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First published online June 13, 2008
Journal of Experimental Biology 211, 2185-2190 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015420
Oxygen consumption by a coral reef sponge
1 Department of Zoology, Tel Aviv University, Tel Aviv, 69978, Israel
2 Inter-University Institute of Marine Sciences in Eilat, PO Box 469, Eilat,
88103, Israel
3 Israel Oceanographic and Limnological Research, National Center for
Mariculture, Eilat, 88112, Israel
* Author for correspondence (e-mail: shpigelm{at}agri.huji.ac.il)
Accepted 10 April 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: sponges, oxygen consumption, energy budget, Red Sea, Negombata magnifica
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Barnes and Bell, 2002). In some
marine habitats sponges are disappearing rapidly, and the lack of knowledge of
their basic physiology impedes detection of the detrimental factors
responsible (Wulff, 2006). In
addition to their ecological significance, sponges are known as producers of
bioactive products. The culture of sponges offers one option for obtaining a
reliable supply source for such active metabolites
(Osinga et al., 1999;
Donia and Hamann, 2003).
Therefore, understanding the energetic needs and constraints that might
influence sponge growth, whether in nature or in culture systems, is of the
high interest, particularly in oligotrophic waters such as those of the Red
Sea.
In aerobic organisms oxygen is required for all energetic processes in the
body, and thus its consumption can indicate the total energy expenditure of an
organism (Kleiber, 1975).
Oxygen can also be used as a measure of the energy requirements for defined
physiological activities, such as digestion, assimilation activity and growth
(McCue, 2006). In mussels, for
example, a reduction in feed elicited a downregulation of their water pumping
rate, resulting in a lower oxygen consumption rate
(Bayne et al., 1985).
Oxygen consumption, calculated on the basis of respiration rates, has been
measured in different species of sponges, such as Mycale sp.,
Tethya cripta, Verongia gigantea
(Reiswig, 1974),
Halichondria panicea (Barthel and
Theede, 1986), Mycale acerata, Isodictya kerguelensis
(Kowalke, 2000) and
Dysidea avara (Reiswig,
1974; Barthel and Theede,
1986; Kowalke,
2000; Coma et al.,
2002).
Several studies have estimated the energy costs of the various
physiological activities in the sponge. Using a theoretical calculation,
Riisgård et al. (Riisgård et
al., 1993) estimated that the energy expenditure for a sponge's
water-pumping activity constitutes less than 1% of its energy loss through
respiration, thus exemplifying the low energy requirements for the sponge's
basic activities. Thomassen and Riisgård
(Thomassen and Riisgård,
1995), showed, in Halichondria panicea, an exceptionally
(in comparison to other invertebrates) high specific dynamic activity (SDA),
defined as an increase in specific respiration rate in response to growth,
that amounted to 139% of the biomass production. They concluded that, for this
sponge, energy for maintenance constitutes only a small fraction of the energy
required for growth, as was suggested for unicellular organisms
(Fenchel, 1982). Here we
provide experimental data that may challenge these theoretical concepts.
The aim of the present research was to determine oxygen consumption of a coral reef sponge, under conditions of full activity, at a reduced activity and while starved (basal rate) to estimate how much of the sponge's total energy expenditure is used for its basal activity, and how much for propelling the water through its body; and ultimately to posit a primary evaluation of sponge growth potential based on the remainder oxygen. For this purpose we employed a new method that we developed based on previous (unpublished) observations. A secondary objective was to validate the accuracy of the experimental methodology used by comparing flow-through with closed-chamber incubations.
The studied sponge, Negombata magnifica (Keller 1889), is
distributed from the Gulf of Aqaba in the north, along the Red Sea, to Djibuti
in the Gulf of Aden in the south (Ilan,
1995). N. magnifica has been found to be a source of the
two bioactive metabolites, latrunculin A and latrunculin B
(Groweiss et al., 1983).
Several experimental methods have been used to measure oxygen consumption
rate in sponges, but the most frequently used is the incubation method
(Cotter, 1978;
Thomassen and Riisgård,
1995; Kowalke,
2000). However, it was noted that incubation in a metabolic
chamber lowered sponge activity, consequently affecting its oxygen consumption
rate (Simpson, 1984). The
flow-through and steady-state systems partially overcome the problem of water
re-filtration by the sponge (reviewed by
Riisgård, 2001). In this
system the organism is kept in an almost unaltered environment by the
continuous supply of fresh seawater. Several studies such as that by Cotter
(Cotter, 1978), have employed
this method to measure oxygen consumption in sponges.
Various sensors have also been employed in studies of oxygen consumption.
The most commonly used methods for oxygen-sensing are polarographic
electrodes, a chemical procedure developed from the Winkler method
(Winkler, 1888), couloximetry,
and the relatively novel method of optrodes
(Gatti et al., 2002). The main
advantage of the latter method is that, unlike the polarographic electrodes,
the optrode does not consume oxygen, its drift over time is expected to be
low, and it is not stirring dependent, thus enabling oxygen measurements in
changing flow regimes (Gatti et al.,
2002).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
The FR of N. magnifica was measured under high, medium and low
water exchange rates (635±6 ml min–1, 355±1 ml
min–1 and 165±2 ml min–1,
respectively). The experimental system consisted of eight identical plastic
3.5 l containers supplied with a small water pump to mix the water and
maintain a constant water flow over the sponge at all inflow water rates, and
thereby avoid any effect of this factor on sponge activity
(Vogel, 1978). Seven
containers were each stocked with a single individual sponge and the eighth
was left empty and used as a control. Fresh seawater was supplied to each
container from a 20 l header tank at an initial high flow rate. The water
inside the header tank and the sponge aquaria was continuously mixed at a rate
of 100 l min–1 and 10 l min–1, respectively.
After 2 h of acclimatization, water samples were collected from the
containers' outflow and from the header tank (representing the containers'
inflow water). The header tank was sampled twice, before and after sample
collection from the containers; the second sample was needed to compensate for
possible changes in plankton/particle concentrations during a sampling period
that was shorter than 4 min. All water samples were collected in duplicates of
1.5 ml and were fixed in glutaraldehyde (G-5882; Sigma, Rehorot, Israel) at a
final concentration of 6%. The same experimental procedure was applied when
testing the other two exchange rates, measured consecutively on the same
sponge individuals. The amount of Synechococcus sp. in the water
samples was counted in a flow cytometer (FACScan, Becton Dickinson, Franklin
Lakes, NJ, USA) using standard procedures
(Marie et al., 2000).
Sponge CR was determined using the following formula
(Riisgård, 2001):
 | (1) |
Sponges and seawater
Individuals of Negombata magnifica were taken randomly from a
stock of sponges cultured at the northern end of the Gulf of Aqaba
(Hadas et al., 2005). These
sponge individuals were already attached to PVC plates. This provided complete
intact individual sponges for all measurements, thus reducing to a minimum
stress related to sponge translocation and positioning in the experimental
systems. The laboratory work was conducted at the Interuniversity Institute
(IUI), Eilat, Israel. For all the experiments non-filtered, ambient water was
pumped directly from the sea. The experiments were conducted in winter when
water temperature was 22.5±1°C. Sponges were brought into the
laboratory 24 h prior to the beginning of the experiment to acclimatize them
to the experimental set-up. During acclimatization, sponges were kept in
individual 3.5 l tanks with a constant supply of flow-through seawater at a
rate of about 1 l min–1.
Measurement of respiration at three activity levels
Three respiration rates were defined, following those measured by Thompson
and Bayne (Thompson and Bayne,
1972) for Mytilus edulis: (1) when the sponge is fully
active and pumping water; (2) when the sponge is at basal (routine) activity;
and (3) when the pumping activity has ceased but the sponge still maintains a
high level of activity. Measurement of the three respiration rates
(sensu Thompson and Bayn,
1972) was carried out in a three-step experiment in which values
were recorded repeatedly in seven sponges, using the steady-state system (each
sponge was measured once). In the first step, water flow was set to 600 ml
min–1 to measure the respiration rate of an active sponge.
Active oxygen consumption was defined as the amount of oxygen consumed when
the oscula are wide open and both filtration and digestion processes are
active.
After this measurement, the water flow was reduced to 100 ml min–1, thus causing the sponge to stop its filtration activity. Oxygen measurement was carried out within 30 min after most of the sponge's oscula had contracted, indicating significant decrease in pumping activity, defined as reduced activity state.
The final measurement was performed 14 h later, during which the sponges were supplied with seawater filtered online by a 0.2 µm mesh size filter (Suporlife 200, PALL, Biopharmaceuticals, East Hills, NY, USA), at a constant rate of 100 ml min–1. In each activity level, water samples were collected simultaneously from the inflow and outflow currents directly into 50 ml calibrated glass bottles (three consecutive replicates for each measurement at 5 min intervals).
Oxygen concentration in each sampling bottle was determined using a Winkler
automatic titrator (702 SM Titrino, Metrohm, Switzerland). The oxygen
concentrations in the inflow and outflow water were determined as the mean
value of the three replicates. The sponge respiration rate in the steady-state
system was calculated using the following equation:
 | (2) |
O2 is the
respiration rate in a steady-state system (nmol O2
min–1 g–1 wet mass), F1 is the water flow
rate (ml min–1) and C1 and
C2 are the oxygen concentration in inflow and outflow
water, respectively. The average respiration rate of all sponges was
determined as the linear regression coefficient between the individual
respiration rates and the sponge size.
Respiration in a steady-state system
The methodology of the steady-state oxygen measurement was adapted from the
system described by Riisgård
(Riisgård, 2001) and
oxygen concentration was determined using Winkler's method
(Winkler, 1888).
Respiration rate of 17 individual sponges in full activity was measured in a 1 l Perspex respiration chamber constantly supplied with unfiltered seawater (each sponge was measured once). A single pre-weighed sponge individual was placed in a respiration chamber that was sealed and mounted on top of a magnetic stirrer, to guarantee mixing of the water. The water flow rate to the chamber was adjusted to the desired value, maintaining a measurable oxygen gradient between the inflow and outflow water, while also keeping the sponge active. The oxygen concentrations in this experiment were determined by the Winkler method and all measurement procedures and calculations were identical to those performed in the former experiment in the steady-state system.
Each day, prior to measurements, the respiration chamber was sealed without a sponge inside, water exchange rate was set to 100 ml min–1, inflowing and outflowing water were sampled, and the oxygen concentration was measured to estimate non-specific oxygen consumption that could potentially result from respiration of planktonic organisms and from oxidation of organic compounds in the water (chemical oxygen demand).
Respiration in an incubation system
The oxygen measurements were carried out in a Perspex respiration chamber
with an effective volume of 4740 ml, equipped with a water pump to ensure
water mixing. The respiration rate of nine different sponges in the incubation
system was measured; each was measured once. Sponges were acclimatized to the
experimental chamber for 2 h prior to measurements, during which fresh
seawater was constantly supplied. The metabolic chamber was then sealed and
the oxygen concentration was recorded each second for 40 min using an optrode.
Because of the low ratio between sponge respiration rate and chamber volume,
the oxygen concentration inside the chamber never decreased below 95% of the
initial concentration. Measurement started only when the sponge oscula were
wide open, indicating that the sponge was actively pumping water.
Concomitantly, a control oxygen measurement without a sponge was conducted in
the same manner to estimate the electrode drift and the rate of biological
oxygen demand (BOD). The changes in oxygen concentration detected in the
control measurements were used to correct the sponge's measured oxygen
consumption rate.
Oxygen concentration was measured using a single optrode (Ocean Optics
Inc., Dunedin, FL, USA) connected via fiber optics to a light source
(LS-450) and to a spectrometer (USB2000; Ocean Optics Inc.). The operation
software OOIBase32TM (Ocean Optics) controlled the system and the data
were logged automatically into a computer. The optrode was calibrated at the
beginning of each working day according to the Ocean Optics operation manual
(Klimant et al., 1995). The
reference for the calibrations was determined using the Winkler method.
The rate of change in oxygen concentration in the respiration chamber was
determined as the linear regression coefficient. The respiration rate was
analyzed during two phases of the measurement. The first was throughout the
initial 6 min of the measurement, and the second started 15 min after sealing
the chamber and lasted 10 min. The sponge respiration rate
(O2) in the
incubation system was calculated by the following equation:
 | (3) |
O2in is
the oxygen consumption rate in the incubation chamber, expressed in nmol
O2 min–1 g–1 wet mass sponge;
R1 and R2 are the regression
coefficients for sponge respiration and control (each expressed as p.p.m.
O2 day–1; respiration rate had a negative value
and the control always had a positive value); and C is the net
chamber volume (i.e. excluding sponge volume). The units obtained from the
regression were in mg O2 24 h–1. By dividing the
numerator by 32 the oxygen consumption rate is converted to mmol O2
and by further dividing by 1440 it is converted to minutes.
Statistical analysis
Statistical analyses were performed using JMPIN (v 5.0.1a, SAS Institute
Inc., Cary, NC, USA). Variance homogeneity was assessed by Bartlett's test,
and the Shapiro–Wilk test was used to check for normality. Data sets
were log transformed when necessary to meet the requirements of normality and
homogeneity of variance. Difference between the respiration rates at the three
activity levels was tested by applying a one-way ANOVA model with random
effect (the difference between the seven sponges), analyzed using the residual
maximum likelihood (REML) method.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Oxygen consumption rate in the incubation system
The average respiration rate during the first 6 min of the measurement was
29.1±2.8 nmol O2 min–1 g–1
wet mass, significantly decreasing to 14.4±1.4 nmol O2
min–1 g–1 wet mass during the period
15–25 min post chamber sealing (paired t-test, d.f.=8,
t=5.5, P<0.001). No linear regression could be fitted
between the oxygen demand for the two time frames and the sponge wet mass
(slope=0, r2=0.2, N=9, P=0.26 and
slope=0, r2=0.3, N=9, P=0.1,
respectively, Fig. 3).
|
Respiration at three activity levels
Sponge respiration rates at the various activity levels differed
significantly (F8,20=17.5, P<0.001;
Fig. 4). The mean oxygen
consumption of the sponge at the beginning of the experiment (active stage)
was 41.8±3.2 nmol O2 min–1
g–1 wet mass. Thirty minutes after the water flow rate was
reduced (reduced activity stage), average oxygen consumption had significantly
decreased to 31.3±1.8 nmol O2 min–1
g–1 wet mass, a reduction of 25.1±3.6% relative to the
rate at full activity level. At the third measurement (basal stage), the
sponges' oxygen consumption had further decreased to 20.2±1.2 nmol
O2 min–1 g–1 wet mass, a
reduction of 51.6±2.5% relative to a fully active sponge.
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|
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The influence of water flow rate on sponge activity has a direct bearing on the particular experimental system to be deployed. Whereas in a steady-state system it can be controlled, in the commonly used incubation system water exchange does not take place. Thus the latter system might not be suitable for measurement of oxygen consumption rates of a sponge, including N. magnifica. Indeed, comparison of the mean active respiration rate of N. magnifica between the two tested systems revealed that oxygen consumption measured in the steady-state system was 22% higher than the mean value measured during the first 6 min, using the incubation method (37.3±4.6 and 29.1±2.8 nmol O2 min–1 g–1 wet mass, respectively), although the latter is within the confidence limits (95%) of the former. Moreover, sponge mean oxygen consumption in the incubation system was not stable over time and within 15–25 min it had decreased to 14.4±1.4 nmol O2 min–1 g–1 wet mass, which is only 40% of the level found in the steady-state system. This oxygen consumption level is similar to that found in the present study for the sponge basal activity.
It was hypothesized that the manipulation carried out in the present
experiment would result in a lower than normal metabolic rate in the sponge
(Ortmann and Grieshaber,
2003). If so, this would mean that the estimated amount of energy
is a minimal value, and that under `better' experimental conditions the energy
expenditure for maintenance would be higher, with a consequent reduction in
the estimated proportion of energy spent on water filtration. As a
consequence, the proportion between the various activities might change, but
this would not change the fact that most of the N. magnifica energy
is used for maintenance and water propulsion.
Sponge energy expenditure
The oxygen consumption of N. magnifica in the active state was
found to be within the range of other tropical marine sponges
(Table 1), higher than the
respiration rate of Antarctic sponges but lower than that, of, for example,
temperate calcareous sponge Syconciliatum
(Cotter, 1978). Great
interspecies variability in oxygen consumption rate of sponges obviously
exists within the same habitat (Table
1).
|
The oxygen consumption and filtration rates that were found for H.
panicea (Thomassen and
Riisgård, 1995) were 0.6 ml O2
h–1 g–1 (dry mass) and 28.35 ml
min–1 g–1 (dry mass). It was found here that
N. magnifica consumed 0.33 ml O2 h–1
g–1 (dry mass) and filtered water at a rate of 70 ml
min–1 g–1 (dry mass). These results show
that the latter species is more efficient in terms of water pumping, possibly
as an adaptation to the oligotrophic conditions at the northern end of the Red
Sea.
Realizing the existence of a positive correlation between sponge filtration rate and water flow rate through the respiration chamber allowed reduction of the sponge FR to about 25% of the maximal rate (Fig. 1). The instantaneous reaction of a sponge to such manipulation enabled measurement of filtration rate within 30 min after reduction in water exchange rate, which should minimize the effect of other physiological processes (e.g. digestion) on sponge oxygen consumption.
The amount of oxygen required for water pumping activity (maximally
10.6±1.8 nmol O2 min–1 g–1
wet mass) was about 25% of the sponge's total oxygen consumption. This
empirical result is much higher than that estimated for Halichondria
panicea [<1% (Riisgård et
al., 1993)], but it is lower than the level of about 50% reported
for other filter feeders, such as the bivalves Mytilus edulis and
Cardium edule (reviewed by Newell
and Branch, 1980). It is also in accordance with the model
proposed by Willows (Willows,
1992), who demonstrated that under low food concentrations (as in
the oligotrophic coral reefs of the Red Sea) the energy expenditure for water
filtration of suspension feeders is high (the animal has to filter more water
in such environments) and probably sets the upper limit for the filtration
rate.
The basal energetic needs of N. magnifica, defined as the amount
of energy consumed by a starved organism
(Bayne, 1976), were estimated
using a method similar to that used to measure the energetic cost of pumping,
but this time the sponges were maintained for 14 h in 0.2 µm-filtered
seawater. The data (Fig. 1)
show that a complete cessation of water pumping was not achieved (sponge
oscula remained partially open), probably because continuous water flow, at a
minimal rate, is essential to prevent total depletion of oxygen in the sponge
body (Hoffmann et al., 2005);
as such, this minimal pumping can be considered as part of the basal energetic
needs. Demonstrating that this minimal activity is not a transient state that
could lead to the sponge's death, sponges that were maintained for 27 days
under similar conditions lost 22.5% of their organic dry matter during this
period, but suffered no mortality (E.H., unpublished data). The N.
magnifica basal respiration rate was 20.2±1.2 nmol O2
min–1 g–1 wet mass, which was approximately
50% of its respiration rate during the active state.
Approximately 75% of the oxygen consumed by N. magnifica was used
for the energy-demanding processes of sponge maintenance and water propulsion.
This implies that no more than 25% of total oxygen remains for energy
allocated to growth. In comparison, the energy cost per unit of growth in the
polychaete Nereis diversicolor was 26%
(Nielsen et al., 1995). A
growth rate of 0.55% per day of this polychaete, which is comparable to that
of N. magnifica (Hadas et al.,
2005), increases the specific respiration rate of N.
diversicolor by 0.14 mg O2 mg–1
day–1, an increase of total respiration (over maintenance) by
9%. This value is lower than that found in our work for N. magnifica
(25%), but closer than the value of 139% found for Halichondria
panicea (Thomassen and
Riisgård, 1995). The relatively low level of energy that is
potentially available for growth of N. magnifica might imply that
energetic constraints play a significant role in the growth potential of this
sponge. Further studies might reveal whether the sponge growth rate is
restricted by energetic constraints (e.g. if increased food availability would
correlate to faster growth rate) or by other physiological parameters, such as
the rate of diffusion of nutrients between the sponge cells.
The specific respiration rate of N. magnifica was constant for
sponges along the entire tested size range of 10–60 g wet mass. This
finding is in agreement with other studies of sponge respiration
(Cotter, 1978;
Thomassen and Riisgård,
1995) and may distinguish the sponges from other multicellular
organisms, in which the relationship between an organism's age (which is
positively correlated to size) and respiration rate
[M=aWb; where M is total respiration, a
is a parameter (metabolism for unit of weight), W is weight unit and
b is a constant indicating at what speed and in which direction
respiration changes as size increases] is well documented. This difference
between sponges and other metazoans might be explained by the homogeneous
structure of a sponge (Reiswig,
1975), which maintains a constant ratio between body volume and
its gas exchange surface area (Ultsch,
1973); or be due to the experimental use of different sized sponge
fragments rather than individuals of different ages.
|
Acknowledgments |
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References |
|---|
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Barnes, D. K. and Bell, J. J. (2002). Coastal sponge communities of the West Indian Ocean: taxonomic affinities, richness and diversity. Afr. J. Ecol. 40,337 -349.[CrossRef]
Barthel, D. and Gutt, J. (1992). Sponge associations in the Eastern Weddell Sea. Antarct. Sci. 4, 137-150.
Barthel, D. and Theede, H. (1986). A new method for the culture of marine sponges and its application for experimental studies. Ophelia 25,75 -82.
Bayne, B. L. (ed.) (1976). Physiology: I. In Marine Mussels: Their Ecology and Physiology, pp.121 -206. Cambridge: Cambridge University Press.
Bayne, B. L., Brown, D. A., Burns, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., Lowe, D. M., Moore, M. N., Stebbing, A. R. D. and Widdows, J. (1985). The Effect of Stress and Pollution on Marine Animals. New York: Praeger Publishers.
Coma, R., Ribes, M., Gili, J.-M. and Zabala, M. (2002). Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnol. Oceanogr. 47,324 -331.
Cotter, A. J. R. (1978). Re-investigation of size, axial gradients and light as factors affecting the respiration of certain marine sponges. Comp. Biochem. Physiol. 60A,117 -122.[CrossRef]
Donia, M. and Hamann, M. T. (2003). Marine natural products and their potential application as anti-infective agents. Lancet Infect. Dis. 3,338 -348.[CrossRef][Medline]
Fenchel, T. (1982). Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar. Ecol. Prog. Ser. 8,225 -231.[CrossRef]
Gatti, S., Brey, T., Muller, W. E. G., Heilmayer, O. and Holst, G. (2002). Oxygen microoptodes: a new tool for oxygen measurements in aquatic animal ecology. Mar. Biol. 140,1075 -1085.[CrossRef]
Groweiss, A., Shmueli, U. and Kashman, Y. (1983). Marine toxins of Latrunculia magnifica. J. Org. Chem. 48,3512 -3516.[CrossRef]
Hadas, E., Shpigel, M. and Ilan, M. (2005). Sea ranching of the marine sponge Negombata magnifica (Demospongiae, Latrunculiidae) as a first step for latrunculin-B mass production. Aquaculture 244,159 -169.[CrossRef]
Hoffmann, F., Larsen, O., Thiel, V., Rapp, H. T., Pape, T., Michaelis, W. and Reitner, J. (2005). An anaerobic world in sponges. Geomicrobiol. J. 22, 1-10.[CrossRef]
Ilan, M. (1995). Reproductive biology, taxonomy, and aspects of chemical ecology of Latranculiidae (Porifera). Biol. Bull. 188,306 -312.[Abstract]
Kleiber, M. (1975). The Fire of Life – An Introduction to Animal Energetics. Huntington, NY: Robert E. Krieger.
Klimant, I., Meyer, V. and Kuhl, M. (1995). Fiber-optic oxygen microsensors, a new tool in aquatic biology. Limnol. Oceanogr. 40,1159 -1165.
Kowalke, J. (2000). Ecology and energetics of two Antarctic sponges. J. Exp. Mar. Biol. Ecol. 247, 85-97.[CrossRef][Medline]
Marie, D., Simon, N., Guillou, L., Partensky, F. and Vaulot, D. (2000). Flow cytometry analysis of marine picoplankton. In Living Color: Protocols in Flow Cytometry and Cell Sorting (ed. R. A. Diamond and S. De Maggio), pp.422 -454. Berlin, Heidelberg: Springer-Verlag.
McCue, M. D. (2006). Specific dynamic action: a century of investigation. Comp. Biochem. Physiol. 144A,381 -394.
Newell, R. C. and Branch, G. M. (1980). The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. Adv. Mar. Biol. 17,329 -396.
Nielsen, A. M., Eriksen, N. T., Iversen, J. J. L. and Riisgard, H. U. (1995). Feeding, growth and respiration in the polychaetes Nereis diversicolor (facultative filter feeder) and N. virens (omnivorous) – a comparative study. Mar. Ecol. Prog. Ser. 125,149 -158.[CrossRef]
Ortmann, C. and Grieshaber, M. K. (2003).
Energy metabolism and valve closure behaviour in the Asian clam Corbicula
fluminea. J. Exp. Biol.
206,4167
-4178.
Osinga, R., Tramper, J. and Wijffels, R. H. (1999). Cultivation of marine sponges. Mar. Biotechnol. 1,509 -532.[CrossRef][Medline]
Reiswig, H. M. (1974). Water transport, respiration and energetics of three tropical marine sponges. J. Exp. Mar. Biol. Ecol. 14,231 -249.[CrossRef]
Reiswig, H. M. (1975). The aquiferous system of three marine Demospongiae. J. Morphol. 145,493 -502.[CrossRef]
Riisgård, H. U. (2001). On measurement of filtration rates in bivalves – the stony road to reliable data: review and interpretation. Mar. Ecol. Prog. Ser. 211,275 -291.[CrossRef]
Riisgård, H. U., Thomassen, S., Jakobsen, H., Weeks, J. M. and 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.[CrossRef]
Simpson, T. L. (1984). The Cell Biology of Sponges. New York: Springer-Verlag.
Thomassen, S. and Riisgård, H. U. (1995). Growth and energetics of the sponge Halichondria panicea. Mar. Ecol. Prog. Ser. 128,239 -246.[CrossRef]
Thompson, R. J. and Bayne, B. L. (1972). Active metabolism associated with feeding in the mussel Mytilus edulis L. J. Exp. Mar. Biol. Ecol. 9, 111-124.[CrossRef]
Ultsch, G. R. (1973). A theoretical and experimental investigation of the relationships between metabolic rate, body size and oxygen exchange capacity. Respir. Physiol. 18,143 -160.[CrossRef][Medline]
Vogel, S. (1978). Organisms that capture currents. Sci. Am. 239,108 -117.
Willows, R. I. (1992). Optimal digestive investment: a model for filter feeders experiencing variable diets. Limnol. Oceanogr. 37,829 -847.
Winkler, L. W. (1888) The determination of dissolved oxygen in water. Ber. Dtsch. Chem. Ges. 21,2843 -2846.[CrossRef]
Wulff, J. L. (2006). Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biol. Conserve. 127,167 -176.[CrossRef]
Yahel, G., Sharp, J., Marie, D., Hase, C. and Genin, A. (2003). In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon. Limnol. Oceanogr. 48,141 -149.
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