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Journal of Animal
Ecology 2005
74, 313–321
Trade-offs in resistance to competitors and predators, and
their effects on the diversity of tropical marine sponges
Blackwell Publishing, Ltd.
JANIE L. WULFF
Department of Biological Science, Florida State University, Tallahassee, FL 32306–1100, USA
Summary
1. Consistently very high regional diversity of tropical marine sponges reflects a combination of high within-habitat diversity and distinctness of species composition among
habitats. Distinctive sponge faunas of Caribbean coral reefs and mangroves seem to
support the assumption that abiotic factors determine sponge diversity within habitats
and faunal differences between habitats because these habitats differ greatly in abiotic
characteristics and because lower species diversity on mangroves appears to reflect their
inferiority as sponge habitat.
2. A way to test this assumption is provided by unusual mangrove cays in Belize that are
inhabited by the typical Caribbean reef sponge fauna. Reciprocal transplant experiments,
combined with caging (predator-free space) and artificial substrata (competitor-free
space), demonstrated control of community membership by biological interactions for
12 common species: spongivorous predators excluded typical mangrove sponges from
reef sponge assemblages, and reef sponges were excluded from mangrove sponge assemblages by competition.
3. Variation in growth rate was related inversely to variation in defences against predators in the species studied, suggesting a trade-off between resistance to competitors and
to predators.
4. This trade-off influences community structure, as the key importance of competition
for space among mangrove species results in lower within-habitat diversity, while
multiple challenges, including predation, may maintain high diversity of reef sponges.
Differences in species composition between habitats are maintained, as this trade-off
precludes success of individual species as members of both faunas.
5. Most surprising is that typical faunas of mangroves and reefs are not tied to these
habitats by abiotic factors. Greater sponge species diversity on the reef does not necessarily indicate superior conditions for sponges. Instead reefs may be a refuge for species
that grow too slowly to coexist with typical mangrove species.
Key-words: Caribbean, coral reefs, mangroves, Porifera, spongivory.
Journal of Animal Ecology (2005) 74, 313–321
doi: 10.1111/j.1365-2656.2004.00925.x
Introduction
Intriguingly high regional diversity of tropical marine
organisms has been attributed to competition, predation,
mutualism, disturbance, recruitment patterns, geological age, physical habitat structure, areal extent of the
region and various combinations of these. One consistent pattern among taxa and regions is that distinct
species composition in each habitat (i.e. high betweenhabitat diversity) plays an especially important role in
© 2005 British
Ecological Society
Correspondence: Janie L. Wulff, Department of Biological
Science, Florida State University, Tallahassee, FL 32306 –
1100, USA. E-mail: [email protected]
bolstering regional species counts in tropical seas (e.g.
Knowlton & Jackson 1994; Ogden 1997; Paulay 1997).
If species are sorted into habitats by how gracefully
they cope with habitat-characteristic abiotic factors,
the regional species pools for different habitats are
functionally independent of each other. However, if
biotic interactions influence species distributions
across habitats, species could live in different habitats
as distributions of their predators, competitors and
mutualistic partners shift. A metacommunity viewpoint, acknowledging potential linkage of all species
in the region, is then required. Thus as coral reefs
and associated ecosystems slide more desperately
into disrepair, knowing the relative importance of
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J. L. Wulff
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
abiotic and biotic factors in sorting species into different habitats and maintaining within-habitat diversity
of key groups is crucial (e.g. Bellwood & Hughes 2001).
Sponges, like the much better-studied corals, fishes
and shelled molluscs, are especially diverse and abundant, and are players of key functional roles in tropical
marine systems (e.g. Paulay 1997; Diaz & Rützler 2001;
Wulff 2001). However, sponges are set apart by intimidating identification and quantification challenges
that have slowed studies of processes underlying their
diversity patterns. Comprehensive faunal surveys of
tropical sponges (e.g. Alcolado 1994; Zea 1994, 2001;
Reed & Pomponi 1997; Hooper, Kennedy & Quinn
2002) demonstrate distinctive species compositions in
different habitats. Abiotic factors have generally been
held responsible for determining both habitat-distinctive
species composition and within-habitat diversity.
Universally acknowledged unusual chemistry of sponges
has been invoked to explain apparent relative immunity to control by interactions (e.g. Kubanek et al. 2002
and references therein). Reports of sponges being
outcompeted are rare (Sutherland 1980; Thacker et al.
1998), although sponges often outcompete neighbours
of other taxa (e.g. Jackson & Buss 1975; Vicente 1990;
Rützler & Muzik 1993; Aerts & van Soest 1997). Similarly,
predators restrict some sponge species to refuges (e.g.
Wulff 1988, 1995b, 1997b; Dunlap & Pawlik 1996, 1998),
but the influence of predation on sponge diversity has
barely been considered (Wulff 1994, 1997c; van Dam &
Diez 1997).
Caution in interpretation is advised by the possibility that biotic influences can be invisible if they curtail
distributions so effectively that potentially competing
species, or predator and prey species, rarely coexist.
Experiments are required. Coral reefs and mangroves
have distinct sponge faunas that contribute substantially to the region-wide Caribbean tally of over 640
described sponge species (van Soest 1994). An ideal situation for determining the relative importance of biological and abiotic factors for within-habitat diversity
and habitat-distinctive sponge faunas of mangroves
and coral reefs is provided by two sets of mangrove cays
on the Belize Barrier Reef. The sponge fauna on mangrove roots at Twin Cays is typical of mangrove stands
throughout the western Atlantic (Rützler et al. 2000;
Wulff 2000, and references therein), but the sponge fauna
on the Pelican Cays mangroves is unusual in that it is
typical of shallow Caribbean coral reefs (Wulff 2000).
The many abiotic differences that otherwise confound
comparisons between mangroves and coral reefs (reefs
generally have more light, less turbidity, fewer nutrients,
more substratum continuity and more exposure to
physical disturbance) are minimized, facilitating experimental evaluation of biological factors.
The proximate focus of this study was to determine if
biological interactions maintain the distinction between
the typical sponge faunas of mangroves and coral reefs.
Experiments tested two specific hypotheses: (1) sponge
species typical of mangroves are consumed readily
by spongivores and are therefore restricted to typical
mangrove stands from which spongivores are absent
and (2) sponge species typical of coral reefs are prevented from inhabiting typical mangroves by competition from mangrove sponge species, which grow more
rapidly. I used the direct approach of reciprocal transplant experiments between the Pelican Cays and Twin
Cays, augmented by cages (predator-free space) and
artificial substrata (competitor-free space).
Patterns of growth and survival of reciprocally transplanted sponges address the importance of biotic factors for sponge distribution and diversity on three levels,
as follows. (1) Region: do competition and predation
influence the striking distinction between the mangrove
and coral-reef sponge faunas in the Caribbean? (2) Community: does within-habitat sponge diversity reflect the
role of biological interactions in determining faunal
membership? (3) Species: do trade-offs between resistance
to competitors and resistance to predators preclude
success of individual species as members of both faunas?
Methods
 
Twin Cays, a mangrove stand with a typical tropical
western Atlantic mangrove sponge fauna, is a set of offshore cays built on peat banks, pervaded by channels
and bays and surrounded by sediment and sea-grass
meadows (Rützler et al. 2000; Wulff 2000, and references
therein; maps in both papers). In the Pelican Cays,
where a sponge fauna typical of shallow Caribbean
coral reefs inhabits mangrove roots (Wulff 2000), the
mangroves are embedded in peat banks on the tops of
coral reefs. All but four of the 30 most common sponge
species on the Pelican Cays mangroves are common
inhabitants of shallow coral reefs (Wulff 2000). Prop
roots at Twin Cays and the Pelican Cays together
harbour a total of 167 sponge species and distinct forms,
but 78% of those are found in only one of these two sets
of cays, and many of the species that live in both are
rare in one or the other (Rützler et al. 2000).
The site chosen for experiments at Twin Cays, 3 km
north-west of the Carrie Bow Cay research station of
the Smithsonian Institution, is a channel known as
Hidden Creek. In the Pelican Cays, 16 km south-west
of Carrie Bow Cay, two sites were chosen: one at Manatee Cay, on the far side of the pond (200 m away) from
the entrance, and the other at Cat Cay, to the left of and
just 80 m inside the pond entrance. At Carrie Bow Cay,
experiments were established among large corals on
the shallow reef south-west of the island.
 
Six of the most common sponge species at the Pelican
Cays and six of the most common sponge species at
Twin Cays were chosen for transplant experiments. All
of these species had been accorded relative abundance
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Growth-defence
trade-offs and
sponge diversity
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
ranks of ‘3’ (the highest) in their home cays in qualitative evaluations by a group of Caribbean sponge
specialists (Rützler et al. 2000), and all were naturally
absent or rare in the other set of cays.
Species chosen from the Twin Cays community were
Biemna caribea Pulitzer-Finali, Tedania ignis (Duch. &
Mich.), Lissodendoryx isodictyalis (Carter) (all order
Poecilosclerida), Amorphinopsis sp., Halichondria magniconulosa Hechtel (both order Halichondrida) and
Haliclona implexiformis (Hechtel) (order Haplosclerida).
All six species grow as clusters of volcano-shaped
mounds. All except Amorphinopsis sp. are typical of
mangrove roots throughout the Caribbean (Wulff 2000).
Species chosen from the Pelican Cays community were
Iotrochota birotulata (Higgin), Desmapsamma anchorata (Carter), Mycale laevis (Carter), Monanchora
arbuscula (Duch. & Mich.) (all order Poecilosclerida),
Amphimedon compressa Duch. & Mich. (order Haplosclerida) and Aplysina fulva (Pallas) (order Verongida).
Four of these species have erect branching growth
forms, while M. laevis and M. arbuscula form clusters
of mounds from which branches sometimes extend. All
six are among the most common species on shallow
Caribbean coral reefs (see, e.g. Alvarez, Diaz & McLaughlin
1990; Alcolado 1994; Wulff 1994, 2000).
Genotype was controlled in all experiments. From
each individual, pieces (three for Twin Cays sponges,
four for Pelican Cays sponges) were cut to similar size,
shape and distribution of intact surface tissue. Cut
pieces were kept in the field in small mesh baskets until
cut edges healed. The volume of each sponge piece was
measured by displacement of water in a graduated
cylinder. Initial volumes ranged from 3 to 10 cm3, but
most were 4 – 7 cm3. Sponges were transported in a
large cooler that had been soaked in seawater, and the
sponges were never exposed to air except for a second
or two as their volumes were measured.
Three prepared pieces of each of 13–16 individuals
of each of the six species from Twin Cays (typical mangrove sponge fauna) were attached with beaded nylon
cable ties 1 mm in diameter to (1) the original home
root (control), (2) a root at Pelican Cays inside a small
plastic cage (protected from predators) and (3) the
same root at the Pelican Cays but outside the cage. The
four prepared pieces of each of 12–15 individuals of
each of the species from the Pelican Cays (typical shallow coral reef sponge fauna) were attached to (1) the
original home root (control), (2) a root at Twin Cays,
(3) a piece of presoaked pvc pipe (competitor-free
space) suspended among the mangrove roots at Twin
Cays and (4) a piece of clean coral rubble attached to a
stainless steel stake inserted into the reef at Carrie Bow
Cay at about 2·5 m depth (normal habitat for these reef
species). Four pieces of the same size, shape and distribution of surface tissue were the maximum that could
be cut from a single individual of most species, preventing perfect symmetry in the experimental design. However, preliminary experiments and observations had
indicated that no clarity would be lost by not including
cages at Twin Cays or pvc pipes in the Pelicans, and the
fates of mangrove species transplanted to the reef from
Twin Cays were followed in the predation experiments
described below.
Transplants were situated so that no other sponges
or other sessile animals touched them. All 544 transplanted sponges were checked for reattachment and
survival after 2–3 days. After 7 months (February 2002),
a series of external measurements were used to estimate
volumes by approximation to the volumes of appropriate
conglomerations of geometric solids.
To determine growth rates for reef sponges on reefs
without confounding by storm-caused partial mortality,
individuals of four of the reef sponge species were also
grown on Guigalatupo reef, in the San Blas Islands,
Panama, where hurricane damage is almost never a
factor. Individuals of I. birotulata, A. compressa, A. fulva
and D. anchorata were cut to initial sizes in the same
range as those in the Belize experiments (most individuals 4–7 cm3), reattached to substrata on the reef, and
re-measured after 7·6 months.
 
To augment the caging experiments in the Pelican Cays,
Twin Cays sponges were also brought to the Carrie Bow
Cay reef, where greater site accessibility made detailed
observations of fish feeding feasible. Another typical
mangrove species from the order Haplosclerida, H.
curaçaoensis (van Soest), was added to the experiments
to balance taxonomic representation. Fish reacted differently to a blue–yellow morph and a purple morph of
L. isodictyalis, so these were treated as distinct choices.
For each of 12 feeding experiments (one per day),
pieces of each of the eight species or colour morphs were
cut to the same size, 6 cm3, and attached with small
cable ties to coral rubble on stakes. Some sponge species
concentrate defences in their surfaces (Uriz et al. 1996;
Wulff 1997b; Schupp et al. 1999), so surfaces were allowed
to heal before sponges were presented to fish. For each
trial, the stakes were inserted into the reef so that the
sponges appeared to be growing on pieces of coral rubble. All bites taken from the sponges in the first 30 min
were recorded, in the order taken. The time at which
each sponge piece was entirely consumed was recorded.
The sponges were checked again after 1 h and 24 h.
Results
  
Only 3 days after transplantation to the Pelican Cays
mangrove roots, 100% of uncaged individuals of four
of the typical mangrove species had been consumed,
leaving only 39% and 53% of the individuals of Amorphinopsis sp. and H. implexiformis, respectively. Some
caged individuals were also lost, possibly because cages
were attached too loosely. I observed grey angelfish,
Pomacanthus arcuatus (Linnaeus), consuming uncaged
316
J. L. Wulff
experimental sponges and attempting to nudge cages
aside. Survival of controls at Twin Cays was 100%, so it
is possible that the 20-km boat voyage also caused
some mortality of transplanted sponges. Such losses
would not differ between treatments, however, and the
difference in survival between sponges inside and outside
cages was striking (73% vs. 15·3%, significantly different
by the G-test, P < 0·001).
After 7 months, 35% (17/49) of the sponges that had
been alive in cages after 3 days were still alive and had
grown, a few of them large enough to fill the cages. None
of the uncaged sponges survived. When the cages were
removed, the sponges that had survived inside them
were all consumed within 2 days. Survival of controls
on home roots at Twin Cays was 42–100%, depending
on the species (mean 67%; data in Fig. 1).
Mangrove sponges transplanted from Twin Cays to
the Carrie Bow reef did not attract wrasses and other
generalists and scavengers that normally swarm to cut or
broken sponges, because cut surfaces had been allowed
to heal. Grey angelfish P. arcuatus and redband parrotfish Sparisoma aurofrenatum fed on the sponges. The
angelfish spread their attention over all edible sponge
species, taking only a few bites of a sponge and moving
on to a different species. During observations of 506
bites in 130 bouts of uninterrupted feeding, angelfish
always consumed fewer than eight bites of one species
before switching, except for five bouts of feeding on T.
ignis or B. caribea, which continued for from 12 to 31 bites.
These species were the first to be consumed entirely in
every trial. The parrotfish always consumed H. magniconulosa first, and then turned to Amorphinopsis sp.
They chased away fish attempting to feed on these
species and fed on a single sponge until it was gone or
they were chased away.
All sponges of six of the seven species were eliminated from the reef by predation within 24 h, but the
species varied in how readily they were consumed.
Consistent preferences by the fish throughout the
12 days of the experiments divided the sponge species
into four groups: (1) T. ignis and B. caribea were always
consumed within 10 min; (2) H. magniconulosa, Amorphinopsis sp. and the blue colour morph of L. isodictyalis
were consumed within 10 min in 50%, 30% and 18% of
the trials, respectively, and always within the first hour;
(3) purple L. isodictyalis and H. curaçaoensis were never
entirely consumed within the first hour but always
within 24 h; and (4) H. implexiformis was never
consumed within 24 h. Surfaces of H. implexiformis
individuals became colonized by diatoms and they disappeared within 3 days, for unknown reasons.
  
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
Fig. 1. (a) Survival of sponges from the Pelican Cays 7 months
after transplantation to mangrove roots or pvc pipes in Twin
Cays. (b) Mean specific growth (± 1 SE) after 7 months of
sponges transplanted from the Pelican Cays to roots or pvc
pipes at Twin Cays. Individuals with net size decrease
were excluded. Species abbreviated as: Iotr birot, Iotrochota
birotulata; Amph comp, Amphimedon compressa; Apl fulva,
Aplysina fulva; Desm anch, Desmapsamma anchorata; Myc
laevis, Mycale laevis; Mon arbusc, Monanchora arbuscula.
Two of the species (D. anchorata and M. arbuscula)
were traumatized by the 20-km boat ride from the
Pelicans to Twin Cays and no individuals increased in
size, so they were not included in the analysis. The other
four species tolerated the boat ride well, as illustrated
by similar survival without net decrease of controls on
home roots in the Pelicans and transplants to pvc pipes
at Twin Cays (53·5% vs. 50·8%, not significantly different by the G-test, P = 0·5). By 7 months, many of the
initially successful reef sponge transplants on roots at
Twin Cays were reduced to very tiny pieces with virtually
no survival potential, so comparisons between treatments
were confined to individuals that had not decreased in
size. Survival without net decrease was significantly
greater on pvc pipes than on roots (overall 50·8% vs.
25%, G-test, P < 0·001; for individual species, differences were significant by the G-test for I. birotulata and
A. fulva, P < 0·025; and M. laevis, P < 0·05; Fig. 1a).
Specific net growth (standardized by initial volume)
of typical reef species transplanted from Pelican Cays
to Twin Cays reflected heavy partial mortality. To
minimize confounding of growth potential with partial
mortality, individuals with net size decrease were not
included in the analysis. Variances were high (Fig. 1b)
and both members survived in too few genotype pairs
317
Growth-defence
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Fig. 2. Mean specific growth (± 1 SE) of sponge species
typical of shallow Caribbean coral reefs on mangroves in
Belize (open bars) and on a shallow coral reef in San Blas,
Panama (stippled bars). Species names are abbreviated as in
Fig. 1. Sample sizes on mangroves and reef, respectively, Iotr
birot 7, 25; Amph compressa 9, 15; Aply fulva 7, 22; Desm anch
7, 8. Differences are significant by Welch’s approximate t-test
for cases in which variances are different at P < 0·05 for all
species except Desmapsamma anchorata.
to allow the planned paired statistical testing. Net
growth was greater on pvc than on mangrove roots
for Pelican Cays sponges at Twin Cays for all four of the
species (I. birotulata, A. compressa, A. fulva and M. laevis)
for which the comparison could be made (Fig. 1b), but
not significantly so (by Welch’s approximate t-tests for
cases in which variances are unequal).
The cause of mortality and partial mortality of
reef-sponge species from Pelican Cays on Twin Cays
roots was clear, as mangrove sponges had grown over
the transplanted reef sponges. At the time of monitoring, 52% (14/27) of surviving Pelican Cays sponges on
roots were being overgrown. Guided by labelled cable
ties remaining on the roots, the recent demise by overgrowth of nine additional Pelican Cays sponges was
discovered by excavating within neighbouring mangrove
sponges. Mangrove species that overgrew experimental
reef sponges were (in order of decreasing frequency)
T. ignis, B. caribea, H. magniconulosa, H. curaçaoensis,
Spongia tubulifera, and L. isodictyalis. Overgrowth was
not preceded by tissue death.
     
     
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
Typical reef species transplanted from the Pelican Cays
mangroves to the Carrie Bow Cay reef survived poorly,
reflecting passage of a hurricane in the autumn of 2001.
Although some portion of 39% of the individuals was
still alive, 87% of them had decreased in size, many so
drastically that they were smaller than 1 cm3. Confining the analysis to the four species that tolerated the
boat ride well, overall survival with size increase of reef
species on the Carrie Bow Reef was only 19·8% after
7 months, contrasting with the 53·5% of control indi-
Fig. 3. Mean specific growth (± 1 SE) of control individuals
of six sponge species typical of shallow coral reefs (dark bars)
and six species typical of mangrove roots (open bars indicate
rapid consumption by fish, stippled bars indicate moderate
consumption). Reef species abreviated as in Fig. 1; mangrove
species as: Ted ignis, Tedania ignis; Biem car, Biemna caribea;
Halich magn, Halichondria magniconulosa; Amorph sp.,
Amorphinopsis sp.; Liss isod, L. isodictyalis; Halicl imp,
Haliclona implexiformis.
viduals that increased in size on their home roots in the
Pelican Cays (significantly different by the G-test,
P < 0·001).
Three of the species inhabiting both Pelican Cays
mangroves and a shallow reef in Panama (I. birotulata,
A. compressa, A. fulva) had significantly higher specific
growth rates on mangrove roots than on the reef
(Fig. 2; Welch’s approximate t-test for cases in which
variances are unequal, P < 0·05 in all three comparisons). D. anchorata grew much faster than the others
and at nearly the same rate in the two habitats.
Growth rates vary widely among the 12 species (data
from controls avoid confounding of growth with
partial mortality; Fig. 3). All of the reef species except
D. anchorata (an unusually fast-growing species, Aerts
& van Soest 1997; Wulff, in preparation) grew relatively
slowly. The mangrove species fall into two groups: the
very fast-growing species, T. ignis, H. magniconulosa and
B. caribea and a group with intermediate growth rates.
Mangrove and coral-reef species also varied widely
in survival in their home mangrove cays. Survival and
mean specific growth rate of control individuals (Fig. 4)
are not related for the reef species (Kendall’s coefficient
of rank correlation, P >> 0·1), but have a significant
positive relationship for the mangrove species (P = 0·05).
Discussion
     
   
 
Distinct sponge faunas on mangrove roots in the Pelican Cays and Twin Cays are maintained by predation
318
J. L. Wulff
Fig. 4. Specific growth and survival after 7 months for six
species of common, typical reef sponges grown on their home
roots in the Pelican Cays and six species of common, typical
mangrove sponges grown on their home roots in Twin Cays.
Growth and survival were positively correlated (Kendall’s
coefficient of rank correlation; P = 0·05) for mangrove sponges,
but not for reef sponges.
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
and competition, at least for six of the most common
species from each set of cays. Uncaged mangrove sponges
were eliminated quickly by predators in the Pelican
Cays mangroves. Elimination of reef sponges from the
Pelican Cays by competition with quickly growing
typical mangrove species on Twin Cays mangrove roots
was still in progress after 7 months, but many individuals
had already succumbed.
Experiments on the Carrie Bow reef confirm that
predators can prevent common mangrove species from
living on the reef. Sponge-feeding fishes fed as in previous reports of natural feeding in the field. Angelfish
departed from their usual ‘smorgasbord’ feeding (i.e.
continuously moving among sponge species) (Randall
& Hartman 1968; Wulff 1994) only for the two species
they consumed most readily. Parrotfish consumed a
sponge until it was gone or they were chased away, exactly
as they feed on exposed cryptic reef sponges (Wulff
1988, 1997b, 1997c). This is not the first report of reef
fishes eating mangrove sponges. Gut contents of parrotfish
feeding in mangroves contained spicules from one
mangrove species (Dunlap & Pawlik 1998), and videos
of reef fishes feeding on chunks of mangrove sponges on
exposed racks showed consumption of four species (Dunlap
& Pawlik 1996), but details of normal feeding behaviour were lost in feeding melees resulting from sudden
appearances of large pieces of freshly cut sponges.
If spongivores can inhabit Pelican Cays mangroves
and prevent typical mangrove species from living there,
why are these fishes absent from Twin Cays and other
typical Caribbean mangrove stands? Three-dimensional
structure of the reefs in which Pelican Cays mangroves
are embedded may offer fishes hiding places that are
not available in or near typical mangrove stands (Wulff
2000 and additional personal observation). Barracudas
are not absent from mangroves.
Competition among sessile organisms takes longer
to demonstrate than predation, especially when competition is mediated by relative growth rates. Finding
typical reef sponge transplants engulfed entirely by
mangrove sponges that were not touching them when
the experiments were established, while individuals of
the same genotypes and initial sizes were thriving on
pvc pipes less than 0·5 m away, left no doubt that
overgrowth was eliminating reef sponges from Twin
Cays mangroves.
Elimination by overgrowth is unusual for sponges.
There are three reports: adult sponges overgrowing
recent recruits (Reiswig 1973), T. ignis overgrowing
other sponges on settling plates (Sutherland 1980), and
a specific pairwise interaction between an overgrowing
species and an overgrown species (Thacker et al. 1998).
However, most reports on interactions of sponges with
other sponges have suggested or demonstrated mutual
benefit (Rützler 1970; Sará 1970; Wulff 1997a; Wilcox,
Hill & DeMeo 2002). Competitive superiority of mangrove sponges over transplanted reef sponges appears
to be mediated by growth, as there was no evidence of
chemical warfare. The three mangrove species that
smothered neighbouring reef sponge transplants most
frequently were also the three with the fastest growth
rates (Fig. 3). The positive correlation between growth and
survival of mangrove species (Fig. 4) links growth rate
to success in this habitat, suggesting that competition
among the mangrove species is also mediated by relative
growth rates.
The sole reef species with rapid growth was D. anchorata, a uniquely weedy species (Wulff, in preparation).
Lack of a relationship between growth and survival
of the reef sponge species may reflect the variety of
challenges they face, including consumption by fish
and starfish, smothering by sediments and breakage by
physical disturbance (e.g. Wulff 1997a). In such a context, directing resources to concerns other than rapid
growth may make sense.
The passage of a hurricane was reflected in lower
survival of Pelican Cay sponges on the reef, but abiotic
conditions definitely did not inhibit sponges transplanted between mangrove cays, as Twin Cays sponges
thrived inside cages (predator-free) in the Pelicans, and
Pelican Cays sponges thrived on pvc pipes (competitorfree) at Twin Cays.
      
   
Restriction of species to refuges implies that a ‘refuge’
is a less desirable place to live. Cryptic spaces in the reef
frame (Wulff 1988, 1997c) or under rubble (Dunlap &
Pawlik 1996) can constrain the size a sponge achieves,
and referring to these as refuges may be reasonable for
some species. Mangrove roots have also been considered
refuges from predators (e.g. by Dunlap & Pawlik 1996;
Wulff 2000) for mangrove sponge species, although
additional experiments are required to determine if
319
Growth-defence
trade-offs and
sponge diversity
mangrove sponges would grow and survive better in
other habitats if spongivores were eliminated. Facultative mutualism with mangroves may also inhibit habitat
switches of some mangrove species (Ellison, Farnsworth
& Twilley 1996). Data in this report do demonstrate,
however, that sponge species that typically inhabit reefs
can grow and survive substantially better on mangrove
roots than on the reef (Fig. 2). However, the more rapid
growth of reef sponges on mangrove roots is insufficient to prevent overgrowth by still more rapidly growing mangrove species (Fig. 3). Rather than providing
the ideal set of abiotic factors for coral reef sponge
species, the reef may be a refuge for sponge species that
grow too slowly to survive among members of the
mangrove fauna.
-   
   
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
A trade-off between growth rate and defence is suggested by the faster growth and more frequent participation in overgrowth of the three mangrove species that
were consumed most quickly by fishes; intermediate
growth rates of less eagerly consumed mangrove species; and slow growth of the well-defended reef species
(except the unusual D. anchorata). Data on consumption of the typical reef species were not collected in this
study because it takes years to accumulate sufficient
observations of natural feeding on well-defended sponges,
but a hint of an inverse relationship between growth
and defence is seen in data from a 12-year study of
unmanipulated angelfish feeding on a completely
censused sponge community. For the relatively quickly
growing (Fig. 3) I. birotulata the ratio of number of
bites taken to total volume of sponge tissue was 0·07
(426 bites : 6001·3 cm3), while these ratios for the more
slowly growing A. fulva and A. compressa were only 0·02
(72 bites : 3626·3 cm3) and 0·01 (117 bites : 9767·3 cm3),
respectively (data from Wulff 1994 and unpublished).
Trade-offs between growth and defence are well
studied for terrestrial plants (e.g. Messina et al. 2002
and references therein), but directly relevant data are
rare for clonal marine animals. The one direct study of
resource allocation in sponges (Becerro, Turon & Uriz
1995; Uriz et al. 1995) demonstrated shifts by the
encrusting Mediterranean sponge Crambe crambe to
greater investment in defensive and supportive structures, at the expense of somatic growth and reproduction,
in environments where competition was important.
Another study (Hill 1998) has suggested that angelfishes preferentially consume a sponge, Chondrilla
nucula, that may grow quickly; but angelfish preference
was assumed on the basis of gut content data (Randall
& Hartman 1968) which were not corrected for relative
availability of sponge species. This sponge might
overgrow corals if not consumed (Vicente 1990; Hill
1998), so confirmation of fast growth and of angelfish
preference for this species would be especially
interesting.
Negative associations of growth rate with defences
can be interpreted in a variety of ways (see, e.g. Simms
1992) and are complicated by trade-offs among other
aspects of living (see, e.g. Mauricio 1998). Although
comparisons among species are confounded further by
differences in skeletal materials, modes of reproduction
and chemistry, and our virtually complete ignorance
about how costly all these aspects of living actually are,
they can offer insight into influence of trade-offs on
community structure and function.
    
:    
 - 
Sponges are like most other taxa in exhibiting very high
diversity in shallow tropical marine systems (e.g. Paulay
1997). Van Soest (1994) estimated that 640 described
sponge species inhabit the tropical western Atlantic,
and many more await description. Sponges are dominant
space-occupying organisms on reefs (e.g. Diaz & Rützler
2001) and mangrove roots throughout the region
(e.g. Sutherland 1980; Ellison et al. 1996; Rützler et al.
2000; Wulff 2000). The key functional roles played by
sponges in these systems are not covered by other
organisms (Diaz & Rützler 2001; Wulff 2000). Understanding the relative importance of biotic and abiotic
factors in maintaining sponge diversity has become
crucial as conservation becomes more pressing.
Distinctiveness of sponge faunas in different habitats has been attributed to abiotic factors, with which
sponge distributions are often well correlated (see,
e.g.Wilkinson & Evans 1989; Diaz et al. 1990; Alcolado
1994; Zea 1994). However, although abiotic differences
between coral reefs and mangroves are many and well
correlated with differences in the sponge faunas, in this
first experimental test the causal relationship between
abiotic factors and habitat distributions of sponge
species is shown to be secondary.
Within-habitat sponge diversity has also been attributed to abiotic factors. Negative influences have been
attributed to physical disturbance, sunlight and sedimentation (see, e.g. Wilkinson & Evans 1989; Alvarez
et al. 1990; Zea 2001 and references therein). Positive
influences have been attributed to high substratum area,
low turbidity, and close proximity of propagule source
habitats (Rützler et al. 2000). It is probable that all of
these factors could influence sponge diversity, but the
contrasting systems in this study, with 2·5-fold differences in species diversity (57 species at Twin Cays and
147 species in the Pelican Cays were reported by Rützler
et al. 2000), and in which competition or predation
strongly influence membership, suggest a look at how
interactions might also influence within-habitat diversity.
In systems in which effectiveness at gaining space is
key to survival of sessile organisms, competitively dominant species may overwhelm all others, lowering diversity. This expectation must be modified for systems
characterized by discontinuous habitat structure.
320
J. L. Wulff
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
Sutherland (1980) pointed out that the discontinuous
substrata provided by mangrove roots can increase
diversity by preventing space monopolization by competitive dominants across large continuous areas, a key
insight that has subsequently aided understanding of
many other systems. The outcome for the typical mangrove root community is that diversity may be lowered
on a particular root as fast-growing species overwhelm
others, but discontinuous substrata slow elimination
from the system, resulting in moderate overall species
diversity.
In contrast, in the Pelican Cays, where typical reefsponge species live on mangrove roots, spongivores
may prevent community domination by faster-growing
sponge species. This mechanism for maintaining high
diversity of sessile organisms was pointed out early on
by studies of preferential consumption of competitive
dominants by rabbits and starfish (Tansley & Adamson
1925; Paine 1966). If an inverse relationship between
growth rate and defences holds for more species than
the 12 most abundant ones chosen for these experiments, predators are at least partly responsible for the
exceptionally high sponge diversity of the typical
shallow coral reef sponge fauna. This is the opposite
conclusion from previous studies (Dunlap & Pawlik
1996, 1998) which suggested that spongivores decrease
reef sponge diversity by excluding mangrove species.
The ability of mangrove sponge species to outcompete
reef species, demonstrated first in the present study, was
the missing link between spongivory and very high
diversity on reefs.
Substantially poorer survival of sponges transplanted
from the Pelican Cays to the Carrie Bow reef supports
assertions that abiotic factors can serve as filters, excluding some species from a habitat (e.g. Wilkinson & Evans
1989; Alvarez et al. 1990; Alcolado 1994). However, for
species not inhibited by such filters, ecological interactions affect sponge diversity on three scales, as follows.
(1) Region: competition and predation strongly influence the between-habitat diversity of Caribbean mangrove and coral reef sponge faunas. (2) Community:
control of mangrove-fauna membership by competition lowers species diversity, whereas a variety of controls on reef-fauna membership, including predation,
may increase the number of species that coexist on
reefs. (3) Species: the trade-off between growth (resistance to competitors) and resistance to predators
precludes success of individual species as members of
both faunas.
Surprisingly, although members of the typical coral
reef sponge fauna and the typical mangrove root sponge
fauna appear unable to intermix, and thus remain distinct sets of species, these faunas are not actually tied
to the habitats in which they are found normally. The
persistent distinction between these two faunas is not
determined by habitat-characteristic abiotic factors,
but is a community-level reflection of the trade-off
between growth and defences against predators. In our
‘high diversity is good’ context of evaluating ecological
systems, the higher species diversity on coral reefs than
on mangroves has implied that the coral reef is the
superior habitat for tropical sponges. In fact, the higher
diversity may reflect the multiple challenges that make
living on a coral reef more of a struggle for sponges.
Mangroves, with higher nutrients, lower physical disturbance and no predators, offer typical reef sponges
better survival and growth, but trade-offs between
defences and growth put this paradise out of reach as
long as it is inhabited by typical mangrove species that
have traded the ability to cope with challenges for the
ability to grow more rapidly.
Acknowledgements
Fieldwork for this project was supported by the
National Museum of Natural History’s Caribbean
Coral Reef Ecosystems Program (CCRE Contribution
no. 693). I am grateful for the vigorous discussion and
comradeship of fellow participants in the International
Sponge Systematics Workshop convened at Carrie
Bow Cay in 1997. Thoughtful comments from J. Travis,
N. Underwood, D. Ferrell, T. Swain and anonymous
reviewers greatly improved the manuscript.
References
Aerts, L.A.M. & van Soest, R.W.M. (1997) Quantification of
sponge /coral interactions in a physically stressed reef community, NE Colombia. Marine Ecology Progress Series,
148, 125 – 134.
Alcolado, P.M. (1994) General trends in coral reefs sponge
communities in Cuba. Sponges in Time and Space: Biology,
Chemistry, Paleontology (eds R.W.M. van Soest, T.M.G.
van Kempen & J.-C.A.A. Braekman), pp. 251 – 256. A. A.
Balkema, Rotterdam.
Alvarez, B., Diaz, M.C. & Laughlin, R.A. (1990) The sponge
fauna on a fringing coral reef in Venezuela, I. Composition,
distribution, and abundance. New Perspectives in Sponge
Biology (ed. K. Rützler), pp. 358 – 366. Smithsonian Institution Press, Washington DC.
Becerro, M.A., Turon, X. & Uriz, M.J. (1995) Natural variation of toxicity in encrusting sponge Crambe crambe (Schmidt)
in relation to size and environment. Journal of Chemical
Ecology, 21, 1931 – 1946.
Bellwood, D.R. & Hughes, T.P. (2001) Regional-scale
assembly rules and biodiversity of coral reefs. Science, 292,
1532 –1534.
van Dam, R.P. & Diez, C.E. (1997) Predation by hawksbill
turtles at Mona Island, Puerto Rico. Proceedings of the 8th
International Coral Reef Symposium, Panama, 2, 1421–
1426.
Diaz, C., Alvarez, B. & Laughlin, R.A. (1990) The sponge
fauna on a fringing reef in Venezuela, II. Community structure. New Perspectives in Sponge Biology (ed. K. Rützler),
pp. 367 – 375. Smithsonian Institution Press, Washington,
DC.
Diaz, C. & Rützler, K. (2001) Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science,
69, 535 – 546.
Dunlap, M. & Pawlik, J.R. (1996) Video-monitored predation
by Caribbean reef fishes on an array of mangrove and reef
sponges. Marine Biology, 126, 117 – 123.
Dunlap, M. & Pawlik, J.R. (1998) Spongivory by parrotfish in
Florida mangrove and reef habitats. PSZN: Marine Ecology,
19, 325 – 337.
321
Growth-defence
trade-offs and
sponge diversity
© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,
313–321
Ellison, A.M., Farnsworth, E.J. & Twilley, R.R. (1996)
Facultative mutualism between red mangroves and rootfouling sponges in Belizean mangal. Ecology, 77, 2431 –
2444.
Hill, M.S. (1998) Spongivory on Caribbean reefs releases
corals from competition with sponges. Oecologia, 117,
143 – 150.
Hooper, J.N.A., Kennedy, J.A. & Quinn, R.J. (2002) Biodiversity ‘hotspots’. Patterns of richness and endemism, and
taxonomic affinities of tropical Australian sponges (Porifera).
Biodiversity Conservation, 11, 851 – 885.
Jackson, J.B.C. & Buss, L.W. (1975) Allelopathy and spatial
competition among coral reef invertebrates. Proceedings of
the National Academy of Science USA, 72, 5160 – 5163.
Knowlton, N. & Jackson, J.B.C. (1994) New taxonomy and
niche partitioning on coral reefs: jack of all trades or master
of some? Trends in Ecology and Evolution, 9, 7 – 9.
Kubanek, J., Whalen, K.E., Engel, S., Kelly, S.R., Henkel, T.P.,
Fenical, W. & Pawlik, J.R. (2002) Multiple defensive roles
for triterpene glycosides from two Caribbean sponges.
Oecologia, 131, 125 – 136.
Mauricio, R. (1998) Costs of resistance to natural enemies in
field populations of the annual plant Arabidopsis thaliana.
American Naturalist, 151, 20 – 28.
Messina, F.J., Durham, S.L., Richards, J.H. & McArthur, E.D.
(2002) Trade-off between plant growth and defense? A
comparison of sagebrush populations. Oecologia, 131,
43 – 51.
Ogden, J.C. (1997) Ecosystem interactions in the tropical
coastal seascape. Life and Death of Coral Reefs (ed. C.
Birkeland), pp. 288 – 297. Chapman & Hall, New York.
Paine, R.T. (1966) Food web complexity and species diversity.
American Naturalist, 100, 65 – 75.
Paulay, G. (1997) Diversity and distribution of reef organisms.
Life and Death of Coral Reefs (ed. C. Birkeland), pp. 298 –
353. Chapman & Hall, New York.
Randall, J.E. & Hartman, W.D. (1968) Sponge-feeding fishes
of the West Indies. Marine Biology, 1, 216 – 225.
Reed, J.K. & Pomponi, S.A. (1997) Biodiversity and distribution of deep and shallow water sponges in the Bahamas.
Proceedings of the 8th International Coral Reef Symposium,
Panama, 2, 1387 – 1392.
Reiswig, H.M. (1973) Population dynamics of three Jamaican
Demospongiae. Bulletin of Marine Science., 23, 191 – 226.
Rützler, K. (1970) Spatial competition among Porifera:
solution by epizoism. Oecologia, 5, 85 – 95.
Rützler, K., Diaz, M.C., van Soest, R.W.M., Zea, S., Smith,
K.P., Alvarez, B. & Wulff, J.L. (2000) Diversity of sponge
fauna in mangrove ponds, Pelican Cays, Belize. Atoll
Research Bulletin, 477, 231 – 250.
Rützler, K. & Muzik, K. (1993) Terpios hoshinota, a new
cyanobacteriosponge threatening Pacific reefs. Scientia
Marina, 57, 395 – 403.
Sará, M. (1970) Competition and cooperation in sponge
populations. Symposium of the Zoological Society of
London, 25, 273 – 284.
Schupp, P., Eder, C., Paul, V. & Proksch, P. (1999) Distribution of secondary metabolites in the sponge Oceanapia sp.
and its ecological implications. Marine Biology, 135, 573 –
580.
Simms, E.L. (1992) Costs of plant resistance to herbivory.
Plant Resistance to Herbivores and Pathogens (eds R.S. Fritz
& E.L. Simms), pp. 392 – 425. University of Chicago Press,
Chicago.
van Soest, R.W.M., (1994) Demosponge distribution patterns. Sponges in Time and Space: Biology, Chemistry,
Paleontology (eds R.W.M. van Soest, T.M.G. van Kempen,
& J.-C. Braekman), pp. 213–224. A. A. Balkema, Rotterdam.
Sutherland, J.P. (1980) Dynamics of the epibenthic community on roots of the mangrove Rhizophora mangle, at Bahia
de Buche, Venezuela. Marine Biology, 58, 75–84.
Tansley, A.G. & Adamson, R.S. (1925) Studies of the vegetation of the English chalk. III. The chalk grasslands of the
Hampshire–Sussex border. Journal of Ecology, 13, 177–
223.
Thacker, R.W., Becerro, M.A., Lumbang, W.A. & Paul, V.J.
(1998) Allelopathic interactions between sponges of a
tropical reef. Ecology, 79, 1740 –1750.
Uriz, M.J., Becerro, M.A., Tur, J.M. & Turon, X. (1996) Location of toxicity within the Mediterranean sponge Crambe
crambe (Demospongiae: Poecilosclerida). Marine Biology,
124, 583 –590.
Uriz, M.J., Turon, X., Becerro, M.A., Galera, J. & Lozano, J.
(1995) Patterns of resource allocation to somatic, defensive,
and reproductive functions in the Mediterranean encrusting
sponge Crambe crambe (Demospongiae, Poecilosclerida).
Marine Ecology Progress Series, 124, 159 – 170.
Vicente, V. (1990) Overgrowth activity by the encrusting
sponge Chondrilla nucula on a coral reef in Puerto Rico. New
Perspectives in Sponge Biology (ed. K. Rützler), pp. 436–
442. Smithsonian Institution Press, Washington, DC.
Wilcox, T.P., Hill, M. & DeMeo, K. (2002) Observations on a
new two-sponge symbiosis from the Florida Keys. Coral
Reefs, 21, 198 – 204.
Wilkinson, C.R. & Evans, E. (1989) Sponge distribution
across Davies Reef, Great Barrier Reef, relative to location,
depth, and water movement. Coral Reefs, 8, 1–7.
Wulff, J.L. (1988) Fish predation on cryptic sponges of
Caribbean coral reefs. American Zoologist, 28, A166.
Wulff, J.L. (1994) Sponge-feeding by Caribbean angelfishes,
trunkfishes, and filefishes. Sponges in Time and Space: Biology, Chemistry, Paleontology (eds R.W.M. van Soest,
T.M.G. van Kempen & J.-C. Braekman), pp. 265–271.
A. A. Balkema, Rotterdam.
Wulff, J.L. (1995b) Sponge-feeding by the Caribbean starfish
Oreaster reticulatus. Marine Biology, 123, 313–325.
Wulff, J.L. (1997a) Mutualisms among species of coral reef
sponges. Ecology, 78, 146 – 159.
Wulff, J.L. (1997b) Parrotfish predation on cryptic sponges of
Caribbean coral reefs. Marine Biology, 129, 41–52.
Wulff, J.L. (1997c) Causes and consequences of differences in
sponge diversity and abundance between the Caribbean
and eastern Pacific at Panama. Proceedings of the 8th International Coral Reef Symposium, Panama, 2, 377–1382.
Wulff, J.L. (2000) Sponge predators may determine differences in sponge fauna between two sets of mangrove
cays, Belize Barrier Reef. Atoll Research Bulletin, 477, 251–
263.
Wulff, J.L. (2001) Assessing and monitoring coral reef
sponges: why and how? Bulletin of Marine Science, 69,
831 – 846.
Zea, S. (1994) Patterns of sponge and coral abundance in
stressed coral reefs at Santa Marta, Colombian Caribbean.
Sponges in Time and Space: Biology, Chemistry, Paleontology
(eds R.W.M. van Soest, T.M.G. van Kempen & J.-C.
Braekman), pp. 257 – 264. A. A. Balkema, Rotterdam.
Zea, S. (2001) Patterns of sponge (Porifera, Demospongiae)
distribution in remote, oceanic reef complexes of the southwestern Caribbean. Revista de la Acadamia Colombiana de
Ciencias Exactas, Fisicas Y Naturales, 25, 579–592.
Received 28 January 2004; accepted 13 August 2004