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\begin{document}

\title{Extinction debt of Gal\selectlanguage{ngerman}ápagos foundational coral associates: ENSO-related
cold-water bleaching triggers community biodiversity loss and turnover\selectlanguage{english}}



\author[1]{Olivia Rhoades}%
\author[2]{Margarita Brandt}%
\author[3]{Jon Witman}%
\affil[1]{The University of British Columbia Institute for the Oceans and Fisheries}%
\affil[2]{Universidad San Francisco de Quito Colegio de Ciencias Biológicas y Ambientales}%
\affil[3]{Brown University}%


\vspace{-1em}



  
  \date{May 27, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
During a cold La Ni\selectlanguage{ngerman}ña period (August 2007-January 2008) in the central
Galápagos archipelago, 70\% of Pocillopora finger corals were bleached
across three long-term monitoring sites, affording an opportunity to
examine the impact of El Niño Southern Oscillation-related temperature
anomalies on the persistence of these corals and their associated
community of fish and mobile macroinvertebrates. Using a time series
empirical approach, we tagged and tracked the fate of 96 coral heads and
their associates. When surveyed in July 2008, live (recovered) and dead
corals supported similar levels of randomized observed species richness
and Chao 1 estimated species richness. Whereas richness on the surviving
live corals remained fairly stable, Chao 1 estimated richness on dead
corals underwent a nearly 50\% increase between July and January 2009,
thereafter declining to 50\% of originally surveyed richness by February
2010. This nonlinear change in species richness was largely due to
influx and decline in opportunistic generalists including pencil urchin
bioeroders, gastropod snails, and hermit crabs that colonized dead
corals and fed on sessile invertebrates and algae that had initially
recruited to dead and undefended coral substrate. Thus, dead corals
retained high overall species richness until live corals had recovered;
after which richness declined as dead corals eroded and disappeared
(July 2011). Live corals attracted a less speciose but stable assemblage
of mutualistic xanthid crabs and fishes that increased in abundance over
time with the recovery and growth of live coral tissue. Overall, three
physical features of the finger coral habitats (coral vital status,
total surface area, and maximum branch length) predicted the number of
species associated with each colony. The delayed diversity loss of
associated species following La Niña disturbance to a foundation species
represents a local extinction debt of 32-49-month duration. A better
understanding of the scale of extinction debt in foundational marine
ecosystems is needed to quantify the breadth of impacts of climate
oscillations on biodiversity and ecosystem functioning.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\textbf{Title:} Extinction debt of Gal\selectlanguage{ngerman}ápagos foundational coral
associates: ENSO-related cold-water bleaching triggers community
biodiversity loss and turnover

\textbf{Short running title} : Extinction debt of Galápagos corals
associates

\textbf{Authors} : O. Kennedy Rhoades\textsuperscript{1,2,3}, Margarita
Brandt\textsuperscript{4,5}, and Jon D. Witman\textsuperscript{3}

\textsuperscript{1*} Hakai Institute, 1713 Hyacinthe Bay Road, Heriot
Bay, BC V0P 1H0 Canada; \textsuperscript{2*} Institute the Oceans and
Fisheries, University of British Columbia, Vancouver, British Columbia,
V6T 1Z4 Canada; \textsuperscript{3} Department of Ecology, Organismal
and Evolutionary Biology, Brown University, Providence, RI 02912
USA;\textsuperscript{4} Colegio de Ciencias Biológicas y Ambientales
COCIBA, Universidad San Francisco de Quito USFQ, Quito,
Ecuador;\textsuperscript{5} Galapagos Science Center GSC, Universidad
San Francisco de Quito USFQ \& University of North Carolina at Chapel
Hill UNC, Puerto Baquerizo Moreno, Galápagos, Ecuador

\textbf{*} Author's present address (not where work was carried out)

\textbf{Open Research Statement:}

Should the manuscript be accepted, the data supporting the results will
be archived in an appropriate public repository (Dryad, Figshare, or
Hal) and the data DOI will be included at the end of the article.

\textbf{Conflict of Interest:} The authors declare no competing
interest.

\textbf{Acknowledgements}

This work was funded by the United States National Science Foundation
(Award Numbers OCE-1061475, OCE-1450214 and OCE-1623867) to J. D.
Witman. We thank L. Dee for assistance in the field, J. Palardy for
assistance with preliminary data exploration, boat captains (L. Cruz and
W. Aguirre), others (N. Tirado, H. Jager, M. Romoleroux) at the Charles
Darwin Foundation and J. Suarez at Galápagos National Park for their
assistance. This research was performed under permits from the Galápagos
National Park and represents contribution number \_\_\_\_\_\_\_ from the
Charles Darwin Foundation for the Galápagos Islands.

\textbf{Abstract}

During a cold La Niña period (August 2007-January 2008) in the central
Galápagos archipelago, 70\% of \emph{Pocillopora} finger corals were
bleached across three long-term monitoring sites, affording an
opportunity to examine the impact of El Niño Southern
Oscillation-related temperature anomalies on the persistence of these
corals and their associated community of fish and mobile
macroinvertebrates. Using a time series empirical approach, we tagged
and tracked the fate of 96 coral heads and their associates. When
surveyed in July 2008, live (recovered) and dead corals supported
similar levels of randomized observed species richness and Chao 1
estimated species richness. Whereas richness on the surviving live
corals remained fairly stable, Chao 1 estimated richness on dead corals
underwent a nearly 50\% increase between July and January 2009,
thereafter declining to 50\% of originally surveyed richness by February
2010. This nonlinear change in species richness was largely due to
influx and decline in opportunistic generalists including pencil urchin
bioeroders, gastropod snails, and hermit crabs that colonized dead
corals and fed on sessile invertebrates and algae that had initially
recruited to dead and undefended coral substrate. Thus, dead corals
retained high overall species richness until live corals had recovered;
after which richness declined as dead corals eroded and disappeared
(July 2011). Live corals attracted a less speciose but stable assemblage
of mutualistic xanthid crabs and fishes that increased in abundance over
time with the recovery and growth of live coral tissue. Overall, three
physical features of the finger coral habitats (coral vital status,
total surface area, and maximum branch length) predicted the number of
species associated with each colony. The delayed diversity loss of
associated species following La Niña disturbance to a foundation species
represents a local extinction debt of 32-49-month duration. A better
understanding of the scale of extinction debt in foundational marine
ecosystems is needed to quantify the breadth of impacts of climate
oscillations on biodiversity and ecosystem functioning.

\textbf{Keywords} : species richness, foundation species, climate
oscillations, temperature anomalies, coral bleaching, generalists,
specialists

\par\null

\textbf{Main Text}

\textbf{Introduction}

Habitat-forming foundation species such as trees, grasses, salt marshes,
mangroves, kelp, seagrasses and corals have a disproportionately large
influence on other species through provisioning of shelter or food
(Dayton \& Hessler 1972), and by enhancing associated species diversity
(Witman 1985) and multiple ecosystem functions (Ellison et al. 2005,
Angelini et al. 2015). Although foundation species and mutualisms can
serve to buffer the effects of disturbances on natural communities
(Witman 1987, Ellison et al. 2005, Altieri et al. 2007), anthropogenic
impacts are reducing the abundance and distribution of foundation
species (Osland et al. 2013) and decreasing the diversity of associated
flora and fauna (Byrnes et al. 2011, Sorte et al. 2017), thereby
threatening community resilience and functioning (Chapin et al. 1997,
Duffy et al. 2015, De Boeck et al. 2018). Yet many aspects of
whole-community changes associated with disturbance-driven losses of
foundation species remain poorly understood, especially related to the
timing, pattern, and magnitude of associated species loss (Stella et al.
2011, Thomson et al. 2015). Importantly, changes in species abundance or
diversity of communities associated with foundation species may not
occur immediately after a disturbance, resulting in extinction debt, or
a significant time delay prior to the disappearance or local extinction
of a species from a particular habitat patch (Tilman et al. 1994,
Kuussaari et al. 2009, Watts et al. 2020). Problematically, assessing
post-disturbance community-wide biodiversity loss before extinction debt
has been paid could lead to incorrect estimation (usually an
underestimation) of the number and types of associated species
vulnerable to local extinction (Hanski \& Ovaskainen 2002, Watts et al.
2020).

Extinction debt occurs across diverse taxa associated with a range of
foundation species, though it remains poorly understood in marine
ecosystems. For example, the probability and timing of local extinction
differs across taxonomic groups, life history traits, and in the
relationship between associated species and the focal habitat created by
a foundation species (i.e., habitat specialists, generalists) (Kuussaari
et al. 2009, Hylander \& Ehrlén 2013, Watts et al. 2020). The time to
species loss after disturbance also depends on the size of the focal
habitat created by the foundation species and on the intensity of
disturbance (Hylander \& Ehrlén 2013). However, as compared with
plant-dominated terrestrial ecosystems, these and other aspects of
extinction debt remain poorly understood for marine ecosystems
(Kuussaari et al. 2009). Simulations of extinct debt in coral reefs (for
communities of 40 coral species) suggest that extinction debt of
associated invertebrates and fish was up to seven times higher relative
to that of terrestrial forests (Tilman et al. 1994) for the same level
of disturbance (Stone et al. 1996), potentially due to the high
diversity of associated species of invertebrates and fish (Idjadi \&
Edmunds 2006, Stella et al. 2011, Canizales-Flores et al. 2021).
Concerningly, given dramatic declines in coral reefs due to
climate-change related ocean warming, acidification, and disease
(Wellington et al. 2001, Hoegh-Guldberg \& Bruno 2010, Pandolfi et al.
2011, Glynn et al. 2017), extinction debt of coral-associated species
could lead to underestimates of the pace and extent of marine
biodiversity loss (Kuussaari et al. 2009).

Severe climate events can serve as natural field experiments for
examining the effects of climate change-related disturbances on marine
foundation species and associated species diversity (Byrnes et al. 2011,
Sorte et al. 2017), which may also be used to better understand
extinction debt in marine ecosystems. The El Niño Southern Oscillation
(ENSO) is a global climate event characterized by anomalously warm (El
Niño) and cold (La Niña) temperature fluctuations in Pacific ocean
temperatures (Holmgren et al. 2001, Trathan et al. 2007), which are
characterized by temperature anomalies that have increased in intensity
and duration with climate change (Cai et al. 2015), contributing to
declines in foundational kelps, seagrasses, and corals (Dayton et al.
1992, Campbell et al. 2011, Hughes et al. 2017). The growing
appreciation that the frequency and or magnitude of extreme climatic
events is increasing with global climate change underscores the
importance of investigating links among environmental stress, foundation
species and diversity change.

The Galápagos Archipelago is a place of unique marine biodiversity that
has been repeatedly subjected to extreme ENSO events, systematically
reducing coral cover (Glynn et al. 2018) and likely threatening coral-
and reef-associated species (Edgar et al. 2010). Sustained high
temperatures during the ENSO warming phases of 1982-1983 and 1997-1998
resulted in widespread loss of foundational scleractinian corals (95\%
and 27\% declines in cover, respectively) (Glynn 1984, Glynn et al.
2001). Heavy bioerosion of dead corals eliminated much of the reef
matrix, replacing patchy coral reefs with scattered coral heads (Glynn
1984, Glynn et al. 2001). Ongoing ENSO-related cold and warm phases
(2007 La Niña, 2010 El Niño) resulted in further stress-related coral
bleaching and death (Glynn et al. 2017, 2018). These ENSO events
dramatically affected many coral species, the most common of which are
habitat-forming finger corals (family Pocilloporidae), which typically
host a diverse assemblage of invertebrates and fishes (Abele 1976, Glynn
1984, Hickman 1999). These coral-associated species were likely
negatively affected by declines in continuous coral cover (Edgar et al.
2010), as well as potentially by ENSO-related temperature anomalies
(Glynn et al. 2018). However, the effects of ENSO events on
coral-associated community diversity and diversity-function
relationships have yet to be assessed, as is any evidence of
whole-community extinction debt in the Galápagos.

In this study, we examined the effects of a coral bleaching event in the
Galápagos Islands triggered by a cold-water anomaly during the 2007-2008
La Niña on structurally complex \emph{Pocillopora} spp. corals and on
the communities of mobile macroinvertebrates and fishes associated with
them. By measuring changes in the communities, we used a time series
(July 2008, January 2009, July 2009, February 2010) empirical approach
to investigate extinction debt (Kuussaari et al. 2009, Ridding et al.
2021). We tracked the extent of coral bleaching was first surveyed in
January 2008 and the general fate of the finger coral habitats over a
49-month period starting in August 2007 and ending in July 2011 (Figure
S1). This period of time included two additional ENSO-related
temperature events: a La Niña (2008-2009) and an El Niño (2009-2010,
United States National Oceanic and Atmospheric Administration, National
Environmental Satellite Data and Information Service, NOAA/NESDIS,
https://origin.cpc.ncep.noaa.gov/products/analysis\_monitoring/ensostuff/ONI\_v5.php).
Despite another La Niña occurring from October 2008-April 2009 and an El
Niño from June 2009-April 2010, these live corals did not bleach
subsequent to the 2007-2008 La Niña (J. Witman and O. Rhoades, pers.
obs.), suggesting that the 2007-2008 La Niña cold-water anomaly and
bleaching triggered the loss of most of the coral heads.

We addressed the following questions: 1) How did a La Niña-related
cold-water anomaly and associated coral bleaching alter the availability
and quality of finger coral habitats? 2) Did coral bleaching reduce
associated species richness, and 3) if so, was there a time lag in
associated species loss and diversity changes (extinction debt) in the
communities inhabiting corals? 4) Post-bleaching, did the community
structure of associated invertebrates and fishes (species abundance,
composition) differ between dead versus live (recovered) finger corals?
Finally, 5) what attributes of the live and dead foundational finger
coral habitats predicted the species richness of the associated
community? Here we use the term extinction to refer to local extinction,
which is the disappearance of a species from a habitat patch (Kuussaari
et al. 2009, Watts et al. 2020), and not as a reference to regional or
global species' extinctions.

\textbf{Methods}

Subtidal temperatures were recorded at 10-minute intervals during the La
Niña period (NOAA/NESDIS,
https://origin.cpc.ncep.noaa.gov/products/analysis\_monitoring/ensostuff/
ONI\_v5.php) by Onset Tidbit\textsuperscript{TM} loggers placed at 6 and
15 m depth at two of the three study sites: Baltra (00 24.705 S, 090
16.482 W) and Guy Fawkes (00 29.964 S, 090 30.773 W). No temperature
data is available for the third study site Rocas Beagle (00 24. 797 S,
90 37.685 W), due to logger malfunctioning at this site. However,
temperatures were also recorded at 15 m depth at an additional reference
site, Cuatro Hermanos (00 84.787 S, 090 74.908 W), located 40 km
southwest of Guy Fawkes to provide insight into the spatial scale of the
cold-water event. Bleaching of \emph{Pocillopora} corals during cold
water events has been recorded at temperature thresholds of
19\textsuperscript{o}C in the Gulf of California (Paz-García et al.
2012), while temperatures of 18.5-19\textsuperscript{o}C
stressed\emph{P. verrucosa} in lab experiments (Rodríguez-Troncoso et
al. 2013). Sustained cold water temperatures well-below reported
thresholds of 16\textsuperscript{o}C (11 and 12\textsuperscript{o}C,
respectively) resulted in widespread bleaching and mortality of many
scleractinian coral species along the Florida reef tract (Lirman et al.
2011, Kemp et al. 2011). We thus considered the 2007-2008 Galápagos
temperature records for the amount of time (i.e., hours and days) that
temperatures were less than or equal to one or both of two cold-water
thresholds identified in the literature (16\textsuperscript{o}C and
18\textsuperscript{o}C), which serve as conservative indicators of the
low temperature stress to \emph{Pocillopora} colonies (Table 1). In
addition to our temperature loggers, we also obtained information
regarding the cold-water plume from the NOAA Coral Reef Watch (Fig. S2,
extracted from NOAA/NESDIS, https://coralreefwatch.noaa.gov).

As part of our bi-annual biodiversity monitoring surveys we observed
substantial bleaching of finger (Pocilloporidae) and massive (Poritidae,
Pavonidae) corals in the central Galápagos Archipelago. This coral
bleaching occurred during a 5-7-month window, between June 2007 (when
bleaching was not present) and January 2008 (when it was first observed)
(Figure S1). To address our research questions, we first counted using
SCUBA the number of finger coral colonies that were alive, bleached or
dead in January 2008 in 2-3 large plots (30 x 5 m) at 6-12 m depth at
each of the three aforementioned study sites. In July 2008, we marked
dead and live (recovered) finger coral colonies with numbered plastic
tags at 4-15 m depth across larger areas (approximately 600
m\textsuperscript{2}) than the initial survey plots at these sites.
Tagged corals (potentially including \emph{P. verrucosa} , \emph{P.
capitata} , \emph{P. damicornis} , \emph{P. eydouxi} , \emph{P.
meandrina)}were aggregated at the genus level (\emph{Pocillopora} ) due
to the difficulty of identifying them to species, as the coral calcium
carbonate structure of many dead corals had degraded. A total of 96
discrete \emph{Pocillopora} coral heads were tagged and successfully
tracked across all time-series surveys at the three sites (Baltra, n=29,
Guy Fawkes, n=31, and Rocas Beagle, n=36).

We surveyed the fish and mobile macroinvertebrates (1.0 cm total body
length or larger) associated with the tagged corals in July 2008,
January 2009, July 2009, and February 2010. A diver slowly approached
each tagged coral (at a short distance) and first identified and counted
all visible fishes sheltering within, swimming in and out of, or
hovering over the coral head. We only counted fishes within 10 cm of
coral branches, with the exception of juvenile damselfish, which were
included in fish counts but were often slightly further from coral
heads. The diver then approached the coral more closely and identified
all cryptic fishes (e.g., blennies and gobies) and mobile
macroinvertebrates (e.g., crustaceans, echinoderms, and gastropods). One
observer (O. K. Rhoades) conducted all the \emph{in situ} counts to
maintain the consistency of methodology and species identifications.
Gastropods were identified with the assistance of local experts at the
Charles Darwin Research Station. We did not census mobile invertebrates
smaller than 1 cm total body length, nor did we survey sessile
invertebrates or algae that recruited onto the dead corals.

The size of each tagged coral head was measured as the 2D surface area
from an overhead photograph of the colony taken with a quadrapod camera
framer (Witman 1985) designed to hold a Nikonos camera, a 15 mm lens
corrected for barrel distortion and two strobes. Colony photographs were
taken perpendicular to the substrate to obtain a standard overhead view
in a 0.25 m\textsuperscript{2} photo quadrat. We also surveyed the
maximum branch length per coral head. Surveys of the communities
associated with each finger coral head were conducted at a separate time
and during a different dive from photographing of coral area (to avoid
potentially disturbing and displacing fishes from corals with
photography equipment and additional SCUBA divers), and at midday (to
avoid confounding diurnal differences in associated community
composition with variation in associated composition over time), on a
single day at each time point to avoid recounting fish moving among
adjacent coral habitats.

During the initial bleaching survey in January 2008, and on the four
subsequent sampling periods (July 2008 - February 2010), we recorded the
status of tagged corals as live if they had at least 50\% cover of live
tissue. For dead corals, we recorded if they had eroded, broken apart
into rubble, or completely disappeared. A final survey was conducted in
July 2011 at all three sites by J. Witman to only determine the
persistence of the tagged, dead corals.

\emph{Statistical analyses}

We compared the richness of coral-associated macrofauna on live and dead
corals over time, first of all surveyed macrofauna, as well as each for
fishes and mobile macroinvertebrates, separately. We calculated
randomized observed species richness (`observed species richness') of
the community associated with finger coral heads by constructing
randomized Species Accumulation Curves (SACs), calculating the mean SAC
and its standard deviation from random permutations of the data, or
subsampling without replacement (Gotelli \& Colwell 2001). We also
calculated Chao 1 estimated species richness (`Chao 1 estimated
richness') for the entire community, fishes and mobile invertebrates, of
coral heads using the Chao 1 estimator, a non-parametric species
estimator for abundance data (Chao et al. 2009), including 95\%
confidence intervals based on the actual Chao estimator (Colwell \&
Elsensohn 2014).

We also compared the composition of coral-associated macrofauna on live
and dead corals over time by performing a Principal Components Analysis
(PCA) using raw abundances of coral-associated macrofauna as the
response variables and treating each individual coral head in each
survey as an individual sample. The PCA algorithm used unweighted
singular value decomposition on values fitted using unweighted linear
regression of chi-transformed data (Legendre and Legendre 2012). We then
calculated Euclidean dissimilarities in composition using multiscale
bootstrapped resampling.

Finally, we assessed the attributes that predicted associated richness
by constructing linear mixed effects models of associated richness per
coral head, first for all macrofauna, and then each for fishes and
mobile macroinvertebrates. Overhead surface area of the coral colonies
and maximum coral branch length were treated as fixed effects,
individual coral heads and sites included in the model as random
intercepts, and time was treated as a random slope.

We ran mixed effects models using the lme4 R package (Bates et al.
2015), we ran rarefaction (species accumulation curves) and principal
components analysis using the vegan R package (Oksanen et al. 2020), and
we calculated Chao 1 total estimated richness using the SpadeR package
(Chao et al. 2016). All statistical analyses were conducted using R
software (version 3.6.2, R Core Development Team 2017).

\textbf{Results}

\emph{Temperature}

Minimum temperatures at two of the study sites ranged from
13.9\textsuperscript{o}C at Guy Fawkes (at 15 m) to
16.3\textsuperscript{o}C (at 6 m) depth at Baltra, and were similarly
low (14\textsuperscript{o}C) at the Cuatro Hermanos reference site
(Table 1A). Temperatures were at or below the threshold of
18\textsuperscript{o}C for \emph{Pocillopora} bleaching for 6.3 to 34.3
days at Baltra (6 m) and Guy Fawkes (15 m) respectively (Table 1B). At
Guy Fawkes, the subtidal environments experienced the colder bleaching
threshold of 16\textsuperscript{o}C or lower for less than 1 hour at 6
m, but this time period increased to 54.6 hours at 15 m depth.
Temperatures were colder at the Cuatro Hermanos reference site, where
they were 18\textsuperscript{o}C or lower for 59.5 days and
16\textsuperscript{o}C or lower for 5.3 days (Table 1B).

Satellite images of minimum sea surface temperatures (SST) confirmed our
temperature logger data and depicted a cold-water plume moving northwest
along the South American Coast and deflecting offshore to reach our
study area in the central Galápagos. During August-October 2007 the
minimum SST of 15-20\textsuperscript{o}C occurred (Figure S2). This was
likely the origin of the cold water that led to coral bleaching, given
that we recorded substantial temperature declines at 6 and 15 m depth
during this same time period (Figure 1). By January 2008, the minimum
SST had increased to 20-25\textsuperscript{o}C (Figure S2).

\emph{Effects of ENSO-related cold-water anomalies on finger corals}

After the 2007-2008 La Niña bleaching, a minority of bleached corals
recovered their pigmentation and survived, while most corals died and
eroded (Figure 2A). When surveyed 6-13 months post-bleaching in July
2008 (Figure S1), only 24\% (n=26) of surveyed
\emph{Pocillopora}spp\emph{.} colonies had fully recovered their color,
6\% had partially recovered live tissue, but experienced at least
25-75\% tissue loss, and 69\% (n=75) of all bleached coral colonies (as
in Figure 2C) had died and were colonized by mobile and sessile
invertebrates, fish and algae (as in Figure 2D). Subsequent monitoring
between July 2008-February 2010 revealed that 3\% (n=3) of corals had
visibly eroded, 14\% (n=15) had detached from the substrate and broken
into coral rubble, and 12\% (n=13) had completely disappeared, with
their fragments likely washed away by currents. Over this survey period,
live corals (560-616 cm\textsuperscript{2}) had not lost overhead
surface area, whereas dead corals (419-474 cm\textsuperscript{2}) had
lost an average of 13\% overhead surface area and were on average 24\%
smaller than live corals (Figure 2B). All finger corals that had
initially bleached and died at the beginning of the study in January
2008 had disintegrated by July 2011 (Figure 2B). Over the survey period,
the live corals did not bleach or deteriorate subsequent to the
2007-2008 La Niña (J. Witman and O. Rhoades, pers. obs.).

\emph{Post-bleaching shifts in coral-associated species richness}

Randomized observed species richness (Figure 3) and Chao 1 estimated
species richness (Figure 4) of associated species varied significantly
across certain time points and/or between live and dead corals. In July
2008, which was 6-13 months post-bleaching and within the 2007-2008 La
Niña period, live and dead corals supported similar observed (20-21
species) and Chao 1 estimated (40-41 species) total species richness
(Figures 3A, 4A). However, observed total species richness on dead
corals increased to 25 species in January 2009 relative to July 2008
(including seven fishes and 19 macroinvertebrate species), and then it
declined thereafter until February 2010 (Figure 3A). By contrast,
observed total species richness (and observed fish richness) on live
corals was initially higher in July 2008 (and higher than on dead corals
in July 2008) and comprising 20 species (including 9 fishes and 11
macroinvertebrate species), decreased in January 2009, and remained
stable through February 2010 (Figure 3A-B).

Across all sampling dates, Chao 1 mean estimated total richness was
16-41 and 16-61 total species (Figure 4A), 4-10 and 5-16 fish species
(Figure 4B), and 10-21 and 8-73 invertebrate species (Figure 4C)
associated with live and dead corals, respectively. Similar to observed
species richness, between July 2008 and January 2009, Chao 1 estimated
total and invertebrate species richness on dead corals underwent a
nearly 50\% increase, from 41 to 61 total species richness and from 25
to 73 invertebrate richness, then declined significantly to 25 total and
20 invertebrate species richness in July 2009, and ultimately to 16
total and 8 invertebrate species richness in February 2010 (Figure
4A\&C). By contrast, Chao 1 estimated total and invertebrate species
richness on live corals did not significantly differ across most time
points, and fluctuated from 41 to 24 to 35 total species and 21 to 21 to
18 invertebrate species from July 2008 to July 2009, but it
significantly declined to 16 total and 10 invertebrate species richness
in February 2010 (Figure 4A\&C). By contrast, Chao 1 estimated fish
richness declined over time on dead corals (from 16 to 7 to 5 to 9
species) and live corals (from 10 to 4 to 7 to 5 species), and in July
2008 it was significantly higher than in any other time periods (Figure
4B).

\emph{Differences in coral-associated species on live and dead corals}

Principal component analysis (PCA) of the entire community of fish and
mobile macroinvertebrates associated with the finger corals indicated
that the overall species composition of the communities differed
significantly between live and dead corals (Figure 5A, see Figure S3 for
explanation of PCA species scores). Species composition also differed
among certain time points, especially between the first time point (July
2008) relative to other time points for live corals and dead corals, and
between the last time point (February 2010) relative to other time
points for live corals (Figure 5A). Live corals were characterized by
high PC1, which increased across time points, and was strongly
correlated with the presence of mutualistic xanthid crabs \emph{Trapezia
ferruginea} and \emph{Trapezia digitalis} (Figure S3A). Dead corals were
characterized by lower values of PC1, which was strongly correlated with
the presence of the pencil urchin \emph{Eucidaris galapagensis} (Figure
S3A). Relative to the latter points, earlier time points were
characterized by lower PC2 values, which were strongly correlated with
the presence of the pencil urchin and juveniles of the ring-tailed
damselfish \emph{Stegastes beebei} , as well as a speciose assemblage of
opportunistic snails (Figure S3B).

Live and dead corals exhibited strong overlap in fish assemblages
(Figure 5B), but particular differences in the community of associated
invertebrates (Figure 5C-D). With respect to coral-associated fishes,
live and dead corals were dominated by two territorial and residential
fish species: the coral hawkfish \emph{Cirrhitichthys oxycephalus} and
the juvenile ring-tailed damselfish \emph{Stegastes beebei} ; though the
abundance of these species varied seasonally, and ultimately declined by
65\% and 90\%, respectively (particularly on dead corals) between July
2008 and February 2010 (Figure 5B). Other common species at certain time
points (e.g., \emph{Ophioblennius steindachneri} in July 2008
and\emph{Lythrypnus gilberti} in January 2009 on dead corals
and\emph{Thalassoma lucasanum} in July 2008 on live corals) also
exhibited high seasonal variability in abundance (Figure 5B).

With regards to coral-associated invertebrates, dead corals hosted
opportunistic and predatory macroinvertebrate species, dominated by the
pencil urchin \emph{Eucidaris galapagensis} , hermit crabs (Figure 5C),
and a rich assemblage of 16 species of gastropods, especially two
species of \emph{Engina} as well as \emph{Muricopsis zeteki} , which
increased between July 2008 and January 2009 (Figure 5D). The abundance
of pencil urchins on dead corals increased initially by 100\% (21 to 42
individuals) between July 2008 and January 2009, and then declined by
62\% between January 2009 and February 2010 (Figure 5C). Pencil urchins
were observed feeding directly on the calcium carbonate structure of
dead and occasionally bleached live coral tissue, while gastropods and
hermit crabs were frequently observed feeding on the sessile
invertebrates (barnacles, sponges, ascidians, bryozoans) that had
colonized dead coral skeletons (O.K. Rhoades, pers. obs.). By contrast,
the coral-associated invertebrates on live finger corals were dominated
by hundreds of mutualistic xanthid crabs (\emph{Trapezia spp.}
including\emph{Trapezia ferruginea} and \emph{Trapezia digitalis} )
(Figure 5C). The total number of mutualistic crabs increased by 300\%
(71 to 284 individuals) between July 2008 and February 2010 (Figure 5C).
Gastropods were considerably (10 times) more abundant on dead corals
relative to live corals (Figure 5D).

\emph{Relationships between coral habitat attributes and associated
species richness}

Three physical attributes of finger coral habitat structure: coral
status (live/dead) (p\textless{}0.0001), overhead surface area
(p=0.0025) and maximum coral branch length (p=0.0005), predicted the
number of species associated with the corals (Table 2). Ordinary Least
Squares (OLS) regression analysis indicated that total species richness
was positively and linearly related to the top surface area of the
colonies, although the significance and strength of these relationships
varied between live and dead corals and across time points (Figure 6).
Species-area relationships were significant for live corals across all
time points (Figure 6, bottom panel), whereas they were only significant
for dead corals for the two latter time points (Figure 6, top panel).
Surface area also explained a greater proportion of total variation in
species richness for live versus dead corals (r\textsuperscript{2} =
0.26 to r\textsuperscript{2} = 0.62 \emph{versus} r\textsuperscript{2} =
0.15, respectively, Figure 6). The richness of coral-associated
macrofauna increased by 14-22 species per a projected 1.0
m\textsuperscript{2} increase in live coral surface area across time
points, and by 18 species per a projected 1.0
m\textsuperscript{2}increase in dead coral surface area (Figure 6).
Tighter species-area relationships on live corals were driven by fishes
(r\textsuperscript{2}= 0.47 to r\textsuperscript{2} = 0.58) relative to
invertebrates (r\textsuperscript{2} = 0.19 to r\textsuperscript{2} =
0.29). For dead corals, richness of associated species was poorly
predicted by coral surface area for both fishes (r\textsuperscript{2} =
0.08 to r\textsuperscript{2} = 0.14) and invertebrates
(r\textsuperscript{2} = 0.06 to r\textsuperscript{2} = 0.14) (Figure
S4A-B).

Species richness of the associated community was also predicted by the
length of live finger coral branches (Figure S5). The richness of
coral-associated macrofauna increased in live corals by 8-25 species per
a projected 1.0 m increase in coral branch length at three of four time
points (r\textsuperscript{2} = 0.29 to r\textsuperscript{2} = 0.43). On
the other hand, branch length of dead finger corals showed either a weak
positive (r\textsuperscript{2} = 0.21, July 2009) or weak negative
(r\textsuperscript{2} = 0.17, February 2010) relationship with species
richness of the associated community (Figure S5 top panel).

\textbf{Discussion}

Strikingly, nearly 70\% of \emph{Pocillopora} corals bleached and died
between August 2007 and July 2008 at our three study sites in the
Galápagos, which coincided with the 2007-2008 La Niña-related cold-water
anomaly. This represents a major loss of live coral foundational habitat
for associated fishes and mobile macroinvertebrates. Nevertheless, dead
coral colonies were still able to retain the ecosystem function of
hosting high species richness of associated fish and mobile
macroinvertebrates for more than two years after the disturbance.
However, the species composition of these assemblages (and particularly
of invertebrates) significantly varied between mutualistic xanthid crabs
on live corals to opportunistic and predatory pencil urchins, hermit
crabs, and gastropod snails on dead corals, and shifted over time on
live and dead corals. This shift in associated species composition was
likely due to changes in structure and provisioning of food on coral
tissue, and loss or growth of live coral tissue. Furthermore, the
speciose and opportunistic associated assemblage on dead corals
ultimately declined in richness due to erosion and disappearance of
complex coral structure, and likely led to loss of coral-associated
richness after 32-49 months.

\emph{Cold water effects on corals}

Our observations suggest that an ENSO-related cold-water anomaly led to
bleaching and death of finger corals. The bleaching period coincided
with the arrival of a plume of cold water (15-20\textsuperscript{o}C
minimum SST) flowing up the west coast of South America, arriving in the
central Galápagos during October 2007. During this time period, corals
were exposed to temperatures at or below published cold water thresholds
for coral bleaching, including 18\textsuperscript{o}C for up to 34 days
and 16\textsuperscript{o}C or less for 2.3 days at Guy Fawkes (15 m
depth). Temperatures at Baltra (15 m) were at or below the
18\textsuperscript{o}C threshold for 18.8 days. As expected,
temperatures decreased with depth from 6 to 15 m. Longer periods of
unusually cold water occurred at the reference site Cuatro Hermanos
(where corals are rare) likely related to the presence of stronger
upwelling currents relative to those at Guy Fawkes or Rocas Beagle
(Witman et al. 2010).

In general, cold-water coral bleaching has received less attention than
warm water bleaching, although it can cause extensive coral mortality.
For example, (González-Espinosa \& Donner 2020) documented cold-water
coral bleaching at 14 sites in the Eastern Tropical Pacific alone from
1998 -2017. One of these events was reported from the northern islands
of Darwin and Wolf in the Galápagos where bleaching of three coral
species (\emph{Porites lobata, Pocillopora spp.} and \emph{Pavona
clavus} ) occurred in 2007 when SST were 16\textsuperscript{o}C (Glynn
2009, Glynn et al. 2017), which was likely caused by the same La Niña
event reported in this study. Given that climate models predict that the
frequency of extreme La Niña events and associated cold-water anomalies
will increase with climate warming (Cai et al. 2015), our study suggests
that more attention should be paid to the consequences of coral
bleaching caused by low temperatures.

\emph{Coral-associated richness}

Our study of \emph{Pocillopora} colonies in the central Galápagos rocky
subtidal ecosystem contribute to the growing number of studies that show
that finger corals host a diverse assemblage of fish and
invertebrates\emph{.} Our surveys showed that recently
recovered\emph{Pocillopora} colonies supported up to 20 observed species
(randomized observed species richness), and up to 41 total estimated
species (Chao 1 estimated species richness), including nine known fishes
and 11 known mobile macroinvertebrate species. Dead colonies of the same
Genus supported an even greater diversity of up to 25 observed species
and 61 total estimated species, including seven known fishes and 18
known mobile macroinvertebrate species. Even so, these species estimates
are an underestimate of the actual diversity of the entire community of
associated species, since (for ethical considerations) we chose not to
collect corals and exhaustively census the mobile fauna living in the
interstices of the coral, or the sessile invertebrates and algae that
colonized the dead \emph{Pocillopora} colonies.

The biodiversity of communities associated with \emph{Pocillopora}corals
has been extensively studied in other tropical regions, and the range of
our estimated values of species richness (20-41 species associated with
live corals depending on the mode of analysis) falls within the range
(though at the lower end) of published values of\emph{Pocillopora}
communities in other regions. The seminal work of (Abele \& Patton 1976)
demonstrated that off the Pacific coast of Panama (close to the
Galápagos study region), \emph{Pocillopora} colony area predicted the
species richness of the decapod community associated with the corals,
supporting 61 total species of decapods. Subsequent work has found that
36-127 species were found associated with \emph{Pocillopora}corals at
locations from the Red Sea to Hawaii (Britayev et al. 2017).
Consequently, declines in finger coral habitats appear to represent an
important loss of foundational habitat for a diverse assemblage fishes
and invertebrates.

\emph{Extinction debt of coral associates}

Coral associates experienced biodiversity loss multiple years after
disturbance to their foundational habitat, which coincides with loss of
richness in other ecosystems\emph{.} Indeed, bleached and dead finger
coral habitats retained high levels of species richness for 13-19 months
after the bleaching disturbance occurred; in fact, species richness of
mobile macroinvertebrates considerably increased during this time
period. However, this trend was reversed by a significant loss of mobile
macroinvertebrate richness 19-25 months post-bleaching. During the final
survey of associated species, total Chao 1 estimated species richness on
dead corals was significantly lower relative to corals at earlier time
points, and relative to live corals at that time. Depending on how long
after our initial survey (June 2007) bleaching actually occurred, and
how long before our final survey (July 2011) corals disintegrated, we
estimate that it took between 32 and 49 months for the
bleached\emph{Pocillopora} to disintegrate and entirely disappear,
driving the species richness of associated fish and macroinvertebrates
down even further, possibly to zero as their habitat was lost.

\emph{Coral-associated richness on live versus dead corals}

As with standing dead wood forests on land that have died due to disease
or herbivorous insect attacks (Stokland et al. 2012, Seibold et al.
2015, Thorn et al. 2020), bleached and dead finger corals retained their
biodiversity-enhancing function for multiple years after cold-water
bleaching and death. This is both related to the habitat provided by the
complex branching structure of the finger corals, as well as the food
provided by sessile invertebrates and algae that rapidly recruited to
and grew on the dead and undefended corals (Hadfield \& Paul 2001,
McCook et al. 2001). In this study, both overhead surface area and
maximum branch length of \emph{Pocillopora} corals significantly
predicted the number of associated species, aligning with theory that
habitat complexity is a leading predictor of species diversity
(MacArthur \& MacArthur 1961), and that coral colony surface area and
branch length are indicators of the habitable area or volume for
associated fishes and invertebrates (Abele \& Patton 1976, Britayev et
al. 2017). Our study further demonstrated that live tissue area was
particularly important in determining the richness of associated
species; surface area (and coral branch length, to a lesser extent)
accounted for a much greater proportion of the total variation in
species richness on live corals versus dead corals (26-62\%\emph{versus}
15\%). As with other recently disturbed and dead foundational habitats,
live coral habitat has greater structural integrity and complexity
relative to dead coral structure, such that live coral area is more
representative of habitat area. Additionally, dead corals provide
supplementary, ephemeral functions related to provisioning of food,
which differ from the habitat and food functions provided by live
corals, which attract a disproportionately rich assemblage of
opportunistic coral associates.

Accordingly, the richness and composition of the associated communities
differed between live and dead finger coral habitats, and these
differences magnified over time. Though the composition and abundance of
fishes (dominated by coral hawkfishes and juvenile damselfishes) was
similar on live and dead corals, abundance was highest at the first
community census and then fluctuated over time on live corals, while
both fish species decreased in abundance over time on dead corals.
Moreover, live and dead corals exhibited distinct assemblages of
invertebrates, with symbionts and specialists occupying live corals,
versus opportunistic generalists occupying dead corals, and each of
these assemblages became more and more distinct as live corals recovered
and grew, while dead corals simultaneously eroded into rubble and
disappeared.

Species composition on recovered, live corals exhibited a shift over
time toward total dominance by xanthid crabs (genus \emph{Trapezia} ),
highlighting the importance of live coral habitat for this species.
Trapeziid crabs are obligate residents that feed on live coral tissue
while also defending corals from attack (Stewart et al. 2006, Stella et
al. 2011). \emph{Trapezia} crabs exhibited a striking increase in
abundance on live corals between July 2008 and February 2010, possibly
due to redistribution of individuals from recently dead to remaining
live (recovered) corals, which has been found to occur after widespread
bleaching (Glynn et al. 2017), according to colony size
(Canizales-Flores et al. 2021). It is possible that the large increase
in the number of \emph{Trapezia} occupying the live coral habitats from
July 2008 to February 2010 at the Galápagos sites reflects habitat
limitation due to the reduction of live coral habitats after the
bleaching-induced mortality of Pocillopora \emph{spp} ., in addition to
growth of live tissue on those colonies over time. Overall high mobility
of the fish, crustacean, and echinoderm fauna associated with live and
dead corals suggests that active dispersal could explain the surge of
species richness in the dead coral habitats between July 2008-January
2009 and the increase in abundance of \emph{Trapezia} crabs in live
corals. Our results also suggest that a metapopulation perspective
(Hanski \& Ovaskainen 2002) may be a useful conceptual framework for
investigating post-disturbance patterns of live and dead coral habitat
occupancy, at least in this system of discrete finger corals in the
Galápagos, and for tropical reefs of other regions where disturbances
result in increasingly patchily and sparsely-distributed branching coral
colonies.

By contrast, bleached and dead corals exhibited rapid colonization by
opportunistic and transient urchins, crabs, and gastropod snails, which
ultimately declined due to loss of structure. These mobile
macroinvertebrates contributed to a marked, non-linear change in
associated community richness; first an increase in total species
richness on recently dead corals between the first two community surveys
(July 2008-January 2009), and thereafter a striking decrease over the
next 13 months to February 2010. These species included large numbers of
the well-known pencil urchin bioeroder, \emph{Eucidaris galapagensis} ,
as well as hermit crabs and a number of species of gastropod snails.
These species were observed to be feeding on dead coral tissue and
sessile invertebrates, which may have arrived via migration of juveniles
and adults and/or larval recruitment onto undefended coral skeleton
habitats. These species declined in abundance and richness over time as
corals disappeared into rubble, serving to temporarily enhance overall
coral-associated community abundance and richness until obligate
specialists recovered on live corals.

\emph{Consequences of finger coral declines for coral specialists versus
generalists}

Theory predicts that extinction debt should vary depending on the degree
of habitat specificity of associated species (Kuussaari et al. 2009,
Hylander \& Ehrlén 2013, Watts et al. 2020) with generalists
characterized as having broad habitat requirements and specialists
``largely dependent on one particular habitat type'' (Watts et al.
2020). Specialists with low dispersal should have relatively short
duration extinction debt, while generalists with high dispersal would
have the longest extinction debt, as they could utilize other habitats
after a disturbance. Of the \emph{Pocillopora} associated community of
fishes and mobile macroinvertebrates, we have sufficient information on
small-scale (within-habitat) distribution to estimate that at least six
species can be considered largely dependent on the
\emph{Pocillopora}habitat. These include three species of
\emph{Trapezia} crabs which are known obligate \emph{Pocillopora}
mutualists (Glynn 1976, Hickman \& Zimmerman 2000), the spider crab
\emph{Telephyrs cristolipes} described as inhabiting finger corals in
Hickman \& Zimmerman (2000), the corallivorous gastropod
\emph{Babelomurex hindsii} , and the coral hawkfish \emph{Cirrhitichthys
oxycephalus,} which is frequently observed in finger corals and among
black corals in the Galapagos (J. Witman, pers. obs.). As in most
communities of mobile species such as birds (Watts et al. 2020), insects
(Hanski \& Ovaskainen 2002), and reef fishes (Kritzer \& Sale 2006), the
community of fishes and macroinvertebrates associated with live and dead
finger corals represents a mix of habitat and food specialists and
generalists. Future research to identify habitat specialist species on
Galápagos reefs is needed to understand those species most vulnerable to
habitat loss and to overall biodiversity loss following future
temperature stress from climate oscillations.

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\textbf{Tables}

\textbf{Table 1} . Water temperatures (degC) per depth at the two study
sites (Baltra and Guy Fawkes) and at 15 m depth of the reference site
(Cuatro Hermanos) during June 2007- January 2008, including (A) summary
statistics (SD=standard deviation, CV=coefficient of variation), and (B)
the amount of time in hours and days at or below cold-water threshold
temperatures (16 and 18degC) that are known to produce widespread coral
bleaching elsewhere (see main text).

(A)\selectlanguage{english}
\begin{longtable}[]{@{}lllllllll@{}}
\toprule
\textbf{Site} & \textbf{Depth (m)} & \textbf{Recordings (n)} &
\textbf{Mean} & \textbf{Min} & \textbf{Max} & \textbf{Median} &
\textbf{SD} & \textbf{CV}\tabularnewline
Baltra & 6 & 31,560 & 20.9 & 16.3 & 24.7 & 21.2 & 1.5 &
7.2\tabularnewline
& 15 & 31,564 & 20.4 & 15.3 & 24.7 & 20.7 & 1.6 & 7.8\tabularnewline
Guy Fawkes & 6 & 32,520 & 20.2 & 15.8 & 23.6 & 20.3 & 1.2 &
5.8\tabularnewline
& 15 & 32,518 & 19.6 & 13.9 & 23.4 & 19.8 & 1.4 & 7.1\tabularnewline
Cuatro Hermanos & 15 & 32,454 & 18.9 & 14 & 22.5 & 19.0 & 1.3 &
6.9\tabularnewline
\bottomrule
\end{longtable}

(B)\selectlanguage{english}
\begin{longtable}[]{@{}llllll@{}}
\toprule
\textbf{Site} & \textbf{Depth (m)} & \textbf{Hours [?] 16°C}\selectlanguage{ngerman} &
\textbf{Days [?] 16°C}\selectlanguage{ngerman} & \textbf{Hours [?] 18°C}\selectlanguage{ngerman} & \textbf{Days [?]
18°C}\selectlanguage{ngerman}\tabularnewline
Baltra & 6 & NA & NA & 151.5 & 6.3\tabularnewline
& 15 & 14.1 & 0.6 & 451.8 & 18.8\tabularnewline
Guy Fawkes & 6 & 0.7 & NA & 237.3 & 9.8\tabularnewline
& 15 & 54.6 & 2.3 & 825.3 & 34.3\tabularnewline
Cuatro Hermanos & 15 & 127.3 & 5.3 & 1428.1 & 59.5\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 2} . Maximum likelihood (ML) estimates and 95\% confidence
intervals for linear mixed effects model of coral-associated species
richness, including coral status (live/dead), coral overhead surface
area, coral maximum branch length, and the interaction between coral
status and surface area/branch length. Continuous predictors are
centered and standardized, such that the full range of a continuous
predictor is 2 units (compared to 1 unit for categorical predictors).\selectlanguage{english}
\begin{longtable}[]{@{}lll@{}}
\toprule
\textbf{Predictor} & \textbf{ML Estimate, 95\% confidence interval} &
\textbf{Significance}\tabularnewline
Coral status (live vs dead) & 0.54 (0.34, 0.75) & p\textless{}0.0001
***\tabularnewline
Coral overhead surface area & 0.33 (0.12, 0.54) & p=0.0025
*\tabularnewline
Coral max branch length & 0.21 (0.09, 0.32) & p=0.0005 **\tabularnewline
Coral status*Surface area & -0.22 (-0.46, 0.01) & p=0.062
(NS)\tabularnewline
Coral status*Branch length & 0.03 (-0.19, 0.26) & p=0.76
(NS)\tabularnewline
\bottomrule
\end{longtable}

\textbf{Figure legends}

\textbf{Figure 1} . Composite plots of sea surface temperature regimes
at Baltra, Guy Fawkes and Cuatro Hermanos (the reference site for Rocas
Beagle) during the period of coral bleaching. Line color corresponds
with temperatures recorded at 6 m (red) and 15 m (blue). Dashed lines
correspond to the threshold cold temperatures (18\textsuperscript{o}C
and 16\textsuperscript{o}C) that induce bleaching in
\emph{Pocillopora}corals.

\textbf{Figure 2.} (A) Status of coral heads (by \% surveyed with
certain tissue characteristics) and (B) mean and standard error of
overhead surface area of live (black) and dead (gray) coral heads across
the time series (July 2008 to February 2010). Dead corals (but not live
corals) were also surveyed in July 2011. (C) The same tagged coral head,
surveyed in (C) July 2008 and (D) February 2010.

\textbf{Figure 3} . Mean and standard deviation of species accumulation
curves (SACs) of randomized observed associated species richness with
live (black) and dead (gray) \emph{Pocillopora} corals. Associated
species include (A) all surveyed species, (B) fishes and (C) mobile
macroinvertebrate species. Blue and red underlining indicates La Ni\selectlanguage{ngerman}ña
and El Niño periods, respectively.

\textbf{Figure 4.} Means and 95\% confidence intervals of Chao 1
estimated species richness of (A) all surveyed (total) species, (B)
fishes and (C) mobile macroinvertebrates on live (black) versus dead
(gray) corals at each survey date between July 2008 and February 2010.
Note different scales on y-axis. Means with 95\% confidence intervals
that do not overlap the mean of the other group under comparison are
significantly different (Ramsey \& Schafer 2012).

\textbf{Figure 5} . Species composition of coral-associated fishes and
mobile macroinvertebrates surveyed on live versus dead coral heads at
each survey date between July 2008 and February 2010. (A) Biplot of
loadings for principal component 1 (PC1) by principal component 2 (PC2)
from a principal components analysis (PCA) using abundances of
coral-associated macrofauna as the response variables and treating each
individual coral head in each survey as an individual sample. PC1
accounted for 24\% of total variation in composition, while PC2
accounted for 15\% of total variation in composition. Points refer to
the community assemblage associated with individual corals, including
live (square symbols) and dead (circle symbols) corals, sampled at each
of four time points (represented by different colors). The ellipses show
the 95\% confidence regions for the mean centroids of each survey group
(live or dead corals) surveyed at a specific date. Raw abundance of (B)
fishes, (C) crustaceans and echinoderms, and (D) gastropods counted on
live and dead corals across all survey dates. Asterisks (**) indicate
species that are endemic to the Galápagos; ``\emph{other sp. Unknown 1}
'' and ``\emph{other sp. Unknown 2} in part (C) refer to unidentified
crustaceans.

\textbf{Figure 6} . Species-Area relationships, regressing estimated
total richness against coral overhead surface area for individual dead
or live coral heads at each survey date between July 2008 and February
2010. Regression line equations, r-squared values and p-values for
significant relationships are shown. Note that dead corals did not
exhibit significant S-A relationships in July 2008 and January 2009.

\textbf{Hosted file}

\verb`Rhoades-Brandt-Witman 2022 GLPS Figures.docx`  available at \url{https://authorea.com/users/723150/articles/707984-extinction-debt-of-gal%C3%A1pagos-foundational-coral-associates-enso-related-cold-water-bleaching-triggers-community-biodiversity-loss-and-turnover}

\selectlanguage{english}
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\end{document}

