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Porifera Research: Biodiversity, Innovation and Sustainability - 2007
239
How and why do sponges incorporate foreign
material? Strategies in Porifera
Carlo Cerrano(1*), Barbara Calcinai(2), Cristina Gioia Di Camillo(2), Laura Valisano(1), Giorgio Bavestrello(2)
Dipartimento per lo studio del Territorio e delle sue Risorse, C.so Europa, 26, 16132, Genova, Italy.
cerrano@dipteris.unige.it, valisano@dipteris.unige.it
(2)
Dipartimento di Scienze del Mare, Via Brecce Bianche, 60131, Ancona, Italy. b.calcinai@univpm.it,
g.bavestrello@univpm.it, c.dicamillo@univpm.it
(1)
Abstract: The selection and incorporation of foreign materials in sponges is a complex phenomenon: it involves both a
system of recognition of pinacocytes versus sand grain mineralogy and a system of coordination among cells, which transport
and engulf particles in specific areas of the sponge surface. Concerning the mineralogical characteristic of the incorporated
particles, it seems that quartz particles, when incorporated, could play an important role in collagen production. Among
incorporating species, two different modalities can be defined, depending on the habit of the species: i) soft-bottom species
(e.g. genera Oceanapia, Tectitethya, Cliona) engulf particles mainly from the base of their body and select mainly the size
of particles independently from their mineralogical characteristics; engulfed particles, due to their weight, help the sponge
to stabilize and to “anchor“ to the soft substrate; ii) in hard-bottom species (e.g. genera Chondrosia and Ircinia) ectosome
pinacocytes select particles, in relation to their size and mineralogy, and may incorporate them differently in some areas of
their body according to their skeletal arrangement.
Keywords: Porifera, selectivity, sediment incorporation, foreign inclusions, mineralogy
Introduction
Marine organisms, particularly in benthic environments,
have to coexist with a continuous sediment rain and have
adapted to this phenomenon in several ways (Miller et al.
2002). They can react cleaning their surface, more or less
actively, or by trying to exploit sediments to feed or to build
protective and/or structural elements.
Several organisms like protists (Takahashi and Ling 1984),
sponges (Teragawa 1986, Cerrano et al. 1999a), cnidarians
(Haywick and Mueller 1997) annelids (Wilson 1974, Main and
Nelson 1988), molluscs (Min-Da 1984), crustaceans (Dixon
and Moore 1997, Krasnow and Taghon 1997), echinoderms
(Massin and Doumen 1986), and tunicates (Kott 2006) are
able to use foreign material as a cover, to protect or mask their
body, building thecae, coats, tubes or other structures. Among
Porifera and Cnidaria there are examples of species able to
incorporate particles into their body. It’s generally assumed
that this strategy is performed to strengthen the skeleton but
the real meaning of it and the related mechanisms are often
unclear (Teragawa 1986).
One of the most debated problems regarding this
phenomenon is if organisms are able to select foreign
bodies or if they utilise every kind of particle available in
the surrounding environment. Generally this behaviour is
regulated by the ability of organisms to “handle” particles
so that a physical limit related to the particle size has to be
always considered. The most intriguing aspect is the ability
of some species to recognise the mineral characteristics of
the particles and therefore to select them (Bavestrello et al.
1996).
The aim of this paper is to review the incorporation of
foreign bodies in sponges, comparing the strategies of species
living on soft and hard substrates and suggesting possible
physical and biological explanations for this intriguing
behaviour.
Soft-bottom sponges
Even if sponges typically live on hard substrates, there
are several species more or less adapted to soft bottom
environments. These may live loose on the sediment often
partially or completely buried in it and survive well thanks to
some very special adaptations, which limit sponge rolling and
occlusion of aquiferous system by sand.
On soft substrates it is possible to observe sponge fragments
which occasionally may fall from coral or rocky reefs due to the
production of asexual reproductive bodies and/or fragments,
breakage during storms, localised infections by pathogens,
or predator bites (Wulff 1985, Battershill and Bergquist
1990). The survival of unattached fragments depends on their
ability to re-settle in a short span of time to avoid clogging by
sediments (Ilan and Abelson 1995). For these fragments the
incorporation of large amount of foreign bodies is crucial to
assume a gravimetric polarity which allows them to stabilize
and reorganize their aquiferous system.
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We can classify soft bottom sponges into three main groups
according to their adaptative strategies:
i) sponges living on the sediment surface,
ii) sponges partially buried,
iii) sponges with the body completely buried, with particular
anatomic adaptations.
Sponges on the sediment surface
Here we consider sponges that do not live exclusively on
soft substrates but that can easily survive on soft substrates,
fully regaining their vital functions. These non-sessile
specimens have been generally found in shallow sub-littoral
environments (Mercurio et al. 2006, Bell and Barnes 2002)
and in the deep sea (Barthel and Tendal 1993).
Examples of this habit can be found in lagoon environments
(Ise et al. 2004, Mercurio et al. 2006), where several
sponge fragments, often from species living typically on
hard substrates, can be present. In studies performed in the
Caribbean (Cerrano et al. 2004) and the Indonesian (Cerrano
et al. 2002) lagoons, the comparison between environmental
sediments and the particles incorporated by several sponge
species shows that they mainly contain the fraction larger
than 5 mm. Only a few species use the fractions available
in the surrounding substrates without size preferences. The
percentage of incorporated sediments can be highly variable,
between 5 and 99% per sponge dry weight.
A particular case concerns the gamma stage of Cliona
nigricans, an excavating Atlanto-Mediterranean sponge
living symbiotically with zooxanthellae that can grow with
different shapes: endolithic, into coralligenous accretions,
and massive, laid on detritic sediments (Fig. 1A). This
species can engulf from the base (Fig. 1B) huge amounts of
foreign material, up to 99% of its dry weight, being also able
to store the fraction of sediment larger than 5 mm (Calcinai et
al. 1999). Moreover, experimental data indicated that in this
species the mineralogical features of the engulfed particles
can affect morphogenetic processes, in particular quartz
negatively affects the growth of C. nigricans specimens
limiting the development of the oscula in the basal portion
of the sponge that is in direct contact with the grains. On
the contrary, oscula have been observed in specimens living
on calcareous sand (Cerrano et al. 2007), highlighting once
again the importance of substrate chemical composition on
benthic organism distribution and development (Cerrano et al.
1999b, Bavestrello et al. 2003). In massive specimens of C.
nigricans, the aquiferous system opens on the sediment using
a water expulsion mechanisms similar to the one described
for Spheciospongia cuspidifera in Belize (Rützler 1997).
Sponges partially buried in sediments
Several species can live on soft substrates even without
morphological adaptations to this environment. Tectitethya
crypta is a massive, shallow-water sponge common in
the Caribbean and frequently covered by a sediment and/
or algal coat, both on hard and soft bottoms. In lagoon
environments this sponge can occur either loose or anchored,
significantly varying its morphology (Cerrano et al. 2004).
This species incorporates all the granulometric size classes
of nearby benthic sediments, using them in different ways.
In the choanosome, sediments are sorted and distributed
according to their size: fine sediments (40-60 µm) are densely
aggregated in the choanosome, whereas coarse particles are
more evenly distributed in the lower portion of the body
were they contribute to the stability of the sponge (Fig. 1C).
Qualitatively, the choanosomal aggregations of fine sediment
contain more siliceous material than the ambient sediment of
the same size class. Microscopical analysis of the particles
shows that this species selects and incorporates allocthonous
sponge spicules, radiolarians and diatoms (Cerrano et al.
2004).
Another interesting species is Biemna fortis, living in
tropical lagoons in North Sulawesi (Indonesia). This sponge
displays two different growth patterns depending on the
thickness of unconsolidated sediments: when the sediment
layer is thick, the sponge assumes a cylindrical form and
incorporation is low; when there is a thin sediment layer the
sponge adheres to the basal coral rock, developing a massive
buried portion that is generally rich in embedded particles
(Cerrano et al. 2002).
Sponges specialised to psammobiontic habit
All the known species of the genus Oceanapia live on soft
substrates thanks to the ability of producing long fistules that
anchor the sponge body to the loose substrate and discharge
waste-water deep into the sediments (Werding and Sanchez
1991, Bavestrello et al. 2002). The specialisation of this
genus to soft substrates is evidenced also by the differential
production of secondary metabolites used as antipredatory
that are synthesised exclusively in the exposed portions in
O. sagittaria, suggesting that sediments are not just a mere
substrate where sponges can live with low competition but
also a refuge from potential predators (Schupp et al. 1999,
Salomon et al. 2001).
In lagoons O. amboinensis lives buried in unconsolidated
sediments among sea grasses. The sponge develops a massive
body and emerges from the sediment through numerous
closed fistules. The sponge body is whitish, while the
portions protruding from the sediment take an olive green
colour. The buried portion of the body incorporates a high
quantity of foreign materials, selecting particles larger than 2
mm, throughout the pinacoderm. Only exhalant areas, of 1-4
cm2, do not participate in this process (Cerrano et al. 2002,
Bavestrello et al. 2002). Oceanapia fistulosa lives from 15-20
m depth down to at least 80 m, grows partially buried in detritic
sediment (Fig. 1D). The globular sponge body, 5-15 cm in
diameter, bears on its upper side several closed cylindrical
fistules that emerge from the sediment generally covered by
epibionts. On the other side, other buried closed fistules are
strongly rooted in the sediments. The buried portion of the
sponge incorporates a lot of foreign material such as sand,
coral and shell fragments, particularly on the rooted fistules,
which can reach a length of 15-20 cm and 1 cm in diameter,
depending on the thickness and the granulometry of the
unconsolidated sediments. In fine sediments this species, to
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Fig. 1: Examples from soft-bottoms sponges. A. Specimen of Cliona nigricans living on detritic substrates. B. Detail of the lower face
of the sponge with several rocks having highly variable sizes. The fraction bigger than 5 mm is more abundant in the sponge than in the
ambient sediments. Arrows indicate oscular openings. C. Half cut specimen of Tectitethya crypta. White arrows indicate aggregations of fine
sediments, black arrow indicates coarse sediments. D. Drawing of Oceanapia fistulosa with the buried body mass covered by sand grains.
242
get stabilization, produces more rooted fistules, smaller in
diameter but longer than those in coarse sediments.
Hard-bottom sponges
Burial/smothering, scour/abrasion, and changes in the
physical characteristics of the substrate surface are the
three main mechanisms by which sediments may affect
benthic assemblages (Airoldi 2003). On hard substrates
sedimentation is partly due to particles suspended in the water
column and partly due to the detritus that rolls down vertical
cliffs (Bavestrello et al. 1995a). This may cause mechanical
damages in sponges and other benthic filter feeders, especially
by clogging the aquiferous system impeding filtration.
A solution to avoid sedimentation is generally represented
by the colonisation of substrates under overhangs, but in this
situation sponges have to compete with many other sessile
animals that share the same strategy. Other organisms choose
to grow vertically, limiting the surface available for sediments
as happens for several species of the genera Axinella or
Dysidea (Fig. 2A). Other species can clean their pinacoderm
using superficial cellular movements (Bond 1992) that can
easily either remove or take up several kinds of particles
transforming the problem of sediments into an opportunity
to providing a physical support to the skeletal development
(Fig. 2B).
According to Teragawa (1986) the sediment that settles on
the surface of Dysidea etheria may follow different pathways
being i) inhalated through ostia, ii) eliminated by transport or
through dermal membrane oscillations or mucus sloughing,
iii) incorporated into primary fibres, and iv) engulfed
into secondary fibres in case the sponge is overloaded by
sediments.
When sediments are incorporated into spongin fibres it is
possible to consider this localization as definitive but, on the
contrary, a turnover was described for the sediments engulfed
in the cortex of Chondrosia reniformis (Cerrano et al. 1999a).
This species, presenting a collagenous structure and lacking
its own spicules and spongin fibres, when anchored to a
substrate, is able to incorporate foreign material, discerning
from crystalline quartz sand grains and amorphous siliceous
opaline spicules (Bavestrello et al. 1998a, 1998b). Laboratory
experiments have shown that the cells of the sponge ectosome
play a key role in the selection processes: quartz particles
are incorporated while carbonatic particles are agglutinated
and drop out from the sponge ectosome. In C. reniformis
specimens anchored to the substrate, the upper ectosome
can distinguish between silica and carbonates, ability lost in
free, non-attached individuals, which incorporate both. This
behavior indicates that specific receptors are present and can
distinguish among the different mineralogical features of
the sediment. Depending on the environmental conditions
this mechanism can be switched on or off (Bavestrello et al.
1998b).
The turnover of particles inside the body of C. reniformis
is due to the ability of this sponge to dissolve quartz crystals
releasing silicate (Bavestrello et al. 1995b).
In C. reniformis the amount of incorporated sediment was
used as a character to separate different species (Wiedenmayer
1977) while in dictyoceratid sponges the presence of sediment
in fibres or as a dermal crust is considered as a character
to distinguish between different genera (Vacelet 1959).
Nevertheless, Pronzato et al. (2004) considered the amount
of mineral granules a specific character to distinguish Ircinia
felix from I. variabilis.
The evidence of a specific and fine tuned mechanism to
select particles, according to their mineralogical features,
suggests that a mineralogical and granulometric analysis
of incorporated sediments may represent a tool for the
classification of problematic taxonomic groups.
The genus Ircinia is characterised by spongin fibres cored
with foreign debris. In an unpublished investigation we have
compared the foreign bodies incorporated by two sympatric
species of Ircinia (I. variabilis and I. retidermata) inhabiting
two different areas. Results show that part of the sediment
is included into growing fibres, probably definitively, while
another portion is incorporated into the choanosomal tissue
where it is subjected to a quick turn over. In both species,
the material incorporated into fibers and the one engulfed
in the choanosomal tissue are different. Ircinia variabilis
incorporated sponge spicules and sand grains in the same
proportion both in the ectosome and in the mesohyl (here
considered as choanosome excluding fibres). Spongin
fibres include almost only sand grains (Fig. 2C-F). Ircinia
retidermata has a more homogeneous ectosomal coat of quartz
grains. The amounts of ectosomal sediments allowed the
determination of interspecific differences while choanosomal
ones (not considering spongin fibres) are affected by local
sedimentation rates, so that differences at intraspecific and
interspecific level can be similar and not useful for species
classification.
Discussion
Sediment incorporation is a widespread aptitude in sponges
and is observed in species belonging to different not-related
groups (Fig. 3). On the contrary in cnidarians the incorporation
of sediment occurs only in the order Zoanthidaea. With this
exception, several other metazoans use foreign bodies to build
external protective structures, but no one is able to incorporate
foreign bodies in their tissues. In sponges and cnidarians
particles are embedded in the collagenous mesohyl/mesoglea,
and spongin fibres and their incorporation is mediated by the
interaction with dermal cells. In the incorporation processes
the most intriguing aspects relate to the ability of selecting
the mineral features and the size of the foreign bodies and
their transport to definite areas.
Sediment selection based on mineral composition is not
exclusive of hard-bottom sponges but can occur after stable
anchoring also in sponges living on soft bottoms as described
in Tectitethya crypta. On hard bottoms, Ircinia retidermata
Fig. 2: Examples from hard-bottoms sponges. A. Dysidea avara
specimen in its natural environment. B. Detail of the ectosome
with accumulation of sediments on the tip of conules. C. Detail
of the ectosome of Ircinia variabilis. D. Drawing of a section
of I. variabilis. E. Drawing of a single conule of I. variabilis
with detail of a primary fibre and sediment coat. F. Electron
micrograph of a conule of I. variabilis.
243
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Fig. 3: Sponges living both on hard and soft bottoms can incorporate sediment in a selective way or not. The soft bottom sponges that
are specialised to live in unconsolidated sediments (ex. Oceanapia spp.) get true stabilization via peculiar morphological adaptations. In
this case incorporation can be selective towards particles size. Unanchored sponges incorporate without selection until they stabilize, then
their behaviour can become selective. Fixed hard bottom sponges have a selective behaviour both vs. particles mineralogy and/or size.
Unselective behaviour is generally related to stabilization, selection towards particles size can be related to stabilization and/or skeletal
growth, selection towards mineralogy may be related to some biological need.
selects particles, organising quartz grains with homogeneous
size in the ectosome. Although there is some evidence
that in Cliona nigricans the incorporated quartz particles
negatively affect the sponge growth, the sponge incorporates
these particles indiscriminately if they are present in the
surrounding sediments. In Chondrosia reniformis the mineral
discrimination of the upper ectosome may be switched on by
the adhesion of the sponge to the substrate. When attached,
the upper side collects quartz and silicates while the lower
bottom side specifically engulfs the calcareous particles, thus
helping the sponge to attach to the substrate. When unattached,
the sponge does not select and incorporates with modalities
that resemble those described for soft bottom species, being
its priority the stabilisation and a new polarity.
This is a puzzling behaviour because it is not easy to
understand why a sponge selects and engulfs particles to
dissolve them. A possible explanation was suggested by the
evidence that the expression of the gene for collagen was
found to be dependent on the silicate concentration (Krasko
et al. 2000, Nickel and Brümmer 2003). In this way the
induction of collagen production by quartz dissolution may
be hypothesised (Bavestrello et al. 2003).
In soft-substrates specimens, selection is mainly
dimensional. Several sponge species living on soft substrates
select from the environmental sediment mainly the larger
granulometric fractions. Incorporation happens in two
ways: i) pinacocytes may recognise and incorporate only
the larger particles fraction; ii) the pinacoderm may engulf
sediment of all available size classes and subsequently
sort them within the mesohyl, selecting the larger particles
and expelling the smaller ones. In both cases a selection
mechanism at the cellular level has to be hypothesised. This
ability is particularly evident in Tectitethya crypta because of
the presence of two even more different ways to handle fine
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and coarse sediments. Fine sediments are concentrated in the
nuclei within the sponge body while coarse grains are moved
to the base of the sponge to anchor and stabilize by gravity.
The incorporated sediment is used for very different
purposes in different species. Soft-bottom sponges generally
use foreign bodies to anchor and to gain a gravimetric polarity.
This stability allows the sponge to (re)organise its aquiferous
system in the most efficient way.
Hard-bottom sponges use foreign bodies to reinforce
their skeletal structure but this structural use is not the only
possible. The case of Chondrosia indicates that this species
is able to metabolise quartz, with possible effects on the
metabolism of collagen. These data can lead to the hypothesis
that in sponges with a skeleton structured by a spongine net
the inclusion of particles in the growing fibres could stimulate
the production of spongine.
Particle selection and handling has to be related to the self/
non-self recognition mechanisms in sponges. Even if sponges
lack a specific immune system, several cellular processes can
enable discrimination between true symbionts from potential
pathogenic microorganisms (Steindler et al. 2007) or develop
a sort of primitive short-term immune memory, as evidenced
by allografts (Bigger et al. 1982). Recognition mechanisms
are modulated by sponge condition, attached or unattached to
a substrate (Bavestrello et al. 1998b). Several studies suggest
that the allorecognition system may change during ontogeny
and this aspect is generally considered in the case of chimeric
sponges (Maldonado 1998, McGhee 2006). The fusion among
different sponge species in adult phase may help in stabilizing
rolling sponges (Cerrano et al. 2004), and could be related to
the loss of selectivity evidenced in unanchored specimens.
In conclusion the use of sediments depends on the habit of
the species and can be selective (when sponges are stable on
the substrate) or not (when sponges are not stable). Moreover,
the mineralogical composition of particles can affect sponge
growth, in particular quartz that, depending on the species,
can enhance or limit this process.
Acknowledgements
Authors are indebted with Marzia Sidri (Porifarma, Wageningen)
and two anonymous referees for helpful comments. This paper
comes from a lecture hold in the framework of the Biologisches
Kolloquium Wintersemester at the Universitaet of Stuttgart.
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