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First published online July 20, 2006
Journal of Experimental Biology 209, 2839-2846 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02337

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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: michael.nickel{at}bio.uni-stuttgart.de

Accepted 16 May 2006

	Summary

TOP Summary Introduction Materials and methods Results Discussion References

 
Although sponges (Porifera) are basal Metazoa without muscles and a central nervous system, they are able to locomote, which is generally correlated to drastic morphological changes. This behaviour has been known for more almost 150 years, but it is only partly understood. The sponge T. wilhelma displays extraordinary movement and rhythmic body contractions, and is thus a valuable model for the investigation of sponge movement. The aims of the present study were to track T. wilhelma quantitatively on natural and artificial 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 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 such movement has been demonstrated in a sponge. The stability of the skeletal superstructure arrangement during movement suggests that only the cortical tissue is involved in movement, with only local tissue rearrangements. The movement track followed a straight direction for long periods, but directions could be altered instantly. It is most likely that environmental conditions play an important roll in induction of movement. In summary, 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.

Key words: Tethya wilhelma, Porifera, locomotion, behaviour, plasticity, skeleton, rotation

	Introduction

TOP Summary Introduction Materials and methods Results Discussion References

 
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 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

TOP Summary Introduction Materials and methods Results Discussion References

 
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 computer-software (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 2048x1536 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 (P_t) was calculated for the two datasets on artificial substrate according to the eaquation:

with x_t, y_t as calculated trace point coordinates and x_m, y_m as measured coordinates for time point m; m-n_i and m+n_i are time points represented by n_i images before and after image at time point m; 2n_i+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).

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 ß 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

TOP Summary Introduction Materials and methods Results Discussion References

 
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 v_a=107 µm 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 v_a=158 µm h^-1), and the second from t=2475 min to t=6855 with 6.703 mm distance (resulting in v_a=58 µm h^-1). On a plastic substrate, one specimen moved 3.103 mm within 1437 min (Fig. 1C, supplementary material Movie S3), resulting in v_a=130 µm h^-1.

View larger version (88K): [in this window] [in a new window]   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.

View larger version (32K): [in this window] [in a new window]   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.

View larger version (26K): [in this window] [in a new window]   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.

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 v_a=186 µm h^-1 (r²=0.9178) and v_m=184±214 µm h^-1 (N=111); (2) from t=550 min to t=975 min with v_a=24 µm h^-1 (r²=0.1583) and v_m=40±285 µm h^-1 (N=84); and (3) from t=975 min to t=2475 min with v_a=180 µm h^-1 (r²=0.973) and v_m=180±573 µm 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 v_a=126 µm h^-1 (r²=0.9708) and v_m=130±587 µm h^-1 (N=479). The high s.d. of v_m 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) 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 ß), were measured and angle changes (/ß) 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°, ß=-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°, ß=-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 ß 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.

View larger version (137K): [in this window] [in a new window]   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; ß, 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.

View larger version (51K): [in this window] [in a new window]   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.

	Discussion

TOP Summary Introduction Materials and methods Results Discussion References

 
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 µm 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, 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 µm h^-1 to 186 µm 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 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. 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.

	Acknowledgments

 
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).

	Footnotes

 
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/209/15/2839/DC1

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