Download Symbiotic relationships between sponges and other organisms from

Porifera Research: Biodiversity, Innovation and Sustainability - 2007
147
Symbiotic relationships between sponges and other
organisms from the Sea of Cortes (Mexican Pacific
coast): same problems, same solutions
Enrique Ávila(1,2*), José Luís Carballo(1), José Antonio Cruz-Barraza(1,2)
Laboratorio de Ecología del Bentos, Instituto de Ciencias del Mar y Limnología. Universidad Nacional Autónoma de
México, Estación Mazatlán, Avenida Joel Montes Camarena S/N, Apartado Postal 811, Mazatlán 82000, México. Tel.
+52 669 985 28 45. Fax: +52 669 982 61 33. [email protected]
(2)
Posgrado en Ciencias del Mar y Limnología, UNAM, Mazatlán, México
(1)
Abstract: This study provides a morphological description of three symbiotic associations between sponges (Haplosclerida)
and other macroorganisms from the Sea of Cortes (Mexican Pacific Ocean). These associations include: (1) a two-sponge
association (Haliclona sonorensis/Geodia media), (2) a sponge-red macroalga association (Haliclona caerulea/Jania adherens)
and (3), a sponge-coral association (Chalinula nematifera/Pocillopora spp.). So far these interactions seem to be obligatory
for the sponges (Haliclona spp. and C. nematifera), since we have never found them living in isolation. Interestingly, similar
associations have been described from other places around the world. Associations quite similar to (1) have been described
from the Caribbean, and associations (2) and (3) are comparable to others described from the Western Pacific. Instead of
comparing these associations with their “sibling” associations worldwide, we discussed the ability of haplosclerid sponges
to form symbiotic associations with other organisms, since these sponges pertain to the group of which the most associations
have been described.
Keywords: Sea of Cortes, sponge-alga, sponge-coral, symbiotic associations, two-sponge
Introduction
Sponges are one of the major phyla found in the hardsubstrate marine benthos (Sarà and Vacelet 1973). One of their
more interesting characteristics is that they are able to establish
a great diversity of relationships (mutualism, commensalism
and parasitism) with unicellular and multicellular organisms
(Palumbi 1985, Rützler 1990, Magnino and Gaino 1998, Ilan
et al. 1999, Wulff 1999, Thakur and Müller 2004).
Most of these relationships have been reported in the
Caribbean (West 1979, Rützler 1990, Wulff 1997a, 1997b,
1999, Wilcox et al. 2002), Mediterranean Sea (Uriz et al.
1992, Gaino and Sará 1994), Red Sea (Meroz and Ilan 1995,
Ilan et al. 1999), Indo-Pacific region (Steindler et al. 2002,
Calcinai et al. 2004) and Western Pacific (Vacelet 1981,
Trautman et al. 2000). Surprisingly, in a large number of
cases, the same species are involved in similar interactions in
different oceans (Ilan et al. 1999, Wulff 2006). For example,
the sponges Haliclona caerulea Hechtel, 1965, Haliclona
cymaeformis Esper, 1794 and Dysidea janiae (Duchassaing
and Michelotti, 1864) are species found to establish similar
interactions with red macroalgae (Vacelet 1981, Rützler 1990,
Trautman et al. 2000, Carballo and Ávila 2004). However, it is
unknown whether this group of “cosmopolitan” associations
occurs in the East Pacific Ocean.
The order Haplosclerida (Demospongiae) is the group
in which the most of the symbiotic relationships have been
registered with the family Chalinidae Gray, 1867 accounting
for more than 50% of the associations described in this
order (see discussion). Sponges of this order can establish
associations with microorganisms such as bacteria (Vacelet et
al. 2001), cyanobacteria (Steindler et al. 2002), dinoflagellates
(Garson et al. 1998) and zoochlorellae (Frost and Williamson
1980), and with macroorganisms such as polychaetes (Dauer
1974), macroalgae (Vacelet 1981), mangroves (Ellison et al.
1996), barnacles (Ilan et al. 1999), hydrozoans (Schuchert
2003), anthozoans (West 1979), ophiurids (Henkel and
Pawlik 2005), insects (Gaino et al. 2004) and other sponges
(Wilcox et al. 2002).
In the present study, we describe three interactions involving
haplosclerid sponges from the Sea of Cortes (Mexican Pacific
Ocean). They are a two-sponge association (Haliclona
sonorensis-Geodia media), a sponge-alga association
(Haliclona caerulea-Jania adherens) and a sponge-coral
association (Chalinula nematifera-Pocillopora spp.). We
discuss the surprising parallelism that exists worldwide,
given that very similar interactions occur in different oceans.
In addition, we comment on the characteristics that this group
– in which more symbiotic relationships have been registered –
has in order to establish these symbiotic associations.
148
Material and methods
Specimens of the three associations were collected by
SCUBA diving from 2 to 12 m depth, in four localities from
the Sea of Cortes (Eastern Pacific Ocean, Mexico) (Fig. 1).
We followed the techniques described by Rützler (1974) for
spicule and tissue preparations for light microscopy. Crosssections of the specimens were washed in distilled water
and then dried on a cover glass and coated with gold for
scanning electron microscope (SEM) observations. A number
of 20 to 50 spicules chosen randomly were measured (length
x width) from each of the specimens studied. The number
between brackets in each description is the average. After
the description, the specimens were fixed in formaldehyde
4% and after 24 h they were transferred to 70% alcohol for
their preservation. All the specimens were deposited in the
Colección de Esponjas of the Instituto de Ciencias del Mar
y Limnología, UNAM (LEB-ICML-UNAM), in Mazatlán
(Mexico).
In the Haliclona sonorensis/Geodia media association, the
surface of G. media covered by H. sonorensis was estimated.
First we took photographs of the specimens, then we
determined the covered area (%) using the computer program
Coral Point Count with Excel extensions (CPCe) (Kohler and
Gill 2006). The frequency of the C. nematifera/Pocillopora
spp. association was determined in three transects of 50 m
length at a depth between 4 to 6 m. In each one of these
transects we chose 20 colonies of coral at random, and
determined the percentage of these containing sponge. In
the same area, we also checked if the sponge was on another
type of substratum. For each sample of the association we
determined the species of coral and estimated the percentage
of the colony overgrown by the sponge as number of branches
with sponge of the total of branches.
Results
Association Haliclona sonorensis Cruz-Barraza and
Carballo, 2006 – Geodia media Bowerbank, 1873
Material examined. Eleven specimens of the association
were collected between 2 and 5 m depth in two localities
from the northern Sea of Cortes: Punta Cazón (Bahía Kino,
Sonora, 28°52’20” N, 112°02’01” W), and Punta Pinta (La
Choya, Puerto Peñasco, Sonora, 31°18’05” N, 113°59’11”
W) (Fig. 1), from August 2000 to April 2005.
Description of the species involved in the association. The
epizoic sponge was identified as Haliclona sonorensis CruzBarraza and Carballo, 2006, which is a cushion-shaped sponge
from 2 to 5 mm in thickness (Fig. 2A). Consistency is soft,
compressible, but fragile and brittle. The surface is smooth
and the ectosomic layer is not easily detachable. The color is
pinkish violet in life and ocre or light brown in alcohol. The
oscules are scarce, and circular or oval-shaped (from 0.5 to 1
mm in diameter), situated at the summits of volcano-shaped
elevations. The skeletal material is constituted by oxeas that
measure: 77-(112)-150 x 2-(5.6)-10 µm.
The supporting sponge was identified as Geodia media
Bowerbank, 1873. This is a massive-incrusting to massive
amorphous sponge (from 3.5 to 8 cm thick). The surface is
irregular, smooth to the naked eye, but finely rough to the
touch. The natural color of the surface is from dark-brown to
white. The choanosome is yellowish or beige. Small ostialpores from 150 to 300 µm are regularly distributed on the
surface. The oscules are contained in several small, circular
or oval-shaped well-defined flattened sieves (containing
from 7 to more than 100 oscules). The oscules measure from
0.22 to 2.5 mm in diameter. Consistency of the ectosome is
very hard due to the cortex of sterrasters. The choanosome
is cavernous and very densely spiculated, with a firm and
slightly compressible consistency. The skeletal material is
constituted by megascleres: oxeas, 620-(1430)-1950 x 10(31)-42 µm; large styles, 620-(1077)-1260 x 22-(36)-45
µm; strongyloxeas, 150-(197.2)-292 x 2.5-(4.9)-7.5 µm;
plagiotriaenes, 550-(1078)-1700 µm rabdome length; and
anatriaenes, 1120-(1410)-2040 µm rabdome length, and
microscleres: sterrasters, 25-(62.8)-90 µm oxyasters, 20(27.2)-45 µm; oxyspherasters, 6.3-(9.5)-13 µm.
Description of the association. The specimens of the
association were found attached to the rocky substrata,
covering areas from 8 x 6.5 to 20 x 15 cm, approximately.
H. sonorensis forms a thin layer that covers up to 57 % of
the surface of G. media, while the surface that is not covered
by the sponge is occupied by other epibionts (green and red
algae, bryozoans, polychaetes and bivalves). Only the oscular
areas (from 1 to 4 cm in diameter) are free of these epibionts
(Fig. 2A). In some cases, more than one individual of H.
sonorensis was observed on a same specimen of Geodia, which
was evident by their different tonality of coloration. Despite
being interwoven, Haliclona was unattached in some areas,
where we observed that the external tissue of Geodia did not
seem to be damaged by the epizoic sponge (Fig. 2B, C). The
area of G. media lacking epibionts has a rough texture due
to the external layer of sterrasters (Fig. 2C, D), but the SEM
showed that the megascleres (triaenes and oxeas) of G. media
protrude the surface in the areas covered by Haliclona (Fig.
2C, F) penetrating in the Haliclona sonorensis tissue (Fig.
2D, E). There were spicules (oxeas) of H. sonorensis inside
the ostias and embedded in the choanosome of G. media, and
there were also sterrasters of G. media in the choanosome of
H. sonorensis.
Haliclona sonorensis has been invariably found living on
the surface of G. media which suggests that this species needs
to live in association with G. media.
Association Chalinula nematifera (de Laubenfels, 1954)
– Pocillopora spp. Lamarck, 1816
Material examined. A total of ten specimens of this
association were collected between 3 and 12 m depth in
three sites from Isabel Island (Bahía Tiburones, Playa Las
Monas and Playa Iguanas), Nayarit, Mexico (28°52’20” N,
112°02’01” W) (Fig. 1), from December 2003 to July 2006.
Morphological description of the species in the association.
The epizootic sponge has been identified as Chalinula
nematifera (de Laubenfels, 1954). This is an encrusting
sponge of violet color (1-4 mm thickness). This sponge grows
only on live corals found in Isabel Island (Fig. 3). The surface
is smooth to the naked eye, but it is punctated and shaggy in
some places. Oscules are abundant, circular, from 4 to 6 mm
149
Fig. 1: Sampling localities
(letters). The numbers indicate
the site where specimens of each
sponge association were collected:
(1) two-sponge association, (2)
sponge-alga association and (3)
sponge-coral association.
in diameter, and regularly distributed on the surface. They
are situated at the summits of volcano-shaped elevations.
Consistency is soft and spongy, somewhat elastic and slimy.
The skeleton consists of oxeas: 87-(98)-112.5 x 2.5-(4.4)-5
µm. Our specimens also show the characteristic pale threads
through the body as described by de Laubenfels (1954),
which presumably is a symbiotic fungus (WF Prud’homme
van Reine, comments in de Weerdt 2002).
The coral species on which C. nematifera was found
were identified as Pocillopora damicornis Linnaeus, 1758,
P. meandrina Dana, 1846, P. capitata Verrill, 1864 and P.
verrucosa Ellis and Solander, 1786. In general, these coral
species have characteristic shape because they form densely
ramified colonies. They have calices crowded together over
regularly-spaced wart-like projections (verrucae) (P. capitata
and P. verrucosa).
Description of the association. C. nematifera was found
always on live ramified corals that live in areas exposed to
light, most frequently with P. verrucosa (67%), and never on
another type of substratum. Nevertheless, it is possible to find
these species of coral (mentioned above) without the sponge.
Approximately 17% of the Pocillopora colonies studied
had C. nematifera in association. In these sponge/coral
interactions, C. nematifera can cover branches partially or
totally (5±5.12% of the total of branches of the colony), and
in all these cases we observed that the surface of the covered
coral has no polyps. This sponge adhered firmly to the coral
and is not easy to detach it from the substratum without
breaking it. In fact, through the SEM images, we observed
that the skeletal structure of the sponge seems to be cemented
to the coral septa by spongin layers (Fig. 3C).
Association Haliclona caerulea Hechtel, 1965 – Jania
adherens Lamouroux, 1816
Material examined. Sixteen specimens of the sponge-alga
association were collected from ten sites from the Mazatlán
Bay (23º13’49’’ N, 106º27’43’’ W), Sinaloa, Mexico (Fig. 1),
between 2 to 6 m depth, from November 1997 until October
2003.
Morphological description of the species in the association. Haliclona (Gellius) caerulea is a massive sponge (from
150
Fig. 2: Haliclona sonorensis
– ­ Geodia media association. A.
two-sponge association containing
several epibionts on its surface
except on the osculate area.
B. cross section of a specimen
showing the Geodia surface almost
totally covered by Haliclona
sonorensis. D. SEM image
showing the surface contact of the
two interacting sponges, and C,
E, F. the megascleres of Geodia
protruding its ectosome, which are
used as anchorage for the external
sponge. The arrow in F shows
an ostium of the internal sponge.
Scale bars: A and B= 2 cm, C= 5
mm, D= 500 µm, E= 200 µm, F=
500 µm.
3 to 13 cm high), white or beige in life and very brittle. The
skeleton is constituted by oxeas (82.5-(177.3)-210 µm) and
sigmas (17.5-(21.6)-30 µm). The sponge has an unispicular
ectosomal skeleton, formed by an isotropic tangential reticulation of oxeas, and the choanosomal skeleton is a somewhat
confused reticulation of uni-multispicular primary and secondary lines that are difficult to appreciate because of their
association with the alga (Fig. 4B).
The alga was identified as Jania adherens Lamouroux,
1816, which is an articulated erect red macroalga. The alga is
pink with white joints, repeatedly branched, with a calcified
thallus (from 0.4 to 0.5 mm diameter) except at the genicula.
Description of the association. This sponge lives in intimate
association with the red calcareous alga Jania adherens. The
association consists of a massive and compact form where the
sponge completely fills the spaces between the algal branches
(Fig. 4A). The sponge generally covers the alga, and the algal
branches very rarely protrude beyond the association surface.
The morphology of the association is derived from the growth
form of both organisms. Specimens of this association are lo-
151
Fig. 3: A. Chalinula nematifera –
Pocillopora spp. association. B. C.
nematifera tissue in close contact
with the coral polyps (arrows). C.
SEM image showing the skeletal
structure of the sponge cemented
to the coral septae (arrows). Scale
bars A= 1 cm, B= 2000 µm, C =
100 µm.
cally abundant in rocky substrate environments (2-6 m depth),
in areas of strong wave force. However, in these places, it is
not possible to find the two species living in isolation, even
though J. adherens lives in isolation in the intertidal zone.
Jania adherens forms compact turfs approximately 2 cm high
in the intertidal zone. However, in the subtidal zone (in association with H. caerulea) it reaches up to 13 cm in height. In
the images obtained by SEM, we observed that the spicules
of H. caerulea adhere firmly to the stalks of J. adherens by
means of a fine spongin layer (Fig. 4C). We also observed that
the primary lines of the sponge are partially replaced by the
macroalgal thallus.
Discussion
Two-sponge association
Interactions among two or more sponges of different
species, including cases of mutualism (Wilcox et al. 2002),
parasitism (Wulff 1999) or space competition (Rützler 1970,
Wulff 2006) have been previously recorded.
A two-sponge association quite similar to ours was
described recently from the Florida Keys (Wilcox et al.
2002). In both cases, as it has also been documented for other
two-sponge associations (Sim 1998, Wilcox et al. 2002),
152
Fig. 4: A. Haliclona caerulea
– Jania adherens association.
B. SEM images showing the
skeletal structure of H. caerulea,
which are partially substituted by
the J. adherens branches in the
association, and C. a close up of
a spicule secondary line adhered
to the algal thallus by means of a
fine spongine layer. Scale bars A=
1 cm, B= 300 µm, C= 60 µm.
Haliclona sp. seems to be anchored on the protruding spicules
of Geodia spp.
There are studies that suggest that growth and survival
increases when certain sponges of different species live in
association, because they have different susceptibility to
factors such as burial by sediment, fragmentation, predation
and pathogens (Wulff 1997a, 1999, Engel and Pawlik 2005,
Wulff 2006). However, in the association from the Florida
Keys, it was suggested that it could be a mutualistic and
obligatory symbiosis, where the external sponge protects
its host from the predation, while Geodia sp. offers it a sure
substratum for its survival (Wilcox et al. 2002).
However, it is interesting to comment that the Caribbean
sponge Geodia gibberosa is chemically undefended against
turtle and fish predation (Dunlap and Pawlik 1996, 1998), and
uses its chemical products to attract fouling organisms. This
could resemble Geodia sp. in association with Haliclona sp.
(Wilcox et al. 2002), since one of the benefits acquired by the
sponge Geodia cydonium fouled by the red alga Rytyphlöea
tinctoria is the protection against the adverse effects of
ultraviolet radiation, allowing the specimens to live under
illuminated habitats (Mercurio et al. 2006).
It is possible that an obligatory relationship also exists
between H. sonorensis and G. media, at least for H.
sonorensis, since it has not been found in isolation within the
environment where the associations are encountered. In fact,
the high specificity of Haliclona to live with Geodia is very
interesting because this association does not originate in a
highly space-competitive environment like reef ecosystems,
and therefore it could not be a simple case of epizoism due
to space limitation (Rützler 1970). In addition, it is important
to mention that there is no evidence of tissue damage on the
surface of G. media covered by H. sonorensis, as it has been
documented in other two-sponge interactions (Thacker et al.
1998). Although we did not make experiments to test whether
a benefit exists between G. media and H. sonorensis, bioactive
natural products have been described in G. media from the
Sea of Cortes (Pettit et al. 1981, Pettit et al. 1990), that could
attract fouling organisms, similar to Geodia gibberosa (Engel
and Pawlik 2000, Engel and Pawlik 2005).
In the association described here, one or more specimens
of H. sonorensis are found attached to the same G. media
specimen, establishing contact but without fusing. These
observations support the idea that this sponge most likely
colonizes G. media through larval settlement, in order to
obtain an appropriate substratum for its survival (Wulff
1997b, Wilcox et al. 2002).
Sponge-coral association
Sponge-coral interactions are common in coral reefs where
strong competition for space exists and where it is frequent
that aggressive sponges overgrow the coral (Aerts 1998).
The sponge Chalinula nematifera has been described
previously overgrowing hard corals in reefs from the WestCentral Pacific (de Laubenfels 1954). Surprisingly, this species
also seems to be specifically attracted to pocilloporid corals
from the Sea of Cortes, since it has not been found colonizing
other types of substratum. Nevertheless, the species of coral
associated with this sponge can be found in an isolated form.
This suggests that it could be an obligatory relationship for
the sponge, and facultative for the host (Pocillopora spp.).
We also suggest that this relationship can have negative
outcome for the coral, since the sponge seems to be killing the
coral tissue, similar to what has been documented for several
sponge/coral interactions (Jackson and Buss 1975, PlucerRosario 1987, Macintyre et al. 2000, Aerts 2000, Rützler
2002, de Voogd et al. 2004, Coles and Bolick 2006, Gochfeld
153
et al. 2006). However, we do not know if C. nematifera uses
chemical products to kill the coral polyps (Nishiyama and
Bakus 1999) or if it simply smothers them (Wulff 1999).
Some authors have suggested that the ability of sponges
to overgrow corals appears to depend on their growth rate
and form (Aerts 2000). For example, in the sponge Terpios
hoshinota, it was suggested that its success to overgrow large
extensions of live corals is due to a fast spreading rate, aided
by fast asexual propagation (fragmentation) (Plucer-Rosario
1987, Rützler and Muzik 1993).
Chalinula nematifera possibly finds a substratum that
offers multiple protected microhabitats in pocilloporid corals,
since they are densely ramified species which are often used
as microhabitats by several organisms (Patton 1974). Thus,
C. nematifera could likely benefit by finding an appropriate
substratum that offers protection against environmental
factors (e.g. UV radiation, sedimentation and/or predation).
This is an advantage that it could not find with the other
non-branched coral species (Porites, Psammocora, Pavona
and Fungia) that inhabit the same site as the C. nematifera/
Pocillopora spp. association, most likely because they do not
offer this kind of physical protection.
Although in most of the sponge-coral interactions that
have been described, it has been found that these relationships
seem to be negative for the coral (de Voogd et al. 2004, Coles
and Bolick 2006, Gochfeld et al. 2006, López-Victoria et al.
2006), there are also documented cases of mutualisms; for
example, the sponge Mycale laevis Carter 1882 which is
found encrusting on the lower surfaces of flattened reef corals
(mainly on Montastrea annularis) in the Caribbean Sea. M.
laevis benefits by colonizing a substrate that is free from other
sessile organisms. In turn, the coral benefits from an increased
feeding efficiency as a result of water currents produced by
the sponge and it is protected from invasion by boring sponges
(Goreau and Hartman 1966). In the case of sponge/octocoral
associations, the sponge generally obtains structural support
from its partner and the octocoral obtains protection against
predation (van Soest 1987, Calcinai et al. 2004). In addition,
it has been documented that both organisms also benefit by
increasing their dispersal capacity (Calcinai et al. 2004).
and Ávila 2004, Carballo et al. 2006). However, in spite of
the similarities of these two interactions, the H. caerulea/
J. adherens association does not live in an oligotrophic
environment in the Bay of Mazatlán (see Carballo 2006).
Our investigations into the H. caerulea-Jania adherens
association suggests that this is an obligatory and mutualistic
association, where both organisms benefit by increased growth,
widespread their distribution area toward an environment
where none can inhabit by itself, and by the acquisition of
a structural support that gives them bigger rigidity than their
free-living form (Ávila and Carballo 2004, Carballo and Ávila
2004, Carballo et al. 2006). H. caerulea can also substitute
part of its skeletal structure (mainly primary lines) with the
branches of J. adherens, reducing the investment in spicule
production (Carballo et al. 2006), as it has been documented
in other sponge symbioses (de Laubenfels 1950, Vacelet
1981, Rützler 1990, Uriz et al. 1992). In addition, it has been
demonstrated that H. caerulea in association with J. adherens
(from the Pacific coast of Panama) acquires the benefit of
being protected against fish predation (Wulff 1997a).
On the other hand, H. caerulea has never been found
in isolated form at the depth range where the sponge-alga
association lives in the Bay of Mazatlán, because it has a very
fragile structure, and it is unable to live in that environment,
which is characterized by strong water movement (Carballo
et al. 2006). Although this association reproduces mainly by
fragmentation, larval settlements of H. caerulea have been
registered in the intertidal zone where J. adherens inhabits in
isolated form (Ávila and Carballo 2006). In fact, laboratory
experiments demonstrated that the larvae of H. caerulea can
select J. adherens as substratum while rejecting others (Ávila
and Carballo 2006), probably because the alga fronds offer
a shady and tangled microrefuge, which could increase the
post-settlement survival (Buss 1979, Maldonado and Uriz
1998).
On the other hand, it is important to add that this association
has also been found in other localities in Mexico, such as
Tuxpan, Veracruz (in the Gulf of Mexico) and Manzanillo,
Colima and Huatulco, Oaxaca (in the Mexican Pacific)
(personal observations).
Sponge-alga association
The diversity of associations among the haplosclerid
sponges
Associations between sponges and photosynthetic
organisms are important not only for the partners, but also
for the ecosystem they inhabit, because they can contribute
significantly to the primary productivity, mainly in
oligothrophic ecosystems (Wilkinson 1983, Steindler et al.
2002). One of the most-studied sponge/macroalga symbioses
is the Haliclona cymaeformis/Ceratodictyon spongiosum
association (from the Great Barrier Reef, Australia)
(Trautman et al. 2000, Trautman and Hinde 2002, Davy et
al. 2002), which we could consider as a “sibling” association
of the H. caerulea/J. adherens association described here.
In both cases the mutualistic association derives similar
benefits for the partners (such as protection against physical
disturbances, structural support, high dispersal capacity
through fragmentation), and in both cases the sponge is a
species of Haliclona that lives associated with a red macroalga
(Trautman et al. 2000, Trautman and Hinde 2002, Carballo
The three symbiotic sponges (H. sonorensis, C. nematifera
and H. caerulea) described in this study belong to the order
Haplosclerida, which is one of the most diverse groups of the
phylum Porifera (Hooper and van Soest 2002). Upon revising
the literature, we have found that most of the sponges (21%
of 248 cases) that have been previously recorded establishing
associations with other taxa (see introduction), belong to the
order Haplosclerida, and mostly to the family Chalinidae
(50% of 51 registrations) (Fig. 5) (Dauer 1974, Vacelet 1981,
Ellison et al. 1996, Garson et al. 1998, Ilan et al. 1999, Vacelet
et al. 2001, Steindler et al. 2002, Wilcox et al. 2002, among
others). These associations have been recorded mainly in
shallow tropical and subtropical environments (such as coral
reefs), which are characterized by a high competition for
space and food by the organisms that inhabit there. It seems
that some sponges have probably “learned” to associate with
154
Fig. 5: A. Symbiotic associations
between sponges and other
organisms registered in the
different orders of the class
Demospongiae and B. in the order
Haplosclerida.
other organisms that offer them some kind of protection
against environmental factors (such as fish predation,
sedimentation, UV radiation, tissue resistance). For example,
in the Geodia sp./Haliclona sp. association, it has been
suggested that Geodia sp. is chemically defended against fish
predation and protected from sedimentation by the sponge
partner (Wilcox et al. 2002). In another haploclerid species
such as Haliclona cymaeformis and Haliclona implexiformis
that live associated with photosynthetic organisms (macroalga
and mangrove respectively), it has been demonstrated that
nutrient translocation also exists between the sponge and
its host (Ellison et al. 1996, Davy et al. 2002). In the case
of species that shelter cyanobacteria (e.g. Adocia atra and
Haliclona debilis) in their tissue, it has been suggested that
they can benefit by protecting their surface from UV-radiation
and/or obtain an alternative source of food (Rützler 1990,
Steindler et al. 2002). It has also been suggested that they
reinforce their skeletal structure using their partner to avoid
being broken into fragments by the current, as is the case
of H. caerulea (Carballo et al. 2006) and H. cymaeformis
(Trautman and Hinde 2002).
On the other hand, there are many bioactive compounds
known in haplosclerid sponges (Frincke and Faulkner
1982, Isaacs and Kashman 1992, van Soest and Braekman
1999), which can also be used for different purposes such as
antifoulants (Sera et al. 2002), as antimicrobial compounds
(Xue et al. 2004, Ely et al. 2004) or in competition for space
(Nishiyama and Bakus 1999).
Conclusions
In general, it seems that in the sponge/sponge and
sponge/macroalga associations the relationships are usually
mutualistic, or at least no type of damage has been evidenced
among the associated organisms. In contrast, in most of the
non-boring sponges associated to ramified corals that have
been described (including C. nematifera/Pocillopora spp.
association), the relationship seems to be negative for the coral
species. Nevertheless, it is necessary to do more experimental
and population dynamics studies of these associations in
order to understand more about the complexity of their life
history and their ecological importance in the ecosystem they
inhabit.
Acknowledgements
We are grateful to the following sources of funding: CONABIO
FB666/S019/99, CONABIO FB789/AA004/02, CONABIO
DJ007/26 and CONACYT SEP-2003- C02-42550. This work
was carried out under permission of SAGARPA (Permit numbers:
DGOPA.02476.220306.0985 and DGOPA.06648.140807.3121).
We thank Clara Ramírez, Pedro Allende and Victoria Montes for
help with the literature and images, German Ramírez and Carlos
Suárez for their computer assistance, Cayetano Robles, Gonzalo
Pérez and Cristina Vega for their assistance in the field sampling,
and the Director Parque Nacional Isla Isabel Jorge Castrejón for the
availability and the permission conferred for the collection of the
samples in Isabel island.
155
References
Aerts LAM (1998) Sponge/coral interactions in Caribbean reefs:
analysis of overgrowth patterns in relation to species identity and
cover. Mar Ecol Prog Ser 175:241-249
Aerts LAM (2000) Dynamics behind standoff interactions in three
reef sponge species and the coral Montastraea cavernosa. PSZN
Mar Ecol 21: 191-204
Ávila E, Carballo JL (2004) Growth and standing stock biomass of
a mutualistic association between the sponge Haliclona caerulea
and the red alga Jania adherens. Symbiosis 36(3): 225-244
Ávila E, Carballo JL (2006) Habitat selection by larvae of
the symbiotic sponge Haliclona caerulea (Hechtel, 1965)
(Demospongiae, Haplosclerida). Symbiosis 41: 21-29
Buss LW (1979) Bryozoan overgrowth interactions-the
interdependence of competition for space and food. Nature 281:
475-477
Calcinai B, Bavestrello G, Cerrano C (2004) Dispersal and
association of two alien species in the Indonesian coral reefs:
the octocoral Carijoa riisei and the demosponge Desmapsamma
anchorata. J Mar Biol Assoc UK 84: 937-941
Carballo JL (2006) Effect of natural sedimentation on the structure
of tropical rocky sponge assemblages. Ecoscience 13: 119-130
Carballo JL, Ávila E (2004) Population dynamics of a mutualistic
interaction between the sponge Haliclona caerulea, and the red
alga Jania adherens. Mar Ecol Prog Ser 279: 93-104
Carballo JL, Ávila E, Enríquez S, Camacho L (2006) Phenotypic
plasticity in a mutualistic association between the sponge Haliclona
caerulea and the calcareous macroalga Jania adherens induced
by transplanting experiments. I: morphological responses of the
sponge. Mar Biol 148: 467-478
Coles SL, Bolick H (2006) Assessment of invasiveness of the orange
keyhole sponge Mycale armata in Kâne’ohe Bay, O’ahu, Hawai’i.
7th Int Sponge Symp (abstract) pp. 110
Cruz-Barraza JA, Carballo JL (2006) A new species of Haliclona
(Demospongiae: Haplosclerida) living in association with Geodia
media Bowerbank (Mexican Pacific coast). Zootaxa 1343: 43-54
Davy SK, Trautman D, Borowitzka MA, Hinde R (2002) Ammonium
excretion by a sponge and its ecological importance in a spongerhodophyte symbiosis. J Exp Biol 205: 3505-3511
Dauer DM (1974) Polychaete fauna associated with Gulf of Mexico
sponges. Florida Scientist 36: 192-196
de Laubenfels MW (1950) The sponges of Kaneohe Bay, Oahu. Pac
Sci 4(1): 3-36
de Laubenfels MW (1954) The sponges of the west-central Pacific.
Oreg St Monogr Zool 7: 1-306
de Voogd N, Becking LE, Hoeksema BW, Noor A, van Soest
RWM (2004) Sponge interactions with spatial competitors in the
Spermonde Archipelago. In: Pansini M, Pronzato R, Bavestrello
G, Manconi R (eds). Sponge science in the new millennium. Boll
Mus Ist Biol Univ Genova 68: 253-261
de Weerdt WH (2002) Family Chalinidae Gray. In: Hooper JNA, van
Soest RWM (eds). Systema Porifera: a guide to the classification
of sponges. Kluwer Academic/Plenum Publishers, New York. pp.
852-873
Dunlap M, Pawlik JR (1996) Video-monitored predation by
Caribbean reef fishes on an array of mangrove and reef sponges.
Mar Biol 126: 117-123
Dunlap M, Pawlik JR (1998) Spongivory by parrotfish in Florida
mangrove and reef habitats. PSZN Mar Ecol 19: 325-337
Ellison AM, Farnsworth EJ, Twilley RR (1996) Facultative
mutualism between red mangroves and root-fouling sponges in
Belizean mangal. Ecology 77(8): 2431-2444
Ely R, Supriya T, Naik CG (2004) Antimicrobial activity of marine
organisms collected off the coast of South East. India. J Exp Mar
Biol Ecol 309: 121-127
Engel S, Pawlik JR (2000) Allelopathic activities of sponge extracts.
Mar Ecol Prog Ser 207: 273-281
Engel S, Pawlik JR (2005) Interactions among Florida sponges. II.
Mangrove habitats. Mar Ecol Prog Ser 303: 145-152
Frincke JM, Faulkner DJ (1982) Antimicrobial metabolites of the
sponge Reniera sp. J Am Chem Soc 104: 265-269
Frost TM, Williamson CE (1980) In situ determination of the
effect of symbiotic algae on the growth of the freshwater sponge
Spongilla lacustris. Ecology 61: 1361-1370
Gaino E, Lancioni T, La Porta G, Todini B (2004) The consortium
of the sponge Ephydatia fluviatilis (L.) living on the common
reed Phragmites australis in Lake Piediluco (central Italy).
Hydrobiologia 520: 175-178
Gaino E, Sarà M (1994) Siliceous spicules of Tethya seychellensis
(Porifera) support the growth of a green alga: A possible light
conducting system. Mar Ecol Prog Ser 108: 147-151
Garson MJ, Flowers AE, Webb RI, Charan RD, McCaffrey EJ (1998)
A sponge/dinoflagellate association in the haplosclerid sponge
Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll
density gradient fractionation. Cell Tissue Res 293: 365-373
Gochfeld D, Harrison L, Olson J, Lesser MP, Ankisetty S, Slattery M
(2006) Allelopathic effects of the Caribbean sponge Svenzea zeai
on the coral Montastrea annularis. In: Custódio MR, Lôbo-Hajdu
G, Hajdu E, Muricy G (eds). 7th International Sponge Symposium Book of Abstracts (Armação dos Búzios, Brazil). Museu Nacional,
Série Livros, vol. 16. pp. 116
Goreau TF, Hartman WD (1966) Sponge: effect on the form of reef
corals. Science 151: 343-344
Henkel TO, Pawlik JR (2005) Habitat use by sponge-dwelling
brittlestars. Mar Biol 146: 301-313
Hooper NA, van Soest RWM (2002) Systema Porifera: a guide to the
classification of sponges. Kluwer Academic, Plenum Publishers,
New York
Ilan M, Loya Y, Kolbasov GA, Brickner I (1999) Sponge inhabiting
barnacles on coral reefs. Mar Biol 133: 709-716
Isaacs S, Kasbman Y (1992) Shaagrockol B and C; two
hexaprenylhydroquinone disulfates from the Red Sea sponge
Toxiclona toxius. Tetrahedron Lett 33: 2227-2230
Jackson JBC, Buss L (1975) Allelopathy and spatial competition
among coral reef invertebrates. Proc Natl Acad Sci 72: 5160-5163
Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions
(CPCe): A Visual Basic program for the determination of coral and
substrate coverage using random point count methodology. Comp
Geosci 32: 1259-1269
López-Victoria M, Zea S, Weil E (2006) Competition for space
between encrusting excavating Caribbean sponges and other coral
reef organisms. Mar Ecol Prog Ser 312: 113-121
Macintyre IG, Precht WF, Aronson RB (2000) Origin of the Pelican
Cays ponds, Belize. Atoll Res Bull 466: 1-11
Magnino G, Gaino E (1998) Haplosyllis spongicola (Grübe)
(Polychaeta, Syllidae) associated with two species of sponges from
East Africa (Tanzania, Indian Ocean). PSZN Mar Ecol 19: 77-87
156
Maldonado M, Uriz MJ (1998) Microrefuge exploitation by subtidal
encrusting sponges: patterns of settlement and post-settlement
survival. Mar Ecol Prog Ser 174: 141-150.
Mercurio M, Corriero G, Gaino E (2006) Sessile and non-sessile
morphs of Geodia cydonium (Jameson) (Porifera, Demospongiae)
in two semi-enclosed Mediterranean bays. Mar Biol 148: 489-501
Meroz E, Ilan M (1995) Cohabitation of a coral reef sponge and a
scyphozoan. Mar Biol 124: 453-459
Nishiyama GK, Bakus GK (1999) Release of allelochemicals by
three tropical sponges (Demospongiae) and their toxic effects on
coral substrate competitors. Memoir Queensl Mus 44: 411-417
Palumbi SR (1985) Spatial variation in an algal-sponge
commensalism and the evolution of ecological interactions. Am
Nat 126: 267-274
Patton WK (1974) Community structure among the animals
inhabiting the coral Pocillopora damicornis at Heron Island,
Australia. Bull Mar Sci 14(2): 212-243
Pettit GR, Rideout JA, Hasler JA (1981) Isolation of geodiastatins
1 and 2 from the marine sponge Geodia mesotriaena. J Nat Prod
44(5): 588-92
Pettit GR, Rideout JA, Hasler JA (1990) Isolation of geodiatoxins
2 and 4 from the marine sponge Geodia mesotriaena. Comp Bio
Physiol Part C 96(2): 305-6
Plucer-Rosario G (1987) The effect of substratum on the growth of
Terpios, an encrusting sponge which kills corals. Coral Reefs 5(4):
197-200
Rützler K (1970) Spatial competition among Porifera: solution by
epizoism. Oecologia 5: 85-95
Rützler K (1974) The burrowing sponges of Bermuda. Smithson
Contrib Zool 165:1-32
Rützler K (1990) Associations between Caribbean sponges and
photosynthetic organisms. In: Rützler K (ed). New perspectives
in sponge biology. Smithsonian Institution Press, Washington DC.
pp. 455-466
Rützler K (2002) Impact of crustose clionid sponges on Caribbean
Reef corals. Acta Geol Hisp 37: 61-72
Rützler K, Muzik K (1993) Terpios hoshinota, a new
cyanobacteriosponge threatening Pacific reefs. In: Uriz MJ, Rützler
K (eds). Recent Advances in Ecology and Systematics of Sponges.
Sci Mar 57(4): 395-403
Sarà M, Vacelet (1973) Écologie des Démosponges. In: Grassé PP
(ed). Spongiaires. Anatomie, Physiologie, Systématique, Écologie.
Masson de Cie, Paris. pp. 462-576
Schuchert P (2003) Hydroids (Cnidaria, Hydrozoa) of the Danish
expedition to the Kei Islands. Steenstrupia 27: 137-256
Sera Y, Adachi K, Fujii K, Shizuri Y (2002) Isolation of
Haliclonamides: New peptides as antifouling substances from a
marine sponge species, Haliclona. Mar Biotechnol 3: 441-446
Sim CJ (1998) Two-sponge association from Komun Island,
Korea. In: Watanabe Y, Fusetani, N (eds). Sponge sciences:
multidisciplinary perspectives. Springer-Verlag, Tokyo. pp 109117
Steindler L, Beer S, Ilan M (2002) Photosymbiosis in intertidal and
subtidal tropical sponges. Symbiosis 33:263-273
Thacker RW, Becerro MA, Lumbang WA, Paula VJ (1998)
Allelopathic interactions between sponges on a tropical reef.
Ecology 79(5): 1740-1750
Thakur NL, Müller WEG (2004) Biotechnological potential of
marine sponges. Curr Sci 86(11): 1506-1512
Trautman DA, Hinde R, Borowitzka MA (2000) Population
dynamics of an association between a coral reef sponge and a red
macroalga. J Exp Mar Biol Ecol 244: 87-105
Trautman DA, Hinde R (2002) Sponge/algal symbioses: a diversity
of associations. In: Seckbach J (ed). Symbiosis: Mechanisms and
Model Systems. Kluwer Academic Publishers, Netherlands, 796
pp.
Uriz MJ, Rosell D, Maldonado M (1992) Parasitism, comensalism
or mutualism? The case of Scyphozoa (Coronatae) and horny
sponges. Mar Ecol Prog Ser 81: 247-255
Vacelet J (1981) Algal-sponge symbioses in the coral reefs of New
Caledonia: a morphological study. Proc 4th Int Coral Reef Symp,
Manila 2: 713-719
Vacelet J, Sofyani AA, Lihaibi SA, Kornprobst JM (2001) A new
haplosclerid sponge species from the Red Sea. J Mar Biol Assoc
UK 81: 943-948
van Soest RWM, Braekman JC (1999) Chemosystematics of
Porifera: a review. Memoir Queensl Mus 44: 569-589
West DA (1979) Symbiotic zoanthids (Anthozoa: Cnidaria) of
Puerto Rico. Bull mar Sci 29: 253-271.
Wilcox TP, Hill M, DeMeo K (2002) Observations on a new twosponge symbiosis from the Florida Keys. Coral Reefs 21: 198204
Wilkinson CR (1983) Net primary productivity of coral reef sponges.
Science 219: 410-412
Wulff JL (1997a) Causes and consequences of differences in sponges
diversity and abundance between the Caribbean and eastern Pacific
at Panama. Proc 8th Int Coral Reef Symp, Panama 2: 1377-1382
Wulff JL (1997b) Mutualisms among species of coral reef sponges.
Ecology 78: 146-159
Wulff JL (1999) A sponge that cheats on diffuse mutualism among
other sponge species. Mem Qld Mus 44: 686
Wulff JL (2006) Ecological interactions of marine sponges. Can J
Zool 84: 146-166
Xue S, Zhanga HT, Wua PC, Zhanga W, Yuan Q (2004) Study on
bioactivity of extracts from marine sponges in Chinese Sea. J Exp
Mar Biol Ecol 298: 71-78