ORIGINAL ARTICLE OA 000 EN

Functional
Ecology 1998
Growth dynamics and mortality of the encrusting
12, 631–639 sponge Crambe crambe (Poecilosclerida) in contrasting
habitats: correlation with population structure and
investment in defence
X. TURON,* I. TARJUELO* and M. J. URIZ†
*
Department of Animal Biology (Invertebrates), Faculty of Biology, University of Barcelona, 645 Diagonal Ave,
08028 Barcelona, Spain, and †Centre for Advanced Studies (CSIC), Camí de Sta. Bàrbara, s/n 17300 Blanes
(Girona), Spain

Summary
1. A trade-off was predicted between investment in defence and growth rate in the
encrusting sponge Crambe crambe (Schmidt), while survival rates were expected to
correlate positively with the production of defences. Previous studies have demon-
strated that this sponge is better defended (chemically and physically) in shaded
animal-dominated habitats than in well-illuminated habitats, dominated by algae. It
was determined whether these habitat-associated differences in investment correlate
with differences in growth, regeneration and mortality rates of small specimens (initial
average area less than 100 mm2) of this sponge.
2. In the 2 years of the study the sponge grew slowly (size increased 2·5 times on
average), and showed high interindividual variation in growth rates. A seasonal pattern
was evident, with marked size increases from May to October. Significantly higher
growth rates (on a monthly basis) were found in the well-illuminated habitat during the
second year of study. There was also a negative relationship between monthly growth
rate and toxicity (measured in previous studies). No differences were found in sponge
regeneration rates between communities.
3. Mortality was significantly higher in individuals from the well-illuminated habitat,
and mainly affected the smallest sponges (< 150 mm2).
4. This sponge was significantly more abundant in the shaded habitat, but the mean
size of the sponges was greater in the well-illuminated habitat. The size distributions in
the two communities were also significantly different. Sponges of the smallest size
classes were more abundant in the shaded community.
5. It is concluded that sponges in the shaded habitat, in which investment in defence
was greatest, featured higher survival but grew more slowly than those in the well-
illuminated habitat. Differential mortality and growth observed in the study were
sufficient to explain the patterns of abundance and size distributions of the established
sponge populations from these two habitats.
Key-words: Indeterminate growth, modular animals, population dynamics, resource allocation
Functional Ecology (1998) 12, 631–639

Introduction between investment in defences and growth, while

We aimed to assess whether the between-habitat differ-
ences in investment in defence, structural materials
and reproduction reported in previous studies in the
sponge Crambe crambe (Schmidt) could be related to
differences in growth rates and mortality. A trade-off
between allocation to defence (chemical and physical)
© 1998 British and to reproduction has been reported for this species
Ecological Society (Uriz et al. 1995). We predicted a similar trade-off
survival rates were expected to correlate positively with
the production of defences. We also wanted to deter-
mine whether differences in growth rates and mortality
could explain differences in the abundance and size-
structure of the established sponge populations.
Crambe crambe is one of the most widespread lit-
toral sponges in the north-western Mediterranean,
where it has a wide ecological distribution (Uriz,
Rosell & Martin 1992a). It is a red encrusting form,

631
632 which can reach surface areas of 0·5 m2 in the study
X. Turon et al. zone. At the same time, C. crambe featured strong
bioactivity in general bioassays (Jares-Erijman, Sakai
& Rinehart 1991; Berlinck et al. 1992; Uriz, Martin &
Rosell 1992b), suggesting the production of chemical
defences. These defences appear to perform multiple
ecological roles (Becerro et al. 1994a; Uriz et al.
1996; Becerro, Turon & Uriz 1997). In addition, this
species is a thinly encrusting form and it is therefore
highly surface-dependent, which implies that growth
and mortality rates are influenced by strong space
competition with neighbours. Here we seek to build
on previous knowledge of the variability of other
traits of the biology of C. crambe, namely, investment
in chemical and physical defences, production of lar-
vae, reproductive periods and filtration rates (Becerro,
Uriz & Turon 1995; Uriz et al. 1995; Turon, Becerro
& Uriz 1996a; Turon, Galera & Uriz 1997). Our aim
was to complete the picture of the biological strategy
of this sponge.
Ayling (1983) rightly claimed that almost no data on
growth and regeneration rates in encrusting sponges
existed, and few studies have contributed information
since then (e.g. Pomponi & Meritt 1985; Plucer-
Rosario 1987; Pansini & Pronzato 1990). The same
can be said for sheet-like invertebrates in general. Yet
encrusting invertebrates are a major part of many epi-
faunal assemblages in rocky bottoms, and they are
believed to be efficient competitors for space because
of their morphology (Buss 1979; Jackson 1979).
Studies on population dynamics of this type of organ-
ism, especially if they are coupled with data on energy
allocation, population structure and other traits of their
life history, are needed to explain processes and adap-
tive trends in epifaunal assemblages (Sebens 1987).
Materials and methods
STUDY DESIGN
Growth of C. crambe was studied by monitoring live
specimens at the locality of Blanes, northeast Spain
(western Mediterranean; 41°40·4'N, 2°48·2'E). It was
expected that small sponges would grow faster than
large ones, according to previous observations in sev-
eral sponge species (Dayton 1979). Large specimens
usually occupy all available space (Turon et al. 1996b)
and their growth and shrinking may reflect interactions
with their neighbours rather than their own physiologi-
cal state. Large sponges, on the other hand, are more
likely to suffer partial losses of material and subse-
quent regeneration. It was therefore decided to study
growth rates in small specimens (less than 100 mm2),
which may be assumed to be settlers from one of the
two preceding years, while regeneration rates were
© 1998 British
studied in large specimens (more than 40 000 mm2).
Ecological Society, Differences in growth and mortality were analysed
Functional Ecology, by comparing two contrasting habitats, in which pre-
12, 631–639 vious studies on other biological parameters of this
species had been performed. A thorough description
of these habitats was given in Becerro, Uriz & Turon
(1994b). Briefly, the sampling site consisted of two
parallel vertical walls between 6 and 12 m in depth,
and 3 m apart. These walls were similar in all respects
except for the orientation: one faced north, the other
south. The former received less irradiance than the lat-
ter, and the assemblages that developed on these walls
differed markedly: on the northward-facing wall a
space-limited community (hereafter called the
sciaphilous assemblage) was dominated by encrusting
animal species, mainly sponges. On the southward-
facing wall, erect macroalgae and patches of bare rock
dominated the landscape (hereafter the photophilic
assemblage). Growth form and relative allocation to
structural materials, reproduction and chemical
defences of C. crambe were studied in the same walls
(Becerro et al. 1994b, 1995; Uriz et al. 1995).
Moreover, seasonal fluctuations in the toxicity of this
species had been monitored in the same site (Turon
et al. 1996a).
MONITORING
In November 1994 small specimens (less than
100 mm2) were selected on each wall. Every month
their outlines were traced in situ onto acetate sheets.
The outlines were then digitized and their surface
areas were calculated. Since it was apparent from the
beginning that mortality was higher on the well-illu-
minated wall, new individuals from this wall were
included in the monitoring during the first 4 months of
study. Fusions and divisions of sponges over time
were also recorded. When fusion occurred, the areas
of the sponges before merging were added together to
give a single value per survey. When fission occurred,
the areas of the resulting clonemates were summed in
subsequent measurements. Final numbers of moni-
tored sponges were 24 in the shaded wall and 51 in the
well-illuminated wall. At each sampling time the
water temperature at a depth of 10 m was recorded.
The survey was terminated in January 1997.
For the study of regeneration rates, circular holes
(about 450 mm2) were scraped down to the rock in
each of 10 large (more than 40 000 mm2) specimens
on each wall and their regeneration was monitored
after 2 and 3 weeks by drawing the outlines of the
holes on acetate paper and calculating their areas as
described above. This study was conducted in October
1995 (outside the reproductive season of this species)
and lasted only 3 weeks because it was assumed that
true regeneration would occur only shortly after dam-
age. In fact, after 3 weeks, a film of filamentous algae
was already established in the holes and subsequent
growth could not be considered simple regeneration.
In February 1997, the abundance and size of speci-
mens of C. crambe on each wall were also studied. To
this end, three transect lines, 5 m long, were laid on
each wall. The transects were placed at 6, 7 and 8 m of
633 depth, with their origins laid haphazardly on the walls.
Growth and A 0·25 m stick was then run above and below the
mortality of transects and all sponges larger than 500 mm2 touched
encrusting by the stick at each metre of transect were counted.
sponges Specimens larger than those monitored in the 2-year
survey were selected because our aim was to ascertain
the effects of early mortality and growth on the
structure of the population at later stages. Individual
sizes were estimated by taking two measurements on
each individual, one along its longest axis and one
along the longest dimension perpendicular to the first
one. Both measures were then treated as the axes of an
ellipse whose area was taken as an approximation to
the sponge’s area.
STATISTICAL METHODS
From the changes in area over time, a monthly growth
rate was computed by the formula:
(Am – Am–1)
GRm = ––––––––– eqn 1
Am–1
where Am and Am – 1 are the areas at month m and at
the previous month, respectively. This growth rate is
the monthly change in area, relative to area at the
beginning of the month interval.
Cross-correlation analyses were used to check for
relationships between monthly growth rates and tem-
perature. Spearman rank correlation was used to
assess relationships between size and growth rates in
the month in which the highest mean growth rate was
recorded.
For the comparison of growth rates between walls, a
repeated-measures analysis of variance (Potvin,
Lechowicz & Tardif 1990; Von Ende 1993) was first
tried with habitat as the between-individual factor and
time as the within-individual factor. However, the cir-
cularity assumption, necessary for the use of the uni-
variate repeated-measures analysis (ANOVAR), was
badly violated by our data (Mauchly’s sphericity test).
The multivariate equivalent of this analysis (MANOVAR ,
also called profile analysis) requires the less stringent
assumption of homogeneity of the variance–covariance
matrix, which was nevertheless not met in our case
(Box M-test). No transformation succeeded in render-
ing the data amenable to these analyses. A randomiza-
tion method was therefore used, based on Manly
(1991), which consisted of a two-stage permutation of
the data: first, individuals were randomly reassigned to
the two habitats, and then readings for each individual
were randomly rearranged among observation times.
With this two-level randomization, the overall total
sum of squares, as well as the total between- and
within-subject sums of squares, remain unchanged
(Manly 1991). The sum of squares associated with each
© 1998 British
factor and their interaction is therefore a suitable statis-
Ecological Society, tic on which to test the significance of each effect. The
Functional Ecology, whole series of data was randomized 4999 times (plus
12, 631–639 the observed one) to approximate the null hypothesis
distribution of the sum of squares for each factor and
their interaction, and then how extreme were the
observed values in this distribution was examined. An
effect was judged significant when the observed sum of
squares was exceeded by less than 5% of the corre-
sponding values in the randomization series. An impor-
tant advantage of this method, aside from being
non-parametric, is that it can use all the data set, not just
the sponges that survived until the end of the experi-
ment (ANOVAR/MANOVAR procedures require measure-
ments for each individual at each time interval). For
sponges that were not present at all observation times,
the permutation between times was done only within
the period in which the sponge was in the study.
Survival of sponges was analysed by the life-table
method, and hazard functions were computed for both
walls. Survival on both walls was compared by a
Wilcoxon-type test (Fox 1993). The relationship
between the area attained and survival was analysed
with the Cox proportional hazards model (Fox 1993).
The packages Systat version 5·0 and Statistica version
4·0 were used for the analyses, and the randomization
routine was written in TURBOPASCAL version 6·0.
Results
The time courses of the mean surface area and the
monthly growth rates of the sponges studied, both
habitats pooled, are presented in Fig. 1. The monthly
growth rate was smoothed to avoid noise fluctuations
by a weighed moving average (current value × 0·5 +
previous value × 0·25 + following value × 0·25).
Water temperature readings during the study period
are also shown.
The periods of growth in this species fluctuated sea-
sonally. Gains in area were recorded from May to
October (roughly late spring and summer), while in
late autumn and winter there was no growth of the
colonies, even a small shrinkage relative to the values
in October. The growth rates were negative or close to
0 from October to the beginning of spring, and their
peaks occurred in August 1995 and June 1996.
Cross-correlation studies between monthly growth
rates (both habitats pooled) and temperature revealed
a significant positive correlation between both param-
eters at time lags of 0, 1 and 2 months, and significant
negative correlations at time lags of – 3, – 4 and
– 5 months. This indicated that growth rates covaried
positively with the temperature measured in the two
preceding and the current month, and negatively with
temperature recorded in the subsequent third, fourth
and fifth months.
The relationship between growth rate and size was
analysed in the month with the highest monthly growth
rate (August 1995). The size at the beginning of the
month interval was correlated with the growth rate.
The Spearman correlation coefficient was negative,
indicating a tendency towards lower growth in larger
specimens, but not significant (rs = – 0·119, P = 0·41).
634 When considered separately, the values of monthly
X. Turon et al. growth rates in the two habitats (Fig. 2) revealed a
trend towards increased growth in the well-illuminated
assemblage, which was especially clear during the sec-
ond year of the study. The results of the randomization
test performed on the monthly growth rates are shown
in Table 1. Both time and the interaction between time
and habitat were significant. A significant interaction
term means that the time course of growth was differ-
ent in sponges from the two habitats. Figure 2 reveals
that the differences between habitats occurred mainly
during the second growth season. The first and second
years of study were therefore analysed separately, and
neither the habitat nor the interaction was found to
have a significant effect during the first year, while
only the habitat effect was significant if the second
year of study was considered (Table 1). This difference
in the habitat effect over time led to a significant inter-
action term when both years were considered together.
The pattern of significant results was the same when
the analyses were repeated with just the survivors from
each habitat (not shown).
Mortality was higher in the well-illuminated habitat
(Fig. 2). By the end of the study, only 16 (31%)
sponges survived in this habitat, while 15 (62%)
sponges initially included in the study in the shaded
wall were still alive. The data were analysed by the
life-table method, and differences in mortality were
significant (Gehan’s Wilcoxon test, P < 0·001). There
Fig. 1. Mean values of area and monthly growth rate of C. crambe during the
study period (both habitats pooled). Bars are standard errors. The water temperature
at – 10 m is also indicated.
was no clear temporal pattern in the hazard rates
(probability of a sponge dying in any one interval,
provided it has arrived alive at the beginning of this
interval), except that hazard was high in the pho-
tophilic assemblage during the first part of the study,
resulting in many losses.
The Cox’s regression model between hazard rate
and maximal size attained showed significant negative
relationships between mortality and size in both habi-
tats (P < 0·0001 in both cases). Dead individuals were
mostly sponges smaller than 150 mm2 in surface area.
Few deaths occurred once individuals had attained
sizes above 150 mm2, and none occurred in both habi-
tats in individuals that attained sizes above 450 mm2.
The abundance of sponges larger than 500 mm2,
measured in the transects laid on each wall, was
40·80 ± 3·22 individuals m–2 (mean ± SE) in the
sciaphilous assemblage, and 22·66 ± 2·30 individu-
als m–2 in the photophilic one. The mean size of the
sponges, on the other hand, was 6886 ± 1033 mm2 in
the former habitat and 4118 ± 340 mm2 in the latter.
The between-wall differences were significant for both
variables (Mann–Whitney U-test, P < 0·0001 in both
cases). Figure 3 shows the size–frequency structure of
the sponges in the two habitats. Sponges belonging to
size-classes below 5000 mm2 were more abundant in
the sciaphilous habitat. At the other extreme, some
sponges from the photophilic habitat featured sizes up
to 100 000 mm2, while the maximal sponge size
recorded on the shaded wall was close to 50 000 mm2.
The two frequency distributions were significantly
different (Kolmogorov–Smirnov two-sample test,
P = 0·015).
There were relatively few fusions or fissions during
the study; 14 fission and 12 fusion events occurred
throughout the study in the photophilic assemblage,
5 fissions and 7 fusions in the sciaphilous one (note
that the number of sponges monitored was double in
the former).
Regeneration rates in the two habitats considered,
estimated by the regeneration of holes scraped in
sponge individuals in each wall, did not differ signifi-
cantly between walls (Fig. 4). The holes had closed
slightly more in the sciaphilous sponges after three
weeks, but differences were not significant (t-test,
P = 0·5794).
Discussion
The 2-year monitoring revealed that the growth rate of
small specimens of C. crambe was extremely low,
especially if compared with that reported for massive
demosponges (Dayton 1979) or calcareous sponges
(Johnson 1979). Sizes increased on average about 2·5
times in 26 months (Fig. 1), which is surprising given
the very small initial size as compared with the large
individuals common in this habitat (see Fig. 3). Bryan
(1973) and Ayling (1983) similarly reported very slow
growth in several species of encrusting sponge. A high
635 interindividual variability was also apparent in our The growth of C. crambe fluctuated seasonally; in
Growth and study, as seems to be the rule in modular organisms both years sponges increased in size from May to
mortality of (Brunetti & Copello 1978; Dayton 1979; Bak, Sybesma October, coinciding with the rise of sea-water temper-
encrusting & Van Duyl 1981; Ayling 1983; Wulff 1985; Todd & atures. Seasonal patterns are common in temperate
sponges Turner 1988; Stocker 1991; Turon & Becerro 1992). habitats (Elvin 1976; Osman 1977; Sutherland &
Some specimens of C. crambe remained small through- Karlson 1977; Sebens 1986). For sponges, seasonal
out the study period. Other individuals were ‘success- cycles with higher growth rates in winter–early spring
ful’ in that they increased in size throughout the study. (the reverse of what we have found) have been
In some cases, individuals that had attained a moderate reported by Johnson (1979). In contrast, Ayling (1983)
size regressed to a very small surface area. These cases found fluctuations in sponge sizes not related to sea-
were, however, rare in our study. Although some fission sonal or reproductive cycles, and no seasonal pattern
and fusion of sponges did occur, the fragment dynamics of growth has been observed in other Mediterranean
of small individuals of this species is much less relevant species (Pansini & Pronzato 1990). Alternating cycles
to its demography than that reported for other encrust- of allocation to reproduction and growth are usually
ing invertebrates (Bak et al. 1981; Stocker 1991) or for proposed to explain seasonal fluctuations in growth
branching sponges (Wulff 1991). rate. However, as small sponges were selected, repro-
ductive activity could not explain the cycles found.
Larvae were not observed in the colonies monitored
and, in a previous survey, it was found that only 10%
and 20% of sponges smaller than 1000 mm2 were
reproductive in the sciaphilous and photophilic
assemblages, respectively (Uriz et al. 1995). Turon
et al. (1996a) reported seasonal differences in toxicity
levels and thus investment in chemical defence of C.
crambe in this area. Although the study was per-
formed on different individuals and in different years,
if the monthly mean values of toxicity found by Turon
et al. (1996a) are tentatively analysed against the
monthly growth rates (both years averaged) found in
the present survey, a significant negative relationship
appears (Pearson correlation coefficient = – 0·702,
n = 12, P = 0·019).
It was found that growth rates were not signifi-
cantly correlated to size in the month in which the
highest growth rate was recorded. This was as
expected for organisms featuring indeterminate
growth (Jackson 1979). In particular, in sheet-like
forms, no allometric adjustment of surface/volume
ratio is necessary (Ryland & Warner 1986), so growth
rate can be maintained, at least theoretically, indefi-
nitely. However, it was found that the correlation
coefficient was negative (even if not significant), indi-
cating a tendency towards declining growth rates with
size. Dayton (1979) found higher growth rates in
small sponges than in larger ones, while Fell &
Lewandroski (1981) did not find the growth of
Fig. 2. Time course of the mean values of monthly growth rate (bars are standard
errors) and percentage survivorship of C. crambe in the two habitats studied. Halichondria sp. related clearly to size. Turon &
Becerro (1992) found significant negative relation-
ships between growth rate and size in four encrusting
Table 1. Significance levels obtained by randomization for the repeated measures ascidian species. Attenuation of growth with size may
analyses of the growth rates
reflect habitat constraints as sponges occupied the free
Percentage of randomization SS that exceed observed SS space available (Sebens 1987).
Life spans of benthic invertebrates are poorly
Source of variation Both years First year Second year known (Jackson 1986). Our sponges might have been
3·5- or 4·5-years-old at the end of the experiment, if
Habitat 0·766 0·388 0·014
we were right in assuming that they came from the
Time 0·000 0·000 0·000
Habitat × Time 0·026 0·495 0·697 1992 and 1993 recruitments. However, by the end of
the study, none had reached a size comparable even to
SS; sums of squares. medium-sized specimens in the area (see Fig. 3). This
636
X. Turon et al.
Fig. 3. Size–frequency distributions of Crambe crambe in the two habitats surveyed. Numbers in the abscissa indicate the
upper limits of the size-class intervals (× 103). Note change in interval-width for sizes above 20 000 mm2.
suggests that C. crambe is a remarkably long-lived
species, although calculating life spans from the growth
rates observed is not advisable owing to the decoupling
of age and size in these modular organisms.
As for the between-habitat comparisons of growth
rates, a different time course was found in the two
habitats (significant interaction). This was due to the
growth of sponges during the second year (Fig. 2), in
which growth rates were high in the well-illuminated
wall from April to September, while they remained
close to zero in the shaded habitat. Accordingly, a
significant habitat effect was found when only the
second year was analysed. Mortality rates, on the
other hand, featured clear differences between habi-
tats; survival in sponges from the sciaphilous habitat
was double that of sponges from the photophilic
assemblage. On both walls there was a clear inverse
© 1998 British
Ecological Society,
Functional Ecology, Fig. 4. Time course of the regeneration of holes scraped in
12, 631–639 C. crambe specimens in the two habitats.
relationship between mortality and size (Cox regres-
sion model). Very rarely had a large sponge disap-
peared from one observation to the next, but it was
not uncommon to find a regression in size during the
few months preceding the death of the individual.
Size may act as a refuge against the causes of mortal-
ity in the zone (Sebens 1982). Johnson (1979)
reported that the periods of high mortality in calcare-
ous sponges coincided with the season of slow
growth. In our case, aside from a high mortality dur-
ing the first months of the study (especially in the
photophilic sponges), no clear seasonal trend in
mortality was apparent.
Why mortality was higher in the well-illuminated
wall remains unclear. Damage by passing sea-
urchins during grazing excursions may explain the
loss of small C. crambe colonies, but sea-urchins
were equally abundant on both walls. The number of
echinoids measured in five 5 × 1 m2 transects on
each wall was 3·48 ± 0·46 individuals m–2 (mean ±
SE) on the well-lit wall, and 3·36 ± 0·55 on the
shaded wall. Overgrowth by fast-growing algal
species may be responsible for the higher mortality
rates. Experimental work is needed to address this
question.
Crambe crambe was twice as abundant in the
shaded habitat; here they suffered lower mortality,
but were smaller as a result of slower growth rates.
The size frequency distributions revealed a larger
number of sponges smaller than 5000 mm2 in the
sciaphilous habitat (Fig. 3). These findings are con-
sistent with the idea that mortality is high on the
photophilic wall during the first years of the life. On
the other hand, the specimens that survive on this
wall grow at a faster rate and attain a larger size. For
example, large sponges, in excess of 50 000 mm2,
had been recorded in the photophilic habitat, but not
637 in the sciaphilous one. The patterns of sponge abun-
Growth and dance and size distribution described from these two
mortality of habitats match the pattern expected if mortality and
encrusting differential growth during the first years of life
sponges determined the structure of this population. Other
factors, such as differential settlement preferences,
need not be invoked to explain the patterns
observed. Indeed, we have found evidence that lar-
vae of this sponge do not respond to light gradients
(M. J. Uriz, unpublished data).
Regeneration rates were similar on both walls, and
were quite fast. The rate at which the area of the holes
produced in the sponge surfaces decreased as a result
of sponge regeneration was – 0·456 (SE = 0·077)
during the 3 weeks of the experiment. Consequently,
regeneration rates were much faster than growth rates
in this species, as noted also by Ayling (1983) in
another encrusting sponge. Rapid regeneration has
been considered a mechanism whereby sponges can
maintain their dominance in cryptic reef environments
(Jackson & Palumbi 1978). Similarly, rapid regenera-
tion may contribute in our case to the ability of
sponges to recover lost space (originating from local
perturbations) in the presence of opportunistic colo-
nizers of bare substratum. Fast regeneration and long
life span may contribute to explain why a species with
such a slow growth as C. crambe is an important
member, in terms of cover, of sublittoral assemblages.
In previous studies, differences in biological
parameters in this species between the same two
walls studied have been substantiated: toxicity and
thus investment in chemical defences is higher on
the shaded wall (Becerro et al. 1995). Likewise,
investment in supporting, structural elements
(mainly collagen and fibres) is higher in sciaphilous
sponges (Uriz et al. 1995). The pattern was therefore
one of higher investment in both chemical and phys-
ical defences on the shaded wall. Becerro et al.
(1995) and Uriz et al. (1995) suggested (although
proper experimental confirmation has not yet been
possible) that this pattern may be due to the different
competition pressures in the two habitats; space was
a limiting resource in the sciaphilous assemblage
dominated by slow-growing animal species. A strat-
egy of strong space competition with physical and
chemical defences may develop there, while the pho-
tophilic habitat was dominated by fast-growing,
erect algae, with patches of bare substratum being
freed continuously. A more opportunistic strategy
may be suitable here.
If photophilic specimens invest less in defence, we
expected to find a higher allocation in this habitat to
growth and reproduction. Reproductive investment is
indeed higher in the photophilic sponges, as shown
by Uriz et al. (1995). As for growth, the results
obtained here of the monthly growth rates and the
© 1998 British
Ecological Society, negative correlation between growth rate and toxicity
Functional Ecology, on a temporal basis indicated that growth is slower on
12, 631–639 the wall in which more energy is devoted to defence,
and that growth rates are depressed during the periods
of higher toxicity. The data support the existence of a
trade-off between production of defences and
growth rate. It should also be pointed out that
between-habitat differences in allocation are more
distinct in medium- to large-sized individuals (Uriz
et al. 1995), so the effect of differential investment in
these diverse functions might have been more appar-
ent as specimens grow to larger sizes than those con-
sidered here, which is consistent with the fact that the
between-habitat differences in growth rate appeared
especially in the second year. All this suggests that
longer-term studies are needed to understand better
the interaction between demography and habitat in
this species. Interpretation of our results need some
caution owing to the brevity of the present study.
Differences in mortality, on the other hand, were as
expected. Sponges in the high-mortality site invested
less in structural, long-lasting physical defences
(which may be useless in the competition with fast-
growing algae).
In conclusion, the between-habitat comparison
showed that specimens from the habitat in which the
highest investment in defence had been reported
survived better. A trade-off between growth rate and
production of defence could also be substantiated.
Such a trade-off may be more evident in larger speci-
mens, especially at sizes where the reproductive
activity is high. Differential growth and mortality
can explain the contrasting population structure of
this species in the two habitats. The results are con-
sistent with the idea of a cost associated with invest-
ment in defence, which results in better survival but
at the price of lower reproductive output and slower
growth.
Acknowledgements
We thank A. Davis (University of Wollongong,
Australia) for critically reading the manuscript. M.
Maldonado and R. Martí (CEAB, Spain) helped in the
field work. This research was funded by projects
DGCYT PB94–0015 and MAR95–1764 of the
Spanish Government, and also benefited from the
support of the Catalan Government (GRQ93–8042).
References
Ayling, A.C. (1983) Growth rates and regeneration in thinly
encrusting demospongiae from temperate waters.
Biological Bulletin 165, 343–352.
Bak, R.P.M., Sybesma, J. & Van Duyl, F.C. (1981) The ecol-
ogy of the tropical compound ascidian Trididemnum
solidum. II. Abundance, growth and survival. Marine
Ecology Progress Series 6, 43–52.
Becerro, M.A., López, N.I., Turon, X. & Uriz, M.J. (1994a)
Antimicrobial activity and surface bacterial film in
marine sponges. Journal of Experimental Marine Biology
and Ecology 179, 195–205.
Becerro, M.A., Uriz, M.J. & Turon, X. (1994b) Trends in
space occupation by the encrusting sponge Crambe
638 crambe: variation in shape as a function of size and envi-
X. Turon et al. ronment. Marine Biology 121, 301–307.
Becerro, M.A., Uriz, M.J. & Turon, X. (1995) Natural varia-
tion of toxicity in encrusting sponge Crambe crambe
(Schmidt) in relation to size and environment. Journal of
Chemical Ecology 21, 1931–1946.
Becerro, M.A., Turon, X. & Uriz, M.J. (1997) Multiple func-
tions for secondary metabolites in encrusting marine
invertebrates. Journal of Chemical Ecology 23,
1527–1547.
Berlink, R.G.S., Braeckman, J.C., Daloze, D., Bruno, I.,
Riccio, R., Rogeau, D. & Amade, P. (1992) Crambines C1
and C2: two further ichthyotoxic guanidine alkaloids
from the sponge Crambe crambe. Journal of Natural
Products 55, 528–532.
Brunetti, R. & Copello, M. (1978) Growth and senescence in
colonies of Botryllus schlosseri (Pallas) (Ascidiacea).
Bolletino Zoologico 45, 359–364.
Bryan, P.G. (1973) Growth rate, toxicity and distribution of
the encrusting sponge Terpios sp. (Hadromerida:
Suberitidae) in Guam, Marianas Islands. Micronesica 9,
237–242.
Buss, L.W. (1979) Habitat selection, directional growth and
spatial refuges: why colonial animals have more hiding
places. Biology and Systematics of Colonial Organisms
(eds G. Larwood & B. R. Rosen), pp. 459–497. Academic
Press, London.
Dayton, P.K. (1979) Observations of growth, dispersal and
population dynamics of some sponges in McMurdo
Sound, Antarctica. Colloques Internationaux du CNRS
no. 291 (eds C. Lévi & N. Boury-Esnault), pp. 271–282.
Publications du CNRS, Paris.
Elvin, D.W. (1976) Seasonal growth and reproduction of an
intertidal sponge, Haliclona permollis (Bowerbank).
Biological Bulletin 151, 108–125.
Fell, P.E. & Lewandroski, K.B. (1981) Population dynamics
of the estuarine sponge Halichondria sp., within a New
England Eelgrass Community. Journal of Experimental
Marine Biology and Ecology 55, 49–63.
Fox, G.A. (1993) Failure-time analysis: emergence, flow-
ering, survivorship, and other waiting times. Design
and Analysis of Ecological Experiments (eds S. M.
Scheiner & J. Gurevitch), pp. 113–137. Chapman &
Hall, London.
Jackson, J.B.C. (1979) Morphological strategies of sessile
animals. Biology and Systematics of Colonial Organisms
(eds B. Rosen & G. Larwood), pp. 499–555. Academic
Press, London.
Jackson, J.B.C. (1986) Modes of dispersal of clonal benthic
invertebrates: consequences for species distributions and
genetic structure of local populations. Bulletin of Marine
Science 39 (2), 588–606.
Jackson, J.B.C. & Palumbi, S.R. (1978) Regeneration and
partial predation in cryptic coral reef environments:
Preliminary experiments on sponges and ectoprocts.
Biologie des Spongiaires (eds C. Levi & N. Boury-
Esnault), pp. 303–308. Publications du CNRS, Paris.
Jares-Erijman, E.A., Sakai, R. & Rinehart, K.L. (1991)
Crambescidins: new antiviral and cytotoxic compounds
from the sponge Crambe crambe. Journal of Organic
Chemistry 56, 5712–5715.
Johnson, M.F. (1979) Recruitment, growth, mortality and
seasonal variations in the calcareous sponge Clathrina
coriacea (Montagu) and C. blanca (Miklucho-Maclay)
from Santa Catalina Island, California. Colloques
Internationaux du CNRS no. 291 (eds C. Lévi & N. Boury-
Esnault), pp. 325–334. Publications du CNRS, Paris.
© 1998 British
Manly, F.J. (1991) Randomization and Montecarlo Methods
Ecological Society,
in Biology. Chapman & Hall, London.
Functional Ecology,
Osman, R.W. (1977) The establishment and development of
12, 631–639
a marine epifaunal community. Ecological Monographs
47, 37–63.
Pansini, M. & Pronzato, R. (1990) Observations on the
dynamics of a Mediterranean sponge community. New
Perspectives in Sponge Biology (ed. K. Rützler), pp.
404–415.
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.
Pomponi, S.A. & Meritt, D.W. (1985) Distribution and life
history of the boring sponge Cliona truitti in the upper
Chesapeake Bay. New Perspectives in Sponge Biology
(ed. K. Rützler), pp. 384–390. Smithsonian Institution
Press, Washington, DC.
Potvin, C., Lechowicz, M.J. & Tardif, S. (1990) The statisti-
cal analysis of ecophysiological response curves obtained
from experiments involving repeated measures. Ecology
71, 1389–1400.
Ryland, J.S. & Warner, G.F. (1986) Growth and form in
modular animals: ideas on the size and arrangement of
zooids. Philosophical Transaction of the Royal Society of
London B313, 53–76.
Sebens, K.P. (1982) Competition for space: growth rate,
reproductive output, and scape in size. American
Naturalist 120, 189–197.
Sebens, K.P. (1986) Spatial relationships among encrusting
marine organisms in the New England subtidal zone.
Ecological Monographs 56, 73–96.
Sebens, K.P. (1987) The ecology of intermediate growth in
animals. Annual Review of Ecology and Systematics 18,
371–407.
Stocker, L.J. (1991) Effects of size and shape of colony on
rates of fusion, growth and mortality in a subtidal inverte-
brate. Journal of Experimental Marine Biology and
Ecology 14, 161–175.
Sutherland, J.P. & Karlson, R.H. (1977) Development and
stability of the fouling community at Beaufort, North
Carolina. Ecological Monographs 47, 425–446.
Todd, C.D. & Turner, S.J. (1988) Ecology of intertidal and
sublittoral cryptic epifaunal assemblages. II. Nonlethal
overgrowth of encrusting bryozoans by colonial ascidi-
ans. Journal of Experimental Marine Biology and
Ecology 115, 113–126.
Turon, X. & Becerro, M.A. (1992) Growth and survival of
several ascidian species from the northwestern
Mediterranean. Marine Ecology Progress Series 82,
235–247.
Turon, X., Becerro, M.A. & Uriz, M.J. (1996a) Seasonal
patterns of toxicity in benthic invertebrates: the encrust-
ing sponge Crambe crambe (Poecilosclerida). Oikos 75,
33–40.
Turon, X., Becerro, M.A., Uriz, M.J. & Llopis, J. (1996b)
Small-scale association measures in epibenthic communi-
ties as a clue for allelochemical interactions. Oecologia
108, 351–360.
Turon, X., Galera, J. & Uriz, M.J. (1997) Clearance rates
and aquiferous systems in two sponges with contrasting
life-history strategies. Journal of Experimental Zoology
278, 22–36.
Uriz, M.J., Rosell, D. & Martín, D. (1992a) The sponge pop-
ulation of the Cabrera archipelago (Balearic Islands):
characteristics, distribution and abundance of the most
representative species. Pubblicazioni Stazione Zoologica
di Napoli I: Marine Ecology 113, 101–117.
Uriz, M.J., Martín, D. & Rosell, D. (1992b) Relationship of
biological and taxonomic characteristics to chemically
mediated bioactivity in Mediterranean littoral sponges.
Marine Biology 113, 287–297.
Uriz, M.J., Turon, X., Becerro, M., Galera, J. & Lozano, J.
(1995) Patterns of resource allocation to somatic,
639 defensive, and reproductive functions in the Mediterranean
Growth and encrusting sponge Crambe crambe (Demospongiae,
Poecilosclerida). Marine Ecology Progress Series 124,
mortality of
159–170.
encrusting Uriz, M.J., Turon, X., Becerro, M. & Galera, J. (1996)
sponges Feeding deterrence in sponges. The role of toxicity, phys-
ical defenses, energetic contents, and life-history stage.
Journal of Experimental Marine Biology and Ecology
205, 187–204.
Von Ende, C.N. (1993) Repeated-measures analysis: growth
and other time-dependent measures. Design and Analysis
of Ecological Experiments (eds S. M. Scheiner & J.
Gurevitch), pp. 113–137. Chapman & Hall, London.
Wulff, J.L. (1985) Patterns and processes of size change in
caribbean demosponges of branching morphology. New
Perspectives in Sponge Biology (ed. K. Rützler), pp.
425–435. Smithsonian Institution Press, Washington, D.C.
Wulff, J.L. (1991) Asexual fragmentation, genotype success,
and populations dynamics of erect branching sponges.
Journal of Experimental Marine Biology and Ecology
149, 227–247.
Received 27 March 1997; revised 6 October 1997; accepted
24 November 1997

© 1998 British
Ecological Society,
Functional Ecology,
12, 631–639