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.