L
Journal of Experimental Marine Biology and Ecology 244 (2000) 285–296
www.elsevier.nl / locate / jembe
Clearance capacity of Electra bellula (Bryozoa) in seagrass
meadows of Western Australia
*
Dennis Lisbjerg , Jens Kjerulf Petersen
National Environmental Research Institute, P.O. Box 358, Frederiksborgvej 399, DK-4000 Roskilde, Denmark
Received 15 December 1998; received in revised form 23 March 1999; accepted 6 October 1999
Abstract
Filtration rates were measured as the clearance of algal cells (Rhodomonas sp.) in the laboratory for the bryozoan Electra bellula (Hincks). The colony clearance rates were related to both total and specific (active) area of the colony, and a closer correlation was obtained when relating clearance to specific area. All results were therefore related to specific colony area. On average 49% of total colony area had active zooids. Clearance rates were measured at temperatures ranging from 16 to 248C. Maximum specific clearance rates (Fmax) were from the 2–3 replicates with the highest specific clearance rates out of 3–8 experiments performed with each colony. Fmaxvaried
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from 69 ml h cm at 168C to 107 ml h cm at 248C. Highest Fmaxof 115 ml h cm was 22
measured at 208C. Dry weight (DW) related to total area by WDW55.15 mg cm and ash-free
22 21 21 21 21
dry weight (AFDW) by WAFDW51.15 mg cm . Fmax59.5 l h g DW and 43 l h g AFDW at 228C. The clearance capacity of bryozoan communities in seagrass meadows of Western Australia is estimated by use of these results. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Bryozoans; Clearance rate; Electra bellula; Filtration rate; Temperature effect
1. Introduction
In coastal marine areas macro suspension-feeders such as ascidians, polychaetes, bivalves, and sponges form dense populations. Due to their large filtration capacity, these taxa may potentially process major parts of the water column on a daily basis in shallow areas and affect the levels of the phytoplankton and other suspended particles in the water column (e.g. Doering and Oviatt, 1986; Loo and Rosenberg, 1989; Petersen
*Corresponding author. Tel.: 145-46-301-295; fax: 145-46-301-211. E-mail address: [email protected] (D. Lisbjerg)
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and Riisgard, 1992; Cloern, 1996). Lemmens et al. (1996a) estimated the biomass and filtering capacity of several benthic groups in seagrass meadows of Western Australia, and concluded that ascidians and polychaetes are the two groups of macrofauna that contribute most to community filtering capacity. These groups have been studied further (Clapin, 1996; Lemmens et al., 1996b; Lemmens and Petersen, in prep.). Because of their minute size, epifauna such as bryozoans, spirobids, and cirripeds have often been neglected in community analysis assessing the flux between the water column and benthic communities. However, Lemmens et al. (1996a) found that small epifaunal suspension-feeders also contribute considerably to the total filtering capacity and especially bryozoans may be of significance.
Literature concerning the role of bryozoans in an ecological perspective is very limited. In the few early works by Menon (1974) and Bullivant (1968) experiments were performed in order to measure bryozoan filtration rates at different temperatures and different food concentrations. They obtained filtration rates measured as the clearance i.e. the reduction in the number of algae in a beaker containing a colony. In several later studies (e.g. Strathmann, 1982; Best and Thorpe, 1986, 1994; Sanderson et al., 1994;
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Riisgard and Manrıquez, 1997) pumping rates have been estimated from particle velocity within the lophophores and the cross-sectional area of the lophophores. Best and Thorpe (1983) calculated feeding rates by timing the frequency of pharynx emptying, assuming equal size of the bolus formed before emptying, and estimating the volume and number of cells the bolus contains.
In order to estimate the clearance capacity of bryozoans in ecological terms, individual clearance rate and population densities are needed, but also morphological and life cycle variations within the bryozoan group is important; all species are polymorphic to some extent, implying that some zooids within a colony might be specialized as e.g. some sort of defence organs (avicularia or vibracularia, spinozooids) ´ or involved in reproduction, forming distinct male / female zooids or ovicells (Silen, 1977). Because of this partitioning, only a part of the colony will contain actively feeding zooids. Also, in bryozoans, the feeding zooids perform a cycle of polypide regression (brown body formation) and regeneration, which is dependent on food availability (Bayer et al., 1994). Due to this cycling, an even lesser part of the colony may be actively feeding at any time and this must be addressed when estimating colony clearance capacity. In the present study clearance rate of a bryozoan species common to the seagrass meadows of the southern hemisphere is measured in order to elucidate bryozoan colony clearance as a function of temperature. Emphasis is on bryozoan clearance capacity and its ecological implications.
2. Materials and methods
2.1. Location and species
Electra bellula (Hincks) is an encrusting bryozoan species known throughout tropical
300mm long and 250mm wide with a lophophore of about 300mm high and 250mm in diameter with 10–12 tentacles.
Electra bellula was collected in Amphibolis sp. seagrass beds in Marmion lagoon,
Perth, Western Australia in a depth of 4–6 m of water. E. bellula live as epifauna on the leaves of the Amphibolis sp. but are more commonly found on the epiphyte Dictyopteris sp. Only colonies on Dictyopteris sp. were used. Under dissecting stereomicroscope, a piece of leaf containing one colony of E. bellula was cleaned of other epifauna and attached to a slide with cyanoacrylate glue.
The yearly water temperature amplitude in the region is between 16 and 248C (e.g.
Prata, 1989). During the study period (February–March 1997) the water temperature ranged between 22 and 248C. Animals attached to slides were placed in holding tanks at 228C prior to experiments.
2.2. Experiments
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Clearance experiments were measured as described by Petersen and Riisgard (1992). Twelve hours prior to experiments one or two colonies were placed in 250-ml beakers
containing filtered (1 mm) seawater in thermo-constant baths at 2260.28C.
Con-
centrations of the food source Rhodomonas sp. were measured using a Coulter Multisizer II particle counter with a 70-mm orifice. In the present study the formula used
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by Petersen and Riisgard (1992) was modified so as to give the area specific clearance rates (F ): F5V *ln (C /C ) /(A*t), where A is the area of the colony,t is time, V is the0 t
volume of the beaker and C and C the algae cell concentration at times 0 and t,0 t
respectively. In order to achieve maximum clearance rates, experiments were replicated 3 to 8 times with each beaker. For each beaker, the 2–3 replicates with the highest clearance rates were regarded as the colony potential, i.e. the maximum clearance rate (Fmax). This procedure excludes replicates in which feeding activity was lowered due to stress caused by handling or other disturbances in execution of the experiments. Returning of the subsamples after counting the algae cells on the Coulter Counter may influence the clearance rates of the bryozoan colonies. A change in zooid behaviour was noticed by Bullivant (1968), when subsamples from algae concentration analysis were returned to the beaker. The phenomenon has later been discussed (see Best and Thorpe, 1994), and may be due to the electric charge through the water during analysis. Such effects were also observed in this study in preliminary experiments, hence, subsamples were not returned. Instead an equal volume containing approximately the same algae concentrations were added. The difference in cell concentrations between the experimen-tal beaker and the volume added was taken into account when calculating the clearance rates.
The effects of water temperature were studied in a temperature range of 16 to 248C,
with 28C intervals (i.e. 16, 18, 20, 22 and 248C). Before experiments, the temperature was altered by two degrees every 2 days to allow the organisms to acclimatize. Initial
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algal cell concentrations varied between 1500 and 3000 cells ml . Sampling intervals
varied between 40 min at 168C, 30 min at 18 and 208C, and 20 min at 248C. Colony
are flat making accurate estimates of the areas of the encrusting E. bellula colonies possible. Photos of the colonies were taken with a Nikonos V 35-mm lens mounted with a 1:1 extension tube, using a flash directly behind the colonies. Measurements of colony areas were obtained on scanned pictures, using a computer. The guts of the active zooids could easily be distinguished by their red colour, resulting from the captured
Rhodomonas sp. From this, the specific areas were estimated. To relate area to weight,
areas of 36 colonies were measured. Under dissecting microscope these colonies were carefully scraped off the Dictyopteris sp. and weighed. Dry weight was measured after
.48 h in 60–708C, and ash-free dry weight after ashing at 4758C for a minimum of 4 h.
3. Results
At 228C, the maximum colony clearance rates (Fmax) as a function of total and
specific colony area are shown in Figs. 1 and 2. Fmaxvaried linearly with both total and specific area of the colony, but the correlation was more pronounced for the specific area
2 2
(r 50.95 versus r 50.81, n531). Fmax for the specific colony area was 105
Fig. 2. Electra bellula. Maximum clearance rate (Fmax) based on the specific area of the colony (active zooids) at 228C (n531).
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ml h cm . Fmax for the total area was 47% of this, which is in agreement with the
active / total area ratio given in Fig. 3 of 48% active zooids within colonies.
Wet weight (WW), dry weight (DW) and ash-free dry weight (AFDW) of 36 colonies were related to the colony area, total area and specific area. Correlations were higher for the total area of the colony (Table 1). Colony weight consists mainly of the calcified parts which are non-variable in the activity cycling performed by individual zooids. Change in weight due to activity variation is therefore minimal and a regression using the specific area does not enhance correlation between area and weight.
Based on the relation between area and Fmax and area and weight it is possible to
calculate the weight-specific clearance rate. For the total colony area Fmax at 228C was
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9.5 l h g DW, and 20 l h g DW (|90 l h g AFDW) if only the weight of
active zooids are considered. On the scanned pictures, the mean number of zooids per
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area was found to be 1265 zooids cm . Knowing the area of the active part of the
colony, the number of feeding zooids was estimated. Thus the clearance rate was
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calculated to 0.08 ml h zooid .
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Fmax for the specific colony area varied from 69 ml h cm at 168C to 107
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Fig. 3. Electra bellula. Relation between area of active part of colony (specific area) and total area (n531).
including 95% confidence intervals are shown in Fig. 4. The Q10 value from 16 to 248C is 1.7, whereas looking at the interval 16 to 208C Q10 is 3.6.
4. Discussion
‘Filtration rate’ is a widely used term, referring to the total water volume (volume per
Table 1
Electra bellula. Relation between weight and area of colonies
2
Weight r Number of
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(mg cm ) animals
Wet weight Total area 35.3 0.94 36
Specific area 70.2 0.49 29
Dry weight Total area 5.2 0.98 36
Specific area 10.1 0.49 29
Ash-free dry weight Total area 1.2 0.68 33
Fig. 4. Electra bellula. Maximum specific clearance rate (Fmax) as a function of temperature — 95% confidence intervals are indicated, n is the number of colonies.
unit time) processed in a filtering apparatus in order to catch particles. This can be found using an indirect method measuring the clearance of particles (Coughlan, 1969). The clearance rate is calculated based on the change in particle concentration in a given volume of water. The filtration rate is then the volume of water that has been cleared for particles assuming 100% retention efficiency (RE) of the filtering apparatus (e.g. de
˚ ˚
Villiers et al., 1989; Menon, 1974; Petersen and Riisgard, 1992; Riisgard et al., 1993). ‘Pumping rate’ (Q ) is used to emphasize filtration rates based on the total water volume passing through the filter (Coughlan, 1969) regardless of the amount of particles being retained. Q is found by direct methods estimating the water velocity and the size of the
´ ˚
filtering apparatus (e.g. Fiala-Medioni, 1978; Best and Thorpe, 1986; Riisgard and ´
Manrıquez, 1997) or by mounting a tube directly to the organism (Gerrodette and Flechsig, 1979). The relation between clearance rate and pumping rate can be described
as: F5Q3RE. E.g. ascidians retain 100% of the particles larger than the openings in
the gill sac and rates of clearance and pumping are similar. However, in bryozoans the retention efficiency is a combination of the retention efficiency of the laterofrontal cilia (RE ) and the retention efficiency of the tentacle crown (RE ), thus Flfc t 5Q3RElfc3
˚
forming a row on each side of the tentacles. The spacing between tentacles increases with the distance from the mouth region, making the lophophore filter an open structure. In water pumped through the lophophore filter, particles larger than |5mm are retained
maximally by the laterofrontal cilia but are able to pass through the gaps between the
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tentacles. Riisgard and Manrıquez (1997) found a RE of approximately 25% byt
comparing pumping rates based on the speed of algae through the lophophore with clearance rates of 6-mm particles of Electra pilosa assuming a RElfc of 100%. Assuming
that a RE of 25% also applies for E. bellula, the pumping rate would be 0.33 mlt
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˚ ´
h zooid , which is within the range found by Riisgard and Manrıquez (1997) for 15
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bryozoan species of different size, with pumping rates varying from 0.14 ml h zooid
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to 7.49 ml h zooid . Riisgard and Manrıquez (1997) also reported a correlation of
pumping rate as a function of total tentacle length of the lophophore. Based on their
correlation and a tentacle length of |250mm for E. bellula, the pumping rate for E.
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bellula should be 0.31 ml h zooid which is well in agreement with the estimated
values from this study.
In a community analysis, the ability of removing particles out of the water column is comparable, when looking at the clearance capacity amongst different suspension-feeder groups. Lemmens et al. (1996a) assessed the ecological importance of suspension-feeders in seagrass meadows in Western Australia. Determining biomass distribution and quantity and using literature values for clearance rates they estimated population clearance capacity. For the bryozoan group, the clearance rate of a temperate species,
Alcyonidium gelatinosum, was used (Best and Thorpe, 1986). Based on the clearance
rate of Electra bellula it is possible to recalculate these estimates using a tropic species common to the area. Lemmens et al. (1996a) found the biomass of bryozoans in 3
Posidonia and Amphibolis seagrass meadows to be 85.5639.0 and 208.1627.0 10
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zooids m , respectively. If E. bellula is considered representative for all bryozoans, and applying the clearance rate (at 228C) and active / total area ratio found in this study, the
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clearance capacity of bryozoans is estimated to be 80 l d m in the Posidonia
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meadows, compared to 2000 l d m estimated by Lemmens et al. (1996a). The
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clearance estimate in the Amphibolis meadows would be 195 l d m compared with
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5000 l d m (Lemmens et al., 1996a) which is 25 times higher. The estimates in this
study are based on 48% of the zooids being active, which was not taken into account in the previous estimates. The filtration rate of A. gelatinosum estimated by Best and Thorpe (1986) is referred to as clearance rate in their study. It is a rough estimate based on the velocity of particles within the lophophore and therefore corresponds with the pumping rate of other studies. So, in order to compare the two estimates of clearance
˚
capacity, those of A. gelatinosum should be 75% less, using the RE found by Riisgardt
´
and Manrıquez (1997). However, a major part of the difference is probably due to the fact that the zooids of different bryozoan species can vary considerably in size, so that, the clearance rate per zooid varies substantially.
Consequently, by extrapolating clearance rates of the much larger species like A.
gelatinosum will result in a considerable overestimate of the clearance capacity for an
average bryozoan community. To overcome the error in estimating clearance capacity due to zooid size differences, the linear relationship between pumping rate and length of
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be applied. However, to obtain the necessary data would be a tedious work. Another approach would be to collect population densities as weight of colonies. The small zooids of Electra bellula have a lower clearance rate per zooid than species in previous works, but this variation is not as pronounced when comparing the clearance rates of the species by weight (Table 2). The clearance rate of active zooids in E. bellula is 40% less than that of Zoobotryon verticillatum when comparing clearance rate per unit dry weight whereas it is 78% less at the zooid level. Extrapolation community clearance capacity from the weight specific clearance rate of one species is therefore a better estimate than using zooid specific clearance rate.
2
Lemmens et al. (1996a) found 0.4 g AFDW m of bryozoans in Posidonia meadows
22
and 0.6 g AFDW m in Heterozostera meadows in Cockburn Sound. Using the Fmax of
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Electra bellula (1030 l d g AFDW for the total colony area) the clearance capacity
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of bryozoans in the two meadows is estimated to be 410 l d m and 620 l d m
respectively. In Posidonia meadows, the clearance by bryozoans is small compared to the ascidians and amphipods, while filtering organisms are generally lacking in the
Heterozostera meadows, and the bryozoans are one of the most dominant filtering taxa
in these areas.
According to Winston (1978) Electra bellula feeding behaviour is characterised by the formation of temporary clusters. The first zooids to extend their lophophores are soon followed by their neighbours, so that actively feeding clusters can be identified throughout the colony. After withdrawal of all lophophores, new zooids will be the first to re-extend their lophophores, and new clusters will form. Thus, at any time only a fraction of the colony will be feeding. This behaviour may explain how mat-forming colonies separate the inflowing water from the outflowing (filtered) water. A small colony may be able to form a single cluster by this behaviour, where all zooids are feeding simultaneously. In a larger colony it would appear by looking at the gut content, that many zooids have been feeding, but at any time only a fraction is actively filtering. Thus, when calculating the clearance rates based on actively feeding areas (i.e. ‘specific’ area), the clearance rates are expected to be less for large than for small colonies. However the present data do not confirm this (runs test for randomness in residuals of regression in Fig. 2). Most of the colonies had areas with non-feeding zooids,
Table 2
Clearance rates for different species of Bryozoa in previous studies and present work, where clearance has been measured as the decline in algae concentration
Species Filtration rate Filtration rate Temperature Source
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(ml h zooid ) (ml h g DW) (8C)
Zoobotryon verticillatum 0.368 33.7 23–25 Bullivant (1968) a
Conopeum reticulum 0.458 nd 22 Menon (1974)
Electra pilosa 0.389 nd 22 Menon (1974)
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Electra pilosa 0.28 nd 18 Riisgard and Goldson (1997)
˚ ´
Celleporella hyalina 0.17 nd 20 Riisgard and Manrıquez (1997)
Electra crustulenta 0.23 24.7 22 Unpublished
Electra bellula 0.08 20.0 22 Present study
a
Table 3
Calculation of Q10for different bryozoan species
Species Q10 Temperature Based on
interval (8C)
Electra pilosa 1.5 6–22 Menon (1974)
Conopeum reticulum 1.5 6–22 Menon (1974)
˚ ´
Celleporella hyalina 1.4 10–20 Riisgard and Manrıquez (1997)
Electra crustulenta 1.8 6–22 Unpublished
Electra bellula 3.6 16–20 Present study
Electra bellula 1.7 16–24 Present study
characterised by their brown body formation as distinguished on the photos. The gaps created by these inactive zooids might be sufficient for the remainder to be active at all times. The overall activity level of E. bellula colonies lies around 50% (Fig. 3), which is similar to E. pilosa colonies showing an overall activity of 41% (Bayer and Todd, 1996).
Clearance rates were found to increase with increasing temperature (Fig. 4), and thus reached a maximum in the summer months. At the average summer temperature of 228C, Fmax was found to be lower than at 208C. This implies that Electra bellula either
exists at suboptimal conditions during summer or that Fmax at 208C needs to be more
firmly established. Also, a Q10value of 3.6 (16–208C) is high when comparing with Q10
values for clearance rates of other bryozoan species (Table 3). These Q10 values have
been calculated based on previous studies and are in accordance with Q10 values of
macro ciliary suspension-feeders like ascidians, bivalves and polychaetes (e.g. Jørgensen
˚
et al., 1990; Riisgard and Ivarsson, 1990; Petersen et al., 1999), though a higher Q10 has
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been estimated for a marine sponge (Q1054.3 in Riisgard et al., 1993).
When considering the present results, population densities of zooids per area and clearance rates of single zooids are not easily extrapolated to colony clearance due to zooid cycling and other conditions limiting the number of active zooids within the colonies. Also, results of single zooid clearance rates are difficult to extrapolate to larger scale due to the considerable variation in zooid size between species. Using population densities based on dry or ash-free dry weight may provide more reliable estimates of community clearance capacity, especially when clearance capacity is calculated while largely ignoring species composition.
Acknowledgements
Karen Bille Hansen (Zoological Museum, University of Copenhagen) for help with
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identifying the bryozoan species. Dr. Bent Vismann and Dr. Hans Ulrik Riisgard are acknowledged for constructive criticism of the manuscript. [SS]
References
Bayer, M.M., Todd, C.D., 1996. Effect of polypide regression and other parameters in colony growth in the cheilostomate Electra pilosa (L.). In: Gordon, D.P., Smith, A.M., Grant-Mackie, J.A. (Eds.), Bryozoans in Space and Time, NIWA, Wellington, NZ, pp. 29–38.
Bayer, M.M., Cormack, R.M., Todd, C.D., 1994. Influence of food concentration on polypide regression in the marine bryozoan Electra pilosa (L.) (Bryozoa: Cheilostomata). J. Exp. Mar. Biol. Ecol. 178, 35–50. Best, M.A., Thorpe, J.P., 1994. Particle size, clearance rate and feeding efficiency in marine bryozoa. In:
Hayward, P.J., Ryland, J.S., Taylor, P. (Eds.), Biology and Palaeobiology of Bryozoans, Olsen and Olsen, Fredensborg, Denmark, pp. 9–14.
Best, M.A., Thorpe, J.P., 1986. Effects of food particle concentration on feeding current velocity in six species af marine Bryozoa. Mar. Biol. 93 (2), 255–263.
Best, M.A., Thorpe, J.P., 1983. Effects of particle concentration on clearance rate and feeding current velocity in the marine bryozoan Flustrellidra hispida. Mar. Biol. 77, 85–92.
Bullivant, J.S., 1968. The rate of feeding of the bryozoan, Zoobotryon verticillatum. N.Z. J. Mar. Fresh. Res. 2, 111–134.
Clapin, G., 1996. The filtration rate, oxygen consumption and biomass of the introduced polychaete Sabella spallanzanii within Cockburn Sound. Honours Thesis. Edith Cowan University, Joondalup, Australia, 90 pp.
Cloern, J.E., 1996. Phytoplankton bloom dynamics in coastal ecosystems. A review with some general lessons from sustained investigation of San Francisco Bay, California. Rev. Geophys. 34, 127–168.
Coughlan, J., 1969. The estimation of filtering rate from the clearance of suspensions. Mar. Biol. 2, 356–358. de Villiers, C.J., Allanson, B.R., Hodgson, A.N., 1989. The effect of temperature on the filtration rate of Solen
cylindraceus (Hanley) (Mollusca: Bivalvia). S. Afr. J. Zool. 24 (1), 11–17.
Doering, P.H., Oviatt, C.A., 1986. Application of filtration rate models to field populations of bivalves: an assessment using experimental mesocosms. Mar. Ecol. Prog. Ser. 31, 265–275.
´
Fiala-Medioni, A., 1978. Filter-feeding ethology of benthic invertebrates (ascidians) IV. Pumping rate, filtration rate, filtration efficiency. Mar. Biol. 48, 243–249.
Gerrodette, T., Flechsig, A.O., 1979. Sediment-induced reproduction in the pumping rate of the tropical sponge Verongia lacunosa. Mar. Biol. 55, 103–110.
˚
Jørgensen, C.B., Larsen, P.S., Riisgard, H.U., 1990. Effects of the temperature on the mussel pump. Mar. Ecol. Prog. Ser. 45, 205–216.
Lemmens, J.W.T.J., Petersen, J.K., in prep. Filtration rate of ascidians from SW Australia. Mar. Fresh. Res. Lemmens, J.W.T.J., Clapin, G., Lavery, P., Cary, J., 1996a. Filtering capacity of seagrass meadows and other
habitats of Cockburn Sound, Western Australia. Mar. Ecol. Prog. Ser. 143, 187–200.
Lemmens, S., Kirkpatrick, D., Thompson, P., 1996b. The clearance rates of four ascidians from marmion lagoon, western Australia. In: Kuo, J., Philips, R.C., Walker, D.I., Kirkman, H. (Eds.), Seagrass Biology: Proceedings of an International Workshop, University of Western Australia, W.A, pp. 277–282. Loo, L.-O., Rosenberg, R., 1989. Bivalve suspension-feeding dynamics and benthic pelagic coupling in an
eutrophicated marine bay. J. Exp. Mar. Biol. Ecol. 130, 253–276.
Menon, N.R., 1974. Clearance rates of food suspension and food passage rates as a function of temperature in two North-Sea bryozoans. Mar. Biol. 24, 65–67.
˚
Nielsen, C., Riisgard, H.U., 1998. Tentacle structure and filter-feeding in Crisia eburnea and other cyclostomatous bryozoans, with a review of upstream-collecting mechanisms. Mar. Ecol. Prog. Ser. 168, 163–186.
˚
Petersen, J.K., Mayer, S., Knudsen, M.K., 1999. Beat frequency of cilia in the branchial basket in the ascidian, Ciona intestinalis, in relation to temperature and algal cell concentration. Mar. Biol. 133, 185–192. Prata, A.J., 1989. In: A Satellite Sea Surface Temperature Climatology of the Leeuwin Current, Western
Australia, CSIRO Division of Atmospheric Research, Mordilloc, Victoria, p. 5.
˚
Riisgard, H.U., Goldson, A., 1997. Minimal scaling of the lophophore filter-pump in ectoprocts (Bryozoa) excludes physiological regulation of filtration rate of nutritional needs. Test of hypothesis. Mar. Ecol. Prog. Ser. 156, 109–120.
˚
Riisgard, H.U., Ivarsson, N.M., 1990. The crown-filament pump of the suspension-feeding polychaete Sabella penicilus: filtration, effects of temperature, energy cost, and modelling. Mar. Ecol. Prog. Ser. 62, 249–257.
˚ ´
Riisgard, H.U., Manrıquez, P., 1997. Filter-feeding in fifteen marine ectoprocts (Bryozoa): particle capture and water pumping. Mar. Ecol. Prog. Ser. 154, 223–239.
˚
Riisgard, H.U., Thomassen, S., Jakobsen, H., Weeks, J.M., Larsen, P.S., 1993. Suspension feeding in marine sponges Halichondria panicea and Haliclona urceolus: effects of temperature on filtration rate and energy cost of pumping. Mar. Ecol. Prog. Ser. 96, 177–188.
Sanderson, W.G., Thorpe, J.P., Clarke, A., 1994. A preliminary study of feeding rates in the antarctic cheilostomate bryozoan Himantozoum antarcticum. In: Hayward, P.J., Ryland, R.S., Taylor, P.D. (Eds.), Biology and Palaeobiology of Bryozoans, Olsen and Olsen, Fredensborg, Denmark, pp. 167–171. ´
Silen, L., 1977. Polymorphism. In: Woollacott, R.M., Zimmer, R.L. (Eds.), Biology of Bryozoans, Academic Press, New York, San Francisco, London, pp. 183–231.
Strathmann, R.R., 1982. Cinefilms of particle capture by an induced local change of beat of lateral cilia of a bryozoan. J. Exp. Mar. Biol. Ecol. 62, 225–236.
