Fragments or propagules? Reproductive tradeoffs among Callyspongia spp. from Florida coral reefs
ABSTRACT Fragmentation and propagule formation are alternative reproductive strategies found in both plants and animals, with the latter generally providing greater dispersal capability. When both strategies occur, life history theory predicts that resources should be divided between the two. On coral reefs, both strategies are exhibited by branching corals and sponges, which are broken-up after storm events and rapidly recolonize. In this study, we compared two congeneric Caribbean reef sponges, Callyspongia armigera, which is branched and easily fragmented, and C. vaginalis, which is not, to test whether there is a tradeoff in growth and propagule formation for C. armigera relative to C. vaginalis. Both species were equally abundant on coral reefs off Key Largo, Florida (10.1 ± 3.7 vs 11.9 ± 3.0 per 100 m2, respectively), suggesting that they are equally successful relative to two other non-fragmenting congeneric species (C. fallax and C. plicifera) that are much less common. The number of substratum attachment points per sponge was significantly higher for C. armigera compared to C. vaginalis (2.31 ± 1.47 vs 1.03 ± 0.18 sponge−1), providing further evidence of the reliance of C. armigera on fragmentation, and of C. vaginalis on recruitment from larval settlement and subsequent growth. Growth rates in predator-exclusion experiments were ∼4-fold higher for C. armigera compared to C. vaginalis (0.36 ± 0.31 vs 0.08 ± 0.11 % initial mass day−1), but C. armigera produced ∼13-fold fewer propagules than C. vaginalis (0.04 ± 0.22 vs 0.53 ± 1.08 % tissue area). Our results support a tradeoff between growth and propagule output for C. armigera relative to C. vaginalis, suggesting that these closely related sponge species took different evolutionary trajectories in reconciling their resource constraints.
- [show abstract] [hide abstract]
ABSTRACT: Mutation-selection balance in a multi-locus system is investigated theoretically, using a modification of Bulmer's infinitesimal model of selection on a normally-distributed quantitative character, taking the number of mutations per individual (n) to represent the character value. The logarithm of the fitness of an individual with n mutations is assumed to be a quadratic, decreasing function of n. The equilibrium properties of infinitely large asexual populations, random-mating populations lacking genetic recombination, and random-mating populations with arbitrary recombination frequencies are investigated. With 'synergistic' epistasis on the scale of log fitness, such that log fitness declines more steeply as n increases, it is shown that equilibrium mean fitness is least for asexual populations. In sexual populations, mean fitness increases with the number of chromosomes and with the map length per chromosome. With 'diminishing returns' epistasis, such that log fitness declines less steeply as n increases, mean fitness behaves in the opposite way. Selection on asexual variants and genes affecting the rate of genetic recombination in random-mating populations was also studied. With synergistic epistasis, zero recombination always appears to be disfavoured, but free recombination is disfavoured when the mutation rate per genome is sufficiently small, leading to evolutionary stability of maps of intermediate length. With synergistic epistasis, an asexual mutant is unlikely to invade a sexual population if the mutation rate per diploid genome greatly exceeds unity. Recombination is selectively disadvantageous when there is diminishing returns epistasis. These results are compared with the results of previous theoretical studies of this problem, and with experimental data.Genetics Research 07/1990; 55(3):199-221. · 2.00 Impact Factor
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ABSTRACT: Widespread thermal anomalies in 1997-1998, due primarily to regional effects of the El Niño-Southern Oscillation and possibly augmented by global warming, caused severe coral bleaching worldwide. Corals in all habitats along the Belizean barrier reef bleached as a result of elevated sea temperatures in the summer and fall of 1998, and in fore-reef habitats of the outer barrier reef and offshore platforms they showed signs of recovery in 1999. In contrast, coral populations on reefs in the central shelf lagoon died off catastrophically. Based on an analysis of reef cores, this was the first bleaching-induced mass coral mortality in the central lagoon in at least the last 3,000 years. Satellite data for the Channel Cay reef complex, the most intensively studied of the lagoonal reefs, revealed a prolonged period of elevated sea-surface temperatures (SSTs) in the late summer and early fall of 1998. From 18 September to 1 October 1998, anomalies around this reef averaged +2.2°C, peaking at 4.0°C above the local HotSpot threshold. In situ temperature records from a nearby site corroborated the observation that the late summer and early fall of 1998 were extraordinarily warm compared to other years. The lettuce coral, Agaricia tenuifolia, which was the dominant occupant of space on reef slopes in the central lagoon, was nearly eradicated at Channel Cay between October 1998 and January 1999. Although the loss of Ag. tenuifolia opened extensive areas of carbonate substrate for colonization, coral cover remained extremely low and coral recruitment was depressed through March 2001. High densities of the sea urchin Echinometra viridis kept the cover of fleshy and filamentous macroalgae to low levels, but the cover of an encrusting sponge, Chondrilla cf. nucula, increased. Further increases in sponge cover will impede the recovery of Ag. tenuifolia and other coral species by decreasing the availability of substrate for recruitment and growth. If coral populations are depressed on a long-term basis, the vertical accretion of skeletal carbonates at Channel Cay will slow or cease over the coming decades, a time during which global-warming scenarios predict accelerated sea-level rise.01/2002;
Oikos 119: 1417–1422, 2010
© 2009 Th e Authors. Journal compilation © 2010 Oikos
Subject Editor: Martin Solan. Accepted 15 December 2009
Fragments or propagules? Reproductive tradeoffs among
Callyspongia spp. from Florida coral reefs
Wai Leong and Joseph R. Pawlik
W. Leong and J. R. Pawlik (firstname.lastname@example.org), Dept of Biology and Marine Biology and Center for Marine Science, Univ. of North Carolina
Wilmington, 5600 Marvin Moss Lane, Wilmington, NC 28409, USA.
Fragmentation and propagule formation are alternative reproductive strategies found in both plants and animals, with
the latter generally providing greater dispersal capability. When both strategies occur, life history theory predicts that
resources should be divided between the two. On coral reefs, both strategies are exhibited by branching corals and
sponges, which are broken-up after storm events and rapidly recolonize. In this study, we compared two congeneric
Caribbean reef sponges, Callyspongia armigera, which is branched and easily fragmented, and C. vaginalis, which is
not, to test whether there is a tradeoff in growth and propagule formation for C. armigera relative to C. vaginalis. Both
species were equally abundant on coral reefs off Key Largo, Florida (10.1 ? 3.7 vs 11.9 ? 3.0 per 100 m2, respectively),
suggesting that they are equally successful relative to two other non-fragmenting congeneric species (C. fallax and
C. plicifera) that are much less common. Th e number of substratum attachment points per sponge was signifi cantly
higher for C. armigera compared to C. vaginalis (2.31 ? 1.47 vs 1.03 ? 0.18 sponge–1), providing further evidence of
the reliance of C. armigera on fragmentation, and of C. vaginalis on recruitment from larval settlement and subsequent
growth. Growth rates in predator-exclusion experiments were ~4-fold higher for C. armigera compared to C. vaginalis
(0.36 ? 0.31 vs 0.08 ? 0.11 % initial mass day–1), but C. armigera produced ~13-fold fewer propagules than C. vaginalis
(0.04 ? 0.22 vs 0.53 ? 1.08 % tissue area). Our results support a tradeoff between growth and propagule output for
C. armigera relative to C. vaginalis, suggesting that these closely related sponge species took diff erent evolutionary
trajectories in reconciling their resource constraints.
Resource tradeoff s are implicated when two contrasting
life history strategies co-exist (Stearns 1992). For example,
plants may primarily reproduce through propagule forma-
tion (e.g. seeds) or by asexual fragmentation (e.g. rhizomes,
runners, plantlets). Plants allocate resources to physiological
functions such as growth and reproduction from a fi nite
pool (Coley et al. 1985, Bazzaz et al. 1987). A tradeoff arises
when plants allocate resources to vegetative growth for frag-
mentation instead of propagule formation, just as there are
tradeoff s between reproductive and somatic investments in
animals (Cody 1966).
Propagule formation as a reproductive strategy provides
several advantages. Propagules are smaller and lighter than
fragments and are able to disperse further (Gaylord et al.
2002). Also, most propagules are sexual, which confers the
advantages that sexual recombination provides, enabling
selection to break down negative gene combinations at dif-
ferent genetic loci and increase genetic diversity (Hoekstra
2005, Charlesworth 2007). In addition to providing short-
term advantages in rapidly fl uctuating or biologically com-
plex environments where new selective forces constantly
occur, sexual reproduction also decreases competition between
siblings by increasing diversity among them (Williams
1975, Maynard Smith 1978).
Yet, fragmentation also provides benefi ts. By investing
in vegetative growth, plants can increase in biomass that
is directly used to colonize new areas (Abrahamson 1975).
Fragmentation of plants may reduce the spread of infection
between clones (Hay and Kelly 2008). For aquatic plants,
fragments can be carried by fl owing water to colonize new
locations. In one example, reproductive strategies and dis-
persal outcomes were very diff erent for two groups of riv-
erine plants used in disturbance experiments: fragments of
Sparganium emersum and Ranunculus trichophyllus rooted and
re-established themselves quickly, whereas Luronium natans,
Hippuris vulgaris and Elodea canadensis produced propagules
but did not re-establish themselves (Barrat-Segretain 1996,
Barrat-Segretain et al. 1998). In a similar manner, fragments
of the seagrasses Halodule wrightii and Halophila johnsonii
were both able to colonize new substrata after dislodgement,
but the former was viable for a longer period of time and
could disperse over greater distances (Hall et al. 2006). Frag-
mentation is also important to the success of many invasive
aquatic plants. For example, Mimulus guttatus (Truscott
et al. 2006) employs fragmentation and recolonization to
rapidly spread downstream after unpredictable fl ood pulses.
Rapid colonization by fragments explains the success of
the seagrass Posidonia oceanica (Di Carlo et al. 2005) and the
seaweed Caulerpa taxifolia (Smith and Walters 1999) in the
Among animals, clonal taxa (e.g. cnidarians) or those
with indeterminate integration of body plan (e.g. sponges)
also adopt fragmentation as a strategy for reproduction
and dispersal (Tunnicliff e 1981, Lasker 1984, Wulff 1991).
Fragmentation provides particular benefi ts to corals and
sponges that grow on coral reefs. Coral fragments exhibit
higher survivorship than settling coral larvae (Highsmith
1982), and fragments of corals and sponges are able to
repopulate substrata more quickly after disturbances such as
storm damage (Highsmith 1982, Wulff 1995). Because most
coral diseases are spread by contact with infected tissue, it
has been suggested that fragmentation may be a mechanism
for colonies to limit the spread of disease (Highsmith 1982).
Moreover, transplantation of coral fragments has been pro-
posed as a method for repopulating degraded coral reefs
(Shafi r et al. 2001).
Sponges are dominant members of the benthic commu-
nity on Caribbean coral reefs (Targett and Schmahl 1984,
Aronson et al. 2002, Maliao et al. 2008). Only a few studies
have addressed asexual reproduction in Caribbean sponges,
particularly the concept that a branching morphology may
enhance fragmentation (Wulff 1991, 1995). Tsurumi and
Reiswig (1997) noted that the production of propagules
was very infrequent in Aplysina cauliformis, a thinly branch-
ing sponge, and suggested that the branching morphology
may be an adaptation for fragmentation, but they did not
compare propagule production in A. cauliformis with that of
Callyspongia armigera and C. vaginalis are two very
common sponges on Caribbean reefs. Th e former grows
as a branching gray rope, while the latter grows in clus-
ters of gray tubes. Both species brood and release identical-
looking, ciliated parenchymella larvae, ~0.5 mm in length,
which are assumed to be sexual products. However, sperm
have never been observed in histological sections of either
species (Discussion) leaving open the possibility that the
putative larvae are asexual products; therefore, they will be
referred to herein as propagules. Propagules of both spe-
cies swim up into the water column after release from the
sponge, and disperse widely (Lindquist and Hay 1996,
Lindquist et al. 1997, Pawlik unpubl.). Branches of C.
armigera grow in all directions, forming clumps that attach
readily when they come into contact with the substra-
tum or with other branching sponges or gorgonian cor-
als. Fragmentation of this species can be observed after
attack by predatory fi shes (particularly French and gray
angelfi shes, Pomacanthus paru and P. arcuatus; Pawlik
unpubl.). Contrarily, tubes of C. vaginalis cannot reat-
tach to the substratum, and dead or dying specimens can
be seen tumbling over the reef after storms. To determine
whether there is a resource tradeoff for C. armigera relative
to C. vaginalis, we examined rates of growth and propagule
production for each. We also documented the number
of points of attachment per individual sponge for each spe-
cies as an indication of their propensity to fragment. Life
history theory predicts that if resources are limited and
partitioned, a species that reproduces primarily through
fragmentation should grow faster, but produce fewer
propagules as a consequence.
Material and methods
Growth experiments were conducted off Key Largo, Florida,
USA, at North Dry Rocks (25°07’850’’N, 80°17’521’’W)
and Carysfort Reef (25°12’860’’N, 80°12’810’’W), with
additional collections of material for reproductive output
from Conch Wall (24°56’440’’N, 80°27’230’’W). North
Dry Rocks is a shallow patch reef at 8 m depth. Conch Wall
and Carysfort Reef are shallow reef fl ats, at approximately
12 m depth. Both sites are typical for long stretches of hard-
bottom reef in the Florida Keys, where the predominant
substratum is limestone pavement interspersed with small
patches of overlying sand.
A survey was conducted at North Dry Rocks to determine
relative abundances of each sponge species. Ten 20 ? 5 m
band-transects were surveyed along a continuous transect
line and the number of sponge individuals of each species
that lay within the band was recorded. Sponges that grew as a
connected mass were counted as individuals. From the same
transects, the number of points of attachment to the substra-
tum for each individual sponge was counted as a measure of
the ability of each species to reattach, and as a proxy for the
propensity of each species to fragment. Examples of attach-
ment substrata included surfaces that provided a fi rm anchor,
usually limestone, pavement or dead coral, but sometimes
other organisms, such as gorgonians and other sponges.
Growth data were obtained from eight predator-exclusion
experiments conducted at North Dry Rocks or Carysfort
Reef between 1996 and 2007. Th e experimental start dates
were 6 May 1996, 19 May 1997, 12 May 1999, 6 May
2000, 7 May 2002, 5 June 2003, 25 May 2006 and 4 June
2007. Each experiment lasted 124 to 176 days. For each
experiment and each species, 20 cube-shaped cages, 40 cm
on a side, were constructed of vexar plastic mesh having
2 cm2 openings and cable ties and secured onto the lime-
stone substratum with nails. Sponge pieces (~ 40 g wet mass)
were carefully collected from the surrounding reef by slic-
ing fragments off healthy sponges with a scalpel; pieces were
weighed on an electronic scale, tagged, returned to the same
reef and secured with a cable tie to a brick inside the cages. At
the end of the experiment, sponge pieces were retrieved and
weighed in the same way. Growth rates were measured as a
change in mass presented as a percentage of initial mass, and
corrected for duration by dividing by the number of days of
each experiment. Only sponge pieces that remained at the
end of the experiment were included in analyses because it
could not be determined whether missing pieces had died or
been swept away; this left a total of 91 out of 100 and 53 out
of 60 fragments of Callyspongia armigera and C. vaginalis,
respectively. Data from diff erent years were combined
because there was no signifi cant year eff ect for these two spe-
cies in a larger analysis of sponge growth (Leong and Pawlik
To determine reproductive output, fi ve sponges of each
species were collected monthly from Conch Wall in Key
Largo and processed for histology. Because reproductive
timing can diff er, even for species growing under the same
environmental conditions (Riesgo and Maldonado 2008),
samples were collected over an entire year from November
2007 to October 2008. Th ree cubes of tissue, ~1 cm on a
side, were cut from each specimen, and immediately fi xed
in 4% formaldehyde in buff ered sea water. Specimens were
then rinsed with buff er and deionized water, dehydrated
in solutions of increasing concentrations of ethanol (50%,
70%, 95%, 100%), and embedded in paraffi n using toluene
as a clearing agent. Using a rotary microtome, 10 μm sec-
tions were made and stained with haematoxylin and eosin.
Sections were viewed and photographed with a microscope
with an attached camera. A total of 20 views of each speci-
men were haphazardly photographed at 4? magnifi cation to
give a total scanned area of 130 mm2 for each sponge. Th e
surface area of any propagules present was quantifi ed using
the image analysis software ImageJ (Rasband 1997). Surface
area measurements were then converted to a percentage of
the total surface area, termed the reproductive output index
(ROI; Whalan et al. 2007), which was used to compare
relative reproductive output between species.
Two- and one-tailed Student’s t-tests were used to com-
pare diff erences in abundance and growth respectively, for
each sponge species. Because the data were not normally dis-
tributed (p ? 0.001; Shapiro–Wilk test), the non-parametric
Kruskal–Wallis test was used to determine the signifi cance of
diff erences in numbers of attachment points and numbers of
propagules between the two sponge species.
In surveys of North Dry Rocks reef off Key Largo, Florida,
there was no signifi cant diff erence in the abundance of
Callyspongia armigera and C. vaginalis, with mean values of
11.9 and 10.1 sponges per transect, respectively (two-tailed
t-test, t ? 2.101, DF ? 18, p ? 0.2471; Fig. 1). Callyspongia
armigera had an average of 2.22 attachments per individual
sponge, which was signifi cantly more than 1.03 attachments
per individual for C. vaginalis (Kruskal–Wallis, χ2 ? 113.86,
DF ? 1, p ? 0.0001; Fig. 2).
Sponge growth in predator-exclusion experiments was
over four times higher for C. armigera (n ? 91, mean ?
0.358% initial mass day–1) than for C. vaginalis (n ? 53,
mean ? 0.079% initial mass day–1; one-tailed t-test, t ?
6.395, p ? 0.0001; Fig. 3).
Both C. armigera and C. vaginalis brood their propagules
in distinct chambers within the sponge tissue. Propagules
appear identical for both species, are ~0.5mm in length and
can be easily seen without magnifi cation. When reproductive
propagules were present in an individual sponge, the ROI
was comparable between species (1.22 for C. armigera and
1.78 for C. vaginalis). After monthly samples for one year
(n ? 60), only two reproductive individuals of C. armigera
were found, one in March and another in October 2008
(Fig. 5). On the other hand, 18 of 60 samples (30%) of
C. vaginalis exhibited propagules, and there was apparent
seasonality in their production, with propagules found in
December 2007, and from May to September 2008 (Fig. 5).
No sperm were observed in any tissue sample. Overall,
Abundance (per 100m2)
Figure 1. Abundance of Callyspongia armigera (CA) and Callyspon-
gia vaginalis (CV) from band transects at North Dry Rocks reef,
Key Largo, Florida. Mean ? SD, n ? 10.
Average attachments per individual
Figure 2. Average number of attachments per sponge for Cally-
spongia armigera (CA) and Callyspongia vaginalis (CV) from band
transects at North Dry Rocks reef, Key Largo, Florida. Mean ?
SD, n ? 101 and 119 respectively. Asterisk indicates a signifi cant
diff erence in the number of attachment points (Kruskal–Wallis,
p ? 0.0001).
Average growth rate (% initial mass per day)
Figure 3. Relative growth of Callyspongia armigera (CA) and
Callyspongia vaginalis (CV) as percentage wet mass increase day–1
from eight caging experiments conducted at North Dry Rocks,
Key Largo, Florida from 1996 to 2007. Mean ? SD, n ? 91 and
53 respectively. Asterisk indicates a signifi cant diff erence in mean
growth (t-test, p ? 0.0001).
Besides sponges, there are other Caribbean reef inverte-
brates for which a branching growth form is thought to be
advantageous for reproduction by fragmentation. Th e gorgo-
nian Plexaura sp. (Lasker 1984) and staghorn coral Acropora
cervicornis (Tunnicliff e 1981) also reproduce primarily by
clonal fragmentation, with little evidence of propagule for-
mation. Similarly, fragmentation is the primary mode of
reproduction in arborescent and vine-like bryozoans (Th omsen
and Hakansson 1995), and levels of genetic diversity sug-
gest that asexual fragmentation dominates among branch-
ing reef-building corals on the Great Barrier Reef (Ayre and
Hughes 2000). Interestingly, for the Mediterranean sponge
Scopalina lophyropoda, it has been proposed that fragmenta-
tion may enhance dispersal of propagules, because very small
sponge fragments contain and nourish developing embryos
(Maldonado and Uriz 1999), but a similar situation does not
occur in Callyspongia spp., which have large brood chambers
loosely packed with propagules.
Fragmentation is often cited as an evolutionary alterna-
tive to sexual reproduction (Tunnicliff e 1981, Lasker 1984,
Wulff 1991, Th omsen and Håkansson 1995, Ayre and
Hughes 2000, Sherman et al. 2006), and for plants, should
be favored in stable, unchanging environments (Abrahamson
1975, Silvertown 2008). Th is seems contrary to the foregoing
discussion of sponge fragmentation requiring disturbance
events to break sponges apart and disperse them prior to
recolonization. Indeed, without some level of disturbance,
sponge fragmentation would not occur. For another Carib-
bean reef invertebrate, the gorgonian coral Plexaura kuna, a
generalized model relating fragmentation, population struc-
ture and disturbance was proposed by Coff roth and Lasker
(1998). Th ey found the greatest evidence of reproduction
by fragmentation, and the lowest genotypic diversity, at
intermediate levels of disturbance (Coff roth and Lasker
1998). A similar model may be useful in describing the rela-
tive abundances of the two species of Callyspongia: while
C. vaginalis is common on most reefs, C. armigera is abun-
dant only on reefs that experience low to moderate currents
and have high topographic complexity (coral rubble). While
propagules of both species are likely to disperse to most reefs,
strong currents on some reefs may fl ush away fragments of
C. armigera, particularly if low habitat complexity does
not provide microhabitats where fragments can settle long
enough to attach.
Th e present study did not attempt a demographic analysis
of C. armigera and C. vaginalis to quantify their respective
dependence on fragmentation and larval recruitment, as this
would require long-term monitoring and tagging of sponges.
Instead, several lines of evidence support our assumptions
about the life-history diff erences of the two species. Not only
is there abundant evidence of fragmentation of C. armigera
in the fi eld, it can be observed occurring when sponge-
eating fi shes attack this species and leave behind partially
eaten branches (Pawlik unpubl.). Similar attacks on C. vaginalis
leave behind holes in the tubes, which regenerate rapidly
(Walters and Pawlik 2005), but with no dislodgement of the
fi rmly attached sponge. After even moderate storm events,
clusters of branches of C. armigera were broken-up, with
only remnant branches at the initial sites of attachment, and
torn branches scattered and attached about the reef. Indi-
vidual tubes or tube clusters of C. vaginalis usually survived
C. armigera had a signifi cantly lower average annual ROI
than C. vaginalis (Kruskal–Wallis, χ2 ? 15.317, p ? 0.0001;
As for some aquatic plants (Barrat-Segretain 1996, Barrat-
Segretain et al. 1998, Hall et al. 2006), our data support a
resource tradeoff between investment in growth and frag-
mentation versus propagule formation for Callyspongia
armigera relative to C. vaginalis, both of which are equally
abundant on reefs off Key Largo, Florida. By reproducing
primarily through fragmentation, C. armigera can quickly
colonize free substrata after damage due to fi sh predation
or disruption caused by storms, that occur frequently along
the Florida reef tract. Contrarily, Callyspongia vaginalis relies
primarily on propagule formation for reproduction, with the
likely benefi ts associated with greater dispersal potential and
Figure 4. Mean reproductive output of Callyspongia armigera and
Callyspongia vaginalis from Conch Wall, Key Largo, Florida for
November 2007 to October 2008. Mean ? SD, n ? 60. Asterisk
indicates a signifi cant diff erence in ROI (Kruskal–Wallis,
p ? 0.0001).
Figure 5. Mean monthly reproductive output index (percentage
area propagules) of Callyspongia armigera (CA) and Callyspongia
vaginalis (CV) from Conch Wall, Key Largo, Florida for November
2007 to October 2008. Mean ? SD, n ? 5.
Acknowledgements – Funding was provided by the National Science
Foundation, Biological Oceanography Program (OCE-0095724,
0550468) and by NOAA’s Undersea Research Center at the Univ.
of North Carolina Wilmington (NA 96RU-0260). Sponge collec-
tions in Key Largo, Florida, were conducted under National Marine
Sanctuary Permit FKNMS-2001-021 in compliance with the
laws of the State of Florida and the USA. We thank H. Feddern,
T. Henkel, S. McMurray, T.-L. Loh, D. Hines and S. Lopez-Legentil,
and a long list of diving helpers who worked on the growth experi-
ments for assistance in the fi eld and the laboratory. Richard Dillaman
and Mark Gay provided assistance with histological procedures and
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these storms intact, but when dislodged, were observed to be
dead or dying in the sand channels between the reefs, and are
often washed ashore in the beach wrack (Pawlik unpubl.).
Because C. vaginalis grow with their tubes and osculae ori-
ented upward, reattachment of this species would lead to
haphazard re-orientation, and this has not been observed in
the fi eld. Quantifi cation of attachment points for the two
species (Fig. 2) support the qualitative evidence for frag-
mentation vs. reproduction for C. armigera and C. vaginalis,
with more than a two-fold mean diff erence between the two
species, and much higher variance for C. armigera refl ecting
the haphazard eff ects of predation and disturbance. Th e nar-
row variance around 1.0 attachment points per sponge for
C. vaginalis is further evidence that this species grows from
the single point of propagule settlement and subsequent
Callyspongia armigera and C. vaginalis are not the only
Callyspongia species found on reefs in the Florida Keys.
Callyspongia fallax and C. plicifera also occur, but in much
lower abundances. Although reproductive data are lacking
for these species, inspection for brood chambers suggest that
they are less fecund than C. vaginalis (Pawlik unpubl.), but
like C. vaginalis, they are both tube sponges and do not frag-
ment and reattach like C. armigera. A combination of low
reproductive output and the absence of asexual reproduction
by fragmentation for C. fallax and C. plicifera may explain
their low abundance on Caribbean reefs.
Interestingly, sperm were not observed in histological
sections from tissues of either C. armigera or C. vaginalis,
leaving some question as to whether propagules are sexual
or asexual products. Asexual production of larvae in marine
sponges could not be discounted in other studies (Ilan and
Loya 1990). Sperm have been absent in some studies of
sponge reproduction (Fell 1989, Corriero et al. 1996), while
in others, heavily skewed sex ratios for both females (Tsurumi
and Reiswig 1997, Mercurio et al. 2007) and males (Whalan
et al. 2007) have been reported. However, it is more likely
that sperm may be produced diff usely in these species, making
them unrecognizable by light microscopy, or that the time
between sperm development and release is so short that a
monthly sampling scheme would overlook their presence
(Mercurio et al. 2007).
Our study provides the fi rst comparative evidence that
there is a tradeoff between growth and propagule forma-
tion in closely related coral reef sponges that exhibit dif-
ferences in morphology and capacity to fragment. Th is is
likely only one of several tradeoff s in the resource budgets
of Caribbean reef sponges, which may also include wound-
healing after grazing by sponge-eating fi shes (Walters and
Pawlik 2005), and investment in chemical defenses to
deter predation (Pawlik et al. 1995, Pawlik 1997, 1998).
Experimental evidence for these tradeoff s is forthcoming
(Leong and Pawlik unpubl.), but compelling support for
the tradeoff between chemical defense and growth or repro-
duction is evident in the community succession of sponge
recruitment into new habitat provided by an artifi cial reef
shipwreck (Pawlik et al. 2008). It appears that the species
that make up Caribbean reef sponge communities have
taken very diff erent evolutionary trajectories in allocating
metabolic resources to growth, reproduction and chemical