Oecologia (BerJ.) 5, 85-95 (1970)
Spatial Competition among Porifera:
Solution by Epizoism*
KLAUS RUTZLER
Department of Invertebrate Zoology, National Museum of Natural History,
Smithsonian Institution, Washington, D. C. 20560
Received March 15, 1970
Summary. Sponges settling on solid substrates which are separated by sediment
bottoms compete for the limited space. Some species have solved this problem
by occurring as epizoans, thus avoiding the risk of being expelled from the habitat.
The supporting species on the other hand, are specialized in that they possess
skeletogenous ectosomal structures and aquiferous processes to maintain their
integrity and to escape starvation or suffocation. Although specimens are sometimes
intimately interwoven no chimaerid mixing of tissues was observed.
Introduction
In sponges, as in all sedentary organisms, the dispersal of free?
swimming larval stages is controlled by a number of physical and chemical
parameters. Success of settlement and subsequent metamorphosis depends
on the duration of favorable conditions. If these sensitive stages of
the life history are completed successfully, only extreme forces will
endanger the further development of the organism. .
The availability of a suitable substrate is one of the critical factors
for sponge colonization. In shallow water or wherever strong water
movement occurs it should be solid or at least stable enough to permit
development of the organism until sexual maturity is reached. Occa?
sionally, the sponge itself contributes to the stabilization of its substrate
by attaching to and thereby connecting several pieces of substrate
(sand grains, shells, gravel, etc.) unless a sudden storm during estab?
lishment of the colony prevents this effort. The influence of substrate
stability on the species composition of shallow-water sponges in the
Adriatic Sea has been demonstrated in an earlier contribution (Riitzler,
1965a). There also, some mechanisms of spatial competition were
discussed. The most common situation is that fast growing and otherwise
.. This work was supported in part by Smithsonian Research Foundation
Grant Sg 068104. I thank Dr. H. Forstner (Innsbruck) for his assistance in the
field. Miss M. Dwyer prepared the drawings.
7 Oecologia (Berl.), Vol. 5
86 K. Riitzler:
robust species over-grow and suffocate their less vigorous neighbors,
although several observations have been made on sponges which over?
grow each other to a varying degree without any harm to eilher specimen.
It is the purpose of this communication to discuss such species, and
to present quantitative data and anatomical findings on these interspecific
relationships.
Materials and Methods
Spatial competition among sponges was studied in three Adriatic
localities (Istria, Yugoslavia) in May 1962, September 1964 and March
1968. The moderately wind-exposed bays of Korrente Cape and Andrija
Island (Riitzler, 1965 b, Fig. 25) contain stable rocks of 15-200 liters
volume in 1-10 m depth. They could be turned over by two divers in
order to reach the sponge-covered lower surfaces.
At the exposed Cape of Cuvi blocks of 5---':'15 liters were collected
from 1 m depth where they were securely anchored in rock channels
(Riitzler, 1965b, Figs. 25, 30).
In Polari Bay several large boulders (1-3 m3 ) protrude from the
sandy bay bottom in about 1.5-2 m of depth (Riitzler, 1965b, Figs. 25, 32).
Numerous miniature caves measuring 15-40 cm across were eroded
at the bases of the boulders. The sponges clustered on the upper surface
of the cavities.
The sponge crusts and clusters were measured (covered surface area in cm2, to
nearest 0.5 cm), removed with a knife or scalpel, fixed in 4 % formalin in sea-water
and, after a week, transferred to 80% ethylene alcohol. The specimen complexes
were photographed or drawn in the laboratory and then roughly dissected with
razor blades for gross anatomy. Representatiye samples were embedded in paraffin,
or 12% gelatin with subsequent freezing (cryostat) and cut at 7 I.I.m. Mallory's stain
and haemotoxylin-eosin were used for staining.
Results
Species Composition and Quantitative Data. The species composition
on blocks from Korrente, Andrija and Cuvi was quite uniform. Only
encrusting and low-growing (pillow-shaped) specimens were present,
due to the limited vertical spaces between lower rock surface and
sediment of the sea-floor. Tidal and wind-generated currents provide
abundant nutrients and keep the crevices clear of sediments. The
substrate itself provides protection from solar radiation and therefore
inhibits growth of competing algae. The spatial limitations of these
habitats exclude most scraping predators (e.g. echinoids, fishes). In
summary, we are dealing with miniature cave habitats which provide
all favorable conditions for abundant sponge growth but only restricted
substrate areas which are separated by dynamic sediment bottoms.
Spatial Competition among Porifera 87
Fig. 1. Sponge assemblage from miniature cave in Polari Bay (drawing after photo?
graph and preserved specimens before dissecting). The main supporter of most of
the assemblage is Fasciospongia cavernosa (a). Epizoic species which in parts are
also supporters are: Ircinia spinosula (b), Crambe crambe (c), Ircinia oms (d),
Clathrina falcata (e), Buskia sp. (Bryozoa, f), Bycon sp. (g), Antho involvens (h),
Leuconia solida (i), Cornularia cornucopiae (Anthozoa, i) (1/2 x)
The following six of a total of 34 sponge species are dominant in
this environment (values in % of the area covered by the total sponge
population) :
1rcinia oros
~ascios~ia cavernosa
Crambe crambe
A ntho involvens
1rcinia spinosula
Spongia virgultosa
24.7%
14.2%
12.3%
6.8%
6.6%
6.6%
One hundred and thirty four incidences in 54 species combinations
were noted where specimens of the same or of different species were
growing upon each other (Fig. 1). Where necessary, the healthy state
of the overgrown sponge could be confirmed by histological sections.
7?
Table I. Qualitative and quantitative data on sponge epizoism
00
Suppor~ing species Total size Over- Epizoic species Total size Epizoic Degree of 00
(cm2) grown (cm2) area attachment
(No. of area (No. of (cm2) L=Low
specimens) (cm2) specimens) M=Medium
H=High
Penares helleri (0. Schm.) 92.0 (2) 86.0 Prosuberites longispina Tops. 4.0 (I) 4.0 H
Antho involvens (0. Schm.) 109.0 (I) 82.0 H
Pachastrella monolilera 28.5 (3) 24.0 Terpios lugax Duch. and Mich. 4.5 (1) 4.5 H
O. Schm. Myxilla rosacea (Lieberk.) 12.0 (1) 5.0 M
Crambe crambe (0. Schm.) 14.5 (1) 14.5 H
Placospongia decorticans 34.0 (1) 5.5 Clathrina clathrus (0. Schm.) 2.0 (1) 2.0 L
(Hanitsch) Dysidea avara (0. Schm.) 3.5 (1) 3.5 L
Mycale 7nassa (0. Schm.) 18.0 (1) 4.0 Haliclona viscosa Sara 11.5 (1) 4.0 H ~
Antho involvens (0. Schm.) 7.5 (1) 2.5 Clathrina lalcata (H.) 2.5 (1) 2.5 L ~
Agelas oroides (0. Schm.) 53.0 (1) 18.5 Oscarella lobularis (0. Schm.) 18.5 (1) 18.5 M =,..
N
Gelliuslibulatus (0. Schm.) 72.0 (1) 4.5 Aplysilla sui/urea F. E. Schulze 4.5 (4) 4.5 H CD...
Haliclona viscosa Sara 37.0 (2) 7.0 Mycale'rnassa (0. Schm.) 8.5 (1) 7.0 H
Aplysilla sullurea F. E. Schulze 3.5 (6) 3.5 Gellius libulatus (0. Schm.) 122.0 (2) 3.5 H
Dysidea avara I. pallescens 9.0 (1) 2.0 Clathrina lalcata (H.) 2.0 (1) 2.0 L
Spongia virgultosa (0. Schm.) 189.0 (7) 172.0 CI!Lthrin!L clathrus (0. Schm.) 2.5 (1) 2.5 L
Clathrina lalcata (H.) 6.5 (3) 6.5 L
Oscarella lobulari.s (0. Schm.) 6.5 (1) 6.5 M
Spirastrella cunctatrix O. Schm. 15.0 (1) 15.0 M
Crambe crambe (0. Schm.) 56.0 (2) 56.0 M
A nchinoe tenacior Tops. 23.5 (I) 23.5 M
Antho involvens (0. Schm.) 24.0 (I) 17.0 M
Gellius libulatus (0. Schm.) 8.0 (1) 8.0 1\'1
Dysidea avara I. pallescens (0. Schm.) 7.0 (1) 70 L
Ircinia lascicutata (Pallas) 16.5 (1) 9.5 M
Ircinia oros (0. Schm.) 16.5 (1) 16.5 L
lrcinia (S.) spinosuta (0. Schm.) 4.0 (I) 4.0 L
Hippospongia com1nunis (Lam.) 16.5 (1) 8.5 Anchi1we ten!tcior Tops. 8.5 (1) tl.5 1\1
Cucospongia scalar-is O. Schm. 6.5 (I) 4.5 Ircini!t oros (0. Schm.) 4.5 (I) 4.5 L
lrcinia oros (0. Schm.) 476.0 (17) 287.0 Clathrina falcuta (H.) 3.0 (I) 3.0 L
Leuconia solida (0. Schm.) 15 (I) 1.5 1\1
Sycon sp. 0.5 (I) 0.5 L
Geodia cydonium (Jam.) 16.0 (I) 16.0 L
Crambe crambe (0. Schm.) 56.0 (1) 56.0 H
Antko involvens (0. Schm.) 22.5 (I) 12.5 H
Haliclona cratera (0. Schm.) 43.0 (I) 33.0 1\1
Petrosia ficiformis (Poiret) 178.0(1) 26.0 L
Aplysilla sulfurea F. E. Schulze 1.0 (2) 1.0 1\1 Ul
."
Dysidea avara (0. Schm.) 7.5 (I) 7.5 1\1 '".,..lrcinia oras (0. Schm.) 163.0 (3) 123.0 1\1 E
lrcinia (S.) spinosula (0. Schm.) 7.0 (I) 7.0 1\1 ??
lrcinia (S.) 1nuscarum 17.5 (I) 1.5 Aplysilla sulfurea F. E. Schulze 1.5 (I) 1.5 1\1 8'g(0. Schm.) .,..;;:
lcinia (S.) spinosula 211.5 (9) 89.5 Clatkrina falcata (H.) 6.5 (I) 6.5 L o':l
(0. Schm.) Leuconia solida (0. Schm.) 1.5 (I) 1.5 M
'"3
0
Hemimycale columella (Bow.) 14.0 (I) 14.0 H :lO<l
Cra.mbe crambe (0. Schm.) 41.0 (I) 41.0 H '"d0
Antho involvens (0. Schm.) 14.5 (I) 14.5 H ...;:;;
Gellius fibulatus (0. Schm.) 5.0 (I) 5.0 1\1 "i!l
lrcinia oros (0. Schm.) 7.0 (I) 7.0 1\1
Fasciospongia cavernosa 480.0 (10) 452.0 Clatkrina falcuta (H.) 2.0 (I) 2.0 L
(0. Schm.) Leuconia solida (0. Schm.) 9.0 (2) 9.0 1\1
Crambe crambe (0. Schm.) 246.0 (5) 246.0 H
Antko involvens (0. Schm.) 50.0 (2) 50.0 H
Spongia virgultosa (0. Schm.) 31.0 (I) 31.0 M
lrcinia oras (0. Schm.) 162.5 (4) 114.0 H
17 species L 1,751.5 (65) LI,172.5 26 species L 1,608.5 (73) L 1,172.5
00
'"
90 K. Riitzler:
All data relevant to the observed epizoism of Adriatic sponges
are listed in Table 1. The degree of attachment was classified as "low"
when the specimens separated during handling or fixation; as "medium",
if they had to be peeled from each other forcibly; as "high", if mechanical
separation resulted in injuring either of the specimens. For the systematic
description of the species see Riitzler (1965b).
Table 2. Summary of data on sponge epizoism
Position of Number Total Over- Epizoic Degree of
sponges of size of grown area in % attachment (%)
within species specimens area in % of total
association in % of of total specimen H M L
total specimen size
population size
Supporting only 8 21.7 82.5 57.6 27.0 15.4
Epizoic only 17 24.5 78.5 27.5 37.5 35.0
Supporting 9
or epizoic
Supporting 30.5 56.0 27.7 42.5 29.8
Epizoic 23.3 67.0 51.5 36.5 12.0
Total number of specimens: 34. Total size of population: 3,360.0 cm2?
Total number of species combinations: 54. Total contact area: 1,172.5 cm2 ?
Total number of incidences: 134.
A summary of the listed data (Table 1) is given in Table 2. From
this it appears that "supporting only" species are quite specialized in
their function; they share a much higher percentage of coverage and
stronger attachment than the facultative supporters. Of the epizoic
species it can merely be said that either they arrive too late to occupy
the primary substrate or they were expelled thence by their competitors.
However, by means of epizoism they still are able to survive in the
habitat. Whether they again expelled other species commonly occurring
in the area (Riitzler, 1965b) but not found in the studied samples cannot
be decided without experimental evidence. Successions of different
species did not occur during the 6 years' duration of the observations.
Anatomy of Attachrnent. Electron microscopy studies by BnJnsted
and Carlsen (1950) and Borojevic and Levi (1967), revealed that sponges
are attached to their substrate by a layer of interwoven collagen fibrils
secreted on contact with the substrate by basopinacocytes or baso?
pinacoblasts. At least among the species investigated, it is likely that
this "horny" layer corresponds to spongin "A" as understood by
Gross et al. (1956).
Spatial Competition among Poriiera 91
2
Fig. 2. Antlw involvens growing on Penans he/leri. The crevice between the two
specimens and an ostium of Penares can be noted (paraffin ection, 7 fLm Mallory
stain) (50 x)
Fig. 3. Acantho tyles of Antho involven glued onto the cortex of Pena1?es helleTi
(paraffin section, 7 fLID, Mallory stain) (240 X )
Fig. 4. arne preparation a in Fig. 2. Oxeon of PenaTes partly protruding into
Antho (50x)
From Table 1 it become apparent that all upporting pecie which
are frequently or heavily overgrown either have a cortex of iliceou
spicules (Penares, Pachastrella) or belong to kerato e genera (e.g. Spongia,
Ircinia, Fasciospongia). The latter po e a well-developed ecto omal
membrane of parallel bundle of spongin "A" fibrils. How important
is a skeletogenous ecto omal structure for successful overgrowth ~ Is
the integrity of the two specimen involved unimpaired or do incidence
of chimaerid specimens occur, as described by Little (1966) ~
The remarkable case of 100% coverage occurred in one of the species
with cortical siliceous skeleton, Penares helleri. The epizoic Antho
involvens covered and extended beyond it so that the true ituation
wa only discovered in the micro-anatomical preparation (Fig. 2). The
3
4
92 K. Riitzler:
-~-~-G-.
a b c d e
F'ig.5a-e. Ircinia spinosula (stippled) and Ircinia aras in different states of
overgrowing each other (schematic reconstruction; upper row in top view, lower
row in cross section): Ircinia aras is settled (a), expands (b), is being partly over?
grown (c, d), continues to grow at the free ends (d) which fuse together enclosing
part of Ircinia spinosula (e) (1/3X)
question arises as to how Penares is able to sustain its water currents
and hence obtain food and dispose of waste products. Fig. 3 shows how
the spicules (acanthostyles) of Antha are glued onto the cortex of Penares
by means of small patches of spongin. The tissue in between these points
of attachment is elevated leaving a crevice of 30-50 [Lm, Assuming
that this crevice is not an artifact its presence would make the necessary
water circulation possible, In favor of this view is also the fact that ostia
are developed and apparently functional in Penares. The supporting
species suffered complete loss of pigments as the only sign of its unusual
situation. On the other hand, several of the large Penares oxeas were
noted projecting partially into the choanosome of Antha (Fig. 4). This
can be explained as a reaction to too close a contact and consequent
obstruction of water circulation. Similar reactions have been observed
in Tethya (1) (unpublished) which expells its large diactines under
unfavorable conditions.
In most other instances the contact is more intimate, parts of the
supporting specimen, however, still being exposed to water. Usually, the
basal membrane of the epizoic specimen is firmly fused with the ectosomal
membrane of the supporter which in such places has no openings to the
aquiferous system developed.
The history of a case of competition could be reconstructed from
dissection of a mass consisting of two Ircinias (Ircinia aras and Ircinia
spinosula) (Fig. 5). By alternative overgrowing the two specimens were
finally completely interwoven. At the areas of contact the overgrown
specimens had lost all pigments and even the conuli, which are otherwise
typical surface structures.
Spatial Competition among Porifera 93
6
Fig. 6. Close attachment of Crambe cmmbe on b'cinia spinosula; sllrface and basal
membranes fused together (paraffin section, 7 fim, Mallory stain) (240 x)
Fig. 7. Preparation as in Fig. 6; Haliclona viscosa on M ywle massa (240 X )
Fig. 8. Preparation as in Fig. 6; Crambe crambe on Fasciospongia cavemosa (240 X )
Conuli and similar surface processes are not always lost but often
closely duplicated by the epizoic specimen, e.g. Haliclona viscosa on
M veale massa, Crarnbe crarnbe on I rcinia spinosula, I rcin?ia 01'OS on
Fasciospongia eavernosa, Crarnbe crarnbe on Fasciospongia eaverno a
(Figs. 6-8).
Another surface structure - membrane incorporated sand grains
in Ircinias - can either be lost or solidified during contact. For example,
where Crarnbe crarnbe is attached to Ircinia oros the usual netlike sand
structure on the Ircinia surface has turned into a solid sand layer.
Likewise, Leuconia solida is anchored on a thick sand layer on the Ircinia
oros surface. On the other hand, where Haliclona cratera touches b'cinia
oros all conuli, pigment and sandgrains are lacking, the Ircinia is slightly
depressed at the contact area; exceptionally, a concentration of ostia
was developed there. This Haliclona?lrcinia relation is the only one
which can be suspected to be of more than a facultative nature. Haliclona
7
8
94 K. Riitzler:
Fig. 9. Gellius fibulatus supporting and overgrowing Aplysilla sulfurea (left), which
thus also occurs endozoic. Spongia virgultosa (right) overgrown by Gellius, only the
oscular tubes are showing on the surface (1 X )
cratera has usually been found attached to Ircinia oros (Topsent, 1925;
Riitzler, 1966), but also on Ircinia fasciculata (Sara, 1958; 1961) Ircinia
spinosula and Petrosia ficiformis (Riitzler:, 1966).
An unusual relation was observed between Gellius fibulatus and
Aplysilla sulfurea (Fig. 9). The small growing species of Aplysilla not
only settles on Gellius but is enclosed in the tissue as the supporting
specimen grows. Thus it lives in unchanged condition several millimeters
below the Gellius surface using its host's aquiferous system for its own
requirements.
A very close attachment and intermingling occurs between Haliclona
viscosa and M ycale massa. The histological sections, however, reveal
that although both specimens grow into each other in a very complex
way they remain clearly separated by basal and ectosomal membranes
(Fig. 7).
Spongia virgultosa and Fasciospongia cavernosa seem to be specialized
" supporters". In fact, in the course of this work they have never been
observed other than completely overgrown, with the exception of the
oscular tubes or processes which remain uncovered for water exchange
(Fig. 9).
Epizoic organisms other than sponges were rarely seen. The tunicate
Didemnum maculosum (Milne-Edwards) was the only one which was
sometimes closely attached to sponges. Anthozoans, like Cornularia
cornucopiae Pallas and bryozoans, like Buskia sp. use stolons when
settling (Fig. 1). The scyphozoan Stephanoscyphus is a well known
endobiont of sponges. Neither type can be considered as a significant
epizoan of sponges.
To summarize, one might say that skeletogenous surface and basal
structures are always present where epizoism occurs, and they may
even be strengthened by incorporated sand. No chimaerid mixing of
specimens from different species was found. Firm cortical structures and
tubular aquiferous processes facilitate a high degree of epizoism. With
Spatial Competition among Porifera 95
the possible exception of Haliclona cratera all observed incidences are
cases of facultative epizoism.
Further study of more and different isolated substrate types will be
needed to obtain a complete picture of the occurrence and mechanism
of epizoism among sponges. For this purpose the suitability of mangrove
(Rhizophora) roots in certain parts of the tropical Atlantic has already
been pointed out (Riitzler, 1970). A more experimental approach to the
subject might reveal chemical attractions or immunological reactions
influencing the interspecific relations among supporting and epizoic
species.
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Gross, J., Sokal, Z., Raugvie, M.: Structural and chemical studies on the connective
tissue of marine sponges. J. Histochem. Cytochem. 4, 227-246 (1956).
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Riitzler, K.: Systematik und Okologie der Pot'iferen aus Litoral-Schattengebieten
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Topsent, E.: Etude de spongiaires du Golfe de Naples. Arch. Zoo!. expo gen. 63,
623-725 (1925).
Klaus Riitzler
Dept. of Invertebrate Zoology
ational Museum of Natural History
Smithsonian Institution
Washington D.C. 20560. U.S.A.
Universitatsdruckerei H. Sturtz AG Wurzburg
Printed in Germany