Journal of Experimental Marine Biology and Ecology
296 (2003) 13 – 22
www.elsevier.com/locate/jembe
Influence of re-orientation on alignment to flow
and tissue production in a Spongia sp.
(Porifera:Demospongiae:Dictyoceratida)
Justin I. McDonald a,*, Keith A. McGuinness a,
John N.A. Hooper b
a
School of Biological, Environmental and Chemical Sciences, Northern Territory University, Darwin,
NT, 0909, Australia
b
Queensland Museum, P.O. Box 3300 South Brisbane, Queensland, 4101, Australia
Received 30 May 2001; received in revised form 8 May 2003; accepted 10 June 2003
Abstract
Spongia individuals on intertidal reefs in Darwin Harbour displayed a distinct tendency to
orientate towards a strong uni-directional water flow, their longest axis facing across the water
current. Individuals rotated by 90j re-orientated tissue to face across the prevailing currents. There
were significant differences in growth between re-orientated sponges, and both moved control and
undisturbed control treatments. Compared to mean growth rates of
1.27 cm year 1 (from
1
undisturbed controls) and 1.68 cm year (from moved controls), re-orientated individuals had
significantly higher growth rates (46.15 cm year 1). Increased volumetric growth of re-orientated
individuals was not a result of re-arrangement of existing tissue but a consequence of the
production of more sponge tissue, evident by an increase in sponge volume. Increased tissue
production identified in this study may be beneficial to researchers growing sponges for aquaculture
purposes.
D 2003 Elsevier B.V. All rights reserved.
Keywords: Growth; Morphology; Transplant; Water flow; Sponge; Experimental rotation; Intertidal adaptation
* Corresponding author. Current address: School of Plant Biology, Faculty of Natural and Agricultural
Sciences, University of Western Australia, 35 Stirling Highway, Crawley 6009 Western Australia, Australia.
E-mail address: [email protected] (J.I. McDonald).
0022-0981/$ - see front matter D 2003 Elsevier B.V. All rights reserved.
doi:10.1016/S0022-0981(03)00302-2
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J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
1. Introduction
Porifera filter water to obtain organic particles and for respiration purposes, thriving in
waters that are rapidly moving, turbid, high in particulate matter and nutrient rich (Bell and
Barnes, 2000; Hooper, 1992; Hyman, 1949). These animals however, lack any true
musculature and consequently are unable to move in search of food, instead feeding on
organic particles suspended in the water column (Frost, 1978, 1980; Reiswig, 1974;
Riisgård et al., 1993; Pile et al., 1996). As such these animals must be optimally positioned,
and have a morphology that enables them to make effective use of water flow, whilst
reducing potential dislodgement and sediment inundation.
In general, many filter feeding organisms living in strongly bi- or uni-directional
flow exhibit a vertically planar morphology that is believed to be associated with
capture of food particles from the downstream wake, and reducing potential drag and
sedimentation effects (Helmuth and Sebens, 1993; Leversee, 1976; Merz, 1984;
Okamura, 1985; Vogel, 1981; Wainwright et al., 1976; Warner, 1977). However, many
sponge species that live in strong bi- or uni-directional water flows have a horizontally
orientated form. The wake created downstream of a horizontally oriented sponge is less
likely to influence its feeding rate because most of the surface area of the organism is
positioned out of the plane of its own wake (Johnson and Sebens, 1993). The
orientation of sponges relative to prevailing flow is said to enhance feeding and
respiratory capabilities, and has been reported in other filter feeding organisms, e.g.
gorgonians (Wainwright and Dillon, 1969) and barnacles (Ayling, 1976; Otway and
Underwood, 1987).
The optimal morphology for any sponge will be that which ensures maximal
separation of incoming water and the exhalant stream leaving the osculum (Simpson,
1984). This separation of flows would ensure that the sponge is not re-filtering water
that has already been depleted of oxygen and/or food. In terms of overall body form,
sponges display numerous strategies to separate water streams. Many species of
Demospongiae have ostial and oscular faces orientated relative to the prevailing water
flow. These faces can be elevated (e.g. Oceanapia sagittaria, order Haplosclerida)
(Hooper et al., 1993), cup-shaped (e.g. Poterion neptuni, order Hadromerida)(Hyman,
1949) shaped like an elephants ear (e.g. Spongia agaricina, order Dictyoceratida)
(Pronzato et al., 1998) or other body plans to optimise flow separation. In these cases,
separation of inhalant and exhalant water flow is achieved by orientation of the longest
axis perpendicular to the current. Having an inhalant face positioned foremost to the
current ensures that wastes from the exhalant stream are not re-filtered by the animal.
This mechanism is adequate for sponges in waters where water flow direction is
sufficiently predictable to make a more stable morphology advantageous (Bergquist,
1978).
Based upon the above understanding of morphology, it may be expected that Spongia sp.
would display a distinct directional bias in their orientation towards currents. If perpendicular orientation to flow occurs the following hypotheses can be made: H1. Sponges that
are re-orientated will realign their structures so that their longest axis is perpendicular to the
water flow. H2. Sponges that are re-orientated will exhibit a reduced growth rate relative to
control animals.
J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
15
2. Materials and methods
2.1. Species accession number: QM G319187; species number: 1983
2.1.1. Study sites
Darwin Harbour is a relatively shallow tropical estuarine system with a semi-diurnal
macro-tidal environment and an 8-m maximum tidal range (Collins, 1994). Tidal currents
are generally very strong throughout the harbour (ranging from 0.25 to 2 m s 1)
(Semeniuk, 1985; Byrne, 1987).
East Point reef (latitude 12j24V3WS, longitude 130j49V2WE), situated at the mouth of
Darwin Harbour, is a fringing lateritic reef extending approximately 500 m off-shore. The
reef provides habitat for many species of sponge, and has been described as one of the
most diverse and species rich sponge sites in Australia. It has an unusually high
population density and species diversity in a relatively small area (Hooper, 1992,
unpublished). This site experiences considerable water flow (mean 1.4 m s 1) and has
fine sediments ( V 0.53 mm).
2.1.2. Orientation
Preliminary observations on individuals of Spongia sp. revealed that sponges were
orientated with their longest axis perpendicular to the prevailing water current. Compass
bearings of twenty haphazardly selected individuals were taken to determine if this
orientation was prevalent throughout the population (90j perpendicular to flow, 180j
parallel to flow). Rayleigh’s uniformity test was used to calculate the distribution of the
observed directional data relative to that of a random orientation (at 0.05 significance level).
2.1.3. Re-orientation experiment
An experiment was conducted at East Point over a three month period to evaluate the
effects of re-orientation of Spongia sp. to water flow and its effect upon the morphology and
growth of Spongia individuals. The following treatments were established using individuals located in the mid-intertidal zone (exposed at sub 2 m tides).
(a) Undisturbed controls—Five sponges were haphazardly selected. These sponges were
neither moved nor rotated (Fig. 1). This treatment allowed comparisons to be made
between ‘un-manipulated’ and ‘experimentally manipulated’ animals.
(b) Moved controls—Three sponges were detached from the reef with a portion of
substratum and reattached to the substratum in their original orientation (Fig. 1).
These sponges acted as controls for the movement process (moved controls).
(c) Rotated animals—Five sponges were detached from the reef with a portion of
substratum, rotated 90j relative to their original position and prevailing water flow
(Fig. 1) and reattached to the reef.
Sponges used in this experiment were of comparable size and each treatment (reoriented, moved control and undisturbed control) was randomly allocated. A small number
of replicate animals were used due to the relatively low number of Spongia sp. present on
this reef. Each sponge individual had its maximum height, length and width measured.
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J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
Fig. 1. Schematic representation of experimental treatments used.
These linear measures were then used to calculate sponge volume at each census. Each
sponge was measured prior to disturbance then at each monthly census.
Both re-orientated and moved control sponges were fixed to the substratum using
plastic mesh. Holes were cut in the mesh, large enough to leave a margin for growth, and
the mesh then placed over each sponge. Sponges were maintained in position as the
substratum still attached to the sponge was confined beneath the mesh. The mesh structure
was fixed in place using concrete nails hammered into the surrounding substratum.
2.2. Data analysis
2.2.1. Re-orientation experiment
Growth rates between treatments (re-orients, moved controls and undisturbed controls)
were tested using one-way ANOVA (at 0.05 level of significance). Comparisons of growth
rates (in cm3 year 1) between treatments were based upon growth in volume. Growth was
calculated as: volume of sponge at time 4 volume of sponge at time 1.
Data were tested for homogeneity of variance using Cochrans’ test. Variances were
heterogenous, but because some observations were negative transformations could not
easily be used, so a significance level of 0.01 was used for f-tests. Means were compared
after the analysis using Tukey’s test. The harmonic mean of the n’s was used to calculate
the standard error for the test. Paired t-tests were used to test for a significant change in
dimension (height, width, length and volume) between times 1 and 4 in each experimental
group.
Data were analysed using Statistica (Version 5.5 software).
3. Results
Rayleigh’s test of uniformity indicated a significant directional bias in Spongia sp.
( P = 0.00, n = 20). Spongia sp. had its longest axis facing perpendicular to the water flow
(90j), with 90% of sponges measured within a 20j range (Fig. 2).
J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
17
Fig. 2. Relationship between the prevailing water current and the orientation of the longest axis. 0j represents
direction of water flow (n = 20). Concentric circles represent the number of individuals recorded at that bearing
and occur in increments of two radiating from the centre.
3.1. Re-orientation experiment
The experimental re-orientation of Spongia individuals triggered significant changes in
width, length and volume of sponge tissue but no change in height. Growth of re-orients
along the width axis (the axis perpendicular to the water flow) was significantly higher
than either the moved controls or the undisturbed controls (df = 2,10, F = 64.718,
P < 0.001). Length (the axis running parallel to the water flow), showed a significant
decrease in growth relative to moved controls or undisturbed controls (df = 2,10,
F = 13.367, P < 0.01). Height of re-orientated, moved controls and undisturbed controls
showed no significant difference throughout the experiment (df = 2,10, F = 1.034, P>0.01).
Volume of re-orientated sponges increased significantly compared to both control treatments (df = 2,10, F = 37.076, P < 0.001).
Analysis of growth within the re-orientated treatment revealed that width increased
significantly between time 1 and time 4 (df = 4, t = 9.37, P < 0.001), with the greatest period
of change occurring between time 1 and time 2. Width showed a mean increase of 31.3 mm
(mean over 3 months, equating to a growth rate of 125.5 mm year 1). Both moved (width
df = 2, t = 0.55, P = 0.635) and undisturbed controls showed no significant change in width
(df = 4, t = 2.56, P = 0.063) (Fig. 3).
Length in re-orientated individuals, although significantly different between time 1
and time 4 (df = 4, t = 4.33, P = 0.012), showed a much slower response. The greatest
period of change in length occurred between time 2 and time 3. Length showed a
mean decrease of 10.29 mm (mean over 3 months equating to a growth rate of
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J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
Fig. 3. Proportional change in length, width and height (cm) of (a) Spongia individuals that have undergone reorientation and (b) Spongia controls (note: all measures contain F S.E. however errors are very small therefore
may not be easily discernible).
41.16 mm year 1). Controls showed no significant change in length (moved
controls df = 2, t = 3.02, P = 0.094; undisturbed controls df = 4, t = 3.03, P = 0.039)
(Fig. 3).
Height of re-orientated and both control treatments showed no significant change
throughout the experiment (re-orientated df = 4, t = 1.18, P = 0.305; moved controls
df = 2, t = 0.36, P = 0.754; undisturbed controls df = 4, t = 1.0, P = 0.374) (Fig. 3).
Throughout the study, overall volume of re-orientated sponges increased significantly from time 1 to time 4 (df = 4, t = 7.64, P = 0.002). There was no significant
difference in volume of either moved (df = 2, t = 4.06, P = 0.056) or undisturbed control
sponges (df = 4, t = 3.44, P = 0.026). Re-orientated individuals showed a significant
increase in volumetric growth, up to 36 times the growth rate observed in the both
control treatments. Compared to growth rates of 12.7 mm3 year 1 (moved controls)
and
16.8 mm3 year 1 (from undisturbed controls), re-orientated individuals had
significantly higher growth rates (mean 461.5 mm3 year 1) (df = 2,10, F = 37.076,
P < 0.001).
J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
19
4. Discussion
This study identifies previously unreported morphological plasticity and increased
growth rates in Spongia sp. in response to experimental manipulation. Pronzato et al.
(1998) also reported morphological changes in Spongia sp. in response to a range of
environmental variables. In this study Spongia sp. was observed to display a distinct bias in
orientation to strong uni-directional water flow. Individuals were orientated with their
longest axis, and therefore greater surface area, facing perpendicular to the water current
(180j). This confirms reports that orientation perpendicular to water currents may be
optimal for species fitness. Perpendicular orientation is believed to enhance feeding and
respiratory capabilities by ensuring maximum separation of inhalant and exhalant streams
(Vogel and Bretz, 1972; Trammer, 1983). This orientation places the bulk of the sponge
tissue out of the position of its own wake, therefore reducing sediment deposition onto the
sponge and any potential for smothering.
Separation of incoming water and the exhalant stream ensures that the sponge is not refiltering water depleted of oxygen and nutrients. Re-orientation of Spongia sp. within their
environment decreased the volume of sponge tissue perpendicular to water flow, potentially
reducing feeding and respiratory capacities of these individuals by possible mixing of these
streams. This was believed to have stimulated the response observed during this experiment, with re-orientated individuals showing a significant increase in volumetric growth
(re-orientated mean 46.15 cm3 year 1), up to 36 times the growth rate observed in both
control treatments ( 1.27 cm3 year 1 (moved controls) and
1.68 cm3 year 1
(undisturbed controls)). However, the fact that re-orientated individuals exhibited increased
growth rates and volume contradicts the expectations that growth rates would be reduced in
these animals. If re-orientation did indeed cause a reduction in feeding and respiratory
potential as expected, how did the animals mobilise the extensive energy required for the
production of new tissue recorded in this experiment? The rapid and significant increase in
sponge width (the shorter axis re-orientated perpendicular to the flow) occurring between
time 1 and time 2 can be attributed to the significant increase in tissue production
(illustrated by the increase in volume) rather than to re-arrangement of existing sponge
tissue (i.e. movement of tissue from the longer axis to the shorter axis). The energy
necessary for the increased tissue production recorded in the early stages of this experiment
may possibly have relied upon the pre-existing energy reserves within the sponges. These
reserves may have been depleted in the later stages of the study, hence the decrease in tissue
production recorded during this time. Energy storage and mobilisation of these reserves in
sponges is an area that requires further investigation.
Although length (the longer axis re-orientated to run parallel to the water flow)
decreased significantly between time 1 and time 4, the greatest decrease occurred between
times 3 and 4, a slower response than that occurring in width. This slower response may be
a consequence of the reduced energy reserves remaining in the sponge, resulting from the
production of new tissue occurring between time 1 and time 2. Alternately, re-arrangement
of tissue in the length axis may not have been as critical to sponge survival as re-orientating
the width axis for capture of food and oxygen. Re-arrangement of existing material is
potentially less metabolically expensive than the production of new sponge tissue. This
may indicate that tissue production in the surface perpendicular to water flow may be a
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J.I. McDonald et al. / J. Exp. Mar. Biol. Ecol. 296 (2003) 13–22
more effective or faster mechanism for increasing the length of this axis albeit a more
energy demanding one. There was no change in height of re-orientated sponges, both from
time 1 to time 4 and relative to controls. Distance above the substratum was not altered by
the movement of the sponges thus it was unlikely that changes in this dimension should
differ between treatments. Height of these sponges is likely to be optimised for feeding and
respiration in this species.
This experiment illustrates the dynamic nature of sponge morphology and the capacity
for continuous and highly variable remodelling of tissue in these animals (Bond, 1999;
Bond and Harris, 1988; Galera et al., 2000; Kaandorp, 1991, 1994, 1999; McDonald et al.,
2001; Palumbi, 1984, 1986; Pronzato et al., 1998). To our knowledge this is the first study
to report changes in sponge morphology with an increase in tissue production and growth
rates due to re-orientation alone. The fact that Spongia sp. did not exhibit reduced rates of
growth, as may be expected based upon the potentially reduced rates of feeding and O2
intake, and higher risk of sediment smothering, highlights the resilience of this species.
Furthermore, it demonstrates that optimum orientation of this organism to flow is of
fundamental importance to the persistence of Spongia sp. in these intertidal habitats.
Determination of the actual physiological effects of re-orientation is an area that requires
further study, particularly as it relates to feeding and respiration. Increased growth rates and
increased tissue volume (initiated by re-orientation) identified in this study may be
beneficial to researchers growing sponges for bioactive metabolites or other purposes.
Acknowledgements
Thanks to Grey T. Coupland for her help in data collection and editing of this
manuscript. Collection of sponge specimens was made possible under Section 17 of the
Northern Territory Fisheries Act 1995. [AU]
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