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The reproductive biology and early life ecology of a common Caribbean brain coral, Diploria labyrinthiformis (Scleractinia: Faviinae)



Despite the fact that most of the severe demographic bottlenecks in coral populations occur during their earliest life stages, information on the reproductive biology and early life history traits of many coral species is limited and often inferred from adult traits only. This study reports on several atypical aspects of the reproductive biology and early life ecology of the grooved brain coral, Diploria labyrinthiformis (Linnaeus, 1758), a conspicuous reef-building species on Caribbean reefs. The timing of gamete release of D. labyrinthiformis was monitored in Curaçao over eight consecutive months, and embryogenesis, planulae behavior, and settlement rates were observed and quantified. We further studied growth and symbiont acquisition in juvenile D. labyrinthiformis for 3.5 yr and compared settler survival under ambient and nutrient-enriched conditions in situ. Notably, D. labyrinthiformis reproduced during daylight hours in six consecutive monthly spawning events between May and September 2013, with a peak in June. This is the largest number of reproductive events per year ever observed in a broadcast-spawning Caribbean coral species. In settlement experiments, D. labyrinthiformis planulae swam to the bottom of culture containers 13 h after spawning and rapidly settled when provided with settlement cues (42% within 14 h). After 5 months, the survival and growth rates of settled juveniles were 3.7 and 1.9 times higher, respectively, for settlers that acquired zooxanthellae within 1 month after settlement, compared to those that acquired symbionts later on. Nutrient enrichment increased settler survival fourfold, but only for settlers that had acquired symbionts within 1 month after settlement. With at least six reproductive events per year, a short planktonic larval phase, high settlement rates, and a positive response to nutrient enrichment, the broadcast-spawning species D. labyrinthiformis displays a range of reproductive and early life-history traits that are more often associated with brooding coral species, illustrating that classical divisions of coral species by reproductive mode alone do not always reflect the true biology and ecology of their earliest life stages.
The reproductive biology and early life ecology of a common
Caribbean brain coral, Diploria labyrinthiformis (Scleractinia:
´rie F. Chamberland
Skylar Snowden
Kristen L. Marhaver
Dirk Petersen
Mark J. A. Vermeij
Received: 11 May 2016 / Accepted: 12 September 2016
ÓSpringer-Verlag Berlin Heidelberg 2016
Abstract Despite the fact that most of the severe demo-
graphic bottlenecks in coral populations occur during their
earliest life stages, information on the reproductive biology
and early life history traits of many coral species is limited
and often inferred from adult traits only. This study reports
on several atypical aspects of the reproductive biology and
early life ecology of the grooved brain coral, Diploria
labyrinthiformis (Linnaeus, 1758), a conspicuous reef-
building species on Caribbean reefs. The timing of gamete
release of D. labyrinthiformis was monitored in Curac¸ao
over eight consecutive months, and embryogenesis, plan-
ulae behavior, and settlement rates were observed and
quantified. We further studied growth and symbiont
acquisition in juvenile D. labyrinthiformis for 3.5 yr and
compared settler survival under ambient and nutrient-
enriched conditions in situ. Notably, D. labyrinthiformis
reproduced during daylight hours in six consecutive
monthly spawning events between May and September
2013, with a peak in June. This is the largest number of
reproductive events per year ever observed in a broadcast-
spawning Caribbean coral species. In settlement experi-
ments, D. labyrinthiformis planulae swam to the bottom of
culture containers 13 h after spawning and rapidly settled
when provided with settlement cues (42% within 14 h).
After 5 months, the survival and growth rates of settled
juveniles were 3.7 and 1.9 times higher, respectively, for
settlers that acquired zooxanthellae within 1 month after
settlement, compared to those that acquired symbionts later
on. Nutrient enrichment increased settler survival fourfold,
but only for settlers that had acquired symbionts within
1 month after settlement. With at least six reproductive
events per year, a short planktonic larval phase, high set-
tlement rates, and a positive response to nutrient enrich-
ment, the broadcast-spawning species D. labyrinthiformis
displays a range of reproductive and early life-history traits
that are more often associated with brooding coral species,
illustrating that classical divisions of coral species by
reproductive mode alone do not always reflect the true
biology and ecology of their earliest life stages.
Keywords Early life history Brain coral Spawning
Embryogenesis Planula behavior Settlement Post-
settlement growth
Shifts in the taxonomic composition of coral communities
in response to local and global threats have occurred on
coral reefs worldwide, whereby historically dominant reef-
Communicated by Ecology Editor Dr. Alastair Harbourne
Electronic supplementary material The online version of this
article (doi:10.1007/s00338-016-1504-2) contains supplementary
material, which is available to authorized users.
´rie F. Chamberland
CARMABI Foundation, P.O. Box 2090, Piscaderabaai z/n,
Willemstad, Curac¸ao
Aquatic Microbiology, Institute for Biodiversity and
Ecosystem Dynamics, University of Amsterdam, Science
Park 700, 1098 XH Amsterdam, The Netherlands
SECORE International, Columbus Zoo and Aquarium,
9990 Riverside Drive, Powell, OH 43065, USA
Pittsburgh Zoo & PPG Aquarium, One Wild Place,
Pittsburgh, PA 15206, USA
University of California at Merced, 5200 North Lake Road,
Merced, CA 95340, USA
Coral Reefs
DOI 10.1007/s00338-016-1504-2
building species have been replaced by more opportunistic
and stress-tolerant species (Loya et al. 2001; Pratchett
et al. 2011; Darling et al. 2012). For instance, non-
framework-building coral species (e.g., Siderastrea radi-
ans,Porites astreoides, and Agaricia agaricites) are now
abundant on many Caribbean reefs formerly dominated by
acroporids and the Orbicella species complex (Aronson
et al. 2004; Darling et al. 2012). Species traits and life
history characteristics have been used to predict corals’
responses to environmental change (Loya et al. 2001;
Darling et al. 2012), but the mechanisms that allow certain
coral taxa to cope with conditions on present-day reefs are
not yet fully understood. For example, small-sized
brooding corals with fast growth rates and short generation
times are often the first coral species to colonize newly
available space and are capable of dominating in degraded
environments. In contrast, long-lived broadcast-spawning
species are predicted to dominate in undisturbed areas due
to their sensitivity to environmental stressors (Darling
et al. 2012). Such classifications based on life history are
derived from species-specific characteristics that, for the
most part, arise well after a coral has successfully survived
through its earliest life stages (e.g., Loya et al. 2001;
Darling et al. 2012). Yet most of the severe demographic
bottlenecks in coral populations occur during these earliest
life stages (Vermeij and Sandin 2008; Doropoulos et al.
2016); therefore, species-specific early life history
dynamics are likely to underlie ongoing changes in coral
community composition on reefs.
Shifts in species composition are often reinforced by
concordant changes in recruitment patterns. For example,
the absolute abundance of coral juveniles on Curac¸ao has
decreased by more than 50% over the last three decades,
but changes in individual abundances have differed greatly
among species (Vermeij et al. 2011). Juveniles of Acropora
spp. have virtually disappeared from Curac¸aoan reefs,
while weedy and stress-tolerant species such as Siderastrea
spp., Madracis spp., Montastraea cavernosa,
Stephanocoenia intersepta, and Pseudodiploria spp. (Dar-
ling et al. 2012) recruit in greater numbers than they did
three decades ago. Such species produce more offspring at
present and/or possess early life history characteristics that
allow them to better cope with current conditions on Car-
ibbean reefs.
Differences in early life history traits also determine
coral species’ ability to successfully recruit to the same
habitat. For example, planulae of the brooding species
Agaricia humilis are 55% less likely to settle under
thermal stress and under reduced salinity, whereas plan-
ulae of Orbicella faveolata do not experience similar
negative effects under those same stressful conditions
(Hartmann et al. 2013). Settling planulae of different
coral species also display species-specific preferences for
distinct crustose coralline algae (CCA) (Heyward and
Negri 1999), surface orientations and light levels (Bab-
cock and Mundy 1996; Baird et al. 2003). While such
behaviors can potentially explain changes in coral com-
munity composition through time, little information exists
on the earliest life stages of many Caribbean coral spe-
cies. Detailed information on species’ reproductive char-
acteristics (e.g., reproductive mode, timing of
gametogenesis, and fecundity) is available for only
*50% of all Caribbean coral species (e.g., Fadlallah
1983; Szmant 1986). Even less is known about biological
and ecological processes that are important during these
species’ early life stages, from planula development,
survival and behavior, to settlement, post-settlement sur-
vival, and settler growth. Such information would con-
tribute to a better understanding of how species-specific
behaviors in early life stages contribute to the changing
composition of Caribbean coral communities.
Members of the subfamily Faviinae are conspicuous
and abundant reef-building species throughout the Car-
ibbean region (Weil and Vargas 2010). Not much is
known about their reproductive biology and earliest life
stages, despite their high local abundance and higher
current recruitment rates compared to the mid-1970s
(Vermeij et al. 2011). Here we describe the reproductive
biology and early life ecology of the grooved brain coral
Diploria labyrinthiformis (Linnaeus, 1758). This species
is a simultaneous hermaphrodite and one of only two
known Caribbean broadcast-spawning species to repro-
duce during the spring rather than in autumn (Alvarado
et al. 2004; Weil and Vargas 2010; Muller and Vermeij
2011). Information on the earliest life stages of D.
labyrinthiformis does not yet exist, with the exception of
one study comparing settlement rates of planulae on
diseased versus healthy CCAs (Que
´and Nugues 2015).
To describe this species’ reproductive biology, we mon-
itored the timing of gamete release of a D. labyrinthi-
formis population in situ on Curac¸ao for eight consecutive
months in 2013. We further collected and cross-fertilized
gametes to document this species’ embryogenesis, planula
behavior, and settlement rates. Lastly, we described its
early post-settlement biology in terms of settler survival,
growth, onset of symbiosis, and development up to the
age of 3.5 yr. Eutrophication is a factor contributing to
coral reef degradation (Fabricius 2005), but the direct
effects of increased nutrient availability on a coral’s
physiology are not always negative and can vary among
coral taxa (Shantz and Burkepile 2014). Because D.
labyrinthiformis is increasing in abundance on eutrophic
reefs on Curac¸ao (Vermeij et al. 2007), we assessed this
species’ early post-settlement survival and growth rates
in situ under ambient and enriched nutrient conditions for
a period of 5 months.
Coral Reefs
Materials and methods
Study site
This study was carried out on the leeward coast of the
island of Curac¸ao (12°N, 69°W) in the southern Caribbean
Sea. Monitoring for spawning activity and gamete collec-
tion were carried out at Holiday Beach Reef (12°602500 N,
68°5605400W) where D. labyrinthiformis is abundant.
Monitoring of the timing of reproduction
We documented the timing of gamete release of 40 D.
labyrinthiformis colonies between 4 and 9 m depth along a
*200-m-long transect parallel to shore. Only colonies
larger than 100 cm
were included to ensure all colonies
had reached sexual maturity (Weil and Vargas 2010). Each
colony was numbered with a cattle ear tag fixed to the
adjacent substrate. Between April and October 2013, all 40
D. labyrinthiformis colonies were monitored daily from 1 h
before sunset until sunset starting 9 d after the full moon
(AFM) until 14 d AFM. Only 30 colonies were monitored
in July. For each colony, we recorded the occurrence of
gamete release and the time at which it began and ended.
On days when spawning occurred, schools of butterfly-
fishes (Chaetodon capistratus and C. striatus) were
observed swimming from one D. labyrinthiformis colony
to another and feeding on the released gamete bundles
(Muller and Vermeij 2011). In several instances, butter-
flyfishes were observed feeding on or picking at a colony’s
surface when no gametes were visible to divers, suggesting
that they could detect the presence of gamete bundles
inside the polyps and perhaps fed on them before they were
released. To determine whether this behavior indeed
coincided with subsequent spawning of D. labyrinthi-
formis, we tracked the number of butterflyfishes that
swarmed around colonies and fed either on released
gametes or on the colony’s surface and noted the time at
which each behavior started and stopped. We further took
video footage of schools of butterflyfishes feeding on the
bundles released by spawning colonies. From frame-by-
frame analyses of this footage, we approximated the pro-
portion of released bundles that were eaten before they
were no longer preyed on by butterflyfishes.
Collection of gametes and planula rearing
Twelve days AFM in May 2012, we collected egg–sperm
bundles from 11 haphazardly chosen D. labyrinthiformis
colonies between 5 and 12 m depth. Spawning occurred
from 45 to 15 min before sunset, and egg–sperm bundles
were collected by ‘‘tenting’’ colonies with cone-shaped
nets made of plastic tarp. Bundles were collected in plastic,
removable, 50-mL Falcon tubes placed at the top of the
nets and transported to the laboratory within 1 h of col-
lection. Gametes from all colonies were pooled in a 2-L
plastic bowl (Sterilite, MA, USA), and sperm density was
adjusted to *10
cells mL
by adding 0.7-lm-filtered
seawater (Whatman GF/F, GE Life Sciences, PA, USA)
following Hagedorn et al. (2009). Once egg–sperm bundles
broke apart, fertilization was allowed to take place for
90 min after which the embryos were rinsed three times
with filtered seawater in a 1-L plastic fat separator (Scan-
dicrafts Cuisine Internationale, CA, USA) to remove
excess sperm. This was done by pouring out seawater that
contained sperm through the spout of the fat separator after
positively buoyant eggs had concentrated at the surface.
The embryos were then kept in filtered seawater in closed
clear 2-L polystyrene containers (Dart Container Corpo-
ration, MI, USA). Following Vermeij et al. (2006), planula
density was kept low (B1 planula mL
) and the water in
the containers was exchanged daily (*50%) to prevent the
build-up of microbial communities that feed on substances
released (mainly lipids) by deteriorating unfertilized eggs
and/or dying planulae. The larval culture was kept at
*28 °C, which was similar to the daily average sea surface
temperature (SST) in May 2012 (NOAA Coral Reef Watch
Documentation of embryogenesis and planula
Immediately after fertilization, subsamples of 40 embryos
were placed in six individual standard Petri dishes (10 cm
diameter) containing 40 mL of filtered seawater to docu-
ment embryogenesis and planula behavior. Embryogenesis
was documented by photographing the embryos/planulae
under a dissecting microscope at various developmental
stages as defined by Okubo et al. (2013). The behavior of
developing embryos and later planulae was assessed two to
three times a day until day 2 after spawning (AS) and once
on days 3, 4, and 6 AS by recording the number of indi-
viduals that were (1) alive, (2) floating at the surface, (3)
swimming in the water column, (4) swimming on the
bottom, (5) lying on the bottom, or (6) had settled. To
induce settlement and metamorphosis, a small fragment
(*0.25 cm
) of CCA (Hydrolithon boergesenii) was
placed in the center of each Petri dish 89 h AS. The CCA
species H. boergesenii is known to promote settlement of
D. labyrinthiformis planulae (Que
´and Nugues 2015).
Settlement of planulae
Three days AS, all planulae not used for documenting
embryogenesis and planula behavior were transported to
the Curac¸ao Sea Aquarium where they were reared and
Coral Reefs
settled in a land-based nursery system. This system con-
sisted of five flow-through aquaria (acrylic, 215 L 969
H964 W cm) which were continuously supplied with
offshore seawater from the nearby reef. See Chamberland
et al. (2015) for a description of this system. Approxi-
mately 10,000 planulae were transferred to two settlement
containers, each consisting of a plastic container
(36 931 924 cm; Sterilite, MA, USA) filled with *23 L
of 50-lm-filtered seawater and containing 75 ceramic
pottery tripods for settlement surfaces (kiln stilts, 6 cm
diameter; Carl Jaeger Tonindustriebedarf GmbH, Ger-
many; Electronic Supplementary Material, ESM, Fig. S1a,
b). Tripods were previously conditioned for 3 months in
the aquarium system to allow for the development of bio-
films that help induce planula settlement and metamor-
phosis (Heyward and Negri 1999). Filtering the seawater
through a 50-lm mesh ensured the removal of large debris
and sediments while allowing smaller zooxanthellae cells
(5–10 lm) that naturally occurred in the seawater to pass
through. The settlement containers were partially sub-
merged in a larger aquarium to maintain constant water
temperatures (*28 °C), and water inside each container
was refreshed daily (*75%) with filtered seawater to
maintain water quality. Water movement inside each con-
tainer was created by two airlifts placed at opposite corners
of the containers. A subsample of five tripods per container
was inspected daily and photographed under a dissecting
microscope to track settlement and metamorphosis. On day
7 AS, very few planulae remained in the water column and
all the tripods with settlers were transferred to a flow-
through culture system to allow for settler development and
Documentation of post-settlement survival
and growth
To document the survival and growth of D. labyrinthi-
formis settlers under natural conditions, we outplanted 18
tripods each harboring 53 ±21 (mean ±SD) 1-month-old
settlers to a reef next to the Curac¸ao Sea Aquarium
(12°0405900N, 68°5304400 W). Prior to outplanting, the loca-
tion and size (number of polyps) of each settler were
recorded under a dissecting microscope. The presence of
symbionts in their tissue (absent, low density, high density)
was also estimated based on tissue coloration. Clusters
consisting of more than one settler were excluded from the
growth analyses because fusion of two or more individuals
would influence growth and survival estimates (Raymundo
and Maypa 2004). The tripods were secured on the top of
three plastic disks (30 cm diameter) with cable ties and
transported to the reef (ESM Fig. S1c). Each disk had a
central 1-cm-diameter opening and was fixed to the reef at
5–6 m depth by fitting it over a steel bar (1 cm diameter;
65 cm length) that was fixed vertically into the reef (ESM
Fig. S1c). The disks with the tripods were brought back to
the laboratory after 1, 2, and 5 months to quantify the
survival and growth of each recruit as described above, and
after 2 and 5 months, their maximum diameter was also
measured. After the first two surveys, the tripods were
immediately returned to their original location on the reef.
Because only seven tripods still harbored at least one live
D. labyrinthiformis after 5 months, they were not returned
to the reef but were instead kept in our aquarium facilities
and observed for 3 yr.
Assessment of post-settlement survival and growth
under nutrient-enriched conditions
An additional 18 tripods with D. labyrinthiformis settlers
were mapped and outplanted as described above. One slow
release fertilizer spike (9% total N, 12% available P; Jobes
Rose Fertilizer Spike, TX, USA) was placed at the center
of each disk approximately 10 cm away from the tripods
(ESM Fig. S1d) to recreate nutrient-enriched conditions as
in Thacker et al. (2001), who measured tenfold and fivefold
increases in N and P, respectively. The fertilizer spikes
were replaced every 3–4 weeks to ensure continuous
nutrient enrichment, and spikes had never completely dis-
solved before they were replaced. The nutrient-enrichment
plots were located C10 m away from the ambient (un-en-
riched) plots to avoid cross-contamination. Settler survival
and growth rates were assessed as described above and
compared with that of settlers grown under natural
Statistical analysis
Because increases in sea surface temperature (SST) are
known to trigger gamete release in corals (van Woesik
et al. 2006; Keith et al. 2016), a regression analysis was
used to test whether the occurrence of spawning in D.
labyrinthiformis could be predicted based on SSTs recor-
ded on Curac¸ao in 2013. The proportion of colonies that
released gametes during each monthly monitoring period
(n=8) was regressed against the average increase in SST
during the previous month. A maximum likelihood (ML)
approach was used to test for differences in (1) survival
rates (i.e., the proportion of recruits alive at each time point
relative to the initial settler) between recruits grown in
ambient and nutrient-enriched conditions, (2) survival rates
between settlers that acquired symbionts within or later
than 1 month after they settled, and (3) random effects
among disks. We used a binomial distribution to estimate
the most likely probability of survival in each treatment
and their interactions at each time point. A null model with
equal survival probabilities across all treatments (one-
Coral Reefs
parameter model) was compared to models with unequal
survival probabilities between treatment groupings (two- or
three-parameter models). The best-fit values of each model
were estimated based on the summed log likelihood of each
model, and the best combination of treatments was deter-
mined using Akaike’s information criterion. Significant
differences between the best-fit model and all other models
with equal numbers of parameters were assessed with a
post hoc comparison based on the assumption of equal
Bayesian prior expectations. See Hilborn and Mangel
(1997) for details on this statistical approach. After
assumptions of normality and homogeneity were con-
firmed, two-way ANOVA followed by Tukey’s post hoc
pairwise comparisons tested for differences in growth rates
(1) between recruits grown in ambient and nutrient-en-
riched conditions and (2) between settlers that acquired
symbionts within or later than 1 month after they settled.
Timing of reproduction
Of the 40 monitored D. labyrinthiformis colonies, 67.5%
released gametes during one or more of six monthly
spawning events between May and September 2013
(Fig. 1a). Individual colonies reproduced for a maximum
of two consecutive months. A reproductive peak occurred
in the spring (May–July) during which 50.0% of the pop-
ulation spawned, whereas 17.5% of the population
spawned in late summer–early autumn (August–Septem-
ber) (Fig. 1a). Colonies that spawned during the spring did
not spawn later in the year and vice versa. The number of
colonies that spawned each month was not correlated with
the average increase in SST the month before (regression
analysis: p=0.35; Fig. 1a). Spawning always occurred
between 10 and 13 d AFM and peaked on days 11 and 12
AFM (80% of observations, n=59; Fig. 1b). Gamete
release (Fig. 2a) occurred between 52 and 2 min before
sunset and sperm–egg bundles were often released in pul-
ses. Typically, one section of the colony spawned for
5±5 min (mean ±SD) after which all gamete release
stopped, then resumed after 3–20 min. This resulted in 1–3
spawning pulses per colony per day.
When spawning occurred, schools of butterflyfishes
(2–50 individuals) moved from one D. labyrinthiformis
colony to another. They remained around each colony and
inspected its surface for several seconds before moving to
another colony. In some cases, they started feeding on the
colony’s surface when no gametes were visible to divers. In
67% (n=33) of cases where larger schools of butterfly-
fishes (C25 individuals) started feeding on a colony’s
surface, gamete release occurred within 30 min, suggesting
that butterflyfishes were either eating gamete bundles from
inside the polyps or immediately after they were released.
After release, most gamete bundles were eaten by butter-
flyfishes; in most instances, less than *10% of the bundles
escaped predation.
Embryogenesis and planula development
Gamete bundles broke apart *45 min after they were
released (Fig. 2b). Eighty minutes AS, 95% of all eggs
were fertilized and underwent their first holoblastic cleav-
age (Fig. 2c), followed by a second cleavage 30 min later
(Fig. 2d). Cell divisions progressed quickly, and at 3 h AS,
embryos reached an 8- to 32-cell blastomere stage. While
the first two cleavages were symmetrical, cell divisions
Days after the full moon
9 1011121314
Percentage of population observed
Moon cycle (2013)
no spawning
no spawning
ba 30
Sea surface temperature (in °C)
no spawning
no spawning
Fig. 1 Proportion of a Diploria labyrinthiformis population observed spawning (a) each month (bars) relative to sea surface temperatures (line)
and (b) each day relative to the lunar cycle (n=40 colonies)
Coral Reefs
thereafter yielded unequally sized cells, causing the
developing embryos to become irregularly shaped.
Between the 2- and 16-cell stages, one-third of the embryos
broke apart (36 ±13%, n=16 pictures of 11–56
embryos) but the resulting cells (or clusters of cells)
remained viable (Fig. 2e). Embryo breakage was not
always symmetrical, generating smaller embryos that
comprised 1–8 cells. Size variation in developing embryos
increased at this point, but increased mortality resulting
from embryo breakage was not observed (Fig. 3). Five
hours AS, embryos had developed into the morula or
‘prawn-chip’’ stage (64–256 cells) in which embryos were
flattened, but kept their irregularly shaped appearance
(Fig. 2f). Six hours AS, embryos obtained a concave–
convex bowl shape (i.e., blastula) corresponding to the
onset of gastrulation (Fig. 2g). Embryos became rounded
again at 10 h AS and *10% (n=60) displayed small
nodules protruding from one or two sides of their surface
(Fig. 2h).
Planula behavior and settlement
Ten hours AS, embryos started moving for the first time;
1% were observed spinning at the water surface, indicating
their transition from an embryo to a planula. Only 1 h later
95% of the planulae showed the same behavior. At this
point, planulae were ball-shaped and measured
308 ±84 lm(n=56) in diameter. Variation in planula
size was large as a consequence of earlier embryo breakage
observed between 2 and 5 h AS. Planulae subsequently
developed into pear-shaped individuals (Fig. 2i) that
moved away from the surface. By 13 h AS, 60% of the
planulae were lying or swimming on the bottom of the
rearing containers, both in the main culture and in the Petri
Fig. 2 Embryogenesis, planula behavior and settlement, and early
post-settlement development of Diploria labyrinthiformis. Colonies
released sperm-egg bundles (a) between 52 and 2 min before sunset
and between 10 and 13 d after the full moon (AFM) from May
through September. Sperm–egg bundles broke apart (b) ca. 45 min
after spawning (AS). The first holoblastic cleavage (c) occurred
80 min AS, followed by a second holoblastic cleavage 30 min later,
resulting in a four-blastomere-stage zygote (d). At that point many
embryos broke into smaller embryos (e) that remained viable. The
white arrowhead points an ongoing embryo breakage, and the black
arrowhead shows a single-celled embryo resulting from breakage.
After 3 h, embryos were at the 8- to 16-blastomere stage, and after 5 h
they were at the 64- to 256-cell prawn-chip stage (f). Six hours AS,
embryos became bowl-shaped (g) indicating the onset of gastrulation.
Embryos became rounded again after 10 h (h). At that stage ca. 10%
of embryos displayed small nodules protruding from their lateral sides
(shown by arrowhead). After 13 h, embryos had fully developed into
pear-shaped, motile planulae (i). 43% of planulae had settled on
crustose coralline algae 14 h after they were provided with settlement
cues (j). One-month-old juveniles had fully developed tentacles, and
45% had acquired zooxanthellae (k). Six-month-old juveniles dis-
played variable sizes (l) and grew in a plate-like form and were
slightly elevated above the substrate (shown by arrowhead). The first
polyp division resulted in a smaller lateral polyp (m) (shown by the
arrowhead). Three-year-old colonies had divided into 2–4 polyps and
displayed a grooved shape typical of brain corals (n). A 3.5-yr-old
juvenile reached 3 cm in size and had 8 polyps (o). Photograph
credits (a), (cj) S Snowden, (b) R Villaverde, (ko) VF Chamberland
Coral Reefs
dish replicates (Fig. 3). Planulae were first observed set-
tling at 103 h AS (i.e., 14 h after they were provided with
settlement cues), with 43 ±7% (mean ±SE) of all plan-
ulae having completed metamorphosis at that time
(Figs. 2j, 3). After 6 d, 86 ±3% of the initial number of
planulae were alive, of which 64 ±5% had settled
(Fig. 3). The large majority of D. labyrinthiformis planulae
settled on the undersides of the tripods (94.5 ±8.0%,
mean ±SD, n=18 tripods). One month after settlement,
polyps had fully developed tentacles and 45% (n=1893)
of all settlers had acquired zooxanthellae (Fig. 2k).
Post-settlement growth and development
At the time they were introduced to the reef, the 1-month-
old settlers were single polyps that measured \1mm in
diameter. Five months later, recruit size varied consider-
ably and ranged between 0.2 and 6.0 mm (n=106)
(Fig. 2l). Between the ages of 3 and 6 months, primary
polyps increased in diameter at an average rate of
0.21 ±0.03 mm month
(mean ±SE, n=106). Six-
month-old recruits formed large corallites with a thick
tissue layer that started folding into the groove-like pat-
tern typical of brain corals. Recruits grew upward in a
plate-like shape with their edges elevated above the
substratum (Fig. 2l). At the age of 6 months, 100 of 106
surviving recruits still consisted of a single polyp, and the
rest had divided into two-polyp colonies. The division of
the first polyp was always asymmetrical and generated a
colony with a large central polyp and a smaller lateral
polyp (Fig. 2m). A 3-yr-old recruit that survived in our
aquarium facilities reached a maximum diameter of
2.5 cm and consisted of four polyps (Fig. 2n). Polyp
division rates increased rapidly thereafter; the same
recruit doubled in polyp number during the following
6 months (Fig. 2o).
Post-settlement ecology: onset of symbiosis
and nutrient enrichment
When settlers were transferred to the reef, symbiont den-
sities estimated from tissue coloration varied considerably
among individuals; settlers either lacked symbionts alto-
gether (54 ±18%) or contained low (13 ±9%) or high
densities of zooxanthellae (34 ±36%) (mean ±SD,
n=36 tiles; Fig. 4). One month later, only 1.6%
(n=124) of the settlers still did not harbor symbionts.
Settlers that acquired high densities of symbionts within
1 month following settlement had grown into 1.6- and 1.9-
fold larger polyps 2 and 5 months after they were out-
planted, respectively (two-way ANOVA, 2 months:
=15.03, p\0.0001; 5 months: F
p\0.001), and were 3.7 times likelier to survive to the age
of 6 months (11.4 ±2.5%, mean ±SE) than those that
lacked zooxanthellae at the time they were outplanted
(2.9 ±0.9%) (ML, two-parameter model: [ab-
sence] =[low density =high density], p\0.0001;
Fig. 4). When exposed to elevated nutrient concentrations,
recruit survival increased fourfold, but only in recruits that
had acquired zooxanthellae within 1 month following set-
tlement (ML, two-parameter model: [ambi-
ent] =[?N] * [absence] =[?N] * [low density, high
density], p\0.05; Fig. 4). Nutrient enrichment did not
affect settler growth rates (two-way ANOVA, 2 months:
=2.35, p=0.127; 5 months: F
Caribbean broadcast-spawning coral species typically have
one gametogenic cycle per year, which, in the northern
hemisphere, ends in the late summer or early autumn
5 111331395682103153
Percentage of initial individuals
(mean %)
Time after spawning (hrs)
Floating at the surface
Swimming in the column
Swimming on the bottom
Lying on the bottom
CCA added
Fig. 3 Survival, behavior, and
settlement of Diploria
labyrinthiformis embryos and
planulae during the first 6 d
following spawning, and before
and after addition of crustose
coralline algae to promote
settlement. Bars represent the
percentage of the initial number
of embryos (n=40) displaying
each behavior, averaged across
replicates (n=6)
Coral Reefs
(August–October) during one synchronous spawning event
(Fadlallah 1983; Szmant 1986). In contrast, D. labyrinthi-
formis on Curac¸ ao released gametes during six consecutive
months, with a peak in the spring and smaller reproductive
events in the late summer to early autumn (Fig. 1a). This is
the first report of a Caribbean broadcasting species with six
spawning events in a year. Biannual spawning, when
conspecifics spawn in the spring and autumn, occurs in
several Indo-Pacific species. In Australia, 31% of Acropora
species reproduce during both seasons (Gilmour et al.
2016). And similar to these Acropora species, D.
labyrinthiformis colonies on Curac¸ ao also spawned either
in the spring or in the late summer–early autumn, but not
both. Such reproductive isolation between sympatric con-
specifics can result in genetic divergence and has been
proposed as a mechanism for speciation in corals (Dai et al.
2000; Rosser 2015).
Spreading reproductive investments throughout the year
has been proposed as an evolutionary strategy to escape
stressors that occur either randomly or seasonally. Alvar-
ado et al. (2004) suggested that spring spawning by D.
labyrinthiformis in Colombia carries adaptive advantages
due to the higher availability of suitable surfaces for set-
tlement during winter and spring when algal cover is lower
than during other periods of the year. Furthermore, weaker
current and tide regimes during this period could contribute
to higher fertilization rates. A link between spawning times
and seasonal environmental factors was also proposed for
corals in Taiwan (Dai et al. 2000) where offspring pro-
duced during a later reproductive peak would avoid high
Probability of survival (mean ±SE)
Time after outplant (months)
+N +N +N +N +N +N +N+N+N
High symbiont densityLow symbiont densityAbsence of symbionts
Fig. 4 Positive and interactive effect of early symbiont acquisition
and nutrient enrichment on the survivorship of two-week-old Diploria
labyrinthiformis settlers that lacked symbionts (clear bars), or had
acquired low (gray bars) or high symbiont (black bars) densities.
Letters above bars indicate significantly different groups within each
time point as determined by a maximum likelihood analysis with
Coral Reefs
mortality caused by typhoons, heavy rainfall, and bleach-
ing episodes. In the Caribbean, D. labyrinthiformis is the
only known broadcast-spawning species to spread repro-
ductive investments over multiple spawning events within
a year, equivalent to Caribbean brooding species which
typically release planulae year-round (Szmant 1986).
Brooding life histories are generally associated with short-
lived species that produce small numbers of offspring per
brood. Szmant (1986) hypothesized that releasing planulae
over multiple cycles per year rather than all at once can at
least in part offset small brood size and short life spans in
brooding species. Diploria labyrinthiformis could have
adopted this bet-hedging strategy to optimize its overall
fitness by spreading its reproductive output through time to
avoid occasional circumstances that could result in the
complete loss of a year’s reproductive investment. It
remains unclear why reproduction over many months is
atypical of Caribbean broadcast-spawning species, while it
is common in Caribbean brooding and Indo-Pacific coral
The timing of gamete release by D. labyrinthiformis
differs among locations throughout the Caribbean. In
Bonaire, an island 60 km east of Curac¸ao, this species’
reproductive timing is similar to that reported here (E
Muller pers. comm.). However, D. labyrinthiformis repro-
duces during the late summer in Mexico (S Snowden pers.
obs.), while in Puerto Rico (Weil and Vargas 2010) and
Colombia (Alvarado et al. 2004) it spawns only during a
single spawning event in the spring. These differences in
reproductive timing, in terms of one versus multiple
spawning events per year and the season(s) during which
spawning occurs, are not related to latitude, in contrast to
Western Australia where the occurrence of biannual
spawning decreases toward higher latitudes (Rosser 2013).
Although seasonal increases in sea temperature are known
to trigger gamete release in corals (van Woesik et al. 2006;
Keith et al. 2016), the reproductive peak of D. labyrinthi-
formis on Curac¸ao did not correlate with increases in SST
in 2013 (NOAA Coral Reef Watch 2013; Fig. 1a). Thus,
spatial differences in the reproductive timing of D.
labyrinthiformis could be the result of other environmental
cues such as photoperiod (Babcock et al. 1994), regional
wind fields (van Woesik 2010), monthly rainfall (Mendes
and Woodley 2002) or of internal rhythms inherited from
ancestral populations (Rosser 2013).
Most corals reproduce during the night to reduce pre-
dation on gametes by diurnal plankton feeders (Westneat
and Resing 1988). In contrast, several brooding sponges,
ascidians, gorgonians, and bryozoans release distasteful or
chemically defended planulae during the day to reduce the
predation risks associated with daylight spawning (Lind-
quist and Hay 1996). While it is unclear whether egg–
sperm bundles produced by D. labyrinthiformis possess
some form of chemical defense, they were clearly palat-
able to butterflyfishes. Predation by butterflyfishes dra-
matically reduced the number of intact gametes reaching
the surface of the water column (by *90%), and this
appeared to be a major impediment to planula production
in D. labyrinthiformis.
Embryogenesis in D. labyrinthiformis followed the
general sequence of development described for other coral
species (Okubo et al. 2013), with the exception that a third
of the developing embryos broke apart during the first cell
divisions, resulting in large numbers of smaller-sized
embryos. Embryo breakage was first described for A.
millepora in response to hydrodynamic disturbance (Hey-
ward and Negri 2012). Resulting A. millepora embryos
remained viable and developed into normal, although
smaller, planulae and settlers. Diploria labyrinthiformis
planulae generated through fragmentation also showed no
signs of abnormal development and remained viable, albeit
smaller than planulae that developed from non-fragmented
embryos. The production of planktonic clones has been
suggested as a mechanism to increase reproductive output
once the critical step of fertilization is successfully
accomplished (Heyward and Negri 2012). With only
3–31% of the D. labyrinthiformis population releasing
gametes on each spawning day, and with most egg–sperm
bundles being consumed by butterflyfishes upon release,
embryo breakage could in part offset the reduced fertil-
ization success associated with daytime and asynchronous
spawning in this species.
Embryos of D. labyrinthiformis developed rapidly; after
13 h, the majority of motile planulae were negatively
buoyant and 60% of the planulae were already lying or
swimming on the bottom (Fig. 3). Furthermore, almost half
of the planulae settled within 14 h after being provided
with settlement cues (Fig. 3). Short planktonic phases and
rapid settlement are traits normally associated with a
brooding reproductive strategy (Harrison and Wallace
1990; Carlon and Olson 1993), and this suggests a limita-
tion to the dispersal potential of D. labyrinthiformis plan-
ulae relative to other Caribbean broadcasting species
(Miller and Mundy 2003). There is increasing evidence that
not all broadcast-spawned planulae disperse as far as pre-
viously assumed and that subtle species-specific differ-
ences in the duration of embryogenesis and planula
behavior can contribute to observed differences in adult
distributions (Miller and Mundy 2003; Szmant and
Meadows 2006; Tay et al. 2011). Planulae of the Caribbean
broadcasting species O. faveolata develop similarly to
those of D. labyrinthiformis (i.e., time to motility as short
as 15 h AS), but spend between 50 and 75 h in the water
column before they initiate settlement (Szmant and
Meadows 2006). In contrast, D. labyrinthiformis likely has
a much smaller average dispersal distance compared to O.
Coral Reefs
faveolata as it remains planktonic for a much shorter period
of time (13 h). At the other extreme, embryogenesis in A.
palmata lasts much longer than in the aforementioned
species (3.75 d) and motile planulae remain in the water
column for at least 5 d and up to 20 d before moving to the
bottom for settlement (Baums et al. 2005). These differ-
ences in planktonic duration and planula behavior clearly
have important consequences for a species’ dispersal
potential. Describing all coral species with external fertil-
ization simply as broadcast spawners ignores these subtle
but potentially crucial differences. A more refined classi-
fication of species based on reproductive, developmental,
and early life history would allow for a better under-
standing and prediction of the composition and connec-
tivity of coral populations.
Diploria labyrinthiformis recruits had growth rates
similar to those reported for other Caribbean brain corals
(B2-yr-old Colpophyllia natans: 0.2–0.3 mm month
and Pseudodiploria strigosa: 0.4 mm month
; van
Moorsel 1988). Diploria labyrinthiformis recruits grew in a
plate-like shape that was partially elevated above the
substrate (Fig. 2l). A similar growth form was described
for Agaricia agaricites and C. natans by van Moorsel
(1985,1988) who found that this growth strategy reduced
competitive interactions with neighboring organisms such
as filamentous algae compared to coral recruits that grew
encrusted over the substrate. While rapid linear expansion
allows recruits to quickly occupy space on the reef, three-
dimensional rather than two-dimensional growth could
allow young recruits to escape competition when they are
most vulnerable due to their small size (Vermeij and
Sandin 2008; Doropoulos et al. 2016).
Eutrophication generally impedes coral recruitment as
algal growth limits space available for settlement, and
increases post-settlement mortality through algal over-
growth and promotion of microbial growth resulting in
anoxia (Hunte and Wittenberg 1992; Fabricius 2005; Smith
et al. 2006). In light of this, fourfold greater survival of D.
labyrinthiformis settlers under elevated nutrient concen-
trations relative to ambient conditions (Fig. 4) is somewhat
surprising. However, 95% of D. labyrinthiformis planulae
settled on the undersides of the tripods where the benthic
community was dominated by CCAs and not altered by
nutrient enrichment over the course of the experiment
(ESM Fig. S2), in contrast to the community that grew on
the topsides of the tripods which became dominated by
algal turfs (ESM Fig. S1e,f). Interestingly, the positive
effect of nutrients on D. labyrinthiformis was dependent on
the timing of zooxanthellae uptake by the settlers (Fig. 4).
Settlers that acquired symbionts early in life were 3.7 times
likelier to survive to the age of 6 months and grew twice as
large as those that initiated symbiosis later in life. Nutrient
enrichment promotes zooxanthellae cell growth and
subsequent carbon translocation to the coral host (Tanaka
et al. 2006), and a similar influence of nutrient enrichment
on the growth of symbiotic versus aposymbiotic settlers
was described for Acropora digitifera (Tanaka et al. 2013).
Acropora digitifera settlers containing zooxanthellae that
were provided with nutrients had increased growth rates
and were better able to compete with benthic microalgae
compared to settlers that lacked zooxanthellae. Thus, these
and our findings illustrate that nutrient enrichment does not
necessarily result in negative consequences for coral
recruitment, and highlight the importance of the onset of
symbiosis early in life in corals.
Several aspects of the reproductive biology and early
life ecology of D. labyrinthiformis described in this study
are atypical of Caribbean broadcast-spawning species.
While biannual reproduction of sympatric conspecifics in
broadcast spawners has so far only been described for
Indo-Pacific species, this phenomenon occurs in Car-
ibbean species as well. With many reproductive events
per year and a short embryogenic phase followed by rapid
settlement, D. labyrinthiformis displays traits that are
normally associated with brooding species. Our findings
therefore show that early life history characteristics are
not necessarily more similar within than between classi-
cally divided coral groupings such as brooders and
spawners, but that a gradual continuum likely exists with
‘classical’’ broadcast-spawning and brooding species on
either end.
Acknowledgments This research received funding and/or support
from the CARMABI Foundation, SECORE International, the Pitts-
burgh Zoo & PPG Aquarium, the University of Amsterdam, the
Curac¸ao Sea Aquarium, the Fonds de Recherche du Que
´bec- Nature
et Technologies, and the U.S. National Science Foundation (IOS-
1146880, OCE-1323820). We are thankful to our generous volunteers
who spent a cumulative total of 7976 min of their precious time
underwater to document the spawning timing of D. labyrinthiformis.
VF Chamberland also thanks MT Chamberland for her help tagging
and mapping colonies. We thank MW Miller and one anonymous
reviewer for providing us with insightful comments on earlier ver-
sions of this manuscript. Lastly, we are grateful to S Rosalia for our
everlasting memories of her contagious laugh at the CARMABI
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... After a survey of 82 sites along the Mexican Caribbean, Diploria labyrinthiformis was listed as one of eleven most highly susceptible species to this disease due to significant population declines (Á lvarez-Filip et al. 2019). Given that D. labyrinthiformis is a reef-building species (Weil and Vargas 2010;Chamberland et al. 2017) that provides structural complexity (Á lvarez-Filip et al. 2019) such losses are of major concern making it a target species in coral reef restoration and genetic rescue programs. Cryopreservation is potentially an excellent method for gamete conservation of endangered coral species. ...
... The timing of spawning events varies throughout the Caribbean. In Puerto Rico (Weil and Vargas 2010), Colombia (Alvarado-Chaparro et al. 2004), Bonaire (Muller and Vermeij 2011) and Bermuda (Wyers et al. 1991) spawning occurs in the spring and summer, whereas in Curaçao two peaks, in spring and autumn, have been documented (Chamberland et al. 2017). Embryonic development is fast such that within 24-48 h larvae are formed and can settle on suitable substrates (Chamberland et al. 2017). ...
... In Puerto Rico (Weil and Vargas 2010), Colombia (Alvarado-Chaparro et al. 2004), Bonaire (Muller and Vermeij 2011) and Bermuda (Wyers et al. 1991) spawning occurs in the spring and summer, whereas in Curaçao two peaks, in spring and autumn, have been documented (Chamberland et al. 2017). Embryonic development is fast such that within 24-48 h larvae are formed and can settle on suitable substrates (Chamberland et al. 2017). ...
Full-text available
In this study, we evaluated the efficacy of sperm cryopreservation for use in larval-based propagation of Diploria labyrinthiformis and produced offspring that were maintained under controlled conditions. Gametes were collected from colonies in situ in July and August 2017 and 2018. The four largest colonies out of a total of nine appear to be senescent or produce low-quality sperm or eggs. Sperm was cryopreserved for comparison of the effects of storage time on sperm viability. We determined that cry-opreserved sperm from D. labyrinthiformis is viable for at least 13 months for use in in vitro crosses, though their motility is reduced on average by 24% in comparison with fresh sperm. Using frozen sperm to fertilize freshly collected eggs led to successful fertilization, larval yields, settlement and post-settlement survival. In general, these were lower by 23%, 23%, 14% and 8%, respectively, when compared to controls fertilized with fresh sperm. Our results suggest that motility of fresh sperm is not a good indicator of the future fate of larvae because in some cases low motility led to successful settlement. We also found that not all crosses were successful, and that the direction of the cross significantly affects larval yields and settlement. Once symbionts were noticeable within the primary polyps the cryo-recruits were maintained in an ex situ nursery for observation and showed similar survival with respect to recruits produced with fresh sperm. Prior to the 2018 spawning event, Stony Coral Tissue Loss Disease (SCTLD) was detected in the studied colonies and by February 2020 seven of the nine colonies (78%) had succumbed to the disease. The sperm from these colonies was banked in a repository and since then has been used in genetic rescue projects for this species. Thus, we show that cryopreservation is a useful tool in actions designed to recover D. labyrinthiformis and can potentially be applied to other species of corals severely affected by SCTLD or in need of genetic rescue.
... Larval settlement experiments were conducted on the Southern Caribbean island of Curacao, and coral gametes were collected from two sites on the leeward coast of the island: A. palmata from Sea Aquarium (12°4′59″N, 68°53′43″W) and D. labyrinthiformis from the Water Factory (also known as Koredor; 12°6′34″N, 68°57′23″W; Figure S1). Prior to settlement experiments, gametes were reared into larvae based on previously established methods, 23,27,50 which are summarized in the Supporting Information. These species were selected for study because they are important reef-building taxa distributed widely across the Caribbean, Florida, and Gulf of Mexico and whose early life stages have been well-characterized. ...
... These species were selected for study because they are important reef-building taxa distributed widely across the Caribbean, Florida, and Gulf of Mexico and whose early life stages have been well-characterized. 24,27 A relatively stress-resistant coral, D. labyrinthiformis, spawns multiple times per year and settles quickly, allowing iterative testing of materials. Conversely, A. palmata is an ecologically distinct, shallow-water species that no longer recruits in large numbers. ...
... For reference, the average size of A. palmata larvae is ≈700 μm and that of D. labyrinthiformis is ≈300 μm. 27,58 This qualitative description was confirmed by 3D surface analysis of the substrates, which revealed no large differences in mean roughness as a function of glass fiber content ( Figure 3b). This analysis also provided the relative surface area available for larval contact on each substrate type, presented as the surface area ratio, or the factor by which the surface area is increased from a perfectly flat plane (Figure 3b). ...
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The widespread loss of stony reef-building coral populations has been compounded by the low settlement and survival of coral juveniles. To rebuild coral communities, restoration practitioners have developed workflows to settle vulnerable coral larvae in the laboratory and outplant settled juveniles back to natural and artificial reefs. These workflows often make use of natural biochemical settlement cues, which are presented to swimming larvae to induce settlement. This paper establishes the potential for inorganic cues to complement these known biochemical effects. Settlement substrates were fabricated from calcium carbonate, a material present naturally on reefs, and modified with additives including sands, glasses, and alkaline earth carbonates. Experiments with larvae of two Caribbean coral species revealed additive-specific settlement preferences that were independent of bulk surface properties such as mean roughness and wettability. Instead, analyses of the substrates suggest that settling coral larvae can detect localized topographical features more than an order of magnitude smaller than their body width and can sense and positively respond to soluble inorganic minerals such as silica (SiO2) and strontianite (SrCO3). These findings open a new area of research in coral reef restoration, in which composite substrates can be designed with a combination of natural organic and inorganic additives to increase larval settlement and perhaps also improve post-settlement growth, mineralization, and defense.
... For instance, artificial substrates intended for settlement are often conditioned for months on a natural reef or in flow-through aquaria in order to develop algal and microbial films. [21][22][23][24] Alternatively, higher concentrations of biochemical cues are presented to larvae by placing fragments or powders of CCAs directly onto settlement substrates, [25][26][27] by introducing soluble extracts isolated from CCAs into settlement containers, 25,[28][29][30] or by incorporating CCA extracts into solid resins. 20,[31][32] Once larvae have settled and matured into juvenile corals over several weeks to months in protected aquaria or nurseries, they are then outplanted back to degraded reefs to bolster restoration efforts. ...
... 12 For larval studies and larva-based coral propagation, gametes are usually collected at the time of spawning and reared into larvae in a controlled environment. For this study, gamete collection and subsequent larval rearing were based on previously established methods, 23,27,51 which are summarized here. In August of 2019, A. palmata gametes were collected during the spawning event occurring 1 day after the full moon from approximately 10 adult colonies situated between 2 m and 8 m depth. ...
... For reference, the average size of A. palmata larvae is  700 µm and that of D. labyrinthiformis is  300 µm. 27,67 This qualitative description was confirmed by 3D surface analysis of the substrates, which revealed no large differences in mean roughness as a function of glass fiber content (Fig. 4b). This analysis also provided the relative surface area available for larval contact on each substrate type, presented as the surface area ratio, or the factor by which the surface area is increased from a perfectly flat plane (Fig. 4b). ...
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The widespread loss of stony reef-building coral populations has been compounded by pervasive recruitment failure, i.e., the low or absent settlement and survival of coral juveniles. To combat global coral reef stressors and rebuild coral communities, restoration practitioners have developed workflows to rear and settle vulnerable coral larvae in the laboratory and subsequently outplant settled juveniles back to natural and artificial reefs. These workflows often make use of the natural biochemical settlement cues present in crustose coralline algae (CCA), which can be presented to swimming larvae as extracts, fragments, or live algal sheets to induce settlement. In this work, we investigated the potential for inorganic chemical cues to complement these known biochemical effects. We designed settlement substrates made from lime mortar (CaCO3) and varied their composition with the use of synthetic and mineral additives, including sands, glasses, and alkaline earth carbonates. In experiments with larvae of two Caribbean coral species, Acropora palmata (elkhorn coral) and Diploria labyrinthiformis (grooved brain coral), we saw additive-specific settlement preferences (>10-fold settlement increase) in the absence of any external biochemical cues. Interestingly, these settlement trends were independent of bulk surface properties such as surface roughness and wettability. Instead, our results suggest that not only can settling coral larvae sense and positively respond to soluble inorganic materials, but that they can also detect localized topographical features more than an order of magnitude smaller than their body width. Our findings open a new area of research in coral reef restoration, in which engineered substrates can be designed with a combination of organic and inorganic additives to increase larval settlement, and perhaps also improve post-settlement growth, mineralization, and defense.
... Unlike M. flabellata, however, they are both gonochoric, and fertilization for the sponge specifically could be external or internal 89 , an option not available for hermaphroditic broadcasting corals. Chamberland, et al. 90 reported the Caribbean broadcasting coral Diploria labyrinthiformis to spawn for six consecutive months, but that species still had an identifiable, narrow four-day spawning window 10-13 days after the full moon each month. Additionally, unlike some corals that can asexually produce larvae 91,92 , M. flabellata does not self-fertilize 93 , and there were no observations of developing planulae in the histological sections. ...
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Sessile invertebrates often engage in synchronized spawning events to increase likelihood of fertilization. Although coral reefs are well studied, the reproductive behavior of most species and the relative influence of various environmental cues that drive reproduction are not well understood. We conducted a comparative examination of the reproduction of the well-studied Hawaiian coral Montipora capitata and the relatively unknown reproduction of its congener, Montipora flabellata. Both are simultaneous hermaphroditic broadcast spawners that release egg-sperm bundles with external fertilization. Montipora capitata had a distinct reproductive pattern that resulted in coordinated gamete maturation and the synchronized release of thousands of egg-sperm bundles across two spawning pulses tightly coupled to consecutive new moon phases in June and July. Montipora flabellata exhibited a four month reproductive season with spawning that was four-fold less synchronous than M. capitata; its spawning was aperiodic with little linkage to moon phase, a broadly distributed release of only dozens or hundreds of bundles over multiple nights, and a spawning period that ranged from late June through September. The reproductive strategy of M. flabellata might prove detrimental under climate change if increased frequency and severity of bleaching events leave it sparsely populated and local stressors continue to degrade its habitat.
... Egg-sperm bundles were collected from 7 D. labyrinthiformis colonies and 4 C. natans colonies at a depth of 5 -10 m. Larvae were reared following previouslypublished methods [59]- [62] which are also summarized in the Supplementary Information. All larval rearing steps and experiments were performed with 0.5 µm filtered seawater (FSW; spun polypropylene sediment filters, sequential pore sizes of 50 µm, 20 µm, 5 µm, and 0.5 µm, H2O Distributors, Marietta, GA). ...
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Larval settlement in wave-dominated, nearshore environments is the most critical life stage for a vast array of marine invertebrates, yet it is poorly understood and virtually impossible to observe in situ. Using a custom-built flume tank that mimics the oscillatory fluid flow over a shallow coral reef, we show that millimeter-scale benthic topography increases the settlement of slow-swimming coral larvae by an order of magnitude relative to flat substrates. Particle tracking velocimetry of flow fields revealed that millimeter-scale ridges introduced regions of flow recirculation that redirected larvae toward the substrate surface and decreased the local fluid speed, effectively increasing the window of time for larvae to settle. In agreement with experiments, computational fluid dynamics modeling and agent-based larval simulations also showed significantly higher settlement on ridged substrates. These findings highlight how physics-based substrate design can create new opportunities to increase larval recruitment for ecosystem restoration.
... Diploria labyrinthiformis is a common coral species in the Caribbean and, depending on its location, can spawn from April to October before sunset, having a wider and earlier spawning window compared to most broadcast spawning corals in the region (Weil and Vargas 2010;Chamberland et al. 2017). D. labyrinthiformis was selected for this study due to its ability to build 3D structures in reefs, its early and multiple spawning events throughout the year, its high spawning predictability, and the contribution to recent and ongoing research regarding its reproductive potential and early life history stages (Chamberland et al. 2016). ...
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Crustose Coralline Algae (CCA) is a well-known settlement inducer for stony corals and, ultimately, recruitment, a vital component for reef growth and resilience. However, potential impacts of diseased CCA on larval settlement are not fully understood, especially on particular coral species. As oceans continue to warm, coral larvae need to be able to respond to settlement cues in elevated temperatures, yet the combined effects of thermal stress and CCA health status on larval behavior is not well known for most coral species. Here we assessed the effect of elevated temperatures and disease on the ability of the CCA Hydrolithon boergesenii to induce settlement of Diploria labyrinthiformis larvae. D. labyrinthiformis planulae were exposed to 4 substrate combinations (healthy CCA, diseased CCA, bare substratum, and bare tissue culture plate) and three temperatures (27.5°C, 29°C, and 31°C). Overall, settlement started earlier and was 1.5-3x higher at 31°C, regardless of CCA health status, but at this temperature, larval mortality increased two-fold in diseased CCA. Settlement differences between healthy and diseased H. boergesenii were only observed at 29°C, with healthy CCA facilitating twice as much settlement and having 3x lower mortality than diseased. Our findings suggest that, even though larvae can settle in both healthy and diseased CCA, temperature plays an important role in whether larvae will settle or perish. This study highlights the importance of healthy CCA to maintain and increase settlement and the ability of larvae to adapt to a warming ocean, contributing to the knowledge of D. labyrinthiformis larval ecology, valuable for larval rearing for restoration purposes.
... Collection Locations, Sperm Cryopreservation, and Gamete Crosses. The coral reproduction and sperm cryopreservation methods applied in this study are described in previous work (21,23,45,46) and in the SI Appendix, Extended Materials and Methods. Briefly, coral egg-sperm bundles were collected in the field using tents at two locations in Curaçao: Spanish Water (12°4 '13.11 ...
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Assisted gene flow (AGF) is a conservation intervention to accelerate species adaptation to climate change by importing genetic diversity into at-risk populations. Corals exemplify both the need for AGF and its technical challenges; corals have declined in abundance, suffered pervasive reproductive failures, and struggled to adapt to climate change, yet mature corals cannot be easily moved for breeding, and coral gametes lose viability within hours. Here, we report the successful demonstration of AGF in corals using cryopreserved sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata eggs from the western Caribbean (Curaçao) with cryopreserved sperm from genetically distinct populations in the eastern and central Caribbean (Florida and Puerto Rico, respectively). We then confirmed interpopulation parentage in the Curaçao–Florida offspring using 19,696 single-nucleotide polymorphism markers. Thus, we provide evidence of reproductive compatibility of a Caribbean coral across a recognized barrier to gene flow. The 6-mo survival of AGF offspring was 42%, the highest ever achieved in this species, yielding the largest wildlife population ever raised from cryopreserved material. By breeding a critically endangered coral across its range without moving adults, we show that AGF using cryopreservation is a viable conservation tool to increase genetic diversity in threatened marine populations.
... Annual variation of seawater temperature and solar insolation may also influence spawning month (13)(14)(15). Spawning day is assumed to be determined by environmental factors that are controlled by the lunar cycle, such as moonlight and tidal fluctuations, as spawning generally occurs after the full moon (6,11,(16)(17)(18)(19) [some exceptions include Diploria labyrinthiformi, which spawns closer to the new moon (20)]. Corals have been separated into two groups depending on their spawning pattern (9), with one group regularly spawning several days after the full moon, while the other shows more irregularity in their spawning day, though still occurring around the full moon. ...
Synchronized mass coral spawning typically occurs several days after a full moon once a year. It is expected that spawning day is determined by corals sensing environmental change regulated by the lunar cycle (i.e., tide or moonlight); however, the exact regulatory mechanism remains unknown. Here, we demonstrate how moonlight influences the spawning process of coral, Dipsastraea speciosa . When corals in the field were shaded 1 and 3 d before the full moon or 1 d after the full moon, spawning always occurred 5 d after shading commenced. These results suggest moonlight suppresses spawning: a hypothesis supported by laboratory experiments in which we monitored the effects of experimental moonlight (night-light) on spawning day. Different night-light treatments in the laboratory showed that the presence of a dark period between day-light and night-light conditions eliminates the suppressive effect of night-light on spawning. In nature, moonrise gets progressively later during the course of the lunar cycle, shifting to after sunset following the day of the full moon. Our results indicate that this period of darkness between sunset and moonrise triggers synchronized mass spawning of D. speciosa in nature.
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Acropora cervicornis underwent massive mortalities in the Caribbean Sea and its populations have failed to recover after several decades. This study aimed to document the early life history of A. cervicornis from embryogenesis to symbiotic dinoflagellates acquisition. Gametes were collected in Islas del Rosario (Colombia) and a cross-fertilization was performed ex situ. A settlement experiment was performed including two treatments: smooth surfaces and rugose surfaces. Embryogenesis lasted for 63 h and larvae began to settle 8 days after fertilization. There were no significant differences in settlement between rugose (32% ± 16.59) and smooth (21% ± 11.45) surfaces. Survival on rugose surfaces was significantly lower (29% ± 11.71) compared to smooth surfaces (47% ± 35.02), due to the negative effect of sediment accumulation and turf algae. Seventeen days after fertilization 54% ± 4.13 of polyps acquired symbiotic dinoflagellates. This study contributes to the knowledge of early development of A. cervicornis in laboratory conditions, which complements restoration methods based on asexual reproduction.
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The rapidly advancing field of metabolomics encompasses a diverse suite of powerful analytical and bioinformatic tools that can help to reveal the diversity and activity of chemical compounds in individual organisms, species interactions, and entire ecosystems. In this perspective we use examples from studies of coral reefs to illustrate ways in which metabolomics has been and can be applied to understand coastal ecosystems. Examples of new insights that can be provided by metabolomics include resolving metabolite exchange between microbes and animals in holobiont tissues, identifying the relevant metabolite exchanges associated with the onset and maintenance of diverse bacterial endosymbionts, characterizing unknown molecules associated with coral reproductive cues, or defining the suites of compounds involved in coral-algal competition and microbialization of algal-dominated ecosystems. Here we outline sampling, analytical and informatic methods that marine biologists and ecologists can apply to understand the role of chemical processes in ecosystems, with a focus on open access data analysis workflows and democratized databases. This perspective aims to demonstrate that metabolomics tools and bioinformatics approaches which leverage open access chemical databases can provide scientists the opportunity to map detailed metabolic inventories and dynamics for a holistic view of the relationships among reef organisms, their symbionts and their surrounding marine environment.
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Coral spawning times have been linked to multiple environmental factors; however, to what extent these factors act as generalized cues across multiple species and large spatial scales is unknown. We used a unique dataset of coral spawning from 34 reefs in the Indian and Pacific Oceans to test if month of spawning and peak spawning month in assemblages of Acropora spp. can be predicted by sea surface temperature (SST), photosynthetically available radiation, wind speed, current speed, rainfall or sunset time. Contrary to the classic view that high mean SST initiates coral spawning, we found rapid increases in SST to be the best predictor in both cases (month of spawning: R2 = 0.73, peak: R2 = 0.62). Our findings suggest that a rapid increase in SST provides the dominant proximate cue for coral mass spawning over large geographical scales. We hypothesize that coral spawning is ultimately timed to ensure optimal fertilization success.
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Coral spawning on the oceanic reef systems of north-western Australia was recently discovered during autumn and spring, but the degree to which species and particularly colonies participated in one or both of these spawnings was unknown. At the largest of the oceanic reef systems, the participation by colonies in the two discrete spawning events was investigated over three years in 13 species of Acropora corals (n = 1,855 colonies). Seven species spawned during both seasons; five only in autumn and one only in spring. The majority of tagged colonies (n = 218) spawned once a year in the same season, but five colonies from three species spawned during spring and autumn during a single year. Reproductive seasonality was not influenced by spatial variation in habitat conditions, or by Symbiodinium partners in the biannual spawner Acropora tenuis. Colonies of A. tenuis spawning during different seasons separated into two distinct yet cryptic groups, in a bayesian clustering analysis based on multiple microsatellite markers. These groups were associated with a major genetic divergence (G”ST = 0.469), despite evidence of mixed ancestry in a small proportion of individuals. Our results confirm that temporal reproductive isolation is a common feature of Acropora populations at Scott Reef and indicate that spawning season is a genetically determined trait in at least A. tenuis. This reproductive isolation may be punctuated occasionally by interbreeding between genetic groups following favourable environmental conditions, when autumn spawners undergo a second annual gametogenic cycle and spawn during spring.
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Elkhorn coral (Acropora palmata) populations provide important ecological functions on shallow Caribbean reefs, many of which were lost when a disease reduced their abundance by more than 95% beginning in the mid-1970s. Since then, a lack of significant recovery has prompted rehabilitation initiatives throughout the Caribbean. Here, we report the first successful outplanting and long-term survival of A. palmata settlers reared from gametes collected in the field. A. palmata larvae were settled on clay substrates (substrate units) and either outplanted on the reef two weeks after settlement or kept in a land-based nursery. After 2.5 years, the survival rate of A. palmata settlers outplanted two weeks after settlement was 6.8 times higher (3.4%) than that of settlers kept in a land-based nursery (0.5%). Furthermore, 32% of the substrate units on the reef still harbored one or more well-developed recruit compared to 3% for substrate units kept in the nursery. In addition to increasing survival, outplanting A. palmata settlers shortly after settlement reduced the costs to produce at least one 2.5-year-old A. palmata individual from $325 to $13 USD. Thus, this study not only highlights the first successful long-term rearing of this critically endangered coral species, but also shows that early outplanting of sexually reared coral settlers can be more cost-effective than the traditional approach of nursery rearing for restoration efforts aimed at rehabilitating coral populations.
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Drivers of recruitment in sessile marine organisms are often poorly understood, due to the rapidly changing requirements experienced during early ontogeny. The complex suite of physical, biological and ecological interactions beginning at larval settlement involve a series of trade-offs that influence recruitment success. For example, while cryptic settlement within complex microhabitats is a commonly observed phenomenon in sessile marine organisms, it is unclear whether trade-offs between competition in cryptic refuges and predation on exposed surfaces leads to higher recruitment. To explore the trade-offs during the early ontogeny of scleractinian corals, we combined field observations with laboratory and field experiments to develop a mechanistic understanding of coral recruitment success. Multiple experiments conducted over 15 months in Palau (Micronesia) allowed a mechanistic approach to study the individual factors involved in recruitment: settlement behaviour, growth, competition, and predation, as functions of microhabitat and ontogeny. We finally developed and tested a predictive recruitment model with the broader aim of testing whether our empirical insights explained patterns of coral recruitment and quantifying the relative importance of each trade-off. Coral settlement was higher in crevices than exposed microhabitats, but post-settlement bottlenecks differed markedly in the presence (uncaged) and absence (caged) of predators. Incidental predation by herbivores on exposed surfaces at early post-settlement (<3 mm) stages and targeted predation by corallivores at late post-settlement (3-10 mm) stages exceeded competition in crevices as major drivers of mortality. In contrast, when fish were excluded, competition with macroalgae and heterotrophic invertebrates intensified mortality, particularly in crevices. As a result, post-settlement trade-offs were reversed, and recruitment was >2-fold higher on exposed surfaces than crevices. Once post-settlement bottlenecks were overcome, survival was higher on exposed surfaces regardless of fish exclusion. However, maximum recruitment occurred in crevices of uncaged treatments, being 9-fold higher than caged treatments. Overall, we characterise recruitment success throughout the earliest life-history stages of corals and uncover some intriguing trade-offs between growth, competition and predation, highlighting how these change and even reverse during ontogeny and under alternate disturbance regimes.
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Disease outbreaks have been involved in the deterioration of coral reefs worldwide and have been particularly striking among crustose coralline algae (CCA). Although CCA represent important cues for coral settlement, the impact of CCA diseases on the survival and settlement of coral planulae is unknown. Exposing coral larvae to healthy, diseased, and recently dead crusts from three important CCA species, we show a negative effect of disease in the inductive CCA species Hydrolithon boergesenii on larval survivorship of Orbicella faveolata and settlement of O. faveolata and Diploria labyrinthiformis on the CCA surface. No effect was found with the less inductive CCA species Neogoniolithon mamillare and Paragoniolithon accretum. Additionally, a majority of planulae that settled on top of diseased H. boergesenii crusts were on healthy rather than diseased/dying tissue. Our experiments suggest that CCA diseases have the potential to reduce the survivorship and settlement of coral planulae on coral reefs.
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Coral reefs are some of the oldest and most diverse ecosystems on our planet, yet throughout their range coral reefs are declining precipitously, mainly as the consequence of human activities. In situ conservation practices, such as habitat pres-ervation, are an important way to protect coral reefs. However, reefs now face global threats in addition to local impacts. It is therefore critical that ex situ conservation ac-tivities are incorporated into conservation practices for coral reefs. Many coral species reproduce sexually during a limited yearly breeding season. If the resulting larvae are cultured, their husbandry can be very time consuming: time that is often taken away from larval research. Three different types of fl ow-through larval rearing systems were designed and tested during breeding seasons of the elkhorn coral Acropora palmata, the mushroom coral Fungia scutaria, and the caulifl ower coral Pocillopora meandrina. The fl ow-through systems were tested against static bowl rearing, and no difference was observed in the survival of the larvae in two of the species: P 0.12 for A. palmata and P 0.99 for F. scutaria. These results suggested that these chambers may result in signifi cant savings of limited research time during a coral spawning event. However, P. meandrina larval survival was better in bowls than in the fl ow-through chamber (P 0.03). Rearing the maximum number of larvae possible with minimal maintenance will enhance opportunities for larval research, settlement, and growth. This is especially im-portant for species that are now threatened, for which time and information are critical during the breeding season.
Genetic subdivision within a species is a vital component of the evolution of biodiversity. In some species of Acropora corals in Western Australia, con-specific individuals spawn in two seasons six months apart, which has the potential to impede gene flow and result in genetic divergence. Genetic comparison of sympatric spring and autumn spawners of Acropora samoensis was conducted to assess the level of reproductive isolation and genetic divergence between the spawning groups based on multiple loci (13 microsatellite loci, the mitochondrial control region and two nuclear introns). Bayesian clustering and principal co-ordinates analysis of the microsatellite loci showed a high level of genetic differentiation between the spawning groups (F'ST = 0.30; P < 0.001), as did the sequence data from PaxC and Calmodulin (ΦST = 0.97 and 0.31, respectively). At the PaxC locus the autumn- and spring-spawners were associated with two ancient lineages that were separated by an evolutionary distance of 12.7%, over twenty times the level of divergence at the Calmodulin locus (0.5%). Statistical tests indicate divergent selection in PaxC, suggesting this gene may play a role in coral spawning. This study indicates that the autumn- and spring-spawners represent two cryptic species, and highlights the importance of asynchronous spawning as a mechanism influencing speciation in corals. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Initial conditions can generate differences in the biotic composition of spatially disjunct communities, but intense, large-scale perturbations have the potential to reduce or eliminate those historical differences. The latter possibility is of particular concern with respect to coral reefs, which have undergone dramatic changes in the last 25-30 years. This paper reports a case in which two reef systems with different biotic histories were recently perturbed to a single, novel state. We compared millennial-scale records of species dominance from reefs in Bahia Almirante, a coastal lagoon in northwestern Panama, to previously published records from reefs in the shelf lagoon of Belize. Reef cores extracted from Bahia Almirante at 5-10 in water depth revealed that the Panamanian reefs were persistently dissimilar from the Belizean reefs for at least 2000-3000 years prior to the last several decades. The Panamanian reefs were dominated continuously by branching finger corals, Porites spp. (primarily P. furcata). Shifts from the Porites-dominated state to dominance by other coral species were rare, were restricted to small areas, and lasted for decades to centuries. The Belizean reefs were dominated continuously by the staghorn coral Acropora cervicornis in the same depth range during the same period. Excursions from the Acropora-dominated state were again rare and spatially localized. Populations of Ac. cervicornis in the Belizean lagoon were nearly extirpated by an outbreak of white-band disease in the late 1980s, and changes in water quality were apparently detrimental to branching Porites in Bahia Almirante in recent decades. These large-scale perturbations caused the two reef systems to converge on a third, historically unprecedented state: dominance by the lettuce coral Agaricia tenuifolia. Ag. tenuifolia possesses life-history attributes and environmental tolerances that enabled it to become dominant in both disturbed ecosystems. Although the two phase shifts to Ag. tenuifolia differed in both their general mechanisms and specific causes, they had the effect of eliminating the salient difference in benthic composition between the Panamanian and Belizean reefs. The changes in species composition thus obliterated the influence of several thousand years of reef history.