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 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.