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REPORT
The reproductive biology and early life ecology of a common
Caribbean brain coral, Diploria labyrinthiformis (Scleractinia:
Faviinae)
Vale
´rie F. Chamberland
1,2,3
•Skylar Snowden
3,4
•Kristen L. Marhaver
5
•
Dirk Petersen
3
•Mark J. A. Vermeij
1,2
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
Introduction
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.
&Vale
´rie F. Chamberland
chamberland.f.valerie@gmail.com
1
CARMABI Foundation, P.O. Box 2090, Piscaderabaai z/n,
Willemstad, Curac¸ao
2
Aquatic Microbiology, Institute for Biodiversity and
Ecosystem Dynamics, University of Amsterdam, Science
Park 700, 1098 XH Amsterdam, The Netherlands
3
SECORE International, Columbus Zoo and Aquarium,
9990 Riverside Drive, Powell, OH 43065, USA
4
Pittsburgh Zoo & PPG Aquarium, One Wild Place,
Pittsburgh, PA 15206, USA
5
University of California at Merced, 5200 North Lake Road,
Merced, CA 95340, USA
123
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
´re
´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
123
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
2
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
6
cells mL
-1
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
-1
) 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
2013).
Documentation of embryogenesis and planula
behavior
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
2
) 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
´re
´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
123
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
growth.
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
conditions.
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
123
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.
Results
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
0
10
20
30
Days after the full moon
M(ay)
J(une)
J(uly)
A(ugust)
A/S(eptember)
S/O(ctober)
0
10
20
30
40
50
9 1011121314
A M J J A A/S S/O O
Percentage of population observed
spawning
Moon cycle (2013)
no spawning
no spawning
ba 30
29
28
27
26
25
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
123
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), (c–j) S Snowden, (b) R Villaverde, (k–o) VF Chamberland
Coral Reefs
123
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
-1
(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:
F
2,225
=15.03, p\0.0001; 5 months: F
2,104
=7.71
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:
F
1,225
=2.35, p=0.127; 5 months: F
1,104
=0.74,
p=0.391).
Discussion
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
0
10
20
30
40
50
60
70
80
90
100
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
Settled
Dead
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
123
(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
0.0
0.1
0.2
0.3
0.4
0.5
0.6
521
Probability of survival (mean ±SE)
Time after outplant (months)
+N +N +N +N +N +N +N+N+N
a
a
a
a
a
a
a
a
a
a
a
a
b
b
b
b
bb
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
p\0.05
Coral Reefs
123
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
taxa.
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
123
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
-1
;
and Pseudodiploria strigosa: 0.4 mm month
-1
; 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
Foundation.
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