolds numbers allowed the pseudocolony to exploit new patches of food resources, as well as to escape
from predators. Zoothamnium pelagicum has been able to proliferate in the oligotrophic open ocean, while its sessile counterparts
are restricted to eutrophic environments.
© 2017 Elsevier GmbH. All rights reserved.

Keywords: Escape behaviour; Flow pattern; Peritrichous ciliates; Predator avoidance; Protist locomotion; Stalk contraction

Introduction The genus Zoothamnium is one of the largest and most
diverse genera of peritrichs (over 70 nominal species), char-
Peritrich ciliates are a highly diverse group with about one acterized by a colonial growth with individual cells (zooids)
thousand species (approximately 1/7 of all known ciliates). connected by a common stalk. The core of the stalk is a con-
They are an ecologically important in aquatic environments, tinuous myoneme, known as the spasmoneme, and the entire
responsible for water clarification by bacterivory. Most ses- colony contracts as a single unit after the bend of the stalk into
silid peritrichs have a dimorphic life cycle that is temporally a zigzag series of folded segments. Owing to the high speed
dominated by a sessile, suspension-feeding trophont that of stalk contraction, the species of Zoothamnium and other
adheres to inanimate substrates or to aquatic organisms, peritrichs are among the fastest organisms with respect to
and a motile dispersal stage of brief duration, the telotroch their body lengths (Jones et al. 1970; Moriyama et al. 1999;
(Foissner et al., 1992; Lynn 2008). Routledge and Amos 1977; Sugi 1960; Ueda 1954; Vopel
et al. 2002; Weis-Fogh and Amos 1972). The colonies of
many species of Zoothamnium are attached to aquatic plants
E-mail address: fernando.gomez@fitoplancton.com or inanimate substrates, but others are ectocommensal on a

http://dx.doi.org/10.1016/j.ejop.2017.03.004
0932-4739/© 2017 Elsevier GmbH. All rights reserved.
66 F. Gómez / European Journal of Protistology 59 (2017) 65–74

wide variety of pelagic organisms (Herman and Mihursky dishes with a dissection microscope and recorded with same
1964), that may even suffocate the respiration of their ani- digital camera. The pseudocolonies of Z. pelagicum were iso-
mal hosts (Foster et al. 1978). Some species of Zoothamnium lated with a pipette and placed into glass dishes containing
may harbour bacteria in highly specific symbiosis (Bright filtered seawater taken from the sampling site (∼0.7 ␮m nom-
et al. 2014; Ott et al. 1998; Schuster and Bright 2016; Vopel inal pore-size glass fibre filter, Whatman GF/F). Additional
et al. 2002). experiments were carried out by placing the pseudocolonies
Zoothamnium pelagicum was first reported from the Bay of in glass dishes with filtered seawater subsequently passed
Villefranche-sur-Mer, northwestern Mediterranean Sea (Du through a Nuclepore polycarbonate filter (0.2 ␮m pore size).
Plessis 1891), where it was further described in detail (Laval In other cases, supernatant water of microalgae cultures
1968). A mature assemblage of Z. pelagicum is a pseudo- (diatoms, dinoflagellates) was added to provide bacteria as a
colony composed of several colonies joined at the bases of food source. As a tracker to describe the flow field, we added
their stalks; therefore, it is essentially epibiotic on itself. It aliquots of the non-motile unicellular microalgae, Chlorella
shows a circular contour in which each colony constitutes a sp., which is approximately 4 ␮m in diameter and other neu-
fan-shaped branch that contributes to the overall radial sym- trally buoyant detritus from the culture.
metry of the entire assemblage. The telotrochs are produced The contraction of the pseudocolony of Z. pelagicum
by binary fission of macrozooids. The telotroch glides along induces a forward displacement that is here referred to as
the stalks before attaching near the basal ends of existing a jump. These features were too rapid to be observed with
colonies and develops into a full-fledged branch (colony) the time resolution of ordinary video recordings [30 frames
by division of vegetative zooids (Laval 1968). Laval-Peuto per second (fps), 33 milliseconds (ms) between subsequent
and Rassoulzadegan (1988) described a cyanobacterium as frames]. A high-speed camera (Photron FASTCAM SA2
an ectobiont on the zooids and stalk. model 86K-C3, San Diego, USA) was available at the coastal
In the molecular phylogenies, Z. pelagicum branched laboratory in late August 2015. The high-speed camera was
within a basal clade together with Z. alternans, Z. niveum connected to the lateral port of the inverted microscope Olym-
and Z. plumula (Clamp and Williams 2006; Ji et al. 2015; pus IX73. The size of the field view of the high-speed camera
Li et al. 2008; Sun et al. 2016). Zoothamnium pelagicum is is inversely proportional to the recording rate. Initial tests
an exception when compared to its close relatives because showed that the contraction of the pseudocolony lasted for
it is not attached to inanimate substrates nor is it epizoic. It 3 ms. A recording rate of 5000 fps (0.2 ms between sub-
has developed a mechanism of locomotion to colonize the sequent frames) provided more than 10 frames during the
pelagic realm as a free-floating organism. contraction that were enough to characterize it. At this record-
The present study describes the observations of Z. pelag- ing rate, the entire expanded pseudocolony fit with field view
icum from several locations in the Mediterranean Sea and the of the ×10 magnification objective. The jump of the pseudo-
South Atlantic Ocean. For the first time, we present a study colony was recorded at ×4 magnification.
of Z. pelagicum using high-speed video in an attempt to clar- By using an inverted microscope with ordinary objectives,
ify the details of its motile behaviour and the adaptation of a the focal plane is close to the bottom of the settling cham-
peritrich ciliate to the planktonic life as a free-floating form. ber, and a wall effect may influence on the observations. An
additional experimental set-up was used with a long working
distance objective. This allowed to focus further away from
Material and Methods the front of the lens and to record the motile behaviour of
Z. pelagicum more distantly placed from the container walls.
Live pseudocolonies were collected from four coastal sites The aim was to evaluate the incidence of possible a wall effect
in the Mediterranean Sea in France and Spain (Marseilles, comparing the speed values between this optical set-up sys-
Banyuls-sur-Mer, Villefranche-sur-Mer and Valencia) and tem and the inverted microscope. The pseudocolonies were
two sites in the South Atlantic Ocean off the coast of Brazil placed in a square quartz cuvette (10 mm side, 3.5 ml). A ×40
(São Sebastião Channel and Ubatuba). Methods of collection extra-long working distance objective lens (Nikon ELWD
and observation were described in Gómez et al. (2016) and in Plan Fluor 40×) was attached to the high-speed camera.
Appendix S1 (Supplementary data). Observations on motility The video recording rate was adjusted to 1500 fps (0.66 ms
were based on pseudocolonies collected using a phytoplank- between subsequent frames) because the field of view fit
ton net (20 ␮m mesh size) and plankton net (80 ␮m mesh size) with the size of the expanded pseudocolony of Z. pelagicum.
from the surface waters off Ubatuba (23◦ 32 20.15 S; 45◦ Some additional recordings at 2000 fps were done, but the
5 58.94 W, 15 m depth). The live concentrate (20 ␮m mesh expanded pseudocolony did not fit completely in the field of
size) was examined in settling (Utermöhl) chambers (26 mm view. A lower recording rate will increase the field of view,
in diameter, 3 ml volume) with an inverted microscope Olym- but the number of frames recorded during the contraction was
pus IX73 (Olympus Inc., Tokyo, Japan) and recorded with a insufficient.
digital camera (Cyber-shot DSC-W300; Sony, Tokyo, Japan) Swimming paths and speed values were calculated by over-
mounted on the microscope’s eyepiece. The large plank- lapping the frames with different transparency levels and
ton concentrate (80 ␮m mesh size) was examined in glass plotting the positions of reference points with Adobe Pho-
F. Gómez / European Journal of Protistology 59 (2017) 65–74 67

Fig. 1. Light micrographs of Zoothamnium pelagicum from the NW Mediterranean Sea. (a) Marseilles. (b) Villefranche-sur-Mer. (c–p)
Valencia. (a) Micro- and macrozooid pellicle covered by a bacteria. (b) Contracted pseudocolony. (c–h) Different phases of the pseudocolony
expansion. (e) Macrozoids. (f) Microzooids. (g) Terminal zooid. (h) Note the bacteria on the stalk and zooids. (i) Detail of the basal stalks of
several colonies. (j–k) A colony. (l) Macrozooid. (m) Microzooid. (n–p) Note the bacteria on the zooids and stalks. Bar = 50 ␮m.

toshop CS3 (Adobe Systems Incorporated, San Jose, CA, altered because a radial branch (colony) was missing, the
USA). Jump velocities were based on tracks that remained space was covered by another colony that bent at its proximal
in focus (pseudocolonies in lateral view), thus ensuring that end. The core of the stalk, the spasmoneme, was a brilliant
they were parallel to the focus plane. grey homogenous mass that runs uninterrupted throughout
the entire colony, through the stalk and branches into each
individual zooid (Figs. 1 i–k, 2 c). The spasmoneme was
Results absent in the proximal part of the colony. A dark area of
similar appearance to the spasmoneme was present at the
Morphology point where colonies attach to each other (Figs. 1 i, 2 c). The
cortex of the stalk was transparent and apparently flattened,
Observations of Z. pelagicum in the NW Mediterranean and it appeared to be a veil surrounding the spasmoneme
were scarce (Fig. 1a–p). In contrast, Z. pelagicum was (Fig. 1j–k).
more commonly recorded in the tropical waters off Brazil The stalk connected three different types of zooids:
(Fig. 2a–w). Some pseudocolonies were composed of only microzooids (trophic stage), macrozooids (which produce
two opposed colonies (branches) (Fig. 1c–h). The complete telotrochs) and terminal zooids (Figs. 1 e–m, 2 a–b). The
pseudocolonies showed a lens-like shape up to 1.8 mm in microzooids were inverted bell-shaped and distributed along
diameter (Fig. 2a). The colonies (branches) showed a radial the entire branch. The stalks of microzooids in the periph-
orientation and were joined at their proximal ends to the stalk ery of the colony often curved backwards. The macrozooids
of other colonies. The ramification of each colony showed an were roundish to ellipsoidal and the number was variable,
anisotomous pattern (Fig. 2b). If the circular contour was often two cells in the mid-region of the colony (Figs. 1 d–e,
68 F. Gómez / European Journal of Protistology 59 (2017) 65–74

Fig. 2. Light micrographs of Zoothamnium pelagicum from the South Atlantic Ocean. (a) The arrow and arrow head point the macrozooid and
the terminal zooid, respectively. (b) Detail of the distal ramification. (c) Detail of the ends of the stalks of several colonies. (d–g) Pseudocolony
contraction forming two semicircles. (h–j) Contraction forming a triangle. (k–n) Contraction of a pseudocolony with a damaged stalk in one
colony. (n) The inset shows the damaged branch. (o–r) Telotroch gliding along the stalks. (s–t) The arrows point the epizoic bacteria. (u–v)
The arrows point the clusters of the diatom Licmophora. (t, w) The arrowhead points the attached crustacean larva. Time (milliseconds) after
the contraction onset in the bottom corner. Bar = 500 ␮m (a–b, d–n, u, w) and 50 ␮m (c, o–t, v).

2 d). A single terminal zooid was located in the tip of the The pseudocolonies of Z. pelagicum in the Mediterranean
colony. The terminal zooids were more elongated and had a Sea were usually covered by an apparently single type of
longer stalk than the microzooids and protruded beyond the rod-shaped bacteria (Fig. 1a, n–p), while this epibiosis was
rest of the pseudocolony (Fig. 1g). In the expanded condition, rare in the Brazilian pseudocolonies (Fig. 2s–t). As a gen-
the terminal zooids were located in front of the main plane eral trend, the pellicle of the macrozooids tended to be more
of the pseudocolony (Fig. 2a). heavily fouled by bacteria than the microzooids (Fig. 1e,
h). The bacteria were mainly located in the posterior region
of the zooids and the distal ends of the stalks (Fig. 1n–o).
The stalks of the Brazilian pseudocolonies of Z. pelagicum
Epibiosis in Zoothamnium pelagicum were sometimes colonized by clusters of the benthic diatom
Licmophora (Fig. 2u–v). Copepod larvae were sometimes
Due to the mechanism of colony growth, the telotroch of observed attached to the stalks (Fig. 2t, w).
one colony may settle in the proximal end of the stalk of
another colony to develop a new colony. For that reason,
Z. pelagicum is essentially epibiotic on itself. The telotroch Frequency of the pseudocolony contraction
glided along the stalks in the centre of the pseudocolony
exploring for an attachment site (Fig. 2o–r, see video S1 as The pseudocolony of Z. pelagicum remained in the
Supplementary data, https://youtu.be/Tank9iUBUcM). expanded condition, except during the short contractions.
F. Gómez / European Journal of Protistology 59 (2017) 65–74 69

Fig. 3. Time lapse of the contraction of Zoothamnium pelagicum. (a–k) Pseudocolonies in frontal view. (l–ae) Pseudocolonies in lateral view.
(b) The positions of reference points are marked by coloured circles each 0.4 ms. Frame number in the upper right corner. Time (milliseconds)
after the contraction onset in the bottom corner. Frame number in the upper right corner. Bar = 500 ␮m.

The stalk bent in a zigzag conformation and the mass of plementary data, https://youtu.be/Tank9iUBUcM). When the
zooids whipped towards the centre. The different colonies contraction was triggered in one of the colonies, the thrust
of the pseudocolony contracted almost synchronically join- pulled the stalk of the other colonies and induced the con-
ing the radial sections of a circle (Fig. 2d–g) or exceptionally traction of the entire pseudocolony. Accidentally, due to
showing a triangular shape during the contraction (Fig. 2h–j). the sample collection and manipulation, a colony (branch)
There was a large variability in the frequency of the con- did not contract. A section of the stalk was damaged, the
tractions. In the plankton concentrate, the approach to an colony remained attached by the cortex, but the continuity
object or the disturbance by a swimming organism triggered of the spasmoneme was interrupted. The distal part of that
the contraction. The pseudocolony remained contracted if stalk contracted while its damaged section did not contract
the external stimulus (threat) persisted (see video S1 as sup- (Fig. 2k–n).
70 F. Gómez / European Journal of Protistology 59 (2017) 65–74

Contractions were also observed in the absence of pertur- docolonies, even if the pseudocolonies were not in direct
bation. In order to the test the variability of the spontaneous contact. This suggested that a hydromechanical signal (vor-
contractions, a freshly collected pseudocolony was alter- ticity, fluid deformation and/or acceleration) initiated by
natively placed in a glass dish filled with 0.2 ␮m filtered contraction of a pseudocolony was triggering the response
seawater (apparently bacteria-free) and in a glass dish filled of the neighbour pseudocolonies (see video S1 as Supple-
with supernatant water from microalgae cultures (apparently mentary data, https://youtu.be/Tank9iUBUcM).
bacteria-rich). The number of contractions was quantified
each minute during 10 min in undisturbed conditions and Contraction speed
when the pseudocolony did not reach the container bor-
ders. In the bacteria-free water, the number of contractions The different steps of the pseudocolony contraction were
ranged between 7 and 14 per minute (average value of recorded from frames at intervals of 0.2 ms. The contrac-
9.8), while between 7 and 25 min−1 (average value of tions of 20 recently collected pseudocolonies were recorded,
16.0) when the pseudocolony was placed in bacteria-rich including successive contractions of the same pseudocolony.
water. The pseudocolony was subsequently placed in the The contraction was an all-or-nothing feature, and in no case
bacteria-free water and the number of contractions decreased was incomplete or interrupted. In contrast, a new contrac-
to 5–12 contractions min−1 (average 9.1), and increased tion may occur before the pseudocolony was fully expanded.
to 6–17 contractions min−1 (average values 12.0) in the During the contraction, the expanded pseudocolony reduced
bacteria-rich water. its diameter 70–75% in 3–3.2 ms to form a bunch of zooids
In the absence of external perturbations, successive high- (Figs. 2 d–n, 3 a–e, 1 –y). Some colonies were able to
speed camera recordings of the same pseudocolony revealed contract in 2.6 ms, but in all the observations the contrac-
that contraction began in different colonies and zooids. The tion of the entire pseudocolony lasted for 3–3.2 ms. This
terminal zooid did not play a dominant role in triggering the resulted in a median velocity of the distal zooids of about
spontaneous contractions. In the case of contractions induced 180 mm s−1 . The overlapping of subsequent frames revealed
by external stimuli, it should be noted that the terminal zooid faster values in the second quarter after the onset of the con-
of each colony protruded beyond the other zooids and con- traction. The zooids of some colonies reached a peak speed of
sequently is closer to the potential threat. 350 mm s−1 directed towards the centre of the pseudocolony
When several pseudocolonies of Z. pelagicum were placed (Fig. 3b). The recordings with the extra-long distance objec-
in the same glass dish, the contraction of a pseudocolony tive at 1500 fps (0.66 ms between subsequent frames) showed
induced the subsequent contraction of the surrounding pseu-

Fig. 4. Time lapse of the contraction and jump of Zoothamnium pelagicum in lateral view (a–c). Swimming velocities (millimetres per second)
were recorded by plotting the positions after the overlay of the previous frame with transparency. Frame number in the upper right corner.
Bar = 500 ␮m.
F. Gómez / European Journal of Protistology 59 (2017) 65–74 71

that the contraction occurred between 2.66 and 3.33 ms after Discussion
onset (Fig. 3f–k, z–ae).
Nearly all peritrich ciliates inhabit eutrophic (bacteria-
rich) environments usually attached to substrates. Fenchel
(1980) concluded that suspension-feeding ciliates that
depend on particles of bacterial dimensions (0.2–1 ␮m) are
Jump speed less efficient than species specialized on larger food particles,
which restricts suspension feeding ciliates to environments
The contraction of a pseudocolony of Z. pelagicum from rich in bacteria (sediments, patches of dead organic mate-
a lens-like ramified configuration into an almost spherical rial), and excludes from the open ocean. Some examples
bunch of zooids induced a forward jump (from the con- seem to contradict this hypothesis such as Z. pelagicum
cave side). The expanded pseudocolony slowly moved with and the consortium of Vorticella oceanica and the diatom
its concave face in the front. When it touched an obstacle Chaetoceros coarctactus (Nagasawa and Warren 1996).
such as the container walls, the pseudocolony jumped against Several studies revealed that sessile ciliates have higher
to glass wall and it was repelled backwards (see video S1 filtration rates than their equivalent free-swimming coun-
as Supplementary data, https://youtu.be/Tank9iUBUcM). In terparts (Christensen-Dalsgaard and Fenchel 2003; Jonsson
inverted microscopy, a pseudocolony that settled in frontal et al. 2004). Zoothamnium pelagicum has the challenge to
view jumped rapidly out from the focal plane and so the jump colonize an oligotrophic environment with less prey abun-
speed could not be calculated. In order to measure the jump dance, and the lower filtration rates associated with the
speed, the trajectory of the pseudocolony must run parallel to free-swimming forms. Species of Zoothamnium have colo-
the optical plane. This was possible when the pseudocolony nized pelagic waters as epizooties of swimming animal hosts
was observed in lateral view (Fig. 4a–c). These observa- (Foster et al. 1978; Herman and Mihursky 1964). Zootham-
tions revealed that the mature pseudocolonies attained a nium pelagicum is essentially epibiont on itself and it does not
peak speed of 110 mm s−1 at 5 ms after onset of contrac- depend on an unstable living substrate. In molecular phylo-
tion (2 ms after the formation of the bunch) (Fig. 4a–b). genies, Z. pelagicum, Z. plumula, Z. alternans and Z. niveum
Due to the thrust, the pseudocolony displaced for 1–2 mm formed a subclade basal to the other congeneric species and
before to begin the expansion. If the pseudocolony was Epistylis. Zoothamnium pelagicum is distantly related to the
stressed or the perturbation persisted, the pseudocolony known species of Zoothamnium attached to swimming ani-
carried out one or two consecutives cycles of contrac- mal hosts (Clamp and Williams 2006; Ji et al. 2015; Sun
tion/expansion. The observations with the extra-long working et al. 2016). This may suggest that the ancestor of Z. pelag-
distance objective in a cuvette showed similar values and the icum was not a Zoothamnium species that detached from
pseudocolonies jumped with peak speed up to 110 mm s−1 . its animal host and adapted to pelagic life as a free-living
When two pseudocolonies jumped in opposite directions, that form. The close relatives of Z. pelagicum are species with
larger pseudocolony reached 110 mm s−1 , while the smaller a single feather- or cup-shaped colony that live attached to
pseudocolony attained 55 mm s−1 . (Fig. 4c). When a pseu- inanimate substrates. Zoothamnium alternans and especially
docolony touched the wall of the cuvette, the contraction Z. niveum are heavily covered by high-specific ectosymbiotic
repelled it with a peak speed up to 50 mm s−1 (see video bacteria (Bauer-Nebelsick et al. 1996; Bright et al. 2014; Ji
S1, https://youtu.be/Tank9iUBUcM). et al. 2006; Vopel et al. 2002). When compared to its benthic
relatives, Z. pelagicum showed the colonies (branches) with
a radial configuration to form a pseudocolony with circular
contour. Zoothamnium pelagicum can also be colonized by
cyanobacteria (Hausmann and Walz 2007; Laval-Peuto and
Flow field Rassoulzadegan 1988), but this relationship is not obligate
since no symbiotic cyanobacteria were observed in most of
Aliquots of a non-motile unicellular microalga, Chlorella the pseudocolonies in this study. Zoothamnium pelagicum
sp. (∼4 ␮m in diameter) and neutrally buoyant detritus from was unable to prevent the fouling of a Licmophora species,
the culture were added to observe the flow field induced by a diatom genus that is usually found as epibiont on macro-
the contraction and jump. During the contraction, the parti- phytes and pelagic animals (Takano 1983). The colonization
cles located in the front of the pseudocolony were directed by diatoms may increase the risk of detection by visual preda-
sideward. The particles located in the rear of the pseudo- tors. The effect on the locomotion is uncertain because the
colony (convex face) were repelled backwards in a curved presence of diatoms increase the drag during the contraction
path. The particles located in the periphery of the expanded and could favour the jump.
pseudocolony travelled behind it (Fig. 5). The mechanism The locomotion of Z. pelagicum resembles the medusa
of locomotion resembled the power stroke of a medusa that that moves by taking in water in its umbrella-shaped body
push out the water contained in the umbrella (see video S1, and push it out, like a jet propulsion. The umbrella of
https://youtu.be/Tank9iUBUcM).
72 F. Gómez / European Journal of Protistology 59 (2017) 65–74

Fig. 5. Flow pattern after the onset of the contraction of Zoothamnium pelagicum. Micrographs at intervals of two milliseconds. Coloured
circles corresponded to the position of a particle each five frames (1 ms). Flow field is represented by lines. The arrow heads indicate directions
of the vortex rotation. The frame number in the upper left corner. Bar = 500 ␮m.

a medusa is a solid tissue and the power stroke ejects ent zooids, but in case of a threat the terminal zooid that
the water backwards. The branches (colonies) with a reg- protrudes beyond the pseudocolony may act as ‘sentinel’
ular radial and dense arrangement and more synchronic in the front line. The observations of the rhythmic contrac-
contraction are expected to be more efficient and to give tions of pseudocolonies that are not in direct contact suggests
greater thrust after the contraction (Fig. 4c). In an iner- that Z. pelagicum is able to perceive by a hydromechanical
tial (turbulent) regime, the configuration of the branches signal in the surrounding waters (vorticity, fluid deforma-
of Z. pelagicum during the contraction favoured the back- tion and/or acceleration) that triggers the contraction and
wards ejection of water, but inevitably water escaped among jump (see video at https://youtu.be/Tank9iUBUcM). Then,
the branches diminishing the efficiency (Fig. 5, see video Zoothamnium pelagicum thus may be able to detect the water
S1, https://youtu.be/Tank9iUBUcM). Flow is laminar when disturbances due to the approaching predator. Several ciliates
Reynolds number (Re) is low (i.e. the fluid moves smoothly produce a depolarizing mechanoreceptor potential whenever
around the cells and can be considered as moving in lay- the cell surface is stimulated mechanically (Deitmer 1992).
ers between which there is no significant mixing) and flow Short response latencies in ciliates are required to success-
is turbulent when Re is high (Koehl and Strickler 1981). fully escape from approaching predatory copepods (Gemmell
It can be expressed as Re = ρ u L μ−1 where ␳ = density et al. 2015). Jakobsen (2001) determined that the ciliate Stro-
of seawater (1023.5 kg m−3 ), u = velocity, L = characteristic bilidium responds on average 0.62 mm away from the feeding
length and ␮ = dynamic viscosity of seawater at 25 ◦ C current of the approaching predator. Swimming protists such
(0.95 × 10−3 kg m−1 s−1 ). The Reynold number is ∼8 for as the dinoflagellates rarely exceeded speeds of 1 mm s−1
a zooid of 40 ␮m that moves at 200 mm s−1 during the (Jeong et al., 1999). The solitary ciliate Mesodinium rubrum
stalk contraction, and Re is ∼54 during the jump of the (= Myrionecta rubra) attains a velocity of 10 mm s−1 after
contracted pseudocolony (500 ␮m in diameter and speed of 10 ms and the length of jump is 0.16 mm (Fenchel and
100 mm s−1 ). The flow is laminar and the viscous forces pre- Hansen 2006). The solitary ciliates Balanion comatum, Stro-
dominated, especially during the contraction of Z. pelagicum. bilidium sp. and Mesodinium pulex have escape velocities
The more porous nature of a pseudocolony versus the solid of 100–140 body lengths s−1 (Jakobsen 2001). The escap-
tissue of the medusa umbrella might not make contraction ing behaviour of Z. pelagicum consisted in a change of
less efficient at these low Reynold numbers. shape with a reduction of the diameter 70–75% in 3 ms.
The locomotion of Z. pelagicum has the dual function of The zooids moved towards the centre of the pseudocolony
predation avoidance and to exploit new patches of suspended up to 350 mm s−1 . 5 ms after the onset of the contraction, the
food particles and stir bacteria and direct them toward the pseudocolony attained a speed of 110 mm s−1 and jumped
feeding zooids. Small predators are able to attach to the 1–2 mm. The contracted pseudocolony (about 0.45 mm in
branches of Z. pelagicum and consume the zooids one by diameter) is escaping at ∼250 pseudocolony lengths s−1 .
one (Fig. 2t, w). A large assemblage of a naked ciliate may These values suggest that Z. pelagicum can escape with a
be tempting prey for the large pelagic predators. The trans- high success from predation.
parency and the slow movement of the pseudocolony may The sessile peritrich ciliates comprise about 1000 species,
reduce the predation, but other defence is needed when the and only Z. pelagicum and the planktonic phase of Plan-
predator approaches. The contraction is triggered by differ- eticovorticella (Clamp and Coats 2000) proliferates in the
F. Gómez / European Journal of Protistology 59 (2017) 65–74 73

pelagic realm as free-living species. Zoothamnium pelagicum Du Plessis, G., 1891. Note sur un Zoothamnium pélagique inédit.
is a model organism for biophysics. It could be a pioneer and Zool. Anz. 14, 81–83.
may constitute an evolutionary experiment evolved from a Fenchel, T., 1980. Relation between particle size selection and
sessile ancestor. The abundance and distribution of Z. pelag- clearance in suspension-feeding ciliates. Limnol. Oceanogr. 25,
icum in the world’s oceans are probably underestimated 733–738.
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This work was supported by Spanish Ministerio de Ciencia Gómez, F., Qiu, D., Dodge, J.D., Lopes, R.M., Lin, S., 2016. Mor-
y Tecnología [contract JCI-2010-08492] and Brazilian Con- phological and molecular characterization of the dinoflagellate
selho Nacional de Desenvolvimento Científico e Tecnológico Ptychodiscus noctiluca revealed the polyphyletic nature of the
[grant number BJT 370646/2013-14]. This is a contribution order Ptychodiscales (Dinophyceae). J. Phycol. 52, 793–805.
to the French ANR Biodiversity program (ANR BDIV 07 Hausmann, K., Walz, B., 2007. Zoothamnium pelagicum: Ein ses-
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