2839
The Journal of Experimental Biology 209, 2839-2846
Published by The Company of Biologists 2006
doi:10.1242/jeb.02337
Like a ‘rolling stone’: quantitative analysis of the body movement and skeletal
dynamics of the sponge Tethya wilhelma
Michael Nickel
Department of Zoology, Biological Institute, Stuttgart University, 70550 Stuttgart, Germany
e-mail: [email protected]
Accepted 16 May 2006
Summary
Although sponges (Porifera) are basal Metazoa without
stability of the skeletal superstructure arrangement
muscles and a central nervous system, they are able to
during movement suggests that only the cortical tissue
is involved in movement, with only local tissue
locomote, which is generally correlated to drastic
rearrangements. The movement track followed a straight
morphological changes. This behaviour has been known
direction for long periods, but directions could be altered
for more almost 150 years, but it is only partly
instantly. It is most likely that environmental conditions
understood. The sponge T. wilhelma displays
extraordinary movement and rhythmic body contractions,
play an important roll in induction of movement. In
and is thus a valuable model for the investigation of
summary, T. wilhelma resembles the proverbial ‘rolling
stone’ that stays at a given location if the conditions are
sponge movement. The aims of the present study were to
favourable and starts moving when conditions change for
track T. wilhelma quantitatively on natural and artificial
the worse.
substrates, to test for a peristaltic movement mechanism
and to check for the influence of morphological changes.
T. wilhelma displays a unique mode of locomotion among
Supplementary material available online at
http://jeb.biologists.org/cgi/content/full/209/15/2839/DC1
sponges, without reorganizing the whole sponge body. The
overall morphology was stable, and skeletal rotation
during movement was shown; this is the first time that
Key words: Tethya wilhelma, Porifera, locomotion, behaviour,
plasticity, skeleton, rotation.
such movement has been demonstrated in a sponge. The
Introduction
Sponges are basal metazoa that evolved no muscles and no
central nervous system. However, sponges are capable of body
movement, which has been reported several times by various
authors (Carter, 1848; Lieberkühn, 1863; Noll, 1881; Arndt,
1941; Burton, 1948), to mention the most important early
works [for a complete review of early works, see Jones (Jones,
1962)]. Sponge movement has been discussed in the context
of integrative systems in sponges (Jones, 1962). The most
prominent cases of sponge movements are those reported for
Tethya sp. (Bond and Harris, 1988; Fishelson, 1981;
Hebbinghaus, 1996; Nickel and Brümmer, 2004; Sarà et al.,
2001) and Chondrilla sp. (Bond and Harris, 1988; Pronzato,
2004; Sidri, 2005).
A detailed investigation on several sponge species (Bond
and Harris, 1988) showed that sponge movement is a
consequence of organisational plasticity, mainly based on local
amoeboid movements of the cells in the attachment areas of
the sponge. Such a mechanism was suggested before (Jones,
1962), and confirmed in detail later by Bond, who proposed a
continuous anatomical rearrangement for sponges (Bond,
1992). In a generalized attempt, Gaino and coworkers
demonstrated that this organisational plasticity is of high
importance for the ecological success of sponges in general
(Gaino et al., 1995).
Early work (Edmondson, 1946) and later (Fishelson, 1981)
reported that species of the genus Tethya sp. showed
extraordinary motility. However, the movement mechanism
suggested by Fishelson, based on the contraction of body
extensions of Tethya sp. producing a pulling force, was
disproved by later authors (Bond and Harris, 1988; Nickel
and Brümmer, 2004). Recently I found a new species of
Tethya in the Zoological Garden Wilhelma, Stuttgart. The
species was described subsequently as T. wilhelma and has
proved a valid model sponge for work on movement (speeds
up to 2·mm·h–1), contraction and other related questions on
the coordination of these behaviours (Ellwanger et al., 2006;
Ellwanger and Nickel, 2006; Nickel, 2001; Nickel, 2004;
Nickel and Brümmer, 2004; Nickel et al., 2002). In the
present study the movement behaviour is analysed
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2840 M. Nickel
quantitatively for the first time, using digital time-lapse
imaging and quantitative image analysis. Since T. wilhelma
displays regular endogenous body contractions (Nickel,
2004), the question arises as to whether peristalsis or
contractile waves play a role in the movement of this sponge.
Bond and Harris reported that this mode of movement does
not occur in sponges (Bond and Harris, 1988); however, they
had not the technical ability to record and quantify the
contraction behaviour of Tethya sp. in relation to movement.
So this possibility was tested quantitatively in detail in the
present study. Since it has been stated that sponges move via
constant rearrangement of their body and skeleton, I tested,
whether this is also the case in T. wilhelma.
My results clearly show that Tethya sp. display a unique
mode of locomotion among sponges, without reorganizing
the sponge body. The overall morphology is stable during
movement, and for the first time, I demonstrate skeletal
rotation during movement. The movement track follows
straight directions for long periods, but directions can be
altered instantly. The factors inducing locomotion are still
unknown, though it can be stated that environmental conditions
play an important role. The underlying mechanism is
discussed. Overall, T. wilhelma resembles the proverbial
‘rolling stone’ that stays at a given location if the conditions
are favourable, and starts moving when conditions change for
the worse.
Materials and methods
Sponges
Specimens of the sponge Tethya wilhelma (Sarà, Nickel and
Brümmer 2001) (Tethyidae, Hadromerida, Demospongiae)
were obtained from the type locality in the aquarium of the
Zoological-Botanical Garden Wilhelma, Stuttgart, Germany
(Sarà et al., 2001). They were maintained in a 180·l aquarium
at 26°C, filled with running artificial seawater (Nickel and
Brümmer, 2003), under a light:dark cycle of 12·h:12·h.
Sponges were fed 4–5 times a week with suspended
commercial invertebrate food (Artificial Plancton, Aquakultur
Genzel, Fellbach, Germany, www.aquakultur-genzel.de), by
pipetting several ml of suspension to each sponge. Seawater
was changed at a rate of around 10% of the total aquarium
volume every 3–4 weeks.
Experimental settings
One moving specimen of T. wilhelma was imaged inside the
aquarium, settled on a natural substrate (dead coral). A second
moving specimen, settled on the plain glass bottom of a
1000·ml experimental reactor, was imaged from below. For
several days, the sponge was allowed to attach on the basal
optical glass plate of the reactor, which was placed inside the
aquarium. Subsequently, the reactor was taken out, and
connected to the aquarium to allow permanent flow-through of
aerated seawater. A black plastic disc was inserted into the
reactor above the sponge as a background, to allow proper
contrast-rich sub-basal imaging. A third moving specimen,
settled on a plastic substrate, was imaged inside a 250·ml
closed experimental reactor, which allowed a lateral view
(Ellwanger et al., 2006; Nickel, 2004). This reactor consisted
of an aerated experimental chamber, designed on the principles
of airlift reactors, connected to a temperature regulation
unit (F25, Julabo, Seelbach, Germany). Oxygen level and
temperature were monitored using a multi-sensor system (P4,
WTW, Weilheim, Germany), controlled by a computersoftware (MultiLab Pilot 3.0, WTW). A built-in optical glass
filter (Ø 49·mm, D.K. Enterprises, India) allowed proper
imaging from of a lateral view of the sponge.
Digital time-lapse imaging
Digital images of three sponge specimens were taken at a
resolution of 2048⫻1536 pixels at regular intervals of 3·min
(lateral), 5·min (sub-basal) and 30·min (aquarium). This
resulted in three image stacks representing three time series. A
Nikon Coolpix 990E digital camera in manual macro focus and
exposure mode was used to acquire greyscale images. The
camera was connected to a Nikon SB 24 flash unit, set to
manual mode (24·mm, output 1/16). The camera was
controlled by a PC, via USB and the software
DC_RemoteShutter V 2.3.0/V. 1.0 (Madson, 2003). A
reference image including a scale bar placed next to the sponge
was taken for each experimental series, to allow scaling. All
subsequent quantitative image analysis was performed using
ImageJ 1.30 to 1.34 (NIH, Washington, USA), based on built
in functions (Rasband, 1997-2006). For economy of computing
time, the image stacks were cropped to the relevant areas,
excluding background only.
Contraction and movement analysis
To trace the movement of T. wilhelma, a central trace point
within the sponge was defined by an image processing
algorithm, implemented in a macro using ImageJ build-in
functions. (1) For the image series on the natural substrate,
masks were manually created for each image in order to
eliminate the largest bright structures of the background, which
would otherwise interfere with the measurement. This was not
necessary for the two other datasets. (2) The 8-bit images were
converted into 2-bit images, applying a grey value threshold
between 100 and 175, resulting in discrimination between the
white sponge body and the dark background. (3) All internal
holes in the thresholded sponge area were filled automatically.
(4) Smaller bright particles in the background visible after
thresholding were eliminated by repeated erosion by one pixel,
followed by the same number of repeated dilations by one pixel,
with 10 repeats (natural substrate and sub-basal imaging) and
20 repeats (lateral imaging). (5) For the remaining area
representing the sponge body, the area size and the centre of
mass was determined and used as trace point. (6) To
compensate for fast position changes of peripheral buds, which
slightly affect the determined projected area and the trace point
position, a moving average of the trace point (Pt) was calculated
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Movement of the sponge T. wilhelma 2841
for the two datasets on artificial substrate according to the
eaquation:
⎛ xt ⎞
Pt(x,y) = ⎜ ⎟
⎝ yt ⎠
⎛ (xm+xm–n1+...+xm–ni+xm+n1+...+xm+ni) / (2ni+1)⎞
⎟,
=⎜
⎝ (ym+ym–n1+...+ym–ni+ym+n1+...+ym+ni) / (2ni+1)⎠
with xt, yt as calculated trace point coordinates and xm, ym as
measured coordinates for time point m; m–ni and m+ni are time
points represented by ni images before and after image at time
point m; 2ni+1 is the number of data points used for moving
average calculation for each trace point; practically 3, 5 and 7
data points were used.
For visual control, the trace points were plotted onto the
corresponding images and a movie of the time series was
created. For the movies, the image size was reduced to limit
the necessary memory capacity.
For all time periods in which the movement was straight and
parallel to one of the image axis, the movement speed was
calculated for each interval. The uniformity of movement was
checked using an ANOVA based on LSD (Least Significant
Difference) within the Excel add-on WinStat (Fitch, 2005).
(resulting in va=58·␮m·h–1). On a plastic substrate, one
specimen moved 3.103·mm within 1437·min (Fig.·1C,
supplementary material Movie S3), resulting in
va=130·␮m·h–1.
Plotting the central trace point movement (Fig.·2A) and
observing the time-lapse movies (supplementary material
Movies S1–S3), displays that the real distance covered by the
sponge is actually longer, since the movement is not strictly
straight. However, the position of the trace point shifts during
contraction due to asymmetric local contractions of the sponge
tissue that move over the sponge body (Fig.·2B, supplementary
material Movie S3) (see Nickel, 2004). Due to this
superposition of effects, in order to compensate for
contraction-based share of trace point movement, I calculated
a moving average for each of the trace point positions to
analyse the movement in detail (Fig.·3). On the natural
Angle analysis
For parts of the datasets, an angle analysis was performed,
which addressed changes of radial megasclere-bundles of the
skeleton. All angle changes were set in relation to a vertical
image axis. Using ImageJ, the central trace points were set in
relation to manually tracked marker points on the surface of
the sponge. These marker points were tubercles or the bases of
body extensions (Nickel and Brümmer, 2004; Sarà et al.,
2001). Connecting lines were projected between central trace
point a both marker points and the angle changes ␣ and ␤ were
measured by a macro based on build-in ImageJ functions. In
addition, for each dataset, the relative angle ␥ between the
marker points was calculated. For visual control, the
connecting lines were plotted onto the corresponding images
and a movie of the time series was created. For the movies, the
image size was reduced to limit the necessary memory
capacity.
Results
Movement patterns
On all three substrates tested here, T. wilhelma displayed a
continuous body dislocation. On a natural substrate (dead
coral) one specimen moved 3.321·mm within the recording
time of 1860·min (Fig.·1A, supplementary material Movie S1),
resulting in an average speed va=107·␮m·h–1. On a glass plate,
one specimen was followed for a total of 120·h (Fig.·1B,
supplementary material Movie S2). It displayed two major
movement periods, the first from t=0·min to t=2475·min with
6.536·mm distance (resulting in va=158·␮m·h–1), and the
second from t=2475·min to t=6855 with 6.703·mm distance
Fig.·1. The sponge Tethya wilhelma (A) on natural substrate, recorded
from above, (B) a glass plate, recorded from below, with indicated
directional change, and (C) on a plastic substrate, recorded from the
side. Black dots mark the sponge centre at t=0·min, white dots and
corresponding outlines mark the location of the sponge body after the
indicated times (min). Bars=5·mm; indicated axes correspond to
Fig.·2. The complete time-lapse series are displayed in supplementary
material Movies S1–S3.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2842 M. Nickel
Lateral movement: y-direction (mm)
3
2
7
t=7190 min
t=6855 min
6
5
t=4875 min
3
2
1
0
4
1
0
0
–1
1
B
2
3
4
5
6
7
8
9
10 11 12
t=1437 min
1
Lateral movement x-direction (mm)
t=0 min
1
0
360
720
1080
1440
90
80
70
60
50
7
6
5
4
3
2
1
0
3
2
1
0
360
720
1080 1440 1800 2160
C
70
t=0 min
60
0
–3
1800
B
t=2475 min
2
Baso-apical shift:
z-direction (mm)
A
3
–2
–1
0
Lateral movement: x-direction (mm)
Projected body area (mm2)
A
8
50
1
0
Fig.·2. Movement of the central body trace point of T. wilhelma.
(A) Sub-basal view, giving lateral movements in x- and y-direction,
corresponding to Fig.·1B and supplementary material Movie S2; note
the slight shifts due to contraction. (B) Lateral view, giving
movements in the x-direction and body shifts in the z-direction based
on contraction, corresponding to Fig.·1C and supplementary material
Movie S3. Time points are indicated in grey to allow comparison to
supplementary material Movies S2 and S3.
substrate, the movement of T. wilhelma can be subdivided in
three phases (Fig.·3A). A regression analysis of the average
speed va of the three phases and a statistical analysis of the
measured speed vm for each single measurement revealed
similar values: (1) from t=0·min to t=630·min with
va=60·␮m·h–1 (coefficient of correlation r2=0.9512) and
vm=67±73·␮m·h–1 (N=21); (2) from t=1230·min with
va=84·␮m·h–1 (r2=0.9818) and vm=91±69·␮m·h–1 (N=20); and
(3) from t=1230·min to t=1437·min with va=174·␮m·h–1
(r2=0.9896) and vm=154±82·␮m·h–1 (N=22). An ANOVA test
revealed a significant difference (P<0.05) for (3) vs (1) and (2),
while (1) and (2) are not significantly different.
A similar situation can be found for the first period of
movement on the glass substrate from t=0·min to t=2140·min,
which can also be subdivided in three phases: (1) from t=0·min
to t=550·min with va=186·␮m·h–1 (r2=0.9178) and
vm=184±214·␮m·h–1 (N=111); (2) from t=550·min to
t=975·min
with
va=24·␮m·h–1
(r2=0.1583)
and
–1
vm=40±285·␮m·h (N=84); and (3) from t=975·min to
t=2475·min
with
va=180·␮m·h–1
(r2=0.973)
and
–1
–2
–3
–4
0
360
720
1080
1440
Time (min)
Fig.·3. (A) Lateral movement of T. wilhelma on natural substrate
(Fig.·1A), displaying three movement phases; (B) Contraction
(projected body area) and lateral movement of T. wilhelma on a glass
plate (Fig.·1B), with three distinct movement phases; (C) Contraction
(projected body area) and lateral movement of T. wilhelma on a plastic
plate (Fig.·1C), with even movement. For average contraction speeds
and more details, refer to text.
vm=180±573·␮m·h–1 (N=300). For this experiment, an
ANOVA test revealed a significant difference (P<0.05) for (2)
vs (1) and (3), while (1) and (3) are not significantly different.
On the plastic substrate, the specimen moved more
uniformly during the recording from t=0·min to t=1440·min
with va=126·␮m·h–1 (r2=0.9708) and vm=130±587·␮m·h–1
(N=479). The high s.d. of vm in all cases is a result of the
contractions, which disturb the symmetry of the body due to
local contractions. Consequently, the trace point also shifts
during contraction.
In all experiments, the sponges were attached to the
substrate by long body extensions, which displayed dynamic
cellular movements (supplementary material Movies S2, S3)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Movement of the sponge T. wilhelma 2843
as well as stretching and shortening capability. In most cases
the extensions seemed to influence the direction or speed of
movement directly. However, in one case, it seemed that the
five attached extensions defined the movement area of the
sponge (supplementary material Movie S2).
Correlation of movement and contraction
In all three time-lapse recordings that I used for
quantification of the movement of T. wilhelma, the first
impression is that movement is correlated to contraction
(supplementary material Movies S1–S3). For the natural
substrate, the time interval ⌬t=30·min between the images
is too large to allow a proper analysis of sponge
contraction. However, for the glass and plastic substrate
experiments, with ⌬t=5·min and ⌬t=3·min respectively, the
movement can be put in relation to the endogenous
contractions. As stated before, local tissue contractions lead
to deformations of the sponge, which causes the trace point
to shift (compare supplementary material Movies S2, S3),
also displayed in Fig.·3B,C. Nevertheless, from Fig.·3B,C, it
is obvious that body movement is a continuous process not
correlated to contraction: on the glass plate, the trace point
moves 1.003·mm during the first 265·min and there is no
contraction occurring in this period (Fig.·3B). In nearly
all occasions of complete body expansion between the
regular contraction events, the trace point moves
continuously at a constant speed, as can be seen by comparing
the slope of the trace point graph and of the linear regressions
(Fig.·3B,C). The lateral view also clearly displays the
continuous movement during and inbetween contractions
(Fig.·2B).
Skeletal dynamics during movement and contraction
In both experiments on the artificial substrates, the timelapse movies display a rotation of the sponge body
(supplementary material Movies S4, S5). In addition I
observed large changes of internal angles between two surface
markers, like tubercles and body extensions (Fig.·4). For all
markers used, the underlying skeletal structures are strong,
relatively stiff skeletal superstructures, the megasclere bundles,
which expand radially from the skeletal centre of Tethya
species (Nickel et al., 2006; Sarà et al., 2001) (Nickel et al.,
2006b). For both experiments, relative angles between the
vertical image axis and connecting lines from the centre trace
point (TP) and the surface markers, TP–T1 (angle ␣) and
TP–T2 (angle ␤), were measured and angle changes (⌬␣/⌬␤)
were calculated. The same applied for the absolute angle ␥
between TP–T1 and TP–T2, as well as ⌬␥. On the glass plate,
the sponge rotated counterclockwise (as seen from below) on
the baso-apical z-axis (Fig.·4A,B; supplementary material
Movie S4). During the period between t=4850·min and
t=6950·min, I found ⌬␣=–26.3°, ⌬␤=–42.9° and ⌬␥=16.6°
(compare Fig.·5A). On the plastic substrate, the sponge rotated
counterclockwise (as seen from the side) on the lateral y-axis
(Fig.·4C,D; supplementary material Movie S5). During the
period between t=0·min and t=1437·min, I found ⌬␣=–18.1°,
Fig.·4. Changes of angles based on skeletal structures in T. wilhelma.
(A,B) Rotation on baso-apical axis: (A) 4875·min, (B) 6945·min.
(C,D) Rotation on lateral axis: (C) 0·min, (D) 1473·min;
Experimental times in correlation to time-lapse recordings given in
supplementary material Movies S2 and S3; TP, central trace point;
T1/T2, marker points. ␣: angle between vertical image axis and line
TP–T1; ␤, angle between vertical image axis and line TP–T2; ␥
internal angle between lines TP–T1 and TP–T2. Bars=5·mm. For
details on measured angles refer to text and see Fig.·5 and
supplementary material Movies S4 and S5.
⌬␤=–10.5° and ⌬␥=7.6° (compare Fig.·5B). During
contraction the angles change temporally up to 20°, which
again is an effect of local tissue contraction moving over the
body (Fig.·5A). However, like the body movement, changes of
the relative angles ␣ and ␤ are continuous in between
contractions. In contrast, the absolute angle ␥ between two
marker points seems to be influenced more strongly by
contractions, although it also changes slightly during times of
body expansion.
Discussion
The phenomenon of sponge movement was described in the
scientific literature as early as the mid 19th century (Carter,
1848). Although sponge movement was mentioned by several
authors in a number of publications (see above), it was not
addressed as a topic of its own before the work of Bond and
Harris (Bond and Harris, 1988), who first traced the path of the
moving sponge Chondrilla nucula on a glass plate and were
able to find average speeds between 40 and 160·␮m·h–1. The
present work is the first approach to trace sponge movement
quantitatively, using computed image analysis. This allows for
a detailed breakdown of the movement, which is barely
observable in real time, into defined time-steps. Consequently,
THE JOURNAL OF EXPERIMENTAL BIOLOGY
2844 M. Nickel
it is possible to correlate movement behaviour to contraction
behaviour and skeletal superstructure dynamics.
The movement speeds of T. wilhelma found here were
similar on all three substrates and covered a range of 24·␮m·h–1
to 186·␮m·h–1. This range is similar to the one reported for C.
nucula (Bond and Harris, 1988), but slower than the given
values of 1·mm·h–1 to 2·mm·h–1 for some Tethya species
(Fishelson, 1981; Hebbinghaus, 1996; Nickel and Brümmer,
2004). From own observations, it is confirmed that such a fast
movement can occur, but it is not very frequent. The movement
speed range observed here seems to be the usual range.
However, from aquarium observations over several years, as
well as from hundreds of time-lapse recording experiments in
the experimental reactor for contraction analysis, my
experience is that the chances of recording a moving T.
wilhelma specimen are quite low. The reason for this seems to
be that T. wilhelma mainly starts moving when environmental
changes take place. To a certain degree movement can be
induced by altering the position of a specimen inside the
aquarium, either by moving the whole substrate or by
A
Angles (degrees)
225
180
β
135
α
90
γ
45
4875
5235
5595
5955
6315
B
Projected body area (mm2)
90
80
70
60
50
6675
70
60
315
50
β
270
135
γ
90
α
45
0
0
360
720
Time (min)
1080
Fig.·5. Changes of angles based on skeletal structures in T. wilhelma over
time in relation to body contraction (projected body area). (A) Rotation
on baso-apical axis; (B) rotation on lateral axis. Angles are labelled as
defined in Fig.·4. For details refer to text and compare supplementary
material Movies S4 and S5.
detaching the sponge and thus forcing it to attach at a new side.
But even in the latter case, if the conditions do not change too
much, it is more likely to find the sponge attached without
subsequent movement. This is a fact that we utilize for
contraction analysis inside the experimental reactors, where the
specimens have to attach to a plastic substrate (Fig.·1C)
(Ellwanger et al., 2006; Ellwanger and Nickel, 2006; Nickel,
2004).
The tracing of the movement of T. wilhelma showed that:
the sponge is (1) able to move straight over long time-periods;
(2) able to change direction quite instantly. It is unknown how
the sponge coordinates this behaviour. However, T. wilhelma
is able to produce three different types of body extensions
(Nickel and Brümmer, 2004), of which the attached ones
might serve as ‘guide extensions’. Fishelson’s explanation
(Fishelson, 1981) that these extensions are the driving forces,
due to contraction based pulling mechanism, was later
disproved (Bond and Harris, 1988; Nickel, 2004). Amoeboid
movements of basal attached cells mediate the body movement
in Tethya species as well as all other sponges investigated
(Bond and Harris, 1988). Bond and Harris stated that the
body extensions are not necessary for movement in Tethya
species. My own aquarium observations second this.
Nevertheless, in most cases in general and in all cases
shown here, T. wilhelma displayed several long anchored
body extensions, which altered their appearance by
internal cell movements (compare supplementary material
Movies S1–S3) (see Nickel and Brümmer, 2004) and
stretching. From the present observations, especially the
path shown in Fig.·2A (and supplementary material Movie
S2), I conclude that the ‘guide extensions’ determine the
cruising radius of T. wilhelma. Taking into account that a
chemical messenger based integrative system plays a role
in the coordination of contractions (K. Ellwanger, A. Eich
and M. Nickel, manuscript submitted for publication)
(Ellwanger and Nickel, 2006), this may also be the case
for movement. Most likely a signal is created by the
anchoring extensions. The spreading of a signal gradient
and the superposition of several of these gradients could
determine the direction. In the case of C. nucula, it has
recently been shown that positive phototaxis can occur in
sponges (Pronzato, 2004). It is possible that the symbiotic
cyanobacteria of C. nucula are involved in sensing and
signalling. A possible candidate substance involved in the
regulation of directed movements might be cAMP, which
is involved in chemotactic regulation in Dictyostelium
(Lusche et al., 2005) and has been shown to be effective
upon sponge cell movement (Gaino and Magnino, 1996)
and contraction (Ellwanger and Nickel, 2006). However,
this will have to be proved in future experiments. In
addition, physical patterns of tension generated by the
sponge stretching on the substrate may also be part of the
coordination system in moving sponges (Bond and Harris,
1988).
The present experiments clearly show that contraction
is not involved in continuous body dislocation of T.
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Movement of the sponge T. wilhelma 2845
wilhelma, though contraction slightly alters the position of the
body. Hence, peristalsis or locomotory waves are not involved
in the movement.
It has been shown by several authors that continuous cell
movements rearrange the anatomy of sponges during
locomotion (Bond, 1992; Jones, 1962; Pronzato, 2004). Hence
it has been suggested that sponges are in constant morphogenesis
(Gaino et al., 1995; Pronzato, 2004; Sidri, 2005). In contrast
to the shape changes of most sponges during movement, T.
wilhelma retains its shape. The dynamics of the angles between
the megasclere bundles show that movement and contraction
affect the body morphology of T. wilhelma only temporally. The
movement of T. wilhelma is not amoeboid-like. The most
prominent alteration of the body structure is the rotation of the
whole skeleton, either on a baso-apical axis or even on a lateral
axis, which results in a slight rolling movement during body
dislocation. This is the first time that the rotation of a complete,
attached sponge body has been recorded. It is most likely that
lateral rotation is limited, since microtomographic investigations
have shown a certain degree of baso-lateral skeletal organisation
in Tethya minuta (Nickel et al., 2006a), even though the skeleton
is predominantly radial (Sarà, 2002; Sarà and Manara, 1991).
All the results confirm that morphogenetic changes in relation
to body movement in T. wilhelma are limited to the basal
attachment area and the anchoring body extensions. The
movement is directed, but the direction changes.
In the present work, I have shown that T. wilhelma displays
similar movement behaviours on natural and artificial
substrates that did not result in an overall morphological
rearrangement of the sponge body. Hence T. wilhelma behaves
like a proverbial ‘rolling stone’, stopping movement whenever
the environmental characteristics are favourable. The
ecological background of sponge movement has not been
addressed within this study. However, the mentioned aquarium
observations on T. wilhelma point towards a strong ecological
influence upon the movement behaviour. T. wilhelma, and
most likely all of the moving Tethya species, live in habitats
that are exposed to relatively rapid ecological changes, which
require special environmental adaptations (Sarà, 1997; Sarà,
2002; Sarà et al., 2001). In such environments (such as coral
reefs and lagoons) the ability of contraction and movement is
of obvious benefit (Sarà et al., 2001). It is likely that the
evolution of these peculiar and distinct contraction and
movement behaviours (1) were driven by the environmental
pressures existing in these kinds of habitats, and (2) favoured
the evolutionary success of the genus Tethya, consequently
resulting in a worldwide distribution of a large number of
species in different habitats, as has been reported by Sarà and
coworkers (Sarà, 1998; Sarà, 2002; Sarà and Burlando, 1994).
All these special characters and behaviours that have
evolved in the genus Tethya might be among the reasons for
the evolutionary, biogeographic and ecological success of this
particular sponge genus.
This publication is dedicated to Henry M. Reiswig
(Victoria, BC, Canada), in honour of his 70th birthday in 2006
and to acknowledge his great, inspiring contributions to
sponge science. I wish to thank H.-D. Görtz and F. Brümmer
for support, I. Koch and K.-U. Genzel for providing sponges,
and K. Ellwanger, I. Heim, C. Wolf and B. Nickel for
assistance and discussion. A part of this work was funded by
the German Federal Ministry of Education and Research
(BMBF) through project Centre of Excellence BIOTECmarin
(F 0345D).
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