Marked annual coral bleaching resilience of an inshore patch reef in the Florida Keys: A nugget of hope, aberrance, or last man standing?
Marked annual coral bleaching resilience of an inshore patch reef in the Florida Keys: A nugget of hope, aberrance, or last man standing?
Brooke E. Gintert 0 1 2 3 4 5 6
Derek P. Manzello 0 1 2 3 4 5 6
Ian C. Enochs 0 1 2 3 4 5 6
Graham Kolodziej 0 1 2 3 4 5 6
Rene´e Carlton 0 1 2 3 4 5 6
Arthur C. R. Gleason 0 1 2 3 4 5 6
Nuno Gracias 0 1 2 3 4 5 6
Topic Editor Dr. Simon Davy 0 1 2 3 4 5 6
0 Atlantic Oceanographic and Meteorological Laboratories (AOML), NOAA , 4301 Rickenbacker Cswy., Miami, FL 33149 , USA
1 Department of Marine Geosciences, Rosenstiel School of Marine and Atmospheric Science, University of Miami , 4600 Rickenbacker Cswy., Miami, FL 33149 , USA
2 & Derek P. Manzello
3 Vicorob Institute, University of Girona , Girona , Spain
4 Department of Physics, University of Miami , 1320 Campo Sano Ave., Coral Gables, FL 33146 , USA
5 Khaled bin Sultan Living Oceans Foundation , Landover, MD , USA
6 Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric Science, University of Miami , 4600 Rickenbacker Cswy., Miami, FL 33149 , USA
Annual coral bleaching events, which are predicted to occur as early as the next decade in the Florida Keys, are expected to cause catastrophic coral mortality. Despite this, there is little field data on how Caribbean coral communities respond to annual thermal stress events. At Cheeca Rocks, an inshore patch reef near Islamorada, FL, the condition of 4234 coral colonies was followed over 2 yr of subsequent bleaching in 2014 and 2015, the two hottest summers on record for the Florida Keys. In 2014, this site experienced 7.7 degree heating weeks (DHW) and as a result 38.0% of corals bleached and an additional 36.6% were pale or partially bleached. In situ temperatures in summer of 2015 were even warmer, with the site experiencing 9.5 DHW. Despite the increased thermal stress in 2015, only 12.1% of corals were bleached in 2015, which was 3.1 times less than 2014. Partial mortality dropped from 17.6% of surveyed corals to 4.3% between 2014 and 2015, and total colony mortality declined from 3.4 to 1.9% between years. Total colony mortality was low over both years of coral bleaching with 94.7% of colonies surviving from 2014 to 2016. The reduction in bleaching severity and coral mortality associated with a second stronger thermal anomaly provides evidence that the response of Caribbean coral communities to annual bleaching is not strictly temperature dose dependent and that acclimatization responses may be possible even with short recovery periods. Whether the results from Cheeca Rocks represent an aberration or a true resilience potential is the subject of ongoing research.
Cheeca Rocks; Sea temperature heating weeks; Caribbean coral community mosaic; Acclimatization; Degree; Landscape
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Brooke E. Gintert and Derek P. Manzello have contributed equally to
this work.
Introduction
Annual coral bleaching is the greatest future threat to
global coral reef health. Mass coral bleaching, the
breakdown of the symbiosis between coral hosts and their algal
symbionts, occurs when ocean temperatures exceed their
long-term mean summer maximum by 1–2 C for more
than a month
(Hoegh-Guldberg 1999)
. If elevated
temperatures are sustained, coral mortality can occur. Coral
bleaching events have become more common and more
severe as ocean temperatures have increased due to global
climate change and are predicted to intensify over time
(Glynn 1993; Hoegh-Guldberg 1999; Hoegh-Guldberg
et al. 2007; Baker et al. 2008)
. Annual bleaching is
generally predicted to occur by 2050 for all reefs globally and
could occur as early as 2020 for the Florida Keys
(Manzello 2015)
.
Despite these concerns, coral bleaching events can have
a range of potential outcomes. In the worst case, severe
bleaching can lead to near 100% coral mortality with a loss
of reef structural complexity and ecosystem function, as
seen in the Gala´pagos Islands as a result of warming
associated with the 1982–83 El Nino-Southern Oscillation
(ENSO)
(Glynn 1990)
. On the other end of the spectrum,
corals can experience mild or ‘seasonal’ bleaching on an
annual basis with little to no mortality
(Fitt et al. 2000;
Baker et al. 2008)
. The response is generally dose
dependent, such that the greater the magnitude and duration of
the positive deviation from average summertime
temperatures, the greater the bleaching prevalence, severity, and
mortality. There are negative ramifications to thermal
stress and bleaching, even when corals survive the direct
impacts. Thermally stressed and bleached corals are more
disease susceptible, which can cause coral mortality for
years beyond the time period of the thermal anomaly
(Miller et al. 2009; Precht et al. 2016)
. Also, coral growth
and reproductive output can be suppressed for years after
bleaching
(Baird and Marshall 2002; Cantin and Lough
2014; Levitan et al. 2014)
.
Despite a growing consensus that coral reefs will likely
experience annual bleaching conditions across most reefs
before the century is out, very little is known about how
coral communities will respond under annual bleaching
scenarios. Recent experimental work has begun to address
the impacts of annual bleaching
(Grottoli et al. 2014;
Schoepf et al. 2015)
. Interestingly, the response of a given
coral species to a single bleaching event was not a good
predictor of back-to-back bleaching. Published field
observations of annual bleaching are limited thus far to the
Arabian Gulf (Riegl and Purkis 2015).
In 2014 and 2015, reefs of the Florida Keys experienced
successive years of thermal bleaching as part of the
2014–2016 global bleaching event
(NOAA Coral Reef
Watch 2015)
. Corals in southeast Florida and the Florida
Keys began experiencing coral bleaching in late August
2014 that was followed by a second year of bleaching in
2015
(NOAA Coral Reef Watch 2014, 2015)
. At Cheeca
Rocks, Florida Keys, a long-term monitoring station was
established in 2012 as part of NOAA’s National Coral Reef
Monitoring Program
(NOAA Coral Program 2014)
. Since
2012, yearly coral reef image mosaics were acquired over
six permanent reef sites to document detailed coral
community information for over 4000 coral colonies through
time. Here, we use these mosaics to document the impact
of and recovery from the 2014 and 2015 bleaching events
on the coral community at Cheeca Rocks under annual
bleaching conditions.
Methods
Mosaic surveys
Beginning in July 2012, six permanent 10 by 10 m plots
have been surveyed annually using image mosaics at
Cheeca Rocks (24.8977 N, 80.6182 W), which is a shallow
(depth range = 2–6 m) inshore patch reef in the Florida
Keys, offshore of Islamorada (Fig. 1). Each mosaic plot
was delineated using four permanent markers, one tag in
each corner of the 10 m 9 10 m plot. A GPS coordinate
was taken above each tag for geo-referencing and
relocation purposes. A mosaic survey was then performed over
the area delineated by the four corner markers. Plots were
relocated in subsequent surveys by relocating the corner
tags using printed mosaic maps to reduce searching time.
Coral colonies were followed through time based on their
geographic location within the mosaic image. Individual
tagging of coral colonies was not needed using the mosaic
survey method.
A mosaic image is a spatially explicit composite of
hundreds to thousands of down-looking images acquired
over the site. Dual Nikon D7000 cameras, one was set to a
wide angle (24 mm) and one was set to a smaller field of
view (56 mm), were used to capture images from
approximately 2 m above the reef substrate. The pixel footprint of
the wide-angle images is approximately 0.4 mm. Divers
swam the camera system in a dual lawn-mower pattern to
ensure high overlap of site images. Images from the 24-mm
camera were matched and blended into a spatially explicit
composite as described in
Lirman et al. (2007)
. The result
of the mosaic process is a high-resolution photographic
archive of all benthic organisms within the area of interest
that can be used to assess coral community health at the
time of the mosaic survey. Following the creation of the
landscape mosaic, images from the 56-mm camera are
matched to the frames of the landscape mosaic to create a
multilayer mosaic with links to high-resolution still images
as detailed in Gintert et al. (2009). The integrated mosaic
and high-resolution images are used to improve coral
species identification and health assessments as the pixel
footprint of the 56-mm images is approximately 0.18 mm.
During the summer of 2014, pale and partially bleached
corals were documented during annual monitoring at
Cheeca Rocks on August 11–12, 2014. Sea temperatures
surpassed temperatures coincident with past Florida
Keyswide bleaching events at the Molasses Reef Coastal Marine
Automated Network (C-MAN) station on August 14, 2014
(Manzello et al. 2007a)
, and severe bleaching was first
observed in Florida in late August. As a result, additional
bleaching-related mosaic surveys were performed on
September 16–17, 2014, and 6 months later on March
15–17, 2015, to document recovery. Surveys were
conducted during the second bleaching event on October 9,
2015. The follow-up mosaic surveys were performed on
July 11–12, 2016. An example of the mosaics collected at
Cheeca Rocks, Florida, during the 2014 and 2015
bleaching events is shown in Fig. 2.
Mosaic analysis
Initial mosaic images of the six reef plots from 2012 were
geo-referenced using real-world surface coordinates of
permanent site markers. Repeat mosaics were
geo-referenced to the initial mosaic image using permanent reef
features, such as large distinctive corals, that could be
identified by their location within the mosaic plot in
multiple mosaic images. A minimum of 10 of these common
points of interest were used for geo-referencing newly
acquired mosaic images to previous mosaic surveys.
Following geo-referencing, the 2D boundaries of all
coral colonies within the area of interest on each mosaic
image were manually traced to create a colony-specific
polygon in ArcGIS 10.1. For adjacent coral colonies of the
same species, an individual coral colony was identified
when there was no connection of tissue between two
colonies. Coral colonies were identified to species and
assessed for evidence of coral bleaching, disease, partial
and total mortality in each mosaic survey. Polygons of
corals that changed between years (mortality or growth)
were redrawn to reflect the areal extent of living coral
tissue at each survey time period. The severity of coral
bleaching was assessed visually from zoomed-in images
associated with the landscape mosaic. Coral colonies were
assigned to four categories based on the visual appearance
of the coral tissues. Corals that had no visual discoloration
or bleaching of tissues were characterized as not bleached.
Corals that had discoloration of the coral tissue, but did not
have any patches of bleached/white tissue were categorized
as pale. Coral color from the mosaics collected in 2012 and
2013 was used as a reference to differentiate non-bleached
from pale tissues. Corals that had patches of fully bleached/
white tissue that covered part, but not all of the coral
colony, were categorized as partially bleached, and any
coral in which all visible tissue was fully bleached was
categorized as bleached. Bleaching categories and visual
guidelines for distinguishing between bleaching categories
followed the Florida Reef Resilience Program guidelines
(FRRP 2011)
, and the same classification scheme was
applied to all survey years. The same two individuals
through time in successive mosaic surveys (Table 1). The
effects of bleaching in 2014 were evaluated by combining
the estimates of partial and total colony mortality assessed
from the March 2015 and October 2015 mosaic surveys.
Effects of the 2015 bleaching event were assessed from
analysis of mortality documented in the July 2016 mosaic
survey. Qualitative observations on August 23, September
29, and December 14, 2016, confirmed that there was no
appreciable bleaching or disease in 2016.
Temperature record
Temperature was measured every 3 h at the Cheeca Rocks
Moored Autonomous pCO2 buoy (MAP-CO2, depth = 1
m), from January 1, 2013, to December 31, 2016, using a
conductivity-temperature sensor (Model SBE-16 plus v.
2.2, Seabird Electronics). Temperature data were also
analyzed for the nearby Molasses Reef C-MAN station
(25.012 N, 80.376 W). The Molasses Reef C-MAN data
began in 1988 and extended through the end of 2015. A
redundant temperature sensor (Seabird SBE 56) was
attached to the C-MAN station in December 2013 and
provided data for 2016 when the C-MAN data stream was
non-continuous.
There were two small gaps in the Cheeca Rocks
temperature record from August 29 to September 3, 2015 (6 d
conducted all the visual scoring of the mosaic images and
worked together to ensure consistency.
A total of 4234 coral colonies were recorded, identified,
and digitized across the six sites in 2014 and were followed
gap), and May 5–12, 2016 (8 d). The 2016 space was filled
in with temperature data from a temperature probe (Seabird
SBE 56) that was affixed to the reef bottom (3 m)
approximately 250 m east of the buoy. The missing data in
2015 occurred because the buoy was pulled from the reef
due to Tropical Storm Erika. This gap is more problematic
given the decline in sea temperatures that occur with the
passage of tropical storms
(Manzello et al. 2007b)
. To
account for this, we applied the same day-by-day decline in
temperatures relative to August 28 measured at Molasses
Reef coincident with the storm to the Cheeca Rocks daily
average temperature on August 28. The maximum decline
observed during the storm was 0.4 C.
The maximum monthly mean (MMM) temperature of
the Molasses Reef climatology from 1988 to 2005 for
Molasses Reef is 29.9 C
(Manzello et al. 2007a)
. The
calculation of degree heating weeks (DHW) is based on
deviations of sea temperature C 1 C above the MMM
(Liu et al. 2006). However, when DHWs are calculated
based on the MMM value of 29.9 C ? 1 C, the
bleaching threshold of 4 DHW is a poor predictor of historical
bleaching. Instead, mass coral bleaching in the Florida
Keys has been correlated with monthly temperatures
C 30.4 C at Molasses Reef
(Manzello et al. 2007a)
. A
30.9 C bleaching threshold may be erroneously high due
to the fact that the Molasses Reef temperature record did
not begin until 1988 and there is evidence that significant
warming had already occurred in the Florida Keys by this
time
(Kuffner et al. 2015; Manzello 2015)
. Consequently,
we chose to use the observed bleaching threshold of
30.4 C, rather than the calculated theoretic value. We
made the assumption that the MMM is 29.4 C for
Molasses Reef, leading to DHW values for Molasses Reef
that correspond to past bleaching years when DHW [ 4
(Fig. 3a).
Given that we only have 4 yr of temperature data for
Cheeca Rocks, we cannot directly estimate a climatology
or MMM to calculate DHW. We noted that the maximum
running 30-d mean temperatures at Cheeca Rocks were
0.9 C greater than the Molasses Reef value for each year
that data overlapped (2013–2015). To estimate DHW for
Cheeca Rocks, we thus added 0.9 C to the Molasses Reef
estimated MMM to get 30.3 C, yielding a bleaching
threshold of 31.3 C for Cheeca Rocks.
Statistics
The study sampled the same corals repeatedly, and no new
corals were added to the sampled community between
surveys. To compare bleaching and mortality prevalence of
the entire coral community for the two bleaching events,
multivariate permutational analysis of dissimilarity was
conducted on the 15 most abundant corals. Species by
transect matrices were constructed for counts of colonies
for each visual bleaching score (not bleached, pale,
partially bleached, bleached) and mortality. All data were
square-root-transformed to minimize the influence of
disproportionally prevalent species. Analyses were run using
the adonis routine and R Studio
(Team R 2015)
. Years
(2014 vs. 2015 for bleaching; 2015 vs. 2016 for mortality)
and sites (n = 6) were included as factors to test for
significant differences in the two bleaching events, as well as
differences between sites.
For the remaining statistical tests, we only assessed
those eight species that were found at all six sites. To
compare coral cover from 2014 through 2016, a Friedman
test was used followed by Tukey post hoc tests. To
ascertain species-specific trends, we used paired t tests to
assess differences in bleaching and mortality as these data
conformed to the assumptions of a parametric test.
Univariate analyses were performed with SigmaPlot 12.
Results
Temperature
The hottest summer on record based on DHW for the 29-yr
Molasses Reef time series was 2015, followed by 2014
(Table 2, Fig. 3). Temperatures at Cheeca Rocks generally
track the trends observed at Molasses Reef, suggesting that
2014 and 2015 were likely similarly extreme events at
Cheeca Rocks (Fig. 3b). The DHW at both sites were
nearly identical in 2014 (7.7 DHW at Cheeca Rocks and
7.5 DHW at Molasses Reef), while Molasses Reef had 10.9
DHW in 2015 versus 9.5 at Cheeca Rocks. Cheeca Rocks
was warmer than Molasses in 2016 and reached 5.7 DHW.
Prevalence of bleaching and mortality
During the summer of 2014, 74.6% of all corals surveyed
exhibited some form of thermal stress (pale, partially
bleached, or bleached) (Fig. 4a). Orbicella annularis had
the highest bleaching prevalence in 2014 (74.1%),
followed by Porites porites (63.4%), Colpophyllia natans
(57.4%), and Diploria labyrinthiformis (48.3%) (Table 3).
Bleaching prevalence was significantly different between
2014 and 2015 (multivariate permutational analysis of
dissimilarity, p \ 0.01). The percentage of colonies
bleached in 2015 (mean ± SEM = 12.1 ± 4.15%) was 3.1
times less than 2014 (38.0 ± 8.38%). The prevalence of
paling was also different between years (p \ 0.05), but
followed an opposite pattern to bleaching. The prevalence
of pale colonies in 2015 (49.2 ± 5.28%) was 3.8 times
greater than in 2014 (12.7 ± 3.23%).
Molasses Reef
Cheeca Rocks
Year
2013
2014
2015
2016
2014 and 2015
warmest summers
on record
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Like bleaching, mortality was also less severe in 2015
than 2014. Total colony mortality was low following both
the 2014 (3.4% of all colonies) and 2015 (1.9%) bleaching
events (Table 4); 94.7% of colonies survived and
recovered in 2016. Partial mortality also declined from
2014 to 2015 with the percentage of corals that experienced
partial mortality dropping significantly from 17.6% in 2014
to 4.2% in 2015 (p \ 0.001) (Fig. 4b). In 2015, Orbicella
Jan-14
Jan-15
Jan-16
Fig. 3 a Time series of running 30-d mean seawater temperature
from Molasses Reef plotted against climatology and degree heating
weeks (DHW) since 1988, and b running 30-d mean temperatures and
DHW (dashed lines) for Cheeca Rocks and Molasses Reef from 2013
to 2016. Timing of surveys is indicated by gray bars. Asterisks
indicate bleaching observed
(a)
60
50
faveolata had the highest rates of partial mortality, with
43.9% of colonies exhibiting some partial mortality, but
only 0.9% of colonies died (Table 4). Over both years, this
species had the lowest rates of complete mortality. On the
other hand, the three species that had the highest rates of
complete mortality (P. porites, C. natans, and Porites
astreoides) also had high rates of partial mortality.
Seven of the eight species found at all sites had
significantly lower bleaching prevalence in 2015 (Fig. 5b,
Table 3). Only Siderastrea siderea had a slight increase in
bleaching in 2015 with total bleaching increasing from 1.0
to 1.6% of all colonies from 2014 to 2015. In general,
partial bleaching declined slightly (Fig. 3), but this was
only significant for S. siderea and P. astreoides. Partial
bleaching increased for O. annularis (Fig. 5b); this was the
only significant increase in bleaching or partial bleaching.
Partial and complete mortality declined for all of the
common species with only one exception (Fig. 6); more
colonies of P. astreoides died after the 2015 bleaching
event. All eight species had higher rates of paling in 2015,
and this was significant for 7 of the 8 species (Fig. 5c).
Fate tracking of coral colonies
Not only were declines in bleaching severity noted in the
prevalence data, but also fate tracking of the colonies that
bleached in 2014 further illustrated that bleaching was less
severe in 2015 (Fig. 7). Of the coral colonies that were
completely bleached in 2014, less than one-third (31.9%)
were completely bleached the following year (Fig. 7). The
same trend was documented for corals that were partially
Data for the 8 species found at each site are shown in order of relative abundance, as well as total data on the 15 most common species
SEM standard error of the mean
2015
Mean
SEM
Data for the 8 species found at each site are shown, as well as pooled data on the 15 most common species
bleached in 2014. The majority of partially bleached corals
from 2014 were either pale (57.1%) or not bleached
(18.9%) during the thermal stress of 2015. For corals
documented as pale in the summer of 2014, the majority
(74.6%) were documented as pale the following year, with
17.9% showing no visible signs of thermal stress in 2015
(Fig. 7). Only those colonies that were not observed with
visual signs of bleaching stress in 2014 had increased
bleaching prevalence in 2015. In this case, 65.6% of corals
that were not bleached in 2014 were pale in 2015. Only
5.0% of non-bleached corals in 2014 were found to be
either partially bleached or bleached in 2015 (Fig. 7).
The percentage of corals exhibiting partial mortality
declined within each group from 2014 to 2015 (Fig. 8).
Only 2.6% of the completely bleached corals in 2014
suffered complete mortality, and this declined to 1.2% in
2015 (Fig. 8). For corals that were partially bleached in
2014, 2.2% died following the 2014 event compared with
1.3% in the year following the 2015 event. The percentage
of corals documented as pale in 2014 and 2015 had similar
levels of total colony mortality between years (2.3 and
2.9%, respectively). Interestingly, those corals that did not
bleach in 2014 had the highest complete colony mortality
(5.7%).
Bleaching resistance and resilience
Corals that had no visible signs of bleaching (paling, partial
bleaching, or bleached) during both bleaching surveys were
labeled as bleaching resistant. Of the 4100 corals that were
assessed in both years, only 302 (7.4%) showed no signs of
bleaching during both bleaching surveys. Four common
species, Pseudodiploria clivosa, Pseudodiploria strigosa,
O. annularis, and D. labyrinthiformis, had 0% bleaching
resistance, meaning that all surveyed colonies of these
species were documented with some level of bleaching
stress over the 2-yr time period (Fig. 9). Orbicella franksi
was the most resistant species to thermal bleaching with
37.5% of the surveyed colonies showing no signs of
bleaching during either bleaching event. Only three other
coral species, Dichocoenia stokesi (25.7%), S. siderea
(24.3%), and Stephanocoenia intersepta (13.0%), had more
than 10% of their colonies that withstood the anomalously
high temperatures of 2014 and 2015 without signs of
bleaching (Fig. 9).
Bleaching resilience, defined here as the percentage of
colonies within a species that showed visual signs of
bleaching, including those that were partially bleached or
bleached, during the elevated temperatures of 2014 and
2015 without suffering total colony mortality, was [ 92%
for all fifteen of the most common coral species. Eight of
the 15 most common species had 0% complete mortality
which resulted in 100% bleaching resilience (Fig. 9). An
additional five species had between 95 and 100% species
resilience over the time period (Fig. 9). Only two species,
P. astreoides and P. porites, had more than 5% of colonies
suffer complete mortality (\ 95% bleaching resilience
between 2014 and 2016).
Coral cover
Mean coral cover declined 3.7% from 29.2% ± 2.97
(mean ± SE) to 25.5% ± 1.60 over the six permanent
plots between September 2014 and July 2016, which was
significant (Friedman’s test, X2 = 12, p \ 0.001) (Table 5).
This decline was significant for five of the eight most
common species: O. faveolata, S. siderea, P. astreoides, P.
porites, and Montastraea cavernosa. This was driven by
significantly lower coral cover in 2016 relative to cover
before bleaching in 2014 (Tukey post hoc tests, p \ 0.05).
Only M. cavernosa saw a significant decline in coral cover
after the first year of bleaching. Relative coral cover
20
0
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%
(
g-20
n
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c
lea -40
b
n
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eg-60
n
a
h
C-80
Fig. 5 Change in percentage of colonies that were a bleached,
b partially bleached, or c pale during the September 2014 and October
2015 surveys for those species found at all six sites. Asterisk indicates
significant difference. Species abbreviations: Ofav, Orbicella
faveolata; Ssid, Siderastrea siderea; Oann, Orbicella annularis; Past,
Porites astreoides; Cnat, Colpophyllia natans; Ppor, Porites porites;
Mcav, Montastraea cavernosa; Dlab, Diploria labyrinthiformis
increased for S. siderea, O. annularis, C. natans, M.
cavernosa, and D. labyrinthiformis following the bleaching
events of 2014 and 2015 (Table 5), but the order of relative
abundance did not change.
During the longest global bleaching event on record, we
found possible evidence for community-wide
acclimatization from annual coral bleaching at Cheeca Rocks in the
Florida Keys. Bleaching severity and partial mortality were
reduced for the vast majority of coral species following the
2015 event relative to 2014. Despite a 34% increase in
DHWs in the second year of bleaching at Cheeca Rocks in
2015, all but two of the 15 most common coral species had
reductions in bleaching and total mortality between years,
and all 15 had reduced partial mortality following the 2015
event when compared to 2014. The two species that had
Bleached in 2014
B in 2015
PB in 2015
P in 2015
NB in 2015
Complete
Mortality in
2015
Partial
Mortality in
2015
No Mortality
in 2015
Complete
Mortality in
2016
Partial
Mortality in
2016
No Mortality
in 2016
increases in bleaching prevalence (S. intersepta and
Siderastrea radians) were not abundant; they were not
observed at all sites and only made up B 0.2% of the total
coral cover. These species were also highly resistant to
bleaching in both years as \ 8% of all colonies bleached in
either year. Only two species of the fifteen most common
(P. astreoides and S. intersepta) experienced a slight
increase in total colony mortality in 2015; however, the
uptick was \ 2.0% for both these species when all other
species saw reductions in total colony mortality from 2014
to 2015.
Although the idea that corals can be less impacted by a
second bleaching event may seem counterintuitive, this has
been documented before in the eastern tropical Pacific, the
Great Barrier Reef, French Polynesia, SE Asia, the
Maldives, and Kenya
(Glynn et al. 2001; Maynard et al. 2008;
Thompson and van Woesik 2009; Guest et al. 2012;
Pratchett et al. 2013; McClanahan and Muthiga 2014;
McClanahan 2017)
. Other studies have reported the more
intuitive trend of compounded impacts from repeated
thermal stress events (e.g., Neal et al. 2016). All of these
studies, however, deal with bleaching events separated by
multiple years and are not representative of an annual
bleaching scenario. Annual bleaching and disease have
been documented in consecutive years in the Arabian/
Persian Gulf in which the combined effects of disease and
bleaching caused dramatic shifts in coral community
composition over time due to the differential susceptibility
of widespread coral species
(Riegl and Purkis 2015)
.
Riegl
and Purkis (2015)
documented 4 yr of mortality, but this
was initially driven by disease in the first 2 yr. Bleaching
prevalence in their study did not reach levels documented
herein until year three. While disease and temperature
stress are inarguably linked, the Arabian Sea example
Fig. 9 Proportion of corals showing bleaching resistance and
bleaching resilience during both the 2014 and 2015 thermally induced
bleaching events. Bleaching resistance is defined as percentage of
colonies that showed no signs of bleaching during either the 2014 and
the 2015 mosaic sampling events. Bleaching resilience is defined as
percentage of colonies that survived between September 2014 and
July 2016. Species abbreviations: Pcli, Pseudodiploria clivosa; Malc,
Millepora alcicornis; Cnat, Colpophyllia natans; Dlab, Diploria
labyrinthiformis; Dsto, Dichocoenia stokesi; Mcav, Montastraea
cavernosa; Ofra, Orbicella franksi; Ofav, Orbicella faveolata; Ssid,
Siderastrea siderea; Oann, Orbicella annularis; Sint, Stephanocoenia
intersepta; Srad, Siderastrea radians; Pstr, Pseudodiploria strigosa;
Past, Porites astreoides; Ppor, Porites porites
Data for the 8 species found at each site, as well as 15 most common species. Pre-bleaching data are 2014 and post-bleaching recovery data are
2016. SEM is standard error of the mean percent cover. Results of Friedman’s test and Tukey post hoc comparison if applicable. Tukey post hoc
column indicates years that were significantly different
P values abbreviated as follows: *\ 0.05; **\ 0.01; ***\ 0.001
aRepeated measures ANOVA used because data met assumptions, thus represents F value
SEM
4.27
appears to be a disease event that was then exacerbated by
the additive stressor of bleaching.
The community acclimatization and increased survival
noted during repeat bleaching at Cheeca Rocks has not
been observed for all species in experimental studies. Work
simulating annual bleaching conditions in Caribbean corals
found that species responses to back-to-back years of coral
bleaching had varied results, and species responses to a
single bleaching event were not predictive of results in the
following year
(Grottoli et al. 2014; Schoepf et al. 2015)
.
In these experiments, P. astreoides, a so-called winner that
was resilient to a single bleaching event, fared poorly in
terms of its physiological response when bleaching
occurred 2 yr in a row. Conversely, P. divaricata, a
bleaching ‘loser,’ was able to acclimatize and become a
winner, displaying minimal physiological stress in year
two.
The species-specific trends reported by
Grottoli et al.
(2014)
did not clearly play out at Cheeca Rocks. P.
astreoides experienced significantly less bleaching, partial
bleaching, and partial mortality in the second year at
Cheeca Rocks, FL. P. astreoides was, however, the only
species that experienced an increase in total colony
mortality during the second year of bleaching. P. divaricata, a
species that showed marked acclimatization in a second
year of simulated bleaching, is not found at Cheeca Rocks;
however, the related species P. porites
(Prada et al. 2014)
experienced significantly less bleaching and had lower
rates of partial and total mortality in 2015 when compared
to the previous year. P. porites and P. astreoides had the
lowest survival at Cheeca Rocks; 91.5 and 93.7% of
colonies survived, respectively. Thus, relative to the other
coral species, both poritids were losers, but still had high
survival rates over two consecutive years of bleaching.
The annual bleaching response of O. faveolata under
simulated conditions was more complex, as it was more
impacted in the second year of bleaching than the first, but
exhibited a quick recovery
(Grottoli et al. 2014)
. In our
study, O. faveolata exhibited less partial and complete
colony bleaching during the second bleaching event
(Fig. 5). Partial mortality declined from 45.6% in 2014 to
6.2% in 2015. Less than 1% of the O. faveolata colonies
died in 2014 or 2015 (Fig. 7). Overall, the majority of coral
species at Cheeca Rocks followed the pattern displayed by
O. faveolata, in which levels of bleaching and partial
mortality declined from 2014 to 2015, while total colony
mortality was limited in both surveyed years. As a result,
after 1 yr of recovery from annual bleaching, there were no
striking community-level divergence patterns observed
among the dominant coral species at Cheeca Rocks.
Although coral cover declined due to the multi-year
bleaching event from 29.2 to 25.5% across the six surveyed
plots, the relative dominance of the 15 studied species was
the same after the bleaching recovery in 2016 than before
bleaching began in 2014 (Table 3).
It is important to note that we are reporting colorimetric
determinations of bleaching and this is known to have
limitations because visual appearance does not always
conform to physiological performance
(Fitt et al. 2001;
Manzello et al. 2009)
. For example, Grottoli et al. (2014)
found that O. faveolata remained brown in color after the
second year of heat stress, but actually showed greater
physiological impairment than the first year when it turned
white. Future broad-scale surveys should incorporate tissue
sampling for measurement of zooxanthellae densities,
whenever possible, to better quantify coral bleaching.
Furthermore, the addition of standardized color charts
would also increase the robustness of visual scoring
(e.g.,
Siebeck et al. 2009)
. In spite of the limitations of visual
assessments as a signal of coral stress, there is evidence of
resilience at Cheeca Rocks, defined here as the ability of a
coral colony to survive repeated bleaching. Eight of the
fifteen most common corals at Cheeca Rocks had very high
resilience and suffered no total colony mortality between
2014 and 2016, with an additional five species having
[ 95% bleaching resilience over the survey period
(Fig. 9).
The recovery and resilience of corals to bleaching has
been linked to host genotype, shifts in symbiont types,
energy reserves, the ability of corals to supplement energy
demands with heterotrophy, high flow rates, and turbidity
(Edmunds 1994; Nakamura and van Woesik 2001; Baker
et al. 2004; Grottoli et al. 2014; Connolly et al. 2012; Guest
et al. 2016 and others)
. Resistance to bleaching can be
promoted by high thermal variability, thermal history of a
site, high dosages of photosynthetically active radiation
prior to thermal stress, and high cloud cover during times
of thermal stress
(Mumby et al. 2001; Brown et al. 2002;
Thompson and van Woesik 2009)
. It’s possible the patterns
observed in this study could be due to switching to more
heat-tolerant zooxanthellae types, like Symbiodinium
trenchii (D1a), in response to the 2014 bleaching
(e.g.,
LaJeunesse et al. 2009)
. Further study is necessary to
understand the role of symbiont type in the bleaching
dynamics at this site.
It is currently unknown how much the physical
environment of the study reef played in the acclimatization
potential of these corals. Cheeca Rocks is an inshore patch
reef with much higher living coral cover (29.2% in 2014)
than is found elsewhere in the Florida Keys and also the
wider Caribbean
(Gardner et al. 2003; Ruzicka et al. 2013)
.
Patch reef communities in the Florida Keys exist in an
environment that has greater fluctuations in temperature
and increased sedimentation, turbidity, and nutrients
relative to offshore reefs
(Lirman and Fong 2007)
. These
environmental characteristics are typically considered
detrimental to reef development, and yet inshore patch
reefs of the Florida Keys are healthier in terms of percent
coral cover, growth rates, and levels of partial mortality
relative to their offshore counterparts
(Lirman and Fong,
2007)
. These inshore reef sites also experience highly
variable seawater carbonate chemistry, with some of the
highest seasonal aragonite saturation state values ever
documented
(Manzello et al. 2012)
. Coral extension and
calcification of O. faveolata and P. astreoides are higher at
Cheeca Rocks relative to reefs offshore and showed a
marked resilience to previous coral bleaching events
(Manzello et al. 2015a, b)
.
Oliver and Palumbi (2011)
showed that conspecifics that
originate in environments with larger annual temperature
fluctuations have greater heat tolerance than corals that
originate from less fluctuating environments regardless of
symbiont type. The higher turbidity may also be a key
characteristic of Cheeca Rocks as a turbid reef site in
Singapore was shown to be highly resilient to bleaching
(Guest et al. 2016)
. A similar pattern occurred in Palau,
where coral bleaching and mortality were lower in
sheltered bays that experience higher temperatures and lower
irradiance due to high suspended particulate matter
(van
Woesik et al. 2012)
. Light data spanning the two bleaching
events at Cheeca Rocks are unavailable; thus, we cannot
rule out that reduced light in 2015 may have tempered the
bleaching response despite warmer temperatures.
Finally, surveys in 2015 took place later in the year than
they did in 2014 (Fig. 3b). It is possible that the lower
bleaching prevalence in 2015 could be due in part to
seasonally declining temperatures and dosages of light. In
other words, we may have surveyed the coral community
after some recovery had taken place, missing peak
bleaching prevalence. DHWs peaked at Cheeca Rocks
from September 14 to 18, 2015, at 9.5 -weeks. Our surveys
took place on October 9, which was indeed 3 weeks after
this peak. However, DHWs on October 9, 2015, were still
8.1 -weeks, higher than the maximum value reached in
2014 of 7.7 -weeks. Thus, while some recovery may have
taken place in the 3 weeks since peak DHWs, the DHW
values during the 2015 surveys were still greater than the
maximum values reached in 2014. The conclusions of this
study were not solely drawn from the visual surveys of
coral color, but were also based on the incidence of partial
and total colony mortality, both of which declined in 2015
despite higher thermal stress. Even with the limitations
associated with the colorimetric determination of bleaching
and later sampling in 2015, the lower rates of mortality
illustrate the reduced impact during the second year of
bleaching.
The results here provide a degree of tempered optimism,
or ‘nugget of hope,’ that annual coral bleaching may not
result in complete mortality due to compounded stress
events and small recovery periods. These data show that
acclimatization of an entire coral community is possible
under annual bleaching conditions, yet this was not enough
to prevent coral bleaching and mortality entirely in the
second year at Cheeca Rocks. In addition, it is currently
unknown if the multiple years of bleaching studied at
Cheeca Rocks have made the corals more susceptible to
other stressors such as coral disease or additional thermal
stress. Throughout south Florida, there is an ongoing coral
disease event that began coincident with the thermal stress
in 2014 that is having locally catastrophic consequences
(e.g., Precht et al. 2016)
. As of the time that this manuscript
was written, this disease event has yet to impact Cheeca
Rocks.
The coral community at Cheeca Rocks is admittedly
only one reef site that is a clear outlier to the wider trends
in the Florida Keys and Caribbean. Overall, Florida Keys’
reefs have deteriorated greatly since the late 1970s
(Dustan
and Halas 1987; Porter and Meier 1992)
. Coral cover on
offshore reefs is on average \ 5% and continues to decline
(Ruzicka et al. 2013). The disparity between Cheeca
Rocks, which maintained 25% coral cover after the two
warmest summers on record, with the state of reefs in the
wider Florida Keys is striking. This example could simply
be an example of aberrance, or a site that has not yet been
pushed past its particular resilience threshold. It is unclear
if this site could continue to exhibit the same level of
resilience and acclimatization under greater heat stress,
such as DHWs in excess of 10. If not, it may just be a
matter of time before this site experiences a level of heat
stress that causes mass coral mortality. Even with the
documented acclimatization, there was still a 3.7% decline
in coral cover from 2014 to 2016. If this reef loses 2% coral
cover per year under an annual bleaching scenario, then all
coral would be lost by attrition in roughly 13 yr at the
coverage levels in 2016 (25.5% mean coral cover,
Table 5). There would need to be an increase in bleaching
resilience or resistance of this community to persist with
bleaching every year for more than a decade.
The long-term resilience of inshore patch reef
communities in comparison with offshore reefs of the Florida Keys
suggests that these sites are important for understanding
coral resilience potential and can be informative for reef
management in an era of global change, especially if this
site proves to be resistant to the region-wide disease event
as well. Suboptimal environmental conditions appear to
lend some degree of resistance and resilience to bleaching
as has been shown in Singapore and Palau
(van Woesik
et al. 2012; Guest et al. 2016)
and suggest that these reef
sites likely deserve special attention. The next research step
is to try and unravel the biological versus environmental
factors that are leading to the resilience of the coral
community at Cheeca Rocks and compare/contrast the key
attributes with other sites around the globe.
Acknowledgements The authors thank NOAA’s Coral Reef
Conservation Program and Ocean Acidification Program for funding this
work as part of the National Coral Reef Monitoring Program. We
thank the Florida Keys National Marine Sanctuary for their support of
this work (Permits #FKNMS-2011-160 and FKNMS-2016-120).
J. Delaney of FKNMS provided valuable assistance with permitting.
The manuscript contents are solely the opinions of the authors and do
not constitute a statement of policy, decision, or position on behalf of
NOAA or the US Government.
Compliance with ethical standards
Conflict of interest All authors declare that there is no conflict of
interest.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://crea
tivecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
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