58 E
. Jordana et al. J. Exp. Mar. Biol. Ecol. 252 2000 57 –74
suggest that through processes such as nutrition, this species affects the functioning of the coastal benthic ecosystem in this region.
As for all the other serpulids Jorgensen, 1966, D . arietina is a suspension feeder.
Therefore, through the benthic trophic network, one of its major impacts concerns the removal of particles from the water mass overlaying the sediment. Quantitative
information about the filtration and clearance rates in suspension-feeding polychaetes remains rather scarce. One commonly held belief is that this group of suspension-feeders
processes small water volumes and is generally less efficient than other suspension- feeding Dales, 1957. Consequently suspension-feeding polychaetes have more or less
been considered as organisms relying on environmental factors to get the energy they need Merz, 1984. More recently, the ecological role of suspension-feeding in
polychaetes has been demonstrated in some systems Merz, 1984; Davies et al., 1989; Riisgard et al., 1996. Moreover, suspension-feeding polychaetes are described as highly
efficient suspension-clearers, relying on very dilute food resources to live and grow Riisgard and Ivarsson, 1990. Laboratory experiments, especially those conducted to
assess physiological performances e.g. filtration, clearance, and oxygen consumption rates of suspension feeders, were often run on isolated specimens Shumway et al.,
1988; Riisgard and Ivarsson, 1990. Consequently, values measured generally corre- spond to the greatest performance rates of the organisms. Extrapolation of such values to
determine, for instance, the global feeding pressure of a natural population of worms requires knowledge of the average time actually spent feeding by each individual.
In suspension feeders, the intensity of feeding basically depends on filtering capacity and filtering activity i.e. time spent pumping; Foster-Smith, 1976. Such a parameter
sometimes may be affected by factors which that induce co-ordinated responses and even rhythm of activity Leonard, 1989; Sanford et al., 1994; Vedel et al., 1994; Achituv
and Yamaguchi, 1997; Thorin et al., 1998. The assessment of the feeding activity at different time scales and under various environmental conditions is thus essential for
extrapolating feeding rates clearance and ingestion rates to the field.
The aim of the present study is to describe the filtering activity of the serpulid Ditrupa arietina. This description is based on the utilisation of an automated video system that
tracks the opening of the gill fan e.g. indicating that worms were processing water. We looked i for temporal changes in the filtration behaviour of worms from different
populations, and ii at the effect of variations in environmental factors on the filtering activity.
2. Material and methods
2.1. The automated video system The automated video system was developed by one of us J.-C.D. to quantify various
activities of benthic epifauna. This tool permits automated image analysis of video images taken at the sediment surface. Briefly, it consists see Fig. 1 of a video sensor
composed of a charged coupled device CCD; type ICX059 AI from VLSI Vision Ltd. connected to an ADSP 2181 signal microprocessor, a memory board and an interface
E . Jordana et al. J. Exp. Mar. Biol. Ecol. 252 2000 57 –74
59
Fig. 1. The automated video system. A Basic set-up for the experiments. B Main components of the video sensor arrows represent image-analysis processing by the automated video system.
board. The microprocessor is driven by real-time routines uploaded in the permanent memory. These routines control picture acquisition frequency and run images analysis.
Images of the sediment surface are collected by the CCD and transferred to the video working memory of the microprocessor. In the present study, image analysis was
performed on a pixel-by-pixel basis and consisted of computing the differences in grey levels between an image recorded at a given time and a reference image corresponding
to no filtering activity i.e. worms withdrawn inside their tubes. These differences were then stored as numerical objects in the memory board. At the end of a recording session,
data were uploaded through the RS232 port of the interface board to a microcomputer where they were analysed using a set of post-treatment programs. These programs
allowed the recovery of all differences due to the activity of each worm, including when the worms were filtering.
This system was calibrated for the study of filtering activity of D . arietina. Method
validation was achieved by comparing the filtering activities measured using the automated video system with those observed by conventional video recordings. This
60 E
. Jordana et al. J. Exp. Mar. Biol. Ecol. 252 2000 57 –74
procedure showed that with a frame sampling frequency of 60 s, the automated video system was a convenient and suitable tool for studying the filtering activity in D
. arietina.
2.2. Biological material and experimental set-up Worms used during this work were collected by dredging 25 , depth , 30 m either
inside the bay of Banyuls-sur-Mer 428299235N, 3889500E or 20 km north of this bay in `
front of the city of Argeles-sur-Mer 428349607N, 3849847E. Back at the laboratory, worms were placed on a thin layer 2 mm of well-sorted fine sand in tanks length
L 3 width W 3 height H: 2 3 1 3 0.2 m supplied with running ambient sea water. All experiments conducted during this work, except those dedicated to the study of the
effect of hydrodynamics which involved the use of a recirculating flow tank, took place in an aquarium L 3 W 3 H: 60 3 40 3 20 cm filled with 30 l of filtered seawater 1.5
mm. Batches of either 12 or 15 worms were placed upright in a thick layer 10 cm of sand so that the tube openings were 1 cm above the sediment surface. Observations
made in the field and from undisturbed sediment cores sampled at the study sites showed that D
. arietina occurred either lying on or standing up in the sediment. The automated video system localised x, y coordinates in the picture and characterised time, duration
and size of the image modification any movement occurring inside the area of sediment covered by the video sensor. This process provides a rapid and convenient description of
the filtering activity of D . arietina.
2.3. Description of the filtering activity Standard filtration pattern i.e. in absence of any stimulus was characterized in
several experiments run at different periods of the year and on several groups of worms from different populations. We looked at filtration duration for each worm every hour to
determine if the filtering activity of Ditrupa arietina was either regular or irregular during a 24-h period. Worms in batches of 12 or 15 specimens were handled as described
in Section 2.2. and their filtering activity analysed by the automated video sensor during 24 h.
2.4. Monitoring of filtration activity 2.4.1. Comparison between populations
Two experimental time series were run on individuals originating from two different populations to assess whether there were temporal or spatial variations in filtering
activity. Each time series consisted of measurements once a month of filtering activity of one batch of 15 freshly collected worms. The two time series were run from October
1998 to September 1999 and, respectively involved worms collected in the bay of
` Banyuls-sur-Mer and off Argeles-sur-Mer. Worms were acclimated to laboratory
environment 24 h prior the beginning of the experiments. Each experiment lasted 5 h and was run at field temperature near-bottom water temperature was measured once a
week by using a CTD Seabird SBE 19. The experiments were run on specimens that
E . Jordana et al. J. Exp. Mar. Biol. Ecol. 252 2000 57 –74
61
were representative of the frequency size–distribution observed in the corresponding `
population. The population of Argeles-sur-Mer was dominated by large individuals with a mean tube length of 30 mm. The presence of epibiotics on the tubes and the absence of
significant increases in the mean length of the tubes during the entire time series suggested that the worms were in their second year of life Medernach and Gremare,
1998; Merdenach et al., 2000. The population in the bay of Banyuls-sur-Mer was exclusively comprised of young individuals ,1 year old with a mean tubes’ length of
22 mm. These tubes always remained clear of any epibiotics and their mean length steadily increased to reach a mean value of 27 mm by the end of the study. For the
Banyuls-sur-Mer population, the presence of oocytes in the coelomic cavity of 150 randomly collected worms was assessed fortnightly to determine whether the activity of
the gill-crown went through changes during the breeding season.
2.4.2. Effect of worm age Another time series was run during 1997 on a sub-population 428299379N, 3889632E
of the bay of Banyuls-sur-Mer. This sub-population presented was comprised exclusive- ly of 2-year-old individuals. The purpose of the experiment was to determine whether
and how the activity of the gill-crown was affected by worm age. Once a month, from March to December, the filtration activity of 12 worms freshly collected at the
corresponding station was measured by using the automated video system. The age of the population was assessed indirectly by measuring changes in worm density and the
mean individual dry weight.
2.5. Effects of environmental factors Preliminary studies on the filtering activity of D
. arietina i.e. observations made during the calibration and the validation of the automated video system showed the
existence of strong inter-individual variability. A conventional experimental plan based on replication was thus unsuitable to detect significant treatment effects. Therefore we
submitted batches of worms to the successive changes in the values of the test parameter and then used pairwise comparison tests to infer statistically the effect of each treatment
factor. The occurrence of rhythms, as well as synchronicity between individuals, in the filtering activity were checked using spectral analysis.
2.5.1. Effect of the presence of food 2.5.1.1. Experiment 1 Worms were collected on March 1997 within the bay of
Banyuls-sur-Mer. In the laboratory, worms were placed in an aquarium supplied with unfiltered running seawater. One experiment was carried out on: 0, 1, 3, 8, 10, 14, 16,
23, 35, 43, 52, and 58 days after worms collection. Each of these experiments consisted of determining the filtering activity of a batch of 12 worms that were successively
confronted with the absence i.e. filtered 1.2-mm seawater and then to the presence of food in the surrounding water. Confrontations lasted 5 h. The food, the flagellate
4 21
microphyte Dunaliella tertiolecta, was provided at a concentration of 1310 cells ml .
62 E
. Jordana et al. J. Exp. Mar. Biol. Ecol. 252 2000 57 –74
Changes in the filtering activity during the two periods were compared using Wilcoxon signed-rank tests.
2.5.1.2. Experiment 2 Experiments were run during June 1997 on worms from the bay `
of Banyuls-sur-Mer and during October 1997 on worms collected off of Argeles-sur-Mer to assess the effect of food concentration on filtering activity. Batches of 12 worms were
successively exposed to increasing concentrations of D . tertiolecta i.e. 0, 1000, 5000,
21
and 10 000 cells ml . During June, worms were exposed to each concentration for 8
versus 4 h in October. Friedman two-way analysis of variance was performed to detect significant changes in the filtering activity with increasing food concentrations. Signifi-
cant differences between matched samples were tested using Wilcoxon signed-rank tests.
3. Results
