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Symbiont transmission and reproductive mode influence responses of three Hawaiian coral larvae to elevated temperature and nutrients


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Elevated temperatures and nutrients are degrading coral reef ecosystems, but the understanding of how early life stages of reef corals respond to these stressors remains limited. Here, we test the impact of temperature (mean ~ 27 °C vs. ~ 29 °C) and nitrate and phosphate enrichment (ambient, + 5 µM nitrate, + 1 µM phosphate and combined + 5 µM nitrate with 1 µM phosphate) on coral larvae using three Hawaiian coral species with different modes of symbiont transmission and reproduction: Lobactis scutaria (horizontal, gonochoric broadcast spawner), Pocillopora acuta (vertical, hermaphroditic brooder) and Montipora capitata (vertical, hermaphroditic broadcast spawner). Temperature and nutrient effects were species specific and appear antagonistic for L. scutaria and M. capitata, but not for P. acuta. Larvae survivorship in all species was lowest under nitrate enrichment at 27 °C. M. capitata and L. scutaria survivorship increased at 29 °C. However, positive effects of warming on survivorship were lost under high nitrate, but phosphate attenuated nitrate effects when N/P ratios were balanced. P. acuta larvae exhibited high survivorship (> 91%) in all treatments and showed little change in larval size, but lower respiration rates at 29 °C. Elevated nutrients (+N+P) led to the greatest loss in larvae size for aposymbiotic L. scutaria, while positive growth in symbiotic M. capitata larvae was reduced under warming and highest in +N+P treatments. Overall, we report a greater sensitivity of broadcast spawners to warming and nutrient changes compared to a brooding coral species. These results suggest variability in biological responses to warming and nutrient enrichment is influenced by life-history traits, including the presence of symbionts (vertical transmission), in addition to nutrient type and nutrient stoichiometry.
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Symbiont transmission and reproductive mode influence
responses of three Hawaiian coral larvae to elevated temperature
and nutrients
Rebecca M. Kitchen
Madeline Piscetta
Mariana Rocha de Souza
Elizabeth A. Lenz
Daniel W. H. Schar
Ruth D. Gates
Christopher B. Wall
Received: 20 December 2019 / Accepted: 10 February 2020
ÓSpringer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract Elevated temperatures and nutrients are degrad-
ing coral reef ecosystems, but the understanding of how
early life stages of reef corals respond to these stressors
remains limited. Here, we test the impact of temperature
(mean *27 °C vs. *29 °C) and nitrate and phosphate
enrichment (ambient, ?5lM nitrate, ?1lM phosphate
and combined ?5lM nitrate with 1 lM phosphate) on
coral larvae using three Hawaiian coral species with dif-
ferent modes of symbiont transmission and reproduction:
Lobactis scutaria (horizontal, gonochoric broadcast spaw-
ner), Pocillopora acuta (vertical, hermaphroditic brooder)
and Montipora capitata (vertical, hermaphroditic broadcast
spawner). Temperature and nutrient effects were species
specific and appear antagonistic for L. scutaria and M.
capitata, but not for P. acuta. Larvae survivorship in all
species was lowest under nitrate enrichment at 27 °C. M.
capitata and L. scutaria survivorship increased at 29 °C.
However, positive effects of warming on survivorship were
lost under high nitrate, but phosphate attenuated nitrate
effects when N/P ratios were balanced. P. acuta larvae
exhibited high survivorship ([91%) in all treatments and
showed little change in larval size, but lower respiration
rates at 29 °C. Elevated nutrients (?N?P) led to the
greatest loss in larvae size for aposymbiotic L. scutaria,
while positive growth in symbiotic M. capitata larvae was
reduced under warming and highest in ?N?P treatments.
Overall, we report a greater sensitivity of broadcast
spawners to warming and nutrient changes compared to a
brooding coral species. These results suggest variability in
biological responses to warming and nutrient enrichment is
influenced by life-history traits, including the presence of
symbionts (vertical transmission), in addition to nutrient
type and nutrient stoichiometry.
Keywords Coral reefs Larvae Nitrogen Phosphorus
Ka¯ne‘ohe bay Lobactis scutaria Pocillopora acuta
Montipora capitata
Coral reef ecosystems are threatened by global and local
stressors generated by anthropogenic activities [e.g., ocean
warming and acidification (Hughes et al. 2017; Smale et al.
2019), sedimentation (Rogers 1990) and nutrient enrich-
ment (D’Angelo and Wiedenmann 2014)]. In particular,
ocean warming from anthropogenic climate change is
rapidly contributing to the decline of coral reefs through
global episodes of coral bleaching (Hughes et al. 2017).
Bleaching is the disruption of the mutualistic interaction of
the coral and its endosymbiotic algae [family Symbio-
diniaceae (LaJeunesse et al. 2018)] and can cause high
coral mortality with cascading negative effects on the
Topic Editor Anastazia Banaszak
Electronic supplementary material The online version of this
article ( contains sup-
plementary material, which is available to authorized users.
&Christopher B. Wall
Marine Science Center, Northeastern University, 430 Nahant
Road, Nahant, MA 01908, USA
Rosenstiel School of Marine and Atmospheric Science,
University of Miami, 4600 Rickenbacker Causeway, Miami,
FL 33149, USA
Hawai‘i Institute of Marine Biology, University of Hawai‘i at
Ma¯ noa, 46-007 Lilipuna Road, Kaneohe, HI 96744, USA
Pacific Biosciences Research Center, University of Hawai‘i
at Ma¯ noa, 1933 East-West Rd., Honolulu, HI 96816, USA
Coral Reefs
function and services provided by reef ecosystems (Baker
et al. 2008; Figueiredo et al. 2014; Fisch et al. 2019).
Rising sea surface temperatures are also linked to
increasing frequencies of severe storm events worldwide
(Hoyos et al. 2006) with the potential to increase coastal
runoff and nutrient pollution on coral reefs. Freshwater
input and terrestrial runoff from storm events can cause
spikes in nitrogen and phosphorus levels in normally
oligotrophic coral reefs (Drupp et al. 2011). As reef-
building corals are adapted to nutrient-poor conditions,
nutrient enrichment from coastal runoff, agriculture and
sewage in the form of nitrate and phosphate can cause
localized reef degradation (Szmant 2002), decreased cal-
cification rates (Silbiger et al. 2018), disruptions in repro-
ductive and early life stages (Harrison and Ward 2001; Cox
and Ward 2002; Lam et al. 2015; Serrano et al. 2018) and
increased levels of coral disease and bleaching (Vega
Thurber et al. 2014). Shifts in seawater nutrient concen-
tration and/or their stoichiometric balance (i.e., moles of
nitrogen/moles of phosphate) can have different effects on
reef corals. For instance, elevated nitrate levels under low
phosphate (i.e., high N/P ratios) interfere with symbiont
function, causing phosphate starvation, lipid depletion and
photosynthetic malfunction, thereby lowering bleaching
thresholds in response to light and temperature (Wieden-
mann et al. 2013; Ezzat et al. 2016). However, mitigating
dissolved inorganic nutrient pollution and improving water
quality on coral reefs can reduce the sensitivity of corals to
thermal stress (Wooldridge and Done 2009). Therefore,
coastal nutrient concentrations may be central to under-
mining or supporting the physiological resistance of corals
to ocean warming and climate change.
Early developmental stages are vulnerable points in
coral life cycles, and environmental stressors may impact
coral larvae differently or to a greater degree compared to
adult colonies (Putnam et al. 2010). Corals sexually
reproduce by broadcast spawning (i.e., external fertiliza-
tion) or brooding (i.e., internal fertilization), and eggs or
larvae released can inherit symbionts either from their
parent or from the environment (i.e., vertical and horizontal
transmission, respectively). Larvae produced through
broadcast spawning and brooding receive significant par-
ental investment in the form of lipid energy reserves pro-
visioned in the biomass of spawned eggs (85% dry weight)
and brooded larvae (40–60% dry weight) (Harii et al.
2007,2010), and these reserves support the buoyancy,
dispersal and metabolism of larvae during planktonic
stages (Harii et al. 2007; Figueiredo et al. 2012). Consid-
ering the symbiosis between corals and Symbiodiniaceae is
nascent or yet to be established in early life stages, coral
larvae may be wholly (aposymbiotic) or partially (symbi-
otic) dependent on energy reserves for respiratory needs
during planktonic stages, early metamorphosis and
settlement. Early onset of symbiosis through vertical
transmission or rapid symbiont uptake by aposymbiotic
larvae confers the benefits of autotrophic nutrition (Harii
et al. 2007) and benefits post-settlement survival (Suzuki
et al. 2013). However, damage to symbiont photomachin-
ery within larvae by environmental stress (i.e., elevated
light, temperature, nutrient enrichment) creates reactive
oxidative stress and can reduce larvae survivorship (Baird
et al. 2006; Yakovleva et al. 2009). Thus, environmental
conditions, including nutrient enrichment, with the poten-
tial to disrupt the function or establishment of the coral–
Symbiodiniaceae symbiosis or influence coral larvae res-
piration (Edmunds et al. 2001), photosynthesis and energy
reserves catabolism (Rivest et al. 2017) can create energy
shortages with consequences for larval performance (e.g.,
growth, pelagic duration, settlement and survivorship)
(Nakamura et al. 2011).
Although many studies have tested the effects of tem-
perature and/or nutrient enrichment (i.e., nitrogen [nitrate,
ammonium, urea] or phosphate) on adult corals (as
reviewed by Fabricius 2005; Shantz and Burkepile 2014),
studies on the responses of early life stages of coral to
elevated temperature and/or nutrients are sparse and results
often inconclusive. For instance, in the broadcast-spawned
aposymbiotic larvae of Orbicella faveolata and Diploria
strigosa thermal stress increased larvae mortality (Bassim
and Sammarco 2003; Serrano et al. 2018) and increased O.
faveolata respiration (Serrano et al. 2018). However, in
brooded symbiotic larvae the respiration of Porites
astreoides both increased (Olsen et al. 2013) and remained
unchanged (Ross et al. 2012; Serrano et al. 2018)in
response to elevated temperatures. Similar variability has
been noted for Pocillopora damicornis, with elevated
temperatures increasing (Rivest and Hofmann 2014) and
decreasing (Putnam et al. 2013) respiration rates, possibly
due to a combination of environmental history effects on
parents (Rivest et al. 2017), parental energy investments
and maternal bet hedging (Edmunds et al. 2001; Cumbo
et al. 2013). In the few studies examining nutrient effects
on early life stages of corals, nitrate enrichment was shown
to increase respiration and settlement of brooded P.
astreoides larvae (Serrano et al. 2018). Elevated ammo-
nium also increased D. strigosa mortality and decreased
larval settlement, and these effects were additive with
elevated temperatures (Bassim and Sammarco 2003). Ele-
vated ammonium and phosphate impaired fertilization and
development of embryos in broadcast-spawning corals
Acropora longicyathus and Goniastrea aspera (Harrison
and Ward 2001), but nutrients (nitrate, ammonium and
phosphate) had no effect on the fertilization in A. millepora
(Humphrey et al. 2008). In part, uncertainty in nutrient
effects can originate in nutrient identity (i.e., ammonium,
nitrate, urea), their ecological sources (i.e., fish-derived
Coral Reefs
[ammonium], fertilizer runoff [nitrate]) (Shantz and Bur-
kepile 2014) and whether nitrogen enrichment is con-
comitant with phosphate limitations (Ezzat et al. 2016).
Considering nutrient enrichment interferes with the sym-
bionts’ ability to uptake nutrients (Ezzat et al. 2016),
maintain photochemical function (Wiedenmann et al.
2013) and remain within host tissues (Rosset et al.
2017a,b), it is reasonable that coral larvae responses to
nutrient enrichment may depend on the presence or
absence of Symbiodiniaceae. Therefore, modes of sym-
biont transmission (i.e., inherited in egg/larvae, acquired
from environment) and size or energy constraints imposed
on larvae from parental investments (i.e., broadcast
spawned, brooded) may be important factors in disentan-
gling previously inconsistent responses of coral larvae to
dissolve nutrients.
Here, we test the effects of thermal stress and nutrient
enrichment on the larvae of three Hawaiian coral species—
Lobactis scutaria (formerly Fungia scutaria [see Gitten-
berger et al. 2011]), Pocillopora acuta and Montipora
capitata—with different reproductive strategies and sym-
biont transmission modes. Lobactis scutaria and M. capi-
tata are broadcast spawners, while P. acuta is a brooder; L.
scutaria relies on horizontal transmission, while M. capi-
tata and P. acuta acquire symbionts through vertical
transmission (Fig. 1; Table 1). Coral reefs in Ka¯ne‘ohe
Bay have a history of anthropogenic disturbance (i.e.,
sewage pollution, urbanization) coupled with strong natural
stressors (i.e., history of thermal anomalies, high pCO
variance) (Bahr et al. 2015) which have created a model
system for studying resilience in corals. Based on the
current understanding of temperature and nutrient stress on
adults of these coral species and larval responses in other
studies, we tested the following hypotheses: (1) the com-
bined effects of temperature and nutrients will decrease
larval survivorship (Edmunds et al. 2001; Schnitzler et al.
2012; Graham et al. 2015; Serrano et al. 2018), respiration
rates (Putnam et al. 2013) and reduce larvae growth (Ed-
munds et al. 2005) and symbiont densities as is observed in
bleached corals; (2) elevated nutrients (nitrate and phos-
phate) will increase the density of DIN-limited endosym-
bionts in symbiotic larvae, but greater symbiont densities
will exacerbate effects of thermal stress (Fabricius 2005;
Cunning and Baker 2013; Shantz et al. 2016). We also
hypothesize that symbiotic larvae will be more sensitive to
nutrient (especially nitrate) enrichment than aposymbiotic
larvae, as endosymbiont populations will utilize nutrients
for growth (Falkowski et al. 1993; Ezzat et al. 2015). In
addition, a greater size and parental investment in brooded
larvae will result in less sensitivity to temperature stress
compared to smaller broadcast-spawned larvae (Baird et al.
Materials and methods
Gamete collection and larval rearing
Adult corals of L. scutaria (Lamarck 1801), P. acuta
(Lamarck 1816) and M. capitata (Dana 1846) originated
from patch reefs within Ka¯ne‘ohe Bay, Hawai‘i (HIMB
Special Activities Permit 2018, Division of Aquatic
Resources, Hawaii). Gametes or planulae were collected
from parent colonies, and all larvae were reared at the
Hawai‘i Institute of Marine Biology (HIMB, see Supple-
mental Material).
Gametes were collected from L. scutaria adults
(n= 153) on the night of 28 July 2018 and placed into
ambient-temperature, sand-filtered seawater in 19-L buck-
ets. Pooled eggs and sperm were concentrated in the
buckets and allowed to fertilize for 1 h. Remaining sperm
were removed by siphoning the bottom of the buckets, and
eggs were rinsed by replenishing with 1-lm filtered sea-
water (FSW). Embryos were left to develop in buckets
overnight. The following morning, ciliated larvae were
randomly selected and placed into treatment tubes (detailed
below). Adult P. acuta colonies (n= 30) were isolated on
July 30, 2019, into containers with ambient-temperature,
sand-filtered seawater that would flow into vessels with
153-lm mesh. Larvae released from 15 different parent
colonies were collected the following morning, evenly
mixed and placed into treatment tubes on the day of col-
lection. For M. capitata, positively buoyant egg–sperm
bundles released from adult colonies were collected in situ
from Ka¯ne‘ohe Bay on the night of August 10, 2018, using
a 123-lm mesh sieve. Gamete bundles were rinsed with
1-lm FSW in 9.5-L buckets, with one layer of bundles over
the surface of 2 L of FSW. Fertilization occurred in the
buckets for 1 h. Fertilized eggs were gently poured into 5-L
flow-through conical tanks filled with 1-lm ambient-tem-
perature FSW overnight under gentle water motion. M.
capitata larvae were placed into treatment tubes on the
following day once the embryos had reached the prawn
chip stage.
Experimental treatments and sampling
Ecologically relevant temperature treatments were selected
based on average sea surface temperatures during the
summer months in Ka¯ne‘ohe Bay (*27 °C) (NOAA
2019) and mean temperatures recorded during local
bleaching events (*29 °C) (Coles et al. 2018; Wall et al.
2019). Ambient nitrate and phosphate concentrations in
Ka¯ne‘ohe Bay during summer months are low, being ca.
0.5 and 0.1 lM, respectively (Drupp et al. 2011; Wall et al.
2019). Elevated nutrient concentrations (5.0 lM nitrate,
Coral Reefs
1.0 lM phosphate) were chosen based on peak annual
values measured in Ka¯ne‘ohe Bay, which often pulse and
subside during rainy season months (September–February)
(Drupp et al. 2011).
Larvae were exposed to two temperatures (mean of
*27 and 29 °C, AT and HT) and four nutrient concen-
trations (ambient, ?5lM nitrate [NO
], ?1lM phos-
phate [PO
] and combined ?5lM nitrate with ?1lM
phosphate), resulting in eight fully crossed treatments:
ambient-temperature ambient-nutrients (AT/A), high-tem-
perature ambient-nutrients (HT/A), ambient-temperature
high-nitrate (AT/N), high-temperature high-nitrate (HT/N),
ambient-temperature high-phosphate (AT/P), high-tem-
perature high-phosphate (HT/P), ambient-temperature
high-nitrate and phosphate (AT/NP) and high-temperature
high-nitrate and phosphate (HT/NP). For each species, five
0.5 mm
0.1 mm
1 mm
1 mm
Fig. 1 Adult and larvae of the
Hawaiian corals (a,b)Lobactis
scutaria and (c,d)Pocillopora
acuta, with Montipora capitata
(e) adult colonies, (f) eggs and
(g) planulae larvae. Settling P.
acuta larvae (d, top right).
Lobactis scutaria and M.
capitata are broadcast
spawners; P. acuta is a brooder.
Lobactis scutaria larvae are
initially aposymbiotic, while P.
acuta and M. capitata inherit
Symbiodiniaceae through
vertical transmission. (PC: all
authors, except [d: R. Ritson-
Coral Reefs
tube replicates (50-mL Falcon tubes) were used for each
treatment with an initial number of 40 larvae in each tube
replicate for L. scutaria and M. capitata (n= 1600) and 20
larvae in each tube replicate for the larger P. acuta larvae
(n= 800). Larvae of each species were exposed to these
treatments for 5 d, and water changes were conducted
daily. In order to expose all species to treatments for the
same duration, the length of the experiment was based on
approximately the length of time L. scutaria could be kept
alive without the uptake of algal symbionts (Schwarz et al.
1999), which was 4–5 d.
Temperature treatments were set up at HIMB in two
outdoor, shallow water tables with a shade cloth overhead.
Water tables received a steady flow of ambient Ka¯ne‘ohe
Bay seawater (ca. 26–27 °C) with the heated water
table having a 300-W submersible heater to raise temper-
atures 1–2 °C above ambient. Temperature in each tank
was recorded at 15-min intervals with HOBO Water
Temperature Pro v2 Data Loggers (Onset Computer, USA)
throughout the experiment with seawater table tempera-
tures monitored throughout each day using a certified
digital thermometer (5-077-8, accuracy = 0.05 °C, Control
Company, USA). The treatment tubes containing the larvae
were placed upside-down in racks within each water
treatment bath to minimize shading.
Dissolved nutrients analyses
Conical centrifuge tubes containing 45 mL of 0.2-lm FSW
were spiked with nutrient stock solutions (Milli-Q water
with sodium nitrate [NaNO
] to 0.2 mM NO
, and
sodium phosphate dibasic anhydrous [Na
] to 1.0 lM
) to obtain nutrient enrichment treatments (see
Supplemental Material). Measurements showed that nutri-
ent spikes did not alter salinity and pH values beyond
normal ranges for Ka¯ne‘ohe Bay (NOAA 2019) (Table S1).
Treatment seawater was changed daily, and outflow water
at the end of the first and final days of the experiment (Day
4 or 5) was saved from all tubes (n= 5 tubes species
confirm the spiked nutrient treatments remained above
ambient treatment concentrations for the 24-h incubations
between water changes (Table S2). Collected water sam-
ples were kept in a dark cooler on ice, filtered (0.7-lm GF/
F), frozen (-20 °C) and analyzed for nitrate ?nitrite
or N ?N) and phosphate concentrations
(Strickland and Parsons 1972; Parsons et al. 1984), with
] values reported for each treatment.
Biological response variables
Survivorship (i.e., percentage of larvae alive) in each
replicate tube was measured daily during water changes;
swimming larvae or settled spat were counted with the aid
of a dissecting microscope. Larval dark respiration was
measured on the last day of the experiment (L. scutaria
[Day 4], P. acuta and M. capitata [Day 5]) using PreSens
Measurement Studio software (PreSens Precision Sensing
GmbH, Germany) and noninvasive fluorescent oxygen
sensors (PreSens Sensor Spots) affixed on 2-mL glass vials
(n= 3–5 vials treatment
). Due to low sur-
vivorship, replicate tubes in each treatment were pooled for
L. scutaria and M. capitata, with ten larvae treatment
each respiration vial. P. acuta larvae exhibited high sur-
vivorship and were not pooled; instead, larvae (n= 10)
were randomly sampled from each of the five replicate
treatment tubes. Temperature treatments were maintained
using heat blocks, and temperature probes in separate
seawater–blank vials in each heat block were used to
monitor temperature during respiration measurements. P.
acuta and M. capitata larvae were dark adapted for
15–30 min, and respiration was measured in darkness, with
oxygen concentrations measured over 30–120-min inter-
vals to acquire a constant slope. Aposymbiotic L. scutaria
larvae were not dark adapted and had respiration measured
under indirect incandescent light. Final respiration rates
were corrected against seawater-only negative controls
Table 1 Details of the biological traits and reproductive strategies of the three species of Hawaiian corals studied (Lobactis scutaria, Pocil-
lopora acuta and Montipora capitata)
Species Growth form and sexuality Reproductive strategy Symbiont acquisition mode Initial larval size
mean ±SE)
L. scutaria Solitary, gonochoric Broadcast spawner Horizontal transmission: aposymbiotic larvae
acquire free-living symbionts 3–5 d after
spawning event (Schwarz et al. 1999)
47.42 ±0.02
P. acuta Colonial, hermaphroditic Brooder Vertical transmission: symbiotic, fully formed
larvae released from adults (Cumbo et al. 2013)
843.91 ±0.22
M. capitata Colonial, hermaphroditic Broadcast spawner Vertical transmission: eggs equipped with symbionts
that develop into symbiotic larvae once externally
fertilized (Padilla-Gamin
˜o et al. 2012)
219.00 ±0.07
Larval size at the beginning of the experiment
Coral Reefs
(n= 10), normalized by the number of larvae within each
vial and expressed as nmol O
Symbiont cell density for P. acuta and M. capitata was
measured by sonicating preserved larvae, vortexing and
resuspending concentrated algal cells and counting cells
using a hemocytometer (n= 6–8 replicate counts) and an
Olympus BX51 compound microscope (see Supplemental
Materials). Symbiont cell densities were normalized to the
number of larvae within each tube and are presented as
mean symbiont cells larva
To calculate the change in size, larvae were preserved in
diluted zinc formaldehyde fixative (1:4 Z-fix, Sigma-
Aldrich Inc., to 0.2-lm filtered seawater FSW) at the start
and the end of the experiment and stored at 4 °C. For each
species, we used two replicate sets of larvae (n= 10 larvae
) at the start of the experiment and 3–5 sets of larvae
at the end of the experiment. Larvae size at
each sampling point was quantified using MagnaFire
software and an Olympus SZX7 dissecting microscope
equipped with an Olympus America KIH036577 Micro-
scope Camera. Only larvae that were still intact within the
z-fix solution were included in the size analysis. Planar
area was calculated using ImageJ, version 1.51j8 (Schnei-
der et al. 2012).
Statistical analyses
Due to fundamental differences between the three species
studied, biological responses for each species were ana-
lyzed separately. Survivorship data were analyzed using a
Cox proportional hazards model using the survminer
package in R (Kassambara et al. 2019) with nutrient and
temperature treatments as fixed effects and replicate tube as
a random effect. The inclusion of random effects did not
alter model outputs and was dropped from the model.
Model assumptions were checked by testing and visualiz-
ing the Schoenfeld and Martingale residuals. Due to
complete mortality in one P. acuta HT/P tube, this tube
was removed from the analysis. Post hoc testing was
completed using the survival package (Therneau 2015).
Dark respiration and symbiont cell densities were ana-
lyzed with a linear model with nutrient and temperature
treatments as fixed effects; model assumptions were con-
firmed with Shapiro–Wilk and Levene’s tests. One outlier
was removed from both P. acuta and M. capitata respira-
tion rates data. L. scutaria respiration rates were not ana-
lyzed because the oxygen consumption rates for these
small larvae (n= 4–10 vial
) were low and indistin-
guishable from background controls. Post hoc testing was
completed using the emmeans package (Lenth 2019).
Larval size for each species was analyzed using Kruskal–
Wallis nonparametric tests with nutrient and temperature
treatments as fixed effects. Model assumptions were
checked through visualization of residuals, and post hoc
testing was completed using the Dunn test. All analyses
were completed in R, version 3.6.1 (R Core Team 2019).
Data and scripts are publicly available on GitHub https:// (Wall
Nutrient analyses
Mean seawater temperatures followed natural oscillations
throughout the day and averaged from 26.97 to 27.37 °Cin
the AT treatment and 28.72 to 29.17 °C in the HT treat-
ment (Table S1; Fig. 2). On average, daily maximum
temperatures were 28 °C and 31 °C in the AT and HT
treatments, respectively. Nutrients in ambient seawater had
mean (±SE, n= 8) [NO
] and [PO
] of 0.47 and
0.10 lmol L
, with nitrite contributing an additional
0.22 lmol L
. Nitrite concentrations remained low and
constant across all treatments (\0.5 lmol L
). Nutrient
treatments remained elevated during the 24-h incubations
between daily nutrient spikes, with similar nutrient
Temperature (°C)
cM. capitata
L. scutaria Ambient (27°C)
High (29°C)
P. acuta
Fig. 2 Seawater temperatures for three corals (a)Lobactis scutaria,
(b)Pocillopora acuta and (c)Montipora capitata exposed to
orthogonal ambient (27 °C) and high (29 °C) temperatures and four
orthogonal nutrient concentrations (Table S2). Dashed lines indicate
mean temperature for each treatment
Coral Reefs
concentrations in both temperature treatments (Table S2).
Instantaneous light levels measured across the seawater
table at midday averaged 70 ±9lmol photons m
(mean ±SE, n= 26) across experimental days.
Larval survivorship in M. capitata was the most sensitive
to treatment conditions, while P. acuta was the most tol-
erant. L. scutaria survivorship was low overall, with ca.
25–50% survivorship in all treatments within 48 h and
18–29% survivorship by day 4. Overall, L. scutaria sur-
vivorship was negatively affected by nutrient additions
(p\0.001), although nutrient effects were temperature
dependent (p= 0.003) and more pronounced at cooler
temperatures (Table 2, Fig. 3a; Fig. S3). Nitrate alone
reduced survivorship at both temperature treatments;
however, the combined ?N?P treatment increased sur-
vivorship at HT relative to the ambient nutrient control. For
P. acuta larvae, survivorship was impacted by both tem-
perature (p= 0.037) and nutrients (p= 0.003) (Table 2,
S3; Fig. 3b); although, these effects were negligible and
survivorship was [91% in all treatments. Similar to L.
scutaria,P. acuta larvae had the lowest survivorship (91%)
in the AT/N treatment and highest survivorship (98%) in
the HT/NP treatment.
Montipora capitata larval survivorship was the most
sensitive to treatment effects and was affected by temper-
ature, nutrients and their interaction (p\0.001) (Table 2,
S3; Fig. 3c). Overall, survivorship was significantly higher
at HT relative to AT (60% versus 44%) and was reduced by
20% in nitrate enriched treatments compared to all others.
Highest survivorship was observed under ambient nutrients
at HT (71%) and lowest under elevated nitrate at AT
(22%). Relative to nutrient controls, larval survivorship at
27 °C declined with elevated nitrate but increased under
elevated phosphate. Moreover, the negative effects of
nitrate at AT were ameliorated when nitrate and phosphate
were both elevated in the ?N?P treatment (55%). This
pattern contrasts with observations at HT, where M. capi-
tata survivorship declined in all nutrient-enriched treat-
ments, being lowest in treatments where nitrate was
elevated (i.e., HT/N, HT/NP).
Dark respiration rates were only assessed for P. acuta and
M. capitata due to low signal in L. scutaria larvae (see
Materials and Methods). Treatment effects were only seen
in P. acuta larvae which showed ca. 39% less oxygen
consumption when exposed to elevated temperature
(p\0.001) (Table 2, S4; Fig. 4a). Dark respiration rates
of M. capitata larvae were lower compared to those of P.
acuta, but were not affected by treatments (pC0.209)
(Fig. 4b).
Symbiont cell densities
Symbiodiniaceae cell densities normalized per larvae of P.
acuta were not affected by treatments (p= 0.262)
(Tables 2, S4; Fig. 3c). M. capitata symbiont densities,
however, were affected by nutrient treatments (p= 0.008)
(Table 2; Fig. 3d) and ranged between 2000 and 2400
symbiont cells larva
across all treatments. Nitrate- and
phosphate-enriched treatments had the highest densities
(23% and 21% above controls, respectively) with inter-
mediate densities (6% above controls) in the ?N?P
treatment (Fig. 4d).
Larval size
Changes in L. scutaria larvae size were influenced by
nutrients (p\0.001) and its interaction with temperature
(p\0.001). Mean larval size decreased in all treatments
Table 2 Summary of
significant statistics across all
biological metrics for the three
coral species studied
Species Effect Biological response
Survivorship Respiration Symbiont density Larval size
L. scutaria Temp 0.208 – 0.687
Nutrients < 0.001 –– < 0.001
Temp 9nutrients 0.003 –– < 0.001
P. acuta Temp 0.037 < 0.001 0.285 0.117
Nutrients 0.003 0.798 0.640 0.507
Temp 9nutrients 0.205 0.174 0.262 0.191
M. capitata Temp < 0.001 0.839 0.922 0.011
Nutrients < 0.001 0.902 0.008 0.002
Temp 9nutrients < 0.001 0.209 0.068 < 0.001
For complete statistical analyses output, see Supplemental Material
Dashes represent responses that were not measured
Coral Reefs
29°C +Nitrate
L. scutaria
aP. acuta M. capitata
27°C +Phosphate +N+P
Fig. 3 Survivorship for larvae of three coral species exposed to
ambient (solid lines) and high (dashed lines) seawater temperatures
and four nutrient concentrations of ambient (control) and elevated
nitrate (?N) and phosphate (?P) (Table 2). Symbols represent
significant effects (p\0.05) of temperature (asterisk), nutrients
(double tagger), or their interaction (section sign). Values are
mean ±SE (n= 35–200)
Nutrient Treatment
symbiont cells larva-1
0.2 ab
Ambient (27°C)
High (29°C)
P. acuta M. capitata
(nmol O2 consumed larva-1 min-1)
abb ab
Fig. 4 Coral larva (a,b) dark
respiration rates and (c,
d) symbiont cell densities for
Pocillopora acuta and
Montipora capitata in response
to orthogonal temperature and
nutrient treatments. Lobactis
scutaria respiration rates were
poorly resolved and larvae are
aposymbiotic (see Materials and
Methods). Symbols represent
significant effects (p\0.05) of
temperature (asterisk) or
nutrients (double tagger).
Values are mean ±SE
(n= 38–50)
Coral Reefs
by 57–72%, but the largest change in size significantly
different from ambient nutrient controls was observed in
both ?N?P treatments and the HT/P treatments (Fig. 5a).
In contrast, treatments had no significant effect on P. acuta
larval size (Tables 2, S5; Fig. 5b). For M. capitata, larvae
increased in size by 25–57% and this was influenced by
temperature (p= 0.011), nutrients (p= 0.002) and their
interaction (p\0.001). Change in M. capitata larval size
was on average 10% less in HT relative to AT and 7–20%
lower in nitrate or phosphate treatments compared to both
ambient nutrient controls and the ?N?P treatments, which
saw the greatest positive change in larvae size. The AT/A
treatment and the AT/NP treatments grew the most (ca.
56%), while the HT/N treatment grew the least (25%).
Growth rates of all other treatments were between these
two size classes (average percent changes ranging from 30
to 41%) and were not significantly different from one
another (Tables 2, S5, Fig. 5c).
We investigated the performance of three Hawaiian corals
with different symbiont transmission and reproductive
strategies to temperature and nutrient effects. Counter to
our initial hypotheses, a 2 °C elevation in temperature
alone or in combination with elevated nutrients did not
cause overly adverse effects in symbiotic species. In fact,
the naturally cycling elevated temperature regime used
here appeared to ameliorate some of the negative effects of
nutrients on the survivorship of the broadcast-spawned
larvae. Nitrate adversely affected both symbiotic and
aposymbiotic larvae. Phosphate exhibited a stronger neg-
ative effect on the aposymbiotic L. scutaria, and the
combination of ?N?P mitigated the harmful effects of
nitrate in most situations. We also show that the brooded P.
acuta larvae were more tolerant to treatment conditions,
displaying little change in survivorship and no discernible
change in symbiont cell density or larval size, but having
lower respiration rates at high temperature. These results
highlight the responsiveness of coral larvae to changes in
temperature and dissolved nutrients and suggest species-
specific responses may in part originate from fundamental
differences in life-history strategies and the presence of
Symbiodiniaceae in early life stages in relation to modes of
symbiont inheritance.
Thermal stress weakens coral–endosymbiont interac-
tions and reduces larval survivorship (Edmunds et al. 2001;
Randall and Szmant 2009; Schnitzler et al. 2012; Graham
et al. 2017; Serrano et al. 2018); however, the warm (and
variable) temperature treatments (*29 °C) in our study
positively affected larval survivorship and did not produce
lower symbiont densities relative to 27 °C. It should be
noted, however, that many previous studies used higher-
aab b
% change in larval area
Nutrient Treatment
P. acuta M. capitata
L. scutaria
Ambient (27°C)
High (29°C)
Fig. 5 Percent change in larvae size in three coral species in response to orthogonal temperature and nutrient treatments. Symbols (section sign)
represent significant treatment interactions (p\0.05), while letters indicate post hoc contrasts. Values are mean ±SE (n= 15–49)
Coral Reefs
temperature elevations than used in the current study and
revealed negative affects of warming on larvae. For
instance, in studies where temperature was [29 °C, L.
scutaria larvae were unable to establish symbiosis with
Symbiodiniaceae and mortality increased (31 °C) (Schnit-
zler et al. 2012). While P. damicornis larval survivorship
was unaffected by temperatures (27, 30, 32 °C), moderate
bleaching was observed at temperatures above 27 °C
(Haryanti et al. 2015). Here, we observed survivorship in
P. acuta to be resistant to temperature effects, while
aposymbiotic L. scutaria and symbiotic M. capitata larvae
had higher survivorship in the high-temperature treatment
(*29 °C). The absence of clear negative effects of ele-
vated temperature on larval survivorship in the three coral
species used in our study, however, should not be inter-
preted as evidence for negligible effects of rising sea sur-
face temperatures on corals and their offspring. Instead, the
positive effects of elevated temperature on larvae sur-
vivorship (primarily in M. capitata) may be attributed to
the variable thermal regimes mimicking diel temperature
cycles compared to stable treatments, or alternatively,
to the level of thermotolerance in corals from Ka¯ne‘ohe
Bay (Coles et al. 2018). For instance, adult and juvenile
corals exhibit different physiological responses to variable
conditions of temperature (Putnam et al. 2010; Mayfield
et al. 2012), and adult L. scutaria, P. damicornis and M.
capitata corals in Ka¯ne‘ohe Bay have become less sensi-
tive to elevated temperatures over the last 30 yr (Coles
et al. 2018). While our treatments reached daily tempera-
ture maximums of 30–32 °C, these early-stage larvae
appear well equipped to tolerate these high and variable
temperatures, although latent effects of elevated tempera-
ture may manifest post-settlement. Therefore, under eco-
logically relevant and oscillating temperature regimes,
larvae from broadcast-spawning coral species benefited
from small increases in temperature; however, this effect
was most pronounced if larvae had already formed sym-
biosis with Symbiodiniaceae.
Although responses to temperature were moderate,
nutrient enrichment had more pronounced effects. Nutri-
ent-enrichment effects were most negative for survivorship
of M. capitata larvae. Principally, nitrate enrichment re-
duced larval survivorship, whereas the effects of elevated
phosphate were more benign. This is consistent with the
findings of Rosset et al. (2017a,b) that stated high-nitrate/
low-phosphate (i.e., phosphate starvation) conditions are
more detrimental to adult coral survival than high-phos-
phate/low-nitrate conditions. Interestingly in the current
study, elevated nitrate and phosphate together did not
reduce larval survivorship, indicating that negative nutrient
enrichment effects are in part linked to nutrient stoi-
chiometry and the nitrate/phosphate (N/P) ratio. This fur-
ther suggests that phosphate starvation is a significant
driver of negative nutrient impacts on larval survivorship.
This may be especially true in symbiotic larvae, where
greater nitrate availability may weaken host regulation of
symbiont nutrient availability and the integrity of the
symbiosis (Falkowski et al. 1993; Ezzat et al. 2015). In
addition, Ezzat et al. (2016) displayed that adult coral
phosphate uptake increases during thermal stress while
nitrogen acquisition rates decline, suggesting a pivotal role
of phosphate in endosymbiont function. Our results, how-
ever, suggest the capacity for nutrient concentrations to
destabilize coral symbioses and increase thermal sensitivity
may require threshold concentrations or chronic exposures
to elevated nutrients beyond those applied in the current
One of the few studies comparing temperature and
nutrient effects on broadcast-spawned and brooded coral
larvae hypothesized the presence of symbionts in brooded
larvae of P. astreoides increased the sensitivity of this
species to elevated nitrate compared to the aposymbiotic O.
faveolata larvae (Serrano et al. 2018). Elevated nitrate
effects on Symbiodiniaceae can adversely affect a coral’s
thermal tolerance by lowering thresholds to light- and
temperature-induced bleaching (Wiedenmann et al. 2013;
Ezzat et al. 2016); however, temperature and nutrient
treatments in the present study did not reduce symbiont
densities. In fact, M. capitata symbiont densities were
marginally higher in nutrient-enriched treatments com-
pared to controls. In this context, nutrient concentrations
appear to have produced positive outcomes for Symbio-
diniaceae by increasing symbiont cell densities, with the
possibility that corals received more autotrophic nutrition.
However, these effects did not correlate with host fitness,
as the species most affected by temperature and nutrient
treatments (M. capitata) had lowest survivorship under
high nitrate, further highlighting the importance of nutrient
stoichiometry (Wiedenmann et al. 2013). These results
agree with Serrano et al. (2018) that vertical symbiont
transmission relates to nutrient sensitivity, but show these
effects are most significant in broadcast-spawning corals,
possibly due to the small larval size and lower stocks of
inherited energy reserves and symbiont cells compared to
Treatment effects on larval respiration rates were lim-
ited to the brooded larvae of P. acuta, which showed lower
respiration at higher temperatures. These rates were similar
to those measured in other pocilloporid brooded larvae
(Edmunds et al. 2011; Cumbo et al. 2013; Putnam et al.
2013) and adults (Courtial et al. 2018) and agree with the
general pattern of elevated temperature reducing photo-
synthesis/respiration (P/R) ratios in corals (Coles and
Jokiel 1977; Edmunds et al. 2005). Larval respiration may
show a hyperbolic relationship with temperature (Edmunds
et al. 2011), increasing to a threshold and decreasing
Coral Reefs
thereafter once thermal stress damages proteins and dis-
rupts cellular processes (Hochachka and Somero 2002). In
symbiotic larvae, temperature effects on metabolism may
also be influenced by reactive oxygen species generated by
Symbiodiniaceae leading to symbiont expulsion (Weis
2008), as well as larval death (Yakovleva et al. 2009). The
expression of symbiont proteins central in photosynthesis
(i.e., Rubisco) can also decline at elevated temperatures,
leading to energy deficits that may also influence metabolic
costs and respiration rates (Putnam et al. 2013). In our
study, considering the lack of temperature effects on
symbiont densities, lower P. acuta respiration rates at
elevated temperatures may be attributed to host responses
to temperature; however, temperature and nutrient effects
on coral energy usage and acquisition should be further
explored. Finally, the null effect of treatments on M. cap-
itata respiration indicates cellular metabolism in this spe-
cies is less sensitive to 2 °C temperature changes. It should
be noted, however, respiration rates in the present study
(nmol O
) are not normalized to units of
tissue biomass, and the temperature dependency coeffi-
cients (i.e., Q
) for biomass-normalized respiration rates
mg DW
) may not differ among coral species
or life stages at sub-stressful temperature ranges
(25–30 °C) despite differences in overall respiration rates
(Haryanti and Hidaka 2015). Therefore, the metabolism
and respiration rates of adult and juvenile corals may be
equally sensitive to changes in temperature below thermal
thresholds, but the ability for P. damicornis and P. acuta
(this study) larvae to lower respiration rates at high tem-
peratures may benefit larvae survivorship as a metabolic
cost-saving strategy (Haryanti and Hidaka 2015).
Although, the capacity for larvae to mitigate negative
effects of thermal stress may depend on environmental
history and biological attributes such as brood quality (i.e.,
energy reserves, size, competency) and maternal invest-
ments (Putnam et al. 2010; Cumbo et al. 2013).
Changes in larvae size were influenced by the interac-
tion of temperature and nutrients and these effects differed
substantially among species. Larval size in reef corals is
not a good indicator of survivorship (Nozawa and Okubo
2011); however, larger brooded larvae have the potential
for extended pelagic durations (100 d; Richmond 1987),
and we observed minimal changes in larvae size of brooded
P. acuta larvae compared to other species. Larvae size
declined by[50% in all treatments in L. scutatia, possibly
due to the lack of algal symbionts and complete reliance on
energy reserves to meet metabolic costs. Conversely, M.
capitata larval size increased over the 5-d experiment
(*20–50%). The positive change in larvae size may relate
to the lifecycle ontogeny in M. capitata, but could also be
an effect of these larvae inheriting symbionts from their
parents and benefitting from symbiont-derived autotrophy.
Indeed, algal symbionts can transfer 13–27% of photo-
synthates to the host larvae (Richmond 1981), and sym-
biont photosynthesis provides coral larvae with the
capacity to use their lipid energy reserves at lower rates
(Harii et al. 2010), potentially extending larval
Understanding the effect of predicted environmental
changes on coral larvae is essential to predict the success of
coral reefs worldwide. Here, we show the effects of
warming and nutrients are species specific, and were more
pronounced in symbiotic broadcast-spawning species,
affecting respiration, symbiont density and larval sur-
vivorship. Other long-lasting effects of these stressors
could manifest post-settlement, thereby compromising
coral recruitment (Randall and Szmant 2009; Ross et al.
2012; Humanes et al. 2017) and creating profound, long-
lasting effects on the health of coral reefs. Future studies
should include different coral species and test the response
of corals in different life stages to the combined effect of
multiple stressors predicted for future oceans such as
warming, nutrient enrichment and acidification.
Acknowledgements This study was funded by the Paul G. Allen
Family Foundation, Colonel Willys E. Lord and Sandina L. Lord
Endowed Scholarship, an NSF graduate research fellowship to
E.A.L., a Coordenac¸a
˜o de Aperfeic¸oamento de Pessoal de Nı
Superior—Brasil (CAPES) fellowship to M.R.S. and an Environ-
mental Protection Agency STAR Fellowship Assistance Agreement
(FP-91779401-1) to C.B.W. The views expressed in this publication
have not been reviewed or endorsed by the EPA and are solely those
of the authors. We thank the SOEST Laboratory for Analytical Bio-
geochemistry (SLAB) at the University of Hawai‘i at Ma¯noa for
assistance with the nutrient analysis. We would also like to thank K.
Hughes, J. Davidson, C. Drury, A. Huffmyer, C. Harris and D. Chee
for their support. This is HIMB contribution 1786 and SOEST con-
tribution number 10905. We dedicate this manuscript to the life and
legacy of our dear friend and mentor Dr. Ruth Gates.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflicts of
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Coral Reefs
... thermal performance on the fore reef in Mo'orea, French Polynesia. While there are numerous studies investigating how nutrient fluxes affect coral physiology (Fabricius 2005;Ezzat et al. 2016;Kitchen et al. 2020), there is limited information on the effects of low nutrient exposure on the thermal performance of corals (Wiedenmann et al. 2013;D'Angelo and Wiedenmann 2014). The goal of this study was to investigate how in situ, chronic, low-level nutrient enrichment influences (1) the ability for endosymbiont and coral host response variables to contribute to the metabolic functionality of the holobiont and (2) how coral thermal performance metrics shift in response to different nutrient regimes. ...
... We extracted TPC metrics including (1) acute thermal optimum (T opt ), which is the temperature at which the organism is at its (2) maximal rate of performance (l max ), and (3) the rate at a reference temperature (b(T c )) which is often used to compare standardized rates of performance across populations (Angilletta Jr. 2009; Andrews and Schwarzkopf 2012), species (Dell et al., 2011;Sinclair et al., 2012;Bestion et al., 2018), or geographic regions (Angilletta Jr. 2009;Sgrò et al., 2010;Aichelman et al., 2019;Jurriaans and Hoogenboom, 2019;Silbiger et al., 2019). Based on prior research on the relationship between nutrient enrichment and the physiological response of corals to thermal stress (Ezzat et al. 2016;Morris et al. 2019;Kitchen et al. 2020;Krueger et al. 2020), we hypothesized that chronic low-level nutrient enrichment (i.e., nitrogen and phosphorus) will increase endosymbiont densities, chlorophyll a content, tissue biomass, and N content, shift endosymbiont community composition, and result in increased thermal performance of corals (D'Angelo and Wiedenmann 2014; Morris et al. 2019). ...
... Nutrient cycling within the coral holobiont-which includes the algal endosymbionts, microbial communities, and the coral host-is complex. Many studies have investigated the direct and indirect effects of nutrient enrichment on coral reef ecosystems and indicate that endosymbiont population densities are a key factor determining coral performance (Cunning and Baker 2013;Wiedenmann et al. 2013;D'Angelo and Wiedenmann 2014;Cunning et al. 2017;Rosset et al. 2017;Kitchen et al. 2020). A recent study showed that endosymbionts can alter their photophysiology to maintain coral productivity and host nutrition stability over a range of endosymbiont densities (Krueger et al. 2020). ...
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Global- and local-scale anthropogenic stressors have been the main drivers of coral reef decline, causing shifts in coral reef community composition and ecosystem functioning. Excess nutrient enrichment can make corals more vulnerable to ocean warming by suppressing calcification and reducing photosynthetic performance. However, in some environments, corals can exhibit higher growth rates and thermal performance in response to nutrient enrichment. In this study, we measured how chronic nutrient enrichment at low concentrations affected coral physiology, including endosymbiont and coral host response variables, and holobiont metabolic responses of Pocillopora spp. colonies in Mo'orea, French Polynesia. We experimentally enriched corals with dissolved inorganic nitrogen and phosphate for 15 months on an oligotrophic fore reef in Mo'orea. We first characterized symbiont and coral physiological traits due to enrichment and then used thermal performance curves to quantify the relationship between metabolic rates and temperature for experimentally enriched and control coral colonies. We found that endosymbiont densities and total tissue biomass were 54% and 22% higher in nutrient-enriched corals, respectively, relative to controls. Algal endosymbiont nitrogen content cell−1 was 44% lower in enriched corals relative to the control colonies. In addition, thermal performance metrics indicated that the maximal rate of performance for gross photosynthesis was 29% higher and the rate of oxygen evolution at a reference temperature (26.8 °C) for gross photosynthesis was 33% higher in enriched colonies compared to the control colonies. These differences were not attributed to symbiont community composition between corals in different treatments, as C42, a symbiont type in the Cladocopium genus, was the dominant endosymbiont type found in all corals. Together, our results show that in an oligotrophic fore reef environment, nutrient enrichment can cause changes in coral endosymbiont physiology that increase the performance of the coral holobiont.
... The overarching goal was to investigate how natural variation in nutrient and sediment loading influences (1) endosymbiont and coral host response variables, (2) holobiont metabolic response variables and thermal performance metrics (Topt, μmax, and b(Tc)) for gross photosynthesis (GP), dark respiration (Rd), and net light calcification (NC) , and (3) percent cover of P. acuta colonies. Based on what is known about coral-algal symbiosis dynamics (Cunning and Baker, 2013;Muller-Parker et al., 2015;Cunning et al., 2017), I hypothesized that elevated nutrients would increase endosymbiont densities and chlorophyll a content, but compromise host performance when exposed to thermal stress (Wiedenmann et al., 2013;Kitchen et al., 2020). Because nutrient and sediment loading have been found to negatively impact coral functionality (Rogers 1990, Fabricius 2005, I hypothesized that Topt, metabolic rate processes (GP, Rd, NC), performance measures (μmax, b(Tc)), and percent cover would decrease with increases in nutrient and sediment loading. ...
... For the coral response variables, the total tissue biomass (mg cm -2 ) was 22% higher at the enriched site compared to the control (F1,6 = 15.52, p < 0.01; Fig. 2 Cunning et al. 2017, Rosset et al. 2017, Kitchen et al. 2020. A recent study found that the photosynthetic oxygen production per symbiont cell over the observed endosymbiont density range (1 -9 symbiont cells per 500 µm 2 of gastrodermal cross-sectional area) was maintained due to adjustments in symbiont pigment and light utilization (Krueger et al. 2020). ...
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Coral reefs, some of the most diverse ecosystems in the world, face increasing pressures from global and local-scale anthropogenic stressors. Nutrient enrichment and sediment loading could make corals more vulnerable to global climate change by suppressing calcification and reducing their photosynthetic performance. Yet, some nutrient-enriched reef environments have exhibited higher coral growth rates, coral productivity, and coral thermal performance. To properly inform management in coastal coral reef ecosystems, a better understanding of warming and land-based inputs (i.e. sedimentation rates and nutrient loading) on coral reef ecosystems is necessary. This thesis is comprised of two studies that address the ecological and physiological influence of land-based inputs on two branching coral species to thermal stress. The first study tested how a natural nutrient and sedimentation gradient affected multiple facets of coral functionality, including algal endosymbiont and coral host response variables, holobiont metabolic responses, and percent cover of Pocillopora acuta colonies on the north shore fringing reefs in Mo'orea, French Polynesia. Algal endosymbiont % nitrogen content, algal endosymbiont densities, and total chlorophyll a content increased with nutrient input, while algal endosymbiont nitrogen content cell-1 decreased, likely representing competition among algal endosymbionts. Nutrient and sediment loading decreased coral metabolic responses to thermal stress in terms of their thermal performance and metabolic rate processes, and the percent cover of P. acuta colonies decreased by nearly two orders of magnitude along the nutrient gradient. The second study focused on the direct effects of nutrient enrichment on the thermal performance of corals on a fore reef in Mo’orea, French Polynesia. In this study, I measured how chronic nutrient enrichment affected coral physiology, including endosymbiont and coral host response variables, and holobiont metabolic responses of Pocillopora spp. colonies in Mo'orea, French Polynesia. I experimentally enriched corals with nitrogen and phosphorus combined for 15 months on the oligotrophic fore reef of Mo'orea. I first characterized symbiont and coral physiological traits due to enrichment and second used thermal performance curves to quantify the relationship between metabolic rates and temperature for experimentally enriched and control coral colonies. I found that the nutrient enriched corals endosymbiont densities, total chlorophyll a content, and tissue biomass were 54 %, 38 %, and 22 % higher, respectively, while algal endosymbiont nitrogen content cell-1 was 74 % lower relative to the control colonies. In addition, thermal performance metrics indicated that the maximal performance rate for gross photosynthesis was 29 % higher in enriched colonies, while the rate of metabolism at a reference temperature (26.8 °C) for gross photosynthesis was 33% higher compared to the control colonies. These findings illustrate that the relationship between land-based inputs, such as nutrient and sediment loading, and coral physiology is dependent on the local environmental context. Together these results help us better understand how local-scale stressors influence coral functionality and thermal performance in varying reef habitats. By understanding the complexities of coral-nutrient dynamics, research-based reef management approaches can be taken, particularly on where to mediate the influx of land-based inputs into coastal coral reef ecosystems.
... Yet, the effects of nutrients on coral bleaching are complex (Lesser, 2021) and may vary with nutrient type, concentration, stoichiometry, and the duration of exposure Kitchen et al., 2020). For example, persistently high nutrient concentrations may lead to corals increasing their tissue thickness (Barkley et al., 2018); a characteristic that often leads to higher resilience to thermal stress (Loya et al., 2001). ...
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The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.
... Varied responses to nutrient enrichment have additionally been documented in early coral life stages; these responses also vary according to nutrient stoichiometry, other abiotic environmental factors (such as heat, Humanes et al. 2017;Serrano et al. 2018), and life history (i.e., broadcast spawners vs brooders; Kitchen et al. 2020). However, the extent to which impacts of nutrient enrichment carry-over to the next generation through transgenerational effects has not been tested (but see Harrison and Ward 2001). ...
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Local-scale nutrient pollution can alter coral growth and reproductive output, as well as their resident communities of microorganisms (dinoflagellates in the family Symbiodiniaceae, bacteria). Yet, the ways in which nutrient pollution alters coral interactions with their microorganisms are not fully understood, and no studies have tested for transgenerational impacts of nutrient stress on coral holobionts. To investigate this, colonies of Pocillopora acuta were enriched with nitrate in situ for up to one year and monitored for planulation. Gene expression, resident microbial communities and holobiont traits were characterized in adults, as well as in planulae. Although separated by > 5 m, clonality and chimerism were observed in the majority of coral colonies. Lineage- and treatment-specific effects of nitrate treatment were detected in adults and planulae. Nitrate-enriched adults contained higher densities of Symbiodiniaceae and exhibited downregulation of genes involved in the synthesis of nitrogenous compounds. Planulae harbored higher Symbiodiniaceae and bacteria diversity than adults; this study constitutes the first assessment of these microorganisms from individual planulae. Coral-associated bacteria communities were Endozoicomonas-dominated and were not altered by nutrient treatment. Planula-associated bacteria communities differed from their parents but not from parental exposure to nutrients, and no changes in fecundity or settlement success resulted from enrichment. Taken together, these findings suggest that adult corals acclimate to chronic nutrient pollution by harboring higher Symbiodiniaceae densities, with no observed negative effects on the subsequent generation.
... The overarching goal was to investigate how natural variation in nutrient and sediment loading influences (1) endosymbiont and coral host response variables, (2) holobiont metabolic response variables and thermal performance metrics [T opt , μ max and b(T c )] for gross photosynthesis (GP), dark respiration (R d ) and net light calcification (NC), and (3) percent cover of P. acuta colonies. Based on what is known about coral-algal symbiosis dynamics (Cunning and Baker, 2013;Muller-Parker et al., 2015;Cunning et al., 2017), we hypothesized that elevated nutrients would increase endosymbiont densities and chlorophyll a content, but compromise host performance when exposed to thermal stress (Wiedenmann et al., 2013;Kitchen et al., 2020). Because nutrient and sediment loading have been found to negatively impact coral functionality (Rogers, 1990;Fabricius, 2005), we hypothesized that T opt , metabolic rate processes (GP, R d , NC), performance measures [μ max , b(T c )], and percent cover would decrease with elevated nutrient and sediment loading. ...
Coral reefs, one of the most diverse ecosystems in the world, face increasing pressures from global and local anthropogenic stressors. Therefore, a better understanding of the ecological ramifications of warming and land-based inputs (e.g., sedimentation and nutrient loading) on coral reef ecosystems is necessary. In this study, we measured how a natural nutrient and sedimentation gradient affected multiple facets of coral functionality, including endosymbiont and coral host response variables, holobiont metabolic responses, and percent cover of Pocillopora acuta colonies in Mo'orea, French Polynesia. We used thermal performance curves to quantify the relationship between metabolic rates and temperature along the environmental gradient. We found that algal endosymbiont % nitrogen content, endosymbiont densities, and total chlorophyll a content increased with nutrient input, while endosymbiont nitrogen content cell-1 decreased, likely representing competition among the algal endosymbionts. Nutrient and sediment loading decreased coral metabolic responses to thermal stress in terms of their thermal performance and metabolic rate processes. The acute thermal optimum for dark respiration decreased, along with the maximal performance for gross photosynthetic and calcification rates. Gross photosynthetic and calcification rates normalized to a reference temperature (26.8 °C) decreased along the gradient. Lastly, percent cover of P. acuta colonies decreased by nearly two orders of magnitude along the nutrient gradient. These findings illustrate that nutrient and sediment loading affect multiple levels of coral functionality. Understanding how local-scale anthropogenic stressors influence the responses of corals to temperature can inform coral reef management, particularly on the mediation of land-based inputs into coastal coral reef ecosystems.
Prolonged thermal stress and high levels of solar irradiance can disrupt the coral-algal symbiosis and cause bleaching and lowered overall fitness that lead to the likely death of the cnidarian host. Adaptive bleaching and acclimatization of corals, which posits bleaching as an opportunity for the coral host to switch its currently susceptible endosymbionts to more stress-tolerant taxa, offers hope for survival of reefs amid rapidly warming oceans. In this study, we explored the diversity and distribution of coral-zooxanthellae associations in the context of geospatial patterns of sea surface temperature (SST) and thermal anomalies across the Philippine archipelago. Thermal clusters based on annual sea surface temperature means and each site’s frequency of exposure to heat stress were described using three-decade (1985–2018) remotely sensed data. Haphazard sampling of 628 coral fragments was conducted in 14 reef sites over 3 years (2015–2018). Using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) fingerprinting and sequencing of the zooxanthellae ITS2 region, we characterized endosymbiont diversity within four reef-building coral families across archipelagic thermal regimes. Consistency in dominant Symbiodiniaceae taxon was observed in Acropora spp., Porites spp., and Heliopora coerulea. In contrast, the family Pocilloporidae (Pocillopora spp., Seriatopora spp., and Stylophora pistillata) exhibited biogeographic variability in zooxanthellae composition, concordant with inferred occurrences of sustained thermal stress. Multivariate analyses identify two broad Pocilloporidae clusters that correspond with mean SST ranges and frequency of exposure to bleaching-level thermal stress which are largely supported by ANOSIM. Differences in zooxanthellae assemblages may reflect host-specific responses to ecological or environmental gradients across biogeographic regions. Such patterns of variability provide insight and support for the adaptability and potential resilience of coral communities in geographically and oceanographically complex regions, especially amidst the increasing severity of global and local-scale stressors.
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Anthropogenic emission of CO 2 into the atmosphere has been increasing exponentially, causing ocean acidification (OA) and ocean warming (OW). The “business-as-usual” scenario predicts that the atmospheric concentration of CO 2 may exceed 1,000 µatm and seawater temperature may increase by up to 3 °C by the end of the 21 st century. Increases in OA and OW may negatively affect the growth and survival of reef corals. In the present study, we separately examined the effects of OW and OA on the corals Acropora digitifera and Montipora digitata , which are dominant coral species occurring along the Ryukyu Archipelago, Japan, at three temperatures (28 °C, 30 °C, and 32 °C) and following four pCO 2 treatments (400, 600, 800, and 1,000 µatm) in aquarium experiments. In the OW experiment, the calcification rate ( p = 0.02), endosymbiont density, and maximum photosynthetic efficiency ( Fv/Fm ) (both p < 0.0001) decreased significantly at the highest temperature (32 °C) compared to those at the lower temperatures (28 °C and 30 °C) in both species. In the OA experiment, the calcification rate decreased significantly as pCO 2 increased ( p < 0.0001), whereas endosymbiont density, chlorophyll content, and Fv/Fm were not affected. The calcification rate of A. digitifera showed greater decreases from 30 °C to 32 °C than that of M. digitata . The calcification of the two species responded differently to OW and OA. These results suggest that A. digitifera is more sensitive to OW than M. digitata , whereas M. digitata is more sensitive to OA. Thus, differences in the sensitivity of the two coral species to OW and OA might be attributed to differences in the endosymbiont species and high calcification rates, respectively.
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Thermal stress is a major contributor to loss of coral cover, significantly impacting reefs during the third global bleaching event between 2014 and 2017. The long-term persistence of coral reefs depends on acclimatization and adaptation to changing climate, which are influenced greatly by the interactions between bleaching and reproductive success. We observed a genotypically diverse population of Orbicella faveolata before, during, and after consecutive bleaching events in 2014 and 2015 in the Florida Keys. We documented less bleaching during the second event despite 40% more time above local bleaching thresholds and an association between bleaching severity and subsequent spawning. Approximately 75% of colonies experienced the same or less severe bleaching in the second event despite being metabolically compromised, with a substantial minority (~ 35%) faring better in the second event. The second bleaching event also resulted in smaller decreases in chlorophyll content per symbiont cell and symbiont-to-host cell ratio reef-wide, representing less damage to the coral–algal symbiosis. All colonies that recovered quickly (~ 1 month) or did not bleach in 2014 released gametes in 2015, while only 60% of colonies that recovered more slowly did. Bleaching also impacted the amount of gametes released, with more severe bleaching significantly associated with gamete release from < 50% of the colony surface area. Bleaching and spawning outcomes were supported by dynamic physiological changes during bleaching and recovery. Lipid concentration and symbiont-to-host cell ratios collected from the bottom edge of the colony in the middle of the recovery period (February and April) were most important for predicting spawning the following year, highlighting the dynamic interaction between micro-habitats and time in recovery and gametogenesis. This study finds signals of physiological acclimatization in an important reef-building coral and underscores the importance of recovery post-bleaching and reproduction for the persistence of coral reefs.
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Ocean warming and the increased prevalence of coral bleaching events threaten coral reefs. However, the biology of corals during and following bleaching events under field conditions is poorly understood. We examined bleaching and postbleaching recovery in Montipora capitata and Porites compressa corals that either bleached or did not bleach during a 2014 bleaching event at three reef locations in Kāne‘ohe Bay, O‘ahu, Hawai‘i. We measured changes in chlorophylls, tissue biomass, and nutritional plasticity using stable isotopes (δ13C, δ15N). Coral traits showed significant variation among periods, sites, bleaching conditions, and their interactions. Bleached colonies of both species had lower chlorophyll and total biomass, and while M. capitata chlorophyll and biomass recovered 3 months later, P. compressa chlorophyll recovery was location dependent and total biomass of previously bleached colonies remained low. Biomass energy reserves were not affected by bleaching, instead M. capitata proteins and P. compressa biomass energy and lipids declined over time and P. compressa lipids were site specific during bleaching recovery. Stable isotope analyses did not indicate increased heterotrophic nutrition in bleached colonies of either species, during or after thermal stress. Instead, mass balance calculations revealed that variations in δ13C values reflect biomass compositional change (i.e., protein : lipid : carbohydrate ratios). Observed δ15N values reflected spatiotemporal variability in nitrogen sources in both species and bleaching effects on symbiont nitrogen demand in P. compressa. These results highlight the dynamic responses of corals to natural bleaching and recovery and identify the need to consider the influence of biomass composition in the interpretation of isotopic values in corals.
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The global ocean has warmed substantially over the past century, with far-reaching implications for marine ecosystems ¹ . Concurrent with long-term persistent warming, discrete periods of extreme regional ocean warming (marine heatwaves, MHWs) have increased in frequency ² . Here we quantify trends and attributes of MHWs across all ocean basins and examine their biological impacts from species to ecosystems. Multiple regions in the Pacific, Atlantic and Indian Oceans are particularly vulnerable to MHW intensification, due to the co-existence of high levels of biodiversity, a prevalence of species found at their warm range edges or concurrent non-climatic human impacts. The physical attributes of prominent MHWs varied considerably, but all had deleterious impacts across a range of biological processes and taxa, including critical foundation species (corals, seagrasses and kelps). MHWs, which will probably intensify with anthropogenic climate change ³ , are rapidly emerging as forceful agents of disturbance with the capacity to restructure entire ecosystems and disrupt the provision of ecological goods and services in coming decades. © 2019, The Author(s), under exclusive licence to Springer Nature Limited.
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Understanding which factors enhance or mitigate the impact of high temperatures on corals is crucial to predict the severity of coral bleaching worldwide. On the one hand, global warming is usually associated with high ultraviolet radiation levels (UVR), and surface water nutrient depletion due to stratification. On the other hand, eutrophication of coastal reefs increases levels of inorganic nutrients and decreases UVR, so that the effect of different combinations of these stressors on corals is unknown. In this study, we assessed the individual and crossed effects of high temperature, UVR and nutrient level on the key performance variables of the reef building coral Pocillopora damicornis. We found that seawater warming was the major stressor, which induced bleaching and impaired coral photosynthesis and calcification in all nutrient and UVR conditions. The strength of this effect however, was nutrient dependent. Corals maintained in nutrient-depleted conditions experienced the highest decrease in net photosynthesis under thermal stress, while nutrient enrichment (3 μM NO3⁻ and 1 μM PO4⁺) slightly limited the negative impact of temperature through enhanced protein content, photosynthesis and respiration rates. UVR exposure had only an effect on total nitrogen release rates, which significantly decreased under normal growth conditions and tended to decrease also under thermal stress. This result suggests that increased level of UVR will lead to significant changes in the nutrient biogeochemistry of surface reef waters. Overall, our results show that environmental factors have different and interactive effects on each of the coral’s physiological parameters, requiring multifactorial approaches to predict the future of coral reefs.
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The advent of molecular data has transformed the science of organizing and studying life on Earth. Genetics-based evidence provides fundamental insights into the diversity, ecology, and origins of many biological systems, including the mutualisms between metazoan hosts and their micro-algal partners. A well-known example is the dinoflagellate endosymbionts (“zooxanthellae”) that power the growth of stony corals and coral reef ecosystems. Once assumed to encompass a single panmictic species, genetic evidence has revealed a divergent and rich diversity within the zooxanthella genus Symbiodinium. Despite decades of reporting on the significance of this diversity, the formal systematics of these eukaryotic microbes have not kept pace, and a major revision is long overdue. With the consideration of molecular, morphological, physiological, and ecological data, we propose that evolutionarily divergent Symbiodinium “clades” are equivalent to genera in the family Symbiodiniaceae, and we provide formal descriptions for seven of them. Additionally, we recalibrate the molecular clock for the group and amend the date for the earliest diversification of this family to the middle of the Mesozoic Era (∼160 mya). This timing corresponds with the adaptive radiation of analogs to modern shallow-water stony corals during the Jurassic Period and connects the rise of these symbiotic dinoflagellates with the emergence and evolutionary success of reef-building corals. This improved framework acknowledges the Symbiodiniaceae’s long evolutionary history while filling a pronounced taxonomic gap. Its adoption will facilitate scientific dialog and future research on the physiology, ecology, and evolution of these important micro-algae.
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Ocean temperatures have been accelerating at an alarming rate mainly due to anthropogenic fossil fuel emissions. This has led to an increase in the severity and duration of coral bleaching events. Predicted projections for the state of reefs do not take into account the rates of adaptation or acclimatization of corals as these have not as yet been fully documented. To determine any possible changes in thermal tolerances, manipulative experiments were conducted to precisely replicate the initial, pivotal research defining threshold temperatures of corals nearly five decades ago. Statistically higher calcification rates, survivorship, and lower mortality were observed in Montipora capitata, Pocillopora damicornis , and Lobactis scutaria in the present study at 31 °C compared to the original 1970 findings. First whole colony mortality was also observed to occur sooner in 1970 than in 2017 in M. capitata (3 d vs. 15 d respectively), L. scutaria (3 d vs. 17 d), and in P. damicornis (3 d vs. 13 d). Additionally, bleaching occurred sooner in 1970 compared to the 2017 experiment across species. Irradiance was an important factor during the recovery period for mortality but did not significantly alter calcification. Mortality was decreased by 17% with a 50% reduction in irradiance during the recovery period. These findings provide the first evidence of coral acclimatization or adaptation to increasing ocean temperatures for corals collected from the same location and using close replication of the experiment conducted nearly 50 years earlier. An important factor in this increased resistance to elevated temperature may be related to removal of the discharge of treated sewage into Kāne‘ohe Bay and resulting decrease in nitrification and eutrophication. However, this level of increased temperature tolerance may not be occurring rapidly enough to escape the projected increased intensity of bleaching events, as evidenced by the recent 2014 and 2015 high coral mortality in Hawai‘i (34%) and in the tropics worldwide.
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There is a long history of examining the impacts of nutrient pollution and pH on coral reefs. However, little is known about how these two stressors interact and influence coral reef ecosystem functioning. Using a six-week nutrient addition experiment, we measured the impact of elevated nitrate (NO-3) and phosphate (PO3-4) on net community calcification (NCC) and net community production (NCP) rates of individual taxa and combined reef communities. Our study had four major outcomes: (i) NCC rates declined in response to nutrient addition in all substrate types, (ii) the mixed community switched from net calcification to net dissolution under medium and high nutrient conditions, (iii) nutrients augmented pH variability through modified photosynthesis and respiration rates, and (iv) nutrients disrupted the relationship between NCC and aragonite saturation state documented in ambient conditions. These results indicate that the negative effect of NO-3 and PO3-4 addition on reef calcification is likely both a direct physiological response to nutrients and also an indirect response to a shifting pH environment from altered NCP rates. Here, we show that nutrient pollution could make reefs more vulnerable to global changes associated with ocean acidification and accelerate the predicted shift from net accretion to net erosion.
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The effects of multiple stressors on the early life stages of reef-building corals are poorly understood. Elevated temperature is the main physiological driver of mass coral bleaching events, but increasing evidence suggests that other stressors, including elevated dissolved inorganic nitrogen (DIN), may exacerbate the negative effects of thermal stress. To test this hypothesis, we investigated the performance of larvae of Orbicella faveolata and Porites astreoides, two important Caribbean reef coral species with contrasting reproductive and algal transmission modes, under increased temperature and/or elevated DIN. We used a fluorescence-based microplate respirometer to measure the oxygen consumption of coral larvae from both species, and also assessed the effects of these stressors on P. astreoides larval settlement and mortality. Overall, we found that (1) larvae increased their respiration in response to different factors (O. faveolata in response to elevated temperature and P. astreoides in response to elevated nitrate) and (2) P. astreoides larvae showed a significant increase in settlement as a result of elevated nitrate, but higher mortality under elevated temperature. This study shows how microplate respirometry can be successfully used to assess changes in respiration of coral larvae, and our findings suggest that the effects of thermal stress and nitrate enrichment in coral larvae may be species specific and are neither additive nor synergistic for O. faveolata or P. astreoides. These findings may have important consequences for the recruitment and community reassembly of corals to nutrient-polluted reefs that have been impacted by climate change.