Proceedings of 10th International Coral Reef Symposium, 431-437 (2006)
Developmental changes in coral larval buoyancy and vertical
swimming behavior: Implications for
dispersal and connectivity
Alina M. SZMANT* and Melissa G MEADOWS
Center for Marine Science, University of North Carolina at Wilmington, 5600 Marvin K. Moss Ln, Wilmington NC
28409 USA
*Corresponding author: A.M. Szmant
FAX: 910-962-2410, e-mail: szmanta@uncw.edu
Abstract Many hermatypic corals are bro adcast
spawners. Little is known about the dispersal potential of
their planktonic larvae. Settlement can begin 2-3 d ays
post-fertilization, but com petency ma y last for a month or
more. Hyd rogra phic mod els can be use d to estimate larval
dispe rsal, but they require information about the
swimming beha vior of the larvae during transport,
including buoyancy and vertical swimming behavior.
Coral eggs are positively buoyant when released, but
embryos and larvae with time become less buoyant and
acquire the ability to swim downw ards. The time-course
of such d evelo pme ntal changes is ne eded to coup le with
hydro graphic data to mo del dispersal curves. Such da ta
are presented here for the major Caribbean hermatype,
Montastraea faveo lata. Larval buoyancy was measured
as ascent rate in a volumetric pipette, and measured every
6 hours for 3.2 5 hours po st-fertilization. V ertical
swimming behavior was measured as vertical distribution
of the larvae within 2 L graduated cylinders, placed on an
orbital shaker table, measured every 6 hours from 40
hours to 8.5 days p ost-fertilizatio n. Ne wly fertilized eggs
(non-swimming) had an ascent rate of 1.82 mm s-1, and
this decreased linearly to 1.04 mm s-1 over the following
2.3 days, by which tim e many larvae were swimming.
Over 80 % of the larv ae rem ained within the top 4 cm of
the 40 cm-tall cylinder over the first 2.5 days p ost-
fertilization. Diel vertical migration became app arent
after ca. 3 daysdownwards in dark, upwards in light), and
became more pronounced over time. However, even 8
days post-fertilization, less than 20 % of the larvae were
at the bottom of the cylinder at the end of the dark period.
These results show that while some larvae of this species
can settle within a few days, most do not develop strong
bottom seeking behavior until much later, and could be
dispe rsed far from their site of o rigin.
K eywords coral larvae, planulae, swimming behavior,
dispersal
431
Introduction
A current major question in marine eco logy is to
understand the connectivity among widely dispersed
populations, and how this connectivity varies with
distance among localities. The dispersal abilities of
planktonic larvae of sessile benthic marine invertebrates
are important to their eventual reproductive and
recruitment success, as well as to connectivity among
populations. If larvae are retained close to the parental
source (either for behavioral or environmental reasons),
chances of successful local recruitment may be higher
but connectivity with more distant populations will be
low. Ho wever, extensive self-seeding will eventually
lead to low genetic diversity. If, alternatively, most of
the larvae are carried away by currents, they may be
transported away from suitable habitat and/or the larvae
may be in the dangerous plankton for longer periods,
which would decrease their chances o f survivorship to
settleme nt. Potential recruitment to any particular
loca lity will depend on upstream sources of larvae as
well as the co nditions at that site that help retain loca lly
derived larvae (Hughes et al 199 9, 20 00). W hen
observed recruitment rates are low , it may be because
larval supply is too small to over-com e the mortality
rates operating on that life stage, or because a site is in a
system where there is poor larval retention or few
upstream sources of larvae. Thus understanding the
dispersal patterns of larvae is important to understanding
whether a population is supply-side recruitment limited.
The dispersal potential of coral larvae remains poorly
studied because of the small size of the larvae and the
difficulty of qua ntitatively sam pling them in the
plankton. One approach to estimating dispersal potential
is to examine the duration of the competency period.
Some coral species are brooders that release mature
planula larvae which are able to settle within hours of
release (Ha rrison and W allace, 1 990 ). By contrast,
larvae of broad cast spawning corals have by necessity
longer planktonic periods, and thus supposedly the
potential for broader dispersal. But brooded larvae are
larger, and have a com plem ent of algal symb ionts
(zooxanthellae) that can nourish them during a long
planktonic period (Harrison and Wallace 199 0).
Richmond (1988) found that larvae of the brooder,
Pocillopora dam icorn is, remained competent for much
longer than those of the bro adcast spawner, Acropora
tenuis, but based on the long larval competency durations
found by Richmond, both would be expected to have a
high dispersa l ability.
Another approach that has been used to estima te
dispersal potential for corals was to compare coral
recruitment onto settlement plates suspended in the water
column at various distances from an isolated source reef,
Helix Reef, on the Great Barrier Reef (Sammarco and
Andrews 1988, 1989). This study found more coral spat
on settlement plates de ployed 300 m from the reef than
either further away or on the reef proper. These authors
concluded that coral reefs are self-seeding, and that coral
larvae have limited dispersal potential, but their study
suffered from the serious limitation that the plates were
not collected until 7 months after deployment. Given the
high and variable post-settlement mortality experienced
by coral spat (e.g. Babcock and M undy 1996; Szma nt
and Miller, submitted) the Helix experiment was not
properly designed to distinguish the amount of settlement
per se without the confounding effect of po st-settlement
mortality. There is an extensive literature on the
importance of grazing and substrate quality to the
suitability of reef substrate for coral settlement (recently
summarized in Babcock and Mundy 1996), and substrates
suspended in the water column far from the reef were
likely heavily fouled and unlikely candidates for coral
settleme nt. Furthermore, the hydrography surrounding
plates suspended in the water column is not likely the
same as that over a reef. A fast current would prevent
larvae from being retained for long enough to explore
substra te and attach. If a reef were present in the same
area, water currents would be slowed, and to pog rapically
generated eddies would tend to retain larvae.
Several studies have used aerial tracking of coral larval
slicks in the d ays after spawning . In fact, “pink stripes”
several km long were first reported in the open ocean
surrounding Bermuda and were identified as coral slicks
by Butler (1980). Australian investigators have found
evidence for bo th local retention and self-seeding (larvae
trapped in back-reef lagoons) and wide dispersal of coral
larvae from their natal reef depending on local weather
conditions, topography, and hydrography (W illis and
Oliver 1988, 1990; Wolanski et al. 1989). Oliver and
W illis (1987) repo rted slicks 5 km long m ade up of both
dead and live larvae, and found that concentrations of live
larvae were higher in these slicks than in surrounding reef
432
waters.
A modeling approach was used to predict five
different patterns of larval dispersal for coral larvae
originating from the Texas F lower Gardens in the G ulf
of Mexico (Lugo-Fernandez et al. 200 1). These authors
conclude that most of the spawn would remain within 40
km of the spawning source. Several o f the model
patterns have the larvae m oving long d istances over
periods of 30 to 60 days. These predictions did not
take into acco unt the ability of larva e to rem ain
com peten t in the plankton for such long p eriod s.
The larval co mpe tency duration is known for only a
few species, and ranges from 20 d for Acropo ra tenuis
to 100 d for Pocillopora dam icornis (Richmond 19 88),
and from 26 d for Cyphastrea serailia to 56 d for
Goniastrea austr alensis and 78 d for Acanthastrea
lordh owensis (W ilson and Harrison 1998). Szmant
(unpublished) has found a competency period of ca. 30
days for Montastraea faveolata indicating that it has the
ability to disperse over significant distances. Oliver et al
(1992) found that modeled coral larval dispersal patterns
did not co rrelate w ell with ob served larva l abundance
and recruitment patterns, and ascribed this to the fine-
scale three-dimensional flows which occur around
topo graphically com plex structures such as cora l reefs
(e.g. Wo lanski 1988; Wolanski and Hamner 1988;
W olanski et al. 1989). Therefore, approaches are
needed that take into account finer scale circulation
features around coral reefs, as well as differences in the
development and competency behavio rs among coral
species.
In this study, we exam ined the time-course of changes
in buoyancy and the deve lopment of swimming
behaviors of the larvae o f Mo ntastra ea faveolata. This
species is one of the major reef-builders in the
Caribbean, dominates the adult coral community on
many Caribbean reefs as massive colonies meters high,
but is infrequently found in recruit surveys (e.g.
Rylaarsdam 1983; Chiapp one and Sullivan 1995; Miller
et al 2002). M. faveolata is hermaphroditic and
broadcasts large numbers of gametes into the water
column in a mass spawning event that is highly
predictable (Szmant 1986, 19 91; M iller and Szmant, in
review). After gamete bundle release (eggs plus sperm)
large slicks form on the ocean surface, which depending
on weather and local hydrographic cond itions, can last
for a day o r more. The emb ryos take a minim um of 3 to
5 days after fertilization to de velop into competent
planula larvae (Szmant et al. 1997; Szmant and Miller
submitted). The competency period can last up to 30
days (Szm ant and Miller subm itted), but most larvae will
likely attempt to settle within the first two weeks if they
are in the appropriate environment. The eggs, embryos
and planulae will be transported as passive particles by
ocean currents during this early development, until the
larvae lose their positive buoyancy and develop the ability
to position them selves in the water colum n. If time-
courses of such larval transport characteristics were
available, they could be used together with hydro graphic
data in physica l-biological co upled mod els to predict the
dispersal patterns and distances of any given spawn event
from any given reef.
M ethods
Gamete collection and fertilization
Mo ntastrea faveo lata gamete bundles were collected
at Key Largo Dry Rocks (Key Largo, FL) by divers with
large cone-shaped, cloth mesh nets deployed over
individual coral heads. Spawning took place from 11:30-
11:50 pm on August 18, 2003. Collector cups at the cod-
end of the nets were retrieved by the divers and returned
to the research vessel, where the bundles from individual
colonies were combined. Following the break-up of the
gamete bund les, the mixture of gametes from several
dozen colonies was allowed to fertilize for ca. 1 hour,
after which the sperm were washed from the eggs by
repeated rinsing with filtered seawater. Unfertilized eggs
began to break up after ca. 12 hours and were removed
from the culture w ith repeated washes. Eggs (300 to 350
um in diameter), embryos and planula larvae (ca. 500 to
700 um in length) were removed from this culture at
frequent intervals beginning as soo n as possible after
fertilization to measure their buoyancy, and later to be
used for the vertical swimming behavior study described
below.
Buoyancy
The buoyancy of eggs, embryos or larvae was
measured every 6 hours from 0 to 7 8 hours p ost-
fertilization by measuring their ascent rate. The apparatus
used to measure ascent rate consisted o f a 25 ml graduated
pipet mounted to a ring stand . The pipet was filled with
seawater, and a pipettor on top was used to slowly draw
embryos or larvae just into the tip of the pipet. From
there, they rose through the water column within the pipet
at their own accord. Larvae were timed with a stop-watch
as they rose over a d istance of 55 mm, and ascent rates
were calculated. This was repeated for 15 individual
larvae, and an average ascent rate was calculated.
Percentages of larvae that were neutrally buoyant and/or
had developed swimming behavior were also calculated
where applicable.
Vertical swimming behavior
Approximately 1000 early planula larvae were placed
into each of four 2-L graduated cylinders containing 2 L
of filtered sea water at 42 hours after fertilization. The
experimental cylinders were 51 cm tall. The cylinders
were placed on orbital shaker tables to provide water
movement and turbulence important to gas exchange
433
within the cylinders. Tests with dye and buoyant beads
showed that this mixing only penetrated to the bottom of
the top 2 00 m l section within the cylinder. At night, the
cylinders were covered with a card boa rd enclosure to
prevent artificial light from influencing larval behavior.
Approximately every 6 hours for up to 207 hours, the
numbers of larvae within each 200 ml section (= 4.2 cm
vertical depth) of the graduated cylinder were counted.
Due to the high number of larvae residing in the top
layer of the water column, it was difficult to obtain an
accurate count for that dep th interval, and thus those
larvae were not counted. Percentages of the total
number of larvae for all depths excluding those in the top
layer were then calculated for each section of the water
column for each measurement time. Data are plotted
against time of day and distinguished by light conditions
(day / night) at the time of measurement.
Results
Buoyancy
The ascent rate of newly fertilized M ontastraea
faveo lata eggs was 1.8 2 mm /sec. Ascent rate
consistently dropped over time as the larvae became
older, up to an age of 56 hours (linear re gressio n, r 2 =
0.96; Figure 1). At 56 hours, the average ascent rate had
dropped to 1.04 mm/sec and approximately 20% of the
larvae had become neutrally buoyant or developed the
ability to swim vertically within the pipet. By 78 hours
of age, 100% of the planulae were swimming or neutrally
buoyant (Table 1).
Table 1. Percent of larvae that had beco me ne utrally
buoyant or had begun swimming over the time-course of
measurem ent.
Embryo or % %
Larval Age Neutrally Swimming
(hrs) Buoyant
0 - 45 0 0
56 20 0
63.5 -- 67
73 -- 73
78 -- 100
Fig. 1. Ascent rate of larvae in mm/sec as they ro se
through a graduated pipet. As larvae grew older and used
up lipid reserves, buoyancy, expressed here as ascent rate,
was reduced until 56 hours of age when some larvae
became neutrally buoya nt or develo ped the ability to
swim.
Vertical swimming behavior
During the first few measurement intervals (42 hrs to
78 hrs), most of the M. faveolata larvae remained in the
top 200 ml section of the graduated cylinder, and were too
concentrated to count. W ith time, larvae be gan to
descend deepe r into the cylinder and to swim around the
botto m of the cylinder. Larvae were foun d to exhibit a
diel swimming pattern which was weak at first but became
more pronounced by 108 hours after fertilization (Figure
2). They concentrated up near the surface of the water
column during the daylight hours and moved down to
explore the bottom substrate at night. Towards the end of
the expe riment, elongated planulae were quite mobile and
could be observed swimming up and down past each other
in the cylinder
The percentage of larvae observed in the bottom
section of the wa ter column in the early morning, after
maximal time in the dark, increased o ver time . T he
percentage of larvae in the bottom section peaked at 60%
after 127 hours post-fertilization (Figure 3).
Discussion
The time-course of buoyancy and vertical migration
patterns documented here are important parameters that
will influence the path these coral p lanulae will take
during their planktonic development period, and
ultimately where they are likely to settle. Buoyancy as
well as vertical swimming abilities will determine the
position of larvae in the water colum n. The longer a larva
remains as a passive particle ‘stuck’ in the surface layer,
the further it is likely to disperse from its natal reef.
Because current speed and direction vary with depth,
434
Fig. 2. The number of larvae in the bottom section of
the water column of the experimental cylinders were
counted at three times of day while being exposed to diel
cycles of light and darkness. The larvae exhibited a diel
pattern in their exp loration of the cylinder bottom. On
a given day, more larvae were in the bottom section in
the early morning, at the end of the dark period, and
fewer were on the bo ttom in the middle of the day after
exposure to several hou rs of light.
vertical position will also play a role in determining
larval dispersal patterns between spawning and
settleme nt.
Based on measurements of bu oyancy, Montastraea
faveo lata larvae can be treated in hyd rogra phic m ode ls
as passive, positively buoyant particles until 56-78 hours
after spawning. Up to this time, the majority of the coral
embryos and larvae are likely to remain near the surface
of the water column. Hence their transport will be
determined by surface currents. This positively buoyant
stage corresponds with the pre-competency period
(Szmant and Miller, submitted), and thus, the re is
virtually no chance of larval settlement during this time
due both to the inability of the larvae to overcome
buoyancy to reac h the bottom , as well as a physiological
inability to settle.
After 78 hours, M. fa veolata larvae can no longer be
considered passive particles. While these larvae are
small, have only a weak swimming ability, and cannot
swim against horizontal currents, they do have the ability
to change their vertical position in the water column.
Depend ing on how well larvae are able to swim up and
down, this may have a significant influence on transport.
The influence of vertical swimming ability on
horizontal transport has been described for fish larvae
(Kingsford and Choat 1986, Weinstein et al 1980, Dame
and Allen 1996, Bradbu ry and Snelgrove 200 1).
Fig. 3. M orning dep th profiles for larvae in graduated cylinders. Over time, as mo re larva e dev elop the ability to swim
downwards, an increasing number of larvae are found exploring the substrate at the bottom of the water column. This
peaked at 127 hours and then dropped off slightly.
Although coral larvae are much weaker swimm ers,
vertical swimming has the potential for having a
significant effect on the transport of these larvae as it has
been shown for fish larvae.
The deve lopm ent of vertical swimming b ehavior is
also crucial to the ability of larvae to search for su itable
substra te and settle. After more than 200 HPF, fewer than
20 % of the experimental larvae had developed this
downward seeking behavior, as measured at the end of the
dark period. This suggests that the remaining 80 % of the
planulae would remain in the plankton for longer than 8
days before attem pting to settle. Depending on
hydro graphic conditions, most larvae may be able to be
transported over considerable distances before even
developing the downward swimming behavior necessary
for the exploration o f substrate for settlem ent.
435
A recent paper has reported that planulae of two
species of coral reach peak comp etency between 60 and
66 HP F, and the authors claim their data to mean that
corals have lim ited dispersa l abilities and mostly local
recruitment (Miller and Mundy 200 3). H owever, only
10% survivorship was reported, and of that 10% , only
32.3% were settled at the end of the experim ent (10 days
after fertilization). When the authors conclude that the
majo rity of coral larvae settle early, they neglected to take
into account the remaining 68 % of their larvae that were
still swimming after 10 days. Thus, a more parsimonious
interpretation of their data is that while a small percent of
coral larvae become competent after a few days, most are
unab le to settle for a much longer duration. The potential
for dispersal increases with the time it takes a larva to
become competent. Most previous studies claiming
limited dispersal po tential for corals have relied simply on
the soonest competency is reached, and have failed to
consider the fate of the remaining larvae that d id not settle
in their experiments.
Many previous estimates of larval dispersal potential
have neglec ted to take into account the finer physiological
and behavioral dynamics of coral larvae that may
influence their transport. Competency perio d duration is
an imp ortant part of this potential but is known for only
a few species. Long comp etency period s will conve y a
large potential for dispersal for species with that
characteristic. Published competency durations range
from 20 d for Acropo ra tenuis to 100 d for Pocillopora
dam icorn is (Richmond 1988), and from 26 d for
Cyphastrea serailia to 56 d for Go niastre a au stralen sis
and 78 d for Acanthastrea lordho wensis (W ilson and
Harrison 1998). Szmant and M iller (in review) have
found a com peten cy period of ca. 30 days for
Montastraea faveolata indicating that it has the ability to
disperse over significant distances. Lugo-Fernandez et al
(2001) made an assumption in their modeling approach
that coral larvae could remain in the plankton for
prolonged periods and predicted quite extensive dispersal
patterns in the Gulf of Mexico. H owever, even when a
long period of competency is known, it does not suffice to
use this information to pred ict dispersal. This was
demonstrated by Oliver et al. (19 92) when mod els based
on com peten cy failed to accurately p ortray recruitment
patterns. Also, the short-comings of the Helix Reef
experiment( Sammarco and Andrews 1988; 1989)
dem onstrate the importance of hydrography in larval
dispersal experiments and models. These studies reveal
a need for mo re advanced m ode ling if accurate dispersal
patterns are to be predicted. Duration of the passive high
buoyancy period and the interval to onset of vertical
swimming behaviors differ not only between species but
also within a cohort of coral larvae, and they have a large
potential for affecting transport. We suggest that this
information must be includ ed with detailed hydrogra phic
information in ord er to pred ict dispersal patterns.
In the present study, we show that there is a range of
time over which planulae of Mo ntastra ea faveolata
develop the downward swimming behavior pre-requisite
for the search for substrate and settlement. Settlement
assays done in shallow petri dishes especially do not take
this into account. Even after five days, only 60 % of the
larvae, excluding those that were still in the very top of
the cylinder, were exhibiting the dark-period downward
swimming beha vior. A model based on these data would
suggest that less than 60 % of the M. faveolata larvae
derived from a particular spawn event will settle on reefs
that are within 3 to 5 days of transport from the spawn
site, while the remaining 40 % have the potential for
being carried further aw ay. Of course, mortality in the
plankton will diminish the larval supply over time, and
436
thus the num ber o f larvae a vailable to settle will decrease
over time. T he net effect of sup erimp osing a mortality
function on the time-course of development of settlement
behavior by larvae of M . faveolata will be that a higher
percent of the initial spawn will survive to settle within a
5 day transport radius from the natal reef, and that fewer
larvae will survive to settle at great distances. However,
given the large numbers of larvae produced by a major
mass spawn of this species (estimated at 106 eggs per m 2
of live tissue; with a 10 % cove r by this species on a
typical Caribbean reef, a small 100 m x 100 m patch reef
will produce 10 9 eggs) this does not preclude a significant
number of larvae surviving to settle at distances of 10 s to
100s of km from their source. The lack of genetic
structure for this species among widely separated
localities in the Caribb ean suppo rts this conclusion
(population genetic study of Severance 2002).
Acknow ledgements
The idea for this project came out of d iscussions with
colleagues Dr. B arry Ruddick and Chris Taggart from
Dalhousie University. This work was conducted under
perm it FKNM S 2002-066, with funding provided by the
NOAA Restoration Program. This work could not have
been accomp lished without the logistic support from the
FKNM S, especially Bill Valley and Lt. Comm . Dave
Score. Field and lab assistance were provided by a large
number of colleagues, students, and volunteers, espe cially
Dr. Margaret M iller and her staff (Charles Fasano, Dana
W illiams, Mark V ermeij, Iliana Baums), Ben Mason, D r.
M onica Medina, Dr. Mary Alice Coffroth, and TNC
volunteers Loretta Lawrence and B rad R osov.
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