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European Journal of Protistology 59 (2017) 6574

Motile behaviour of the free-living planktonic ciliate

Zoothamnium pelagicum (Ciliophora, Peritrichia)
Fernando Gmez
Carmen Campos Panisse 3, E-11500 Puerto de Santa Mara, 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 7075% in 33.2 ms with peak velocity up to 350 mm s1 . The contraction induced a forward jump of
12 mm that attained a peak speed of 110 mm s1 (250 pseudocolony lengths s1 ) 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

Peritrich ciliates are a highly diverse group with about one
thousand species (approximately 1/7 of all known ciliates).
They are an ecologically important in aquatic environments,
responsible for water clarification by bacterivory. Most ses-
silid peritrichs have a dimorphic life cycle that is temporally
dominated by a sessile, suspension-feeding trophont that
adheres to inanimate substrates or to aquatic organisms,
and a motile dispersal stage of brief duration, the telotroch
(Foissner et al., 1992; Lynn 2008).
E-mail address: fernando.gomez@fitoplancton.com
diverse genera of peritrichs (over 70 nominal species), char-
acterized by a colonial growth with individual cells (zooids)
connected by a common stalk. The core of the stalk is a con-
tinuous myoneme, known as the spasmoneme, and the entire
colony contracts as a single unit after the bend of the stalk into
a zigzag series of folded segments. Owing to the high speed
of stalk contraction, the species of Zoothamnium and other
peritrichs are among the fastest organisms with respect to
their body lengths (Jones et al. 1970; Moriyama et al. 1999;
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
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. Gmez / European Journal of Protistology 59 (2017) 6574
wide variety of pelagic organisms (Herman and Mihursky
1964), that may even suffocate the respiration of their ani-
mal hosts (Foster et al. 1978). Some species of Zoothamnium
may harbour bacteria in highly specific symbiosis (Bright
et al. 2014; Ott et al. 1998; Schuster and Bright 2016; Vopel
et al. 2002).
Zoothamnium pelagicum was first reported from the Bay of
Villefranche-sur-Mer, northwestern Mediterranean Sea (Du
Plessis 1891), where it was further described in detail (Laval
1968). A mature assemblage of Z. pelagicum is a pseudo-
colony composed of several colonies joined at the bases of
their stalks; therefore, it is essentially epibiotic on itself. It
shows a circular contour in which each colony constitutes a
fan-shaped branch that contributes to the overall radial sym-
metry of the entire assemblage. The telotrochs are produced
by binary fission of macrozooids. The telotroch glides along
the stalks before attaching near the basal ends of existing
colonies and develops into a full-fledged branch (colony)
by division of vegetative zooids (Laval 1968). Laval-Peuto
and Rassoulzadegan (1988) described a cyanobacterium as
an ectobiont on the zooids and stalk.
In the molecular phylogenies, Z. pelagicum branched
within a basal clade together with Z. alternans, Z. niveum
and Z. plumula (Clamp and Williams 2006; Ji et al. 2015;
Li et al. 2008; Sun et al. 2016). Zoothamnium pelagicum is
an exception when compared to its close relatives because
it is not attached to inanimate substrates nor is it epizoic. It
has developed a mechanism of locomotion to colonize the
pelagic realm as a free-floating organism.
The present study describes the observations of Z. pelag-
icum from several locations in the Mediterranean Sea and the
South Atlantic Ocean. For the first time, we present a study
of Z. pelagicum using high-speed video in an attempt to clar-
ify the details of its motile behaviour and the adaptation of a
peritrich ciliate to the planktonic life as a free-floating form.
Material and Methods
Live pseudocolonies were collected from four coastal sites
in the Mediterranean Sea in France and Spain (Marseilles,
Banyuls-sur-Mer, Villefranche-sur-Mer and Valencia) and
two sites in the South Atlantic Ocean off the coast of Brazil
(So Sebastio Channel and Ubatuba). Methods of collection
and observation were described in Gmez et al. (2016) and in
Appendix S1 (Supplementary data). Observations on motility
were based on pseudocolonies collected using a phytoplank-
ton net (20 m mesh size) and plankton net (80 m mesh size)
from the surface waters off Ubatuba (23 32 20.15 S; 45
5 58.94 W, 15 m depth). The live concentrate (20 m mesh
size) was examined in settling (Utermhl) chambers (26 mm
in diameter, 3 ml volume) with an inverted microscope Olym-
pus IX73 (Olympus Inc., Tokyo, Japan) and recorded with a
digital camera (Cyber-shot DSC-W300; Sony, Tokyo, Japan)
mounted on the microscopes eyepiece. The large plank-
ton concentrate (80 m mesh size) was examined in glass
dishes with a dissection microscope and recorded with same
digital camera. The pseudocolonies of Z. pelagicum were iso-
lated with a pipette and placed into glass dishes containing
filtered seawater taken from the sampling site (0.7 m nom-
inal pore-size glass fibre filter, Whatman GF/F). Additional
experiments were carried out by placing the pseudocolonies
in glass dishes with filtered seawater subsequently passed
through a Nuclepore polycarbonate filter (0.2 m pore size).
In other cases, supernatant water of microalgae cultures
(diatoms, dinoflagellates) was added to provide bacteria as a
food source. As a tracker to describe the flow field, we added
aliquots of the non-motile unicellular microalgae, Chlorella
sp., which is approximately 4 m in diameter and other neu-
trally buoyant detritus from the culture.
The contraction of the pseudocolony of Z. pelagicum
induces a forward displacement that is here referred to as
a jump. These features were too rapid to be observed with
the time resolution of ordinary video recordings [30 frames
per second (fps), 33 milliseconds (ms) between subsequent
frames]. A high-speed camera (Photron FASTCAM SA2
model 86K-C3, San Diego, USA) was available at the coastal
laboratory in late August 2015. The high-speed camera was
connected to the lateral port of the inverted microscope Olym-
pus IX73. The size of the field view of the high-speed camera
is inversely proportional to the recording rate. Initial tests
showed that the contraction of the pseudocolony lasted for
3 ms. A recording rate of 5000 fps (0.2 ms between sub-
sequent frames) provided more than 10 frames during the
contraction that were enough to characterize it. At this record-
ing rate, the entire expanded pseudocolony fit with field view
of the 10 magnification objective. The jump of the pseudo-
colony was recorded at 4 magnification.
By using an inverted microscope with ordinary objectives,
the focal plane is close to the bottom of the settling cham-
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
the front of the lens and to record the motile behaviour of
Z. pelagicum more distantly placed from the container walls.
The aim was to evaluate the incidence of possible a wall effect
comparing the speed values between this optical set-up sys-
tem and the inverted microscope. The pseudocolonies were
placed in a square quartz cuvette (10 mm side, 3.5 ml). A 40
extra-long working distance objective lens (Nikon ELWD
Plan Fluor 40) was attached to the high-speed camera.
The video recording rate was adjusted to 1500 fps (0.66 ms
between subsequent frames) because the field of view fit
with the size of the expanded pseudocolony of Z. pelagicum.
Some additional recordings at 2000 fps were done, but the
expanded pseudocolony did not fit completely in the field of
view. A lower recording rate will increase the field of view,
but the number of frames recorded during the contraction was
insufficient.
Swimming paths and speed values were calculated by over-
lapping the frames with different transparency levels and
plotting the positions of reference points with Adobe Pho-
 F. Gmez / European Journal of Protistology 59 (2017) 6574 67

Fig. 1. Light micrographs of Zoothamnium pelagicum from the NW Mediterranean Sea. (a) Marseilles. (b) Villefranche-sur-Mer. (cp)
Valencia. (a) Micro- and macrozooid pellicle covered by a bacteria. (b) Contracted pseudocolony. (ch) 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. (jk) A colony. (l) Macrozooid. (m) Microzooid. (np) Note the bacteria on the zooids and stalks. Bar = 50 m.

toshop CS3 (Adobe Systems Incorporated, San Jose, CA,
USA). Jump velocities were based on tracks that remained
in focus (pseudocolonies in lateral view), thus ensuring that
they were parallel to the focus plane.
Results
Morphology
Observations of Z. pelagicum in the NW Mediterranean
were scarce (Fig. 1ap). In contrast, Z. pelagicum was
more commonly recorded in the tropical waters off Brazil
(Fig. 2aw). Some pseudocolonies were composed of only
two opposed colonies (branches) (Fig. 1ch). The complete
pseudocolonies showed a lens-like shape up to 1.8 mm in
diameter (Fig. 2a). The colonies (branches) showed a radial
orientation and were joined at their proximal ends to the stalk
of other colonies. The ramification of each colony showed an
anisotomous pattern (Fig. 2b). If the circular contour was
altered because a radial branch (colony) was missing, the
space was covered by another colony that bent at its proximal
end. The core of the stalk, the spasmoneme, was a brilliant
grey homogenous mass that runs uninterrupted throughout
the entire colony, through the stalk and branches into each
individual zooid (Figs. 1 ik, 2 c). The spasmoneme was
absent in the proximal part of the colony. A dark area of
similar appearance to the spasmoneme was present at the
point where colonies attach to each other (Figs. 1 i, 2 c). The
cortex of the stalk was transparent and apparently flattened,
and it appeared to be a veil surrounding the spasmoneme
(Fig. 1jk).
The stalk connected three different types of zooids:
microzooids (trophic stage), macrozooids (which produce
telotrochs) and terminal zooids (Figs. 1 em, 2 ab). The
microzooids were inverted bell-shaped and distributed along
the entire branch. The stalks of microzooids in the periph-
ery of the colony often curved backwards. The macrozooids
were roundish to ellipsoidal and the number was variable,
often two cells in the mid-region of the colony (Figs. 1 de,
68 F. Gmez / European Journal of Protistology 59 (2017) 6574

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. (dg) Pseudocolony
contraction forming two semicircles. (hj) Contraction forming a triangle. (kn) Contraction of a pseudocolony with a damaged stalk in one
colony. (n) The inset shows the damaged branch. (or) Telotroch gliding along the stalks. (st) The arrows point the epizoic bacteria. (uv)
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 (ab, dn, u, w) and 50 m (c, ot, v).

2 d). A single terminal zooid was located in the tip of the
colony. The terminal zooids were more elongated and had a
longer stalk than the microzooids and protruded beyond the
rest of the pseudocolony (Fig. 1g). In the expanded condition,
the terminal zooids were located in front of the main plane
of the pseudocolony (Fig. 2a).
Epibiosis in Zoothamnium pelagicum
Due to the mechanism of colony growth, the telotroch of
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
glided along the stalks in the centre of the pseudocolony
exploring for an attachment site (Fig. 2or, see video S1 as
Supplementary data, https://youtu.be/Tank9iUBUcM).
The pseudocolonies of Z. pelagicum in the Mediterranean
Sea were usually covered by an apparently single type of
rod-shaped bacteria (Fig. 1a, np), while this epibiosis was
rare in the Brazilian pseudocolonies (Fig. 2st). As a gen-
eral trend, the pellicle of the macrozooids tended to be more
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. 1no).
The stalks of the Brazilian pseudocolonies of Z. pelagicum
were sometimes colonized by clusters of the benthic diatom
Licmophora (Fig. 2uv). Copepod larvae were sometimes
observed attached to the stalks (Fig. 2t, w).
Frequency of the pseudocolony contraction
The pseudocolony of Z. pelagicum remained in the
expanded condition, except during the short contractions.
 F. Gmez / European Journal of Protistology 59 (2017) 6574 69

Fig. 3. Time lapse of the contraction of Zoothamnium pelagicum. (ak) Pseudocolonies in frontal view. (lae) 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
zooids whipped towards the centre. The different colonies
of the pseudocolony contracted almost synchronically join-
ing the radial sections of a circle (Fig. 2dg) or exceptionally
showing a triangular shape during the contraction (Fig. 2hj).
There was a large variability in the frequency of the con-
tractions. In the plankton concentrate, the approach to an
object or the disturbance by a swimming organism triggered
the contraction. The pseudocolony remained contracted if
the external stimulus (threat) persisted (see video S1 as sup-
plementary data, https://youtu.be/Tank9iUBUcM). When the
contraction was triggered in one of the colonies, the thrust
pulled the stalk of the other colonies and induced the con-
traction of the entire pseudocolony. Accidentally, due to
the sample collection and manipulation, a colony (branch)
did not contract. A section of the stalk was damaged, the
colony remained attached by the cortex, but the continuity
of the spasmoneme was interrupted. The distal part of that
stalk contracted while its damaged section did not contract
(Fig. 2kn).
70 F. Gmez / European Journal of Protistology 59 (2017) 6574
Contractions were also observed in the absence of pertur-
bation. In order to the test the variability of the spontaneous
contractions, a freshly collected pseudocolony was alter-
natively placed in a glass dish filled with 0.2 m filtered
seawater (apparently bacteria-free) and in a glass dish filled
with supernatant water from microalgae cultures (apparently
bacteria-rich). The number of contractions was quantified
each minute during 10 min in undisturbed conditions and
when the pseudocolony did not reach the container bor-
ders. In the bacteria-free water, the number of contractions
ranged between 7 and 14 per minute (average value of
9.8), while between 7 and 25 min1 (average value of
16.0) when the pseudocolony was placed in bacteria-rich
water. The pseudocolony was subsequently placed in the
bacteria-free water and the number of contractions decreased
to 512 contractions min1 (average 9.1), and increased
to 617 contractions min1 (average values 12.0) in the
bacteria-rich water.
In the absence of external perturbations, successive high-
speed camera recordings of the same pseudocolony revealed
that contraction began in different colonies and zooids. The
terminal zooid did not play a dominant role in triggering the
spontaneous contractions. In the case of contractions induced
by external stimuli, it should be noted that the terminal zooid
of each colony protruded beyond the other zooids and con-
sequently is closer to the potential threat.
When several pseudocolonies of Z. pelagicum were placed
in the same glass dish, the contraction of a pseudocolony
induced the subsequent contraction of the surrounding pseu-
Fig. 4. Time lapse of the contraction and jump of Zoothamnium pelagicum in lateral view (ac). 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.
docolonies, even if the pseudocolonies were not in direct
contact. This suggested that a hydromechanical signal (vor-
ticity, fluid deformation and/or acceleration) initiated by
contraction of a pseudocolony was triggering the response
of the neighbour pseudocolonies (see video S1 as Supple-
mentary data, https://youtu.be/Tank9iUBUcM).
Contraction speed
The different steps of the pseudocolony contraction were
recorded from frames at intervals of 0.2 ms. The contrac-
tions of 20 recently collected pseudocolonies were recorded,
including successive contractions of the same pseudocolony.
The contraction was an all-or-nothing feature, and in no case
was incomplete or interrupted. In contrast, a new contrac-
tion may occur before the pseudocolony was fully expanded.
During the contraction, the expanded pseudocolony reduced
its diameter 7075% in 33.2 ms to form a bunch of zooids
(Figs. 2 dn, 3 ae, 1 y). Some colonies were able to
contract in 2.6 ms, but in all the observations the contrac-
tion of the entire pseudocolony lasted for 33.2 ms. This
resulted in a median velocity of the distal zooids of about
180 mm s1 . The overlapping of subsequent frames revealed
faster values in the second quarter after the onset of the con-
traction. The zooids of some colonies reached a peak speed of
350 mm s1 directed towards the centre of the pseudocolony
(Fig. 3b). The recordings with the extra-long distance objec-
tive at 1500 fps (0.66 ms between subsequent frames) showed
 F. Gmez / European Journal of Protistology 59 (2017) 6574
that the contraction occurred between 2.66 and 3.33 ms after
onset (Fig. 3fk, zae).
Jump speed
The contraction of a pseudocolony of Z. pelagicum from
a lens-like ramified configuration into an almost spherical
bunch of zooids induced a forward jump (from the con-
cave side). The expanded pseudocolony slowly moved with
its concave face in the front. When it touched an obstacle
such as the container walls, the pseudocolony jumped against
to glass wall and it was repelled backwards (see video S1
as Supplementary data, https://youtu.be/Tank9iUBUcM). In
inverted microscopy, a pseudocolony that settled in frontal
view jumped rapidly out from the focal plane and so the jump
speed could not be calculated. In order to measure the jump
speed, the trajectory of the pseudocolony must run parallel to
the optical plane. This was possible when the pseudocolony
was observed in lateral view (Fig. 4ac). These observa-
tions revealed that the mature pseudocolonies attained a
peak speed of 110 mm s1 at 5 ms after onset of contrac-
tion (2 ms after the formation of the bunch) (Fig. 4ab).
Due to the thrust, the pseudocolony displaced for 12 mm
before to begin the expansion. If the pseudocolony was
stressed or the perturbation persisted, the pseudocolony
carried out one or two consecutives cycles of contrac-
tion/expansion. The observations with the extra-long working
distance objective in a cuvette showed similar values and the
pseudocolonies jumped with peak speed up to 110 mm s1 .
When two pseudocolonies jumped in opposite directions, that
larger pseudocolony reached 110 mm s1 , while the smaller
pseudocolony attained 55 mm s1 . (Fig. 4c). When a pseu-
docolony touched the wall of the cuvette, the contraction
repelled it with a peak speed up to 50 mm s1 (see video
S1, https://youtu.be/Tank9iUBUcM).
Flow field
Aliquots of a non-motile unicellular microalga, Chlorella
sp. (4 m in diameter) and neutrally buoyant detritus from
the culture were added to observe the flow field induced by
the contraction and jump. During the contraction, the parti-
cles located in the front of the pseudocolony were directed
sideward. The particles located in the rear of the pseudo-
colony (convex face) were repelled backwards in a curved
path. The particles located in the periphery of the expanded
pseudocolony travelled behind it (Fig. 5). The mechanism
of locomotion resembled the power stroke of a medusa that
push out the water contained in the umbrella (see video S1,
https://youtu.be/Tank9iUBUcM).
71
Discussion
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 (0.21 m) are
less efficient than species specialized on larger food particles,
which restricts suspension feeding ciliates to environments
rich in bacteria (sediments, patches of dead organic mate-
rial), and excludes from the open ocean. Some examples
seem to contradict this hypothesis such as Z. pelagicum
and the consortium of Vorticella oceanica and the diatom
Chaetoceros coarctactus (Nagasawa and Warren 1996).
Several studies revealed that sessile ciliates have higher
filtration rates than their equivalent free-swimming coun-
terparts (Christensen-Dalsgaard and Fenchel 2003; Jonsson
et al. 2004). Zoothamnium pelagicum has the challenge to
colonize an oligotrophic environment with less prey abun-
dance, and the lower filtration rates associated with the
free-swimming forms. Species of Zoothamnium have colo-
nized pelagic waters as epizooties of swimming animal hosts
(Foster et al. 1978; Herman and Mihursky 1964). Zootham-
nium pelagicum is essentially epibiont on itself and it does not
depend on an unstable living substrate. In molecular phylo-
genies, Z. pelagicum, Z. plumula, Z. alternans and Z. niveum
formed a subclade basal to the other congeneric species and
Epistylis. Zoothamnium pelagicum is distantly related to the
known species of Zoothamnium attached to swimming ani-
mal hosts (Clamp and Williams 2006; Ji et al. 2015; Sun
et al. 2016). This may suggest that the ancestor of Z. pelag-
icum was not a Zoothamnium species that detached from
its animal host and adapted to pelagic life as a free-living
form. The close relatives of Z. pelagicum are species with
a single feather- or cup-shaped colony that live attached to
inanimate substrates. Zoothamnium alternans and especially
Z. niveum are heavily covered by high-specific ectosymbiotic
bacteria (Bauer-Nebelsick et al. 1996; Bright et al. 2014; Ji
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
Rassoulzadegan 1988), but this relationship is not obligate
since no symbiotic cyanobacteria were observed in most of
the pseudocolonies in this study. Zoothamnium pelagicum
was unable to prevent the fouling of a Licmophora species,
a diatom genus that is usually found as epibiont on macro-
phytes and pelagic animals (Takano 1983). The colonization
by diatoms may increase the risk of detection by visual preda-
tors. The effect on the locomotion is uncertain because the
presence of diatoms increase the drag during the contraction
and could favour the jump.
The locomotion of Z. pelagicum resembles the medusa
that moves by taking in water in its umbrella-shaped body
and push it out, like a jet propulsion. The umbrella of
72 F. Gmez / European Journal of Protistology 59 (2017) 6574
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
the water backwards. The branches (colonies) with a reg-
ular radial and dense arrangement and more synchronic
contraction are expected to be more efficient and to give
greater thrust after the contraction (Fig. 4c). In an iner-
tial (turbulent) regime, the configuration of the branches
of Z. pelagicum during the contraction favoured the back-
wards ejection of water, but inevitably water escaped among
the branches diminishing the efficiency (Fig. 5, see video
S1, https://youtu.be/Tank9iUBUcM). Flow is laminar when
Reynolds number (Re) is low (i.e. the fluid moves smoothly
around the cells and can be considered as moving in lay-
ers between which there is no significant mixing) and flow
is turbulent when Re is high (Koehl and Strickler 1981).
It can be expressed as Re = u L 1 where = density
of seawater (1023.5 kg m3 ), u = velocity, L = characteristic
length and = dynamic viscosity of seawater at 25 C
(0.95 103 kg m1 s1 ). The Reynold number is 8 for
a zooid of 40 m that moves at 200 mm s1 during the
stalk contraction, and Re is 54 during the jump of the
contracted pseudocolony (500 m in diameter and speed of
100 mm s1 ). The flow is laminar and the viscous forces pre-
dominated, especially during the contraction of Z. pelagicum.
The more porous nature of a pseudocolony versus the solid
tissue of the medusa umbrella might not make contraction
less efficient at these low Reynold numbers.
The locomotion of Z. pelagicum has the dual function of
predation avoidance and to exploit new patches of suspended
food particles and stir bacteria and direct them toward the
feeding zooids. Small predators are able to attach to the
branches of Z. pelagicum and consume the zooids one by
one (Fig. 2t, w). A large assemblage of a naked ciliate may
be tempting prey for the large pelagic predators. The trans-
parency and the slow movement of the pseudocolony may
reduce the predation, but other defence is needed when the
predator approaches. The contraction is triggered by differ-
ent zooids, but in case of a threat the terminal zooid that
protrudes beyond the pseudocolony may act as sentinel
in the front line. The observations of the rhythmic contrac-
tions of pseudocolonies that are not in direct contact suggests
that Z. pelagicum is able to perceive by a hydromechanical
signal in the surrounding waters (vorticity, fluid deforma-
tion and/or acceleration) that triggers the contraction and
jump (see video at https://youtu.be/Tank9iUBUcM). Then,
Zoothamnium pelagicum thus may be able to detect the water
disturbances due to the approaching predator. Several ciliates
produce a depolarizing mechanoreceptor potential whenever
the cell surface is stimulated mechanically (Deitmer 1992).
Short response latencies in ciliates are required to success-
fully escape from approaching predatory copepods (Gemmell
et al. 2015). Jakobsen (2001) determined that the ciliate Stro-
bilidium responds on average 0.62 mm away from the feeding
current of the approaching predator. Swimming protists such
as the dinoflagellates rarely exceeded speeds of 1 mm s1
(Jeong et al., 1999). The solitary ciliate Mesodinium rubrum
(= Myrionecta rubra) attains a velocity of 10 mm s1 after
10 ms and the length of jump is 0.16 mm (Fenchel and
Hansen 2006). The solitary ciliates Balanion comatum, Stro-
bilidium sp. and Mesodinium pulex have escape velocities
of 100140 body lengths s1 (Jakobsen 2001). The escap-
ing behaviour of Z. pelagicum consisted in a change of
shape with a reduction of the diameter 7075% in 3 ms.
The zooids moved towards the centre of the pseudocolony
up to 350 mm s1 . 5 ms after the onset of the contraction, the
pseudocolony attained a speed of 110 mm s1 and jumped
12 mm. The contracted pseudocolony (about 0.45 mm in
diameter) is escaping at 250 pseudocolony lengths s1 .
These values suggest that Z. pelagicum can escape with a
high success from predation.
The sessile peritrich ciliates comprise about 1000 species,
and only Z. pelagicum and the planktonic phase of Plan-
eticovorticella (Clamp and Coats 2000) proliferates in the
 F. Gmez / European Journal of Protistology 59 (2017) 6574
pelagic realm as free-living species. Zoothamnium pelagicum
is a model organism for biophysics. It could be a pioneer and
may constitute an evolutionary experiment evolved from a
sessile ancestor. The abundance and distribution of Z. pelag-
icum in the worlds oceans are probably underestimated
because this species is hardly recognizable from preserved
material. From live observations, the abundance of Z. pelag-
icum is low in the bottle samples and phytoplankton net tows.
It can be more frequently observed from the concentrates of
large mesh size plankton net tows following the method used
by crustacean or gelatinous plankton researchers, but they
pay little attention to other groups such as the ciliates.
Acknowledgements
This work was supported by Spanish Ministerio de Ciencia
y Tecnologa [contract JCI-2010-08492] and Brazilian Con-
selho Nacional de Desenvolvimento Cientfico e Tecnolgico
[grant number BJT 370646/2013-14]. This is a contribution
to the French ANR Biodiversity program (ANR BDIV 07
004-02 Aquaparadox). I thank R.M. Lopes for the loan of
the high-speed camera and J.R. Strickler for the advices in
use, and two Reviewers for theirs constructive comments.
Appendix A. Supplementary data
Supplementary data associated with this arti-
cle can be found, in the online version, at
http://dx.doi.org/10.1016/j.ejop.2017.03.004.
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