Marginal coral reefs show high susceptibility to phase shift
Graphical abstract
Introduction
Coral reefs provide several substantial ecological services, such as fishing, coastline protection and tourism, have economic value (Costanza et al., 2014) and contain inherent high biodiversity (Connell, 1978) and productivity (Birkeland, 1997). Human activities have damaged coral reefs over the past five decades (Burke et al., 2011; Hughes et al., 2017). This damage reached a level that was described as a “coral reef crisis” (Bellwood et al., 2004; Madin and Madin, 2015), with 20% of reefs degraded globally and an additional 35% threatened as of 2008 (Wilkinson, 2008) and 75% of global coral reefs threatened in some way as of 2010 (Burke et al., 2011; Hughes et al., 2017).
The most drastic consequence of coral reef degradation is the “phase shift” phenomenon (Graham et al., 2014; Hughes et al., 2017). In coral reefs, a phase shift is a change in dominance from reef-building corals to non-reef building groups such as macroalgae or sponges (Done, 1999; Norström et al., 2009). This phenomenon can result from either natural or anthropogenic disturbances (Cruz et al., 2014; Dudgeon et al., 2010). The resulting loss of reef-building capacity could cause the loss of structural complexity (Graham et al., 2014). As a consequence, the reef could lose the capacity to maintain its local diversity (Graham et al., 2015; Harborne et al., 2011; Letourneur et al., 2017) due to loss of habitat heterogeneity and structural complexity, altering trophic structure (Cruz et al., 2015b; Done, 1999; Hempson et al., 2018), harming the structural integrity of the reef over the long-term (Feary et al., 2007) and causing loss of ecosystem services (Bellwood et al., 2004; Graham et al., 2014).
For effective management and mitigation of reef degradation, data that extends geographically across the region of study is necessary to make inferences about regional patterns. The current condition of reefs of interest should be assessed, then cross-referenced with potential local impacts. Faced with a forecast of an increase in phase shift phenomena due to climate change and human activities, a better understanding has become crucial (Hughes et al., 2017; Roff and Mumby, 2012). For macroalgal shifts, a global overview was conducted (excluding the east coast of Africa, Red Sea and Persian Gulf) (Bruno et al., 2009). Such studies on a regional scale, which allow correlation with local impacts, have only been conducted in the Florida Keys, Great Barrier Reef and Hawaiian archipelago (Bruno et al., 2009; Jouffray et al., 2014).
Marginal reefs, those living at the limit of tolerable environmental conditions (e.g. temperature, salinity, light, carbonate saturation state, and/or nutrients) (Perry and Larcombe, 2003), are important because of their potential as an ecological refuge and could be more resistant to effects of climate change than the non-marginal ones due to their more flexible and resistant community of organisms (Couce et al., 2013; Freeman, 2015). By comparing phase shift rates on these reefs to our understanding of those under optimal conditions, we could potentially identify differences in the incidence and severity of phase shifts, along with differences in potential recovery rates for these two types of reef systems. Specific localized incidences of phase shifts have been noted in a few marginal reef systems, such as those in the Keppel Bay, Australia, at the upper limit of light attenuation tolerance for a coral reef (Bennett et al., 2010), Whitsunday Island, Australia, at the upper limit of tolerance to sedimentation and water pollution (DeVantier et al., 1998) and Boca del Toro in Panama, also at the upper limit of tolerance to sedimentation and pollution (Schlöder et al., 2013). Past regional studies of phase shifts, in contrast, have almost exclusively concentrated on reefs under “optimal” conditions, such as in the Florida Keys, Hawaii, and the Great Barrier Reef (Bruno et al., 2009; Jouffray et al., 2014). The lack of regional studies on marginal reefs could have placed a potential bias on the current understanding of how these coral reefs will likely respond to environmental change (Suggett et al., 2012), as conflicting phenomenon have been reported in individually studied locations. While some temperate ecosystems undergo “tropicalization”, where areas usually dominated by algae become dominated by hard corals due to a long-term temperature increase (Figueira and Booth, 2010; Tuckett et al., 2017), others that remain outside coral tolerance limits for additional environmental conditions besides temperature could induce a phase not dominated by corals from that same rise in temperature.
To put phase shifts in the context of geographic effects and a wider range of environmental pressures, this work is a comprehensive examination of the large-scale system of reefs under marginal conditions along the Brazilian coast (0°40′S to 19°40′S). These Southwest Atlantic coral reefs are considered a marginal ecosystem, with corals living at the limit of sedimentation tolerance (Suggett et al., 2012). They occupy approximately 2900 km along the tropical coast; the lateral extent of the reefs across the narrow Brazilian tropical continental shelf is uncertain. Reef area estimates vary from 1200 km2 in total (Spalding et al., 2001) to 8844 km2 for only the Abrolhos Bank region, which extends along 10% of the coastline (Moura et al., 2013). We note that while Bruno et al. (2009) included some of the older macroalgal shift data from Brazil in a phase shift study, only data from the reef check program was included. Those reefs were examined jointly with reefs in the Caribbean Sea, complicating any region-specific conclusion. Most of the available data for the region was excluded, as it was sampled with other methods, such as AGRRA, video transects and photo-quadrats. A comprehensive examination of this region could be used as an indicator of potential future effects on non-marginal reefs around the world.
We re-examined studies along the coast of Brazil to identify potential phase shift phenomena occurring on Southwest Atlantic marginal reefs, evaluate the extent of phase shifts, understand their potential environmental and anthropogenic drivers, and look for evidence of temporal variation in the reef conditions when possible. A few studies have described phase shifts on Southwest Atlantic coral reefs (Bruce et al., 2012; Cruz et al., 2015a; Feitosa and Ferreira, 2014; Pereira et al., 2014). Other studies in Brazil have included descriptions of reef benthic assemblages that have a pattern compatible with the concept of a phase shift (Costa et al., 2008; Costa et al., 2002; Kikuchi et al., 2010; Loiola et al., 2014; Medeiros et al., 2010), which will be included in our analysis.
Section snippets
Methods
In the absence of baseline studies of the historical state of Southwest Atlantic coral reefs, we used two key underlying assumptions to identify phase shifts. First, that historically “normal” or “healthy” coral reefs are dominated by reef-building organisms (≥25% for functional dominance cf. Bruno et al. (2009), noting however that the current highest averages among coral cover estimates in the Southwest Atlantic are 13% in Todos os Santos Bay cf. Cruz et al. (2015a) and 12% for the offshore
Time series comparison
The difference between reefs identified as phase shifted using our instantaneous reef state assessment versus a temporal assessment of the persistence of that shift over multiple years was assessed. We filtered our dataset to identify reefs with three or more temporal replications. That analysis was viable in two areas, Todos os Santos Bay using five sites from three studies (Cruz et al., 2009, Cruz et al., 2015a, Cruz et al., 2015b) and Abrolhos National Park using four sites from one study (
Anthropogenic and natural effects
To assess the relationship between PSIs and potential environmental drivers, we determined or extracted anthropogenic disturbance through population density >100,000 and >1 million people, urbanized surface area, fecal coliform levels on beaches, fertilizer use and port dredging along with distance from the coastline and the geographic coordinates of the sites. The assessed variables for examining anthropogenic effects obviously overlap in scope; we determined within the analysis process which
Results
Seventy benthic community studies of Brazilian coral reefs, post-1994, were reviewed (Supplementary material 1). Of these studies, 23 addressed phase shift (32.8%) but only five (7.1%) recorded or identified one or more reefs exhibiting a phase shift. After eliminating the data at intertidal sites and those containing repeated data, 22 studies remained. From those studies, 121 sites along the Brazilian coast were examined (Supplementary material 2).
The mean coral cover was 9.9% ± 7.9 (SD);
Time series comparison
Temporal data existed for two sites within the examined studies, in Todos os Santos Bay, Salvador and on the Abrolhos Bank, in the Abrolhos National Marine Park. Our primary method, which used only the most recent PSI value at each site, indicated PSI's ranging from −2.38 to 2.78 for five locations in Todos os Santos Bay in Salvador, with three zoanthid-dominated sites and two coral-dominated sites. Examining this data as a time series, three of those five retained the same classification for
Anthropogenic and natural effects
The analysis of the relationship between PSIs and natural drivers indicated a negative correlation between MPSI and distance from the coastline (Spearman correlation r = −0.437, p = 0.002, supplementary material 3). Zoanthid phase shifts were not found on reefs >30 km from the coast, only those near shore; however, the Spearman correlation did not detect a relationship between distance of coast and the zoanthid phase shift index (r = −0.307, p = 0.120). No effect of depth on either macroalgal
Discussion
The rarity of studies recording phase shift events for Southwest Atlantic coral reefs does not necessarily indicate that it is an unusual phenomenon, but perhaps either unstudied or underestimated. A phase shift in a coral reef is, at the root, a decrease in the coral population followed by a persistent increase of a non-reef building organism population (Done, 1999, Done, 1992; Dudgeon et al., 2010), but identifying a decrease in the absence of a base line is not straightforward. In our
Acknowledgments
ICSC acknowledges a postdoctoral fellowship from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (No. 2014/17815-0). LGW acknowledges a postdoctoral fellowship from Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq) (No. 150159/2015-3). RKPK benefits from a CNPq fellowship (PQ 1C), is a researcher of the National Institute of Science and Technology for Marine Tropical Environment (INCTAmbTropic) and of the National Institute of Science and Technology for the
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