Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs

“Fish biomass on remote, uninhabited, and protected atolls in the Central Pacific Ocean and Northwestern Hawaiian Islands is several times to more than an order of magnitude greater than that on well-studied reefs in the Western Pacific Ocean, Indian Ocean, and Caribbean Sea, most of which are unprotected and have been…”

“The response and recovery of the 4 species examined reveal that the bleaching phenomenon is highly dynamic (see also McClanahan et al. 2001).”

“For example, among corals, branching forms, e.g. Acropora and Pocillopora species, generally bleach more strongly than massive corals (e.g. Jim enez, 2001; McClanahan et al., 2001).”

“Although sublethal bleaching events may pass without significant longer term effects (Suggett and Smith 2010), more severe bleaching events can slow coral growth, reduce reproduction, and lead to major mortalities (Szmant and Gassman 1990; Berkelmans and Oliver 1999; McClanahan et al. 2001).”

“…disturbance of coral reefs, whether caused by terrestrial run-off, crown-ofthorns starfish outbreaks, over-fishing, or mass-bleaching events, generally involves increased dominance by benthic algae (Hughes, 1994; McCook, 1999; McClanahan et al., 2001; Diaz-Pulido and McCook, 2002; Wilkinson, 2002).”

“The alternative explanation is that these older parks have experienced environmental degradation, including coral bleaching, degraded water quality, and heavy fishing around the park boundaries (McClanahan and Obura 1997, McClanahan and Mangi 2000, McClanahan et al. 2001).”

“…of water temperature regimes and organism survival is based on descriptive and often site-specific field studies (McField 1999, Loya et al. 2001, McClanahan et al. 2001, Mumby et al. 2001a, Aronson et al. 2002, Berkelmans 2002, Berkelmans et al. 2004) and laboratory experiments, usually with…”

“The sites in the central Maldives, Kenya, and granitic islands of the Seychelles had high levels of mortality (McClanahan 2000, Edwards et al. 2001, McClanahan et al. 2001, Graham et al. 2006) In some areas of the southern Maldives Acropora has recently been observed in high abundance and a number…”

“Coral mortality was widespread, both regionally and globally (Baird & Marshall 1998, Berkelmans & Oliver 1999, Wilkinson 2000, McClanahan et al. 2001, authors’ pers. obs.).”

“2f), a coral species which is relatively tolerant to coral bleaching (McClanahan et al. 2001).”

“Kenyan coral reefs experience heavy fishing pressure as well as thermal stress, which make these reefs fairly unique throughout the western Indian Ocean region (McClanahan et al., 2007b; Maina et al., 2008).”

“The mean annual seawater temperature for the past 17 years is 27 C (McClanahan et al. 2001), with warm-season temperatures averaging 28 C.”

“…prevalence of anthropogenic and climateinduced disturbance and subsequent collapse of several reef systems from coral-to macroalgal dominance highlighted the critical importance of herbivory and brought this research area to the fore (Hughes 1994; McClanahan et al. 2001; Bellwood et al. 2004).”

“…0HT, UK J. Hardcastle Nature Seychelles, The Centre for Environment and Education, P.O. Box 1310, Roche Caiman, Mahé, Seychelles The loss of live coral cover following disturbances such as bleaching is often accompanied by a proliferation of macroalgae (McClanahan et al. 2001; Graham et al. 2006).”

“Indeed, the system-wide removal of herbivores has underpinned shifts to macroalgal dominance on Caribbean (Hughes 1994), Hawaiian (Hunter & Evans 1995) and east African reefs (McClanahan et al. 2001).”

“In spite of this potential for long lasting effects, most assessments of the impact of mass mortality events, especially of bleaching events, have been conducted immediately after the event or only over short observation periods (McClanahan et al. 2001, Baird & Marshall 2002).”

“…mortality in a severe stress event (e.g. the genera Acropora, Pocillopora, Stylophora) and other taxa show high bleaching levels but no or low mortality (e.g. the genera Porites, Astreopora, Turbinaria;Berkelmans and Oliver, 1999; Marshall and Baird, 2000; McClanahan et al., 2001; Obura, 2001).”

“But, there is still little evidence either way (but see McClanahan et al. 2001).”

“…on Caribbean reefs (Williams et al. 2001a,b) and evidence that coral bleaching and disease have precipitated dramatic ecological shifts at several reef locations worldwide (Ostrander et al. 2000, Aronson & Pretch 2001, McClanahan et al. 2001, Diaz-Pulido & McCook 2002, Aronson et al. 2004).”

“Some of these areas exhibit more catastrophic changes marked by phase shifts, where the system flips rapidly from one ecosystem state to another (McClanahan et al. 2001; Bellwood et al. 2004).”

“…2009 7CORAL RESPONSE TO CLIMATE CHANGE 102 yr 1 and l2 ¼ 5.8767 3 103 yr 1, from the crown diameter declines during a bleaching event reported in McClanahan et al. (2001) and the projected area–surfacearea conversion coefficients from Chancerelle (2000) mentioned at the beginning of this…”

“…to bleaching and have a higher mortality than the massive species of Porites and Favia, which are more tolerant of bleaching (Fisk & Done 1985, Harriott 1985, Brown & Suharsono 1990, Gleason 1993, Hoegh-Guldberg & Salvat 1995, Marshall & Baird 2000, McClanahan 2000, McClanahan et al. 2001).”

“Satellite temperature is often well correlated with in situ temperature data when temperature data is pooled over space and time (McClanahan et al. 2001; Aronson et al. 2002).”

“Additionally, assemblages may change regardless of management and disturbance by ENSO, in which case recovery may need to be assessed with respect to contemporary, rather than past conditions, particularly at unmanged sites (A.J. Underwood, personal communication).”

“…direct contact with coral colonies compared to other major functional groups of benthic reef organisms (Barott et al. 2012b, Wild et al. 2014, Jorissen et al. 2016) and rapidly colonize space following large-scale coral mortality (McClanahan et al. 2001, Adjeroud et al. 2009, Mellin et al. 2016).”

“In contrast, detailed analyses of coral cover and community structure in Kenya also indicated a lower recovery of managed reefs than fished reefs.”

“A few field studies have shown evidence of reduced macroalgal cover associated with increases in herbivore abundance in reserves and fisheries management zones (McClanahan et al. 2001, Williams & Polunin 2001, Mumby et al. 2006).”

“However, enhanced coral resilience is not always found in reserves elsewhere in the world (McClanahan et al. 2001), so predictive models for reef communities should include other local factors, such as nutrient loading, that may overwhelm reserve effects.”

“maintaining ecosystem function [22]) by consuming macroalgae that can otherwise outcompete corals when new space becomes available following disturbance [23,24,25,26,27].”

“By far the most abundant (>80% cover) species of soft coral were in the family Alcyoniidae, which have had high levels of impact following bleaching events on other Indian Ocean reefs (McClanahan et al. 2001; Floros et al. 2004).”

“Nonetheless, standard Thalassia herbivory assays in these patch reefs report daily bite frequencies of around 30% (McClanahan and Muthiga, 1998; McClanahan et al., 2001b).”

“A regression test for relationships between mean coral size and mortality of each taxon across the 1998-bleaching event was undertaken using mortality data from before and 6 months after the 1998 bleaching event ( McClanahan et al. 2001 ).”

“In 1998, the El Niño coral bleaching event affected large parts of the Indian Ocean, resulting in widespread coral mortality (e.g. Souter et al., 2000; Spencer et al., 2000; Lindahl et al., 2001; McClanahan et al., 2001).”

“demonstrate reduced resilience and remain in a degraded state with macroalgae continuing to dominate the benthic substratum [7–11].”

“…reefs has raised questions about the vulnerability of inshore reefs to a phase-shift from coral to macroalgal dominance (Done et al. 2007), mirroring observed changes in other coral reef systems around the world (Hughes 1994, McClanahan et al. 2001, Graham et al. 2006, Ledlie et al. 2007).”

“2002; McClanahan and Maina 2003), water flow (Nakamura and van Woesik 2001), fishing management (McClanahan et al. 2001), regions (Marcus and Thorhaug 1981; Coles 1997; McClanahan et al.”

“Sargassum was the dominant alga following phase-shifts to macroalgal dominance on east African reefs (McClanahan et al. 2001; Graham et al. 2006) and in an experimentally induced phase-shift on an inshore reef in the central GBR (Hughes et al. 2007).”

“Coral mortalities at the taxon level and for the 2 monitoring sites were calculated as the differences in the number of colonies per meter of line transect before and after the 1998 thermal anomaly (McClanahan et al. 2001).”

“The removal of macroalgae, and in particular leathery brown macroalgae, by herbivorous fishes is a crucial process on coral reefs, moderating the competition for benthic space between corals and macroalgae and potentially facilitating the recovery of coral populations following macroalgal dominance (McCook 1999; McCla…”

“), while Sargassum is important in other comparatively similar areas (McClanahan et al. 2001; Hoey and Bellwood 2009), with the capacity to dominate coral reef communities after experimental phase shifts (Bellwood et al.”

“1997) or coral bleaching (Done 1999; McClanahan et al. 2001) disturb the system.”

“Trajectories of algal succession on coral reefs are generally expected to progress from bare space to a microalgalfilm, and then tofilamentous turf algae and crustose coralline algae, followed in turn by corticated algae, fleshy macroalgae, and erect and foliose calcified algae (McClanahan, 2000; McClanahan et al., 20…”

“…to disturbance, as seen in patterns of mortality during the bleaching response (Marshall and Baird 2000, McClanahan 2000, Loya et al. 2001, McClanahan et al. 2001, Baird and Marshall 2002), while long-term shifts in community structure will be controlled by both speciesspecific resistance…”

“Sensitivity can take various forms, but here we define and document it as the percentage of bleached corals as a proxy for coral morbidity and mortality (Fitt et al., 2001; McClanahan et al., 2001).”

“…were previously conducted in the context of ecological disturbances such as hurricanes (Hughes 1989; Rogers et al. 1997), El Niño events (McClanahan et al. 2001), changes in the population of herbivores (Lewis 1985; Smith et al. 2001; Thacker et al. 2001) and eutrophication (Goreau…”

“Thin tissue layers of branching corals provide less energy-rich compounds and photosynthetic products, resulting in lower adaptability to drastic environmental changes (Jiménez et al., 2001; Mc Clanahan et al., 2001).”

“decussata has been reported to have mixed to tolerant thermal bleaching characteristics (Marshall and Baird 2000; McClanahan et al. 2001; McClanahan 2004).”

“This is often linked to phase shifts from coral to macroalgal dominance [3,4,5,6].”

“Also in other countries the influence of 1998 coral bleaching on the coral reef ecosystem was of concern [e.g. (McClanahan et al., 2001)].”

“Sargassum was the dominant alga following phase-shifts to macroalgal dominance on east African reefs ( McClanahan et al. 2001; Graham et al. 2006) and in an experimentally induced phase-shift on an inshore reef in the central Great Barrier Reef (GBR; Hughes et al. 2007).”

“Most previous studies either were conducted on reefs that had undergone a bleaching event (McClanahan et al. 2001; Fabricius et al. 2004) or were short-term laboratory experiments that involved temperature manipulation (Edmunds 2005; Fitt et al. 2009; Bellantuono et al. 2012; Oliver & Palumbi…”

“Furthermore, small-scale management actions may not provide much protection against large-scale climate-related disturbances (Graham et al., 2008; McClanahan et al., 2001).”

“Keywords: Coral reefs; Water quality; Disturbance; Sinularia polydactyla; American Samoa; Alcyoniidae”

“…of herbivorous reef fishes in mediating the transition from a healthy, coraldominated state to a less desirable, degraded macroalgal-dominated system (Hughes 1994, McClanahan et al. 2001, Pandolfi et al. 2003, Bellwood et al. 2004, 2006, Graham et al. 2006, Mumby et al. 2006, Hughes et al. 2007).”