A major threat to coral reefs is the phase shift from corals towards macroalgae, promoted by eutrophication and warmer waters and exacerbated by the removal of herbivorous fish by overfishing (Hughes et al. 2007; Ledlie et al. 2007; Pratchett et al. 2014). Key browsing fish species, their impact on reefs and the relationships to fisheries management are geographically variable and still largely unknown from the East African Coast. We characterized the herbivore community and quantified their browsing pressure at six Kenyan reefs within three distinct fisheries management zones, and related realized browsing pressure to herbivore biomasses and other common reef indicators. Browsing pressure on the presented macroalgae was two-fold greater in areas with partial fishing restrictions and up to three times higher at fully protected reefs, and this higher browsing pressure correlated positively with the higher biomasses of herbivorous fish present at these protected reefs. In line with previous studies, only a select few dominant browsers were identified (Puk et al. 2016), the key species varied strongly across reefs (Cvitanovic and Bellwood 2009) and also included herbivores not specifically classified as browsers (Chong-Seng et al. 2014). Browsing pressure correlated poorly with coral cover suggesting that coral-dominated reefs can persist even under low levels of browsing (Cernohorsky et al. 2015; Holbrook et al. 2016). The implication of limited browsing activity, however, is that these reefs might be impaired in their ability to absorb disturbances that stimulate macroalgal growth (Holbrook et al. 2016). Overall, our results affirm that fishing restrictions can have a strong positive influence on herbivorous fish biomass and highlight how this can be expected to increase reef resilience by supporting higher rates of browsing.
Shifts in the herbivore community and strong reductions in key functional groups including browsing, scraping and excavating herbivores were found at the fished study sites, confirming results found at the northern Kenyan coast (Humphries et al. 2015), and potentially undermining the resilience of these reefs (Nyström et al. 2008; Holbrook et al. 2016). Herbivorous fish biomass in the no-take zones and marine reserve (except site 3) was comparable with worldwide averages from protected reefs (Edwards et al. 2013) and this biomass was around 10 times lower at the sites without fishing restrictions. An exception was the macroalgae-dominated study site 3 in the marine reserve, which had an equally low fish biomass as the fished reefs. At this site and at the fished reefs, no large herbivores (> 30 cm) were recorded, indicative of severe overfishing (McClanahan et al. 2008), habitat degradation (Rogers et al. 2018) or both. The observed reductions in herbivore biomass were most striking for large-bodied and functionally important fish such as browsers, scrapers and excavators. This impact of high fishing pressure on key functional groups has been observed worldwide (Edwards et al. 2013; Humphries et al. 2014), but is remarkably severe along the East African Coast (McClanahan et al. 2008; Humphries et al. 2014). It is therefore promising that the small and recently-established community managed no-take zone of Wasini (study site 6) has been able to sidestep this trend and now boasts the highest fish biomass of all the sites studied here, despite its nearshore location (Johansson et al. 2013). Unlike other young community managed reserves in Kenya where only grazers recovered (Humphries et al. 2015), also browsers and scrapers are abundant at Wasini. Our data suggest that of all herbivorous guilds, grazers are least impacted by high fishing pressure, with ‘only’ a three-fold reduction of their biomass at fished sites compared to the no-take zones, conform findings of Heenan et al. (2016) in American Samoa. Sea urchins and territorial damselfish showed highest abundances in fished zones and it is likely that they benefit from reduced competition as well as reduced predation by larger fish (Ceccarelli et al. 2005; McClanahan 2008).
In line with the higher biomasses of roving herbivorous fish, the removal of macroalgae was up to 3-fold greater in the no-take zones and more than two-fold greater in marine reserves compared to the fished zones. Consumption of Sargassum in the no-take zones and marine reserves was higher than found in a previously studied community managed area in northern Kenya where only 20% was consumed in 24 h (Humphries et al. 2015), but somewhat lower than consumption rates (81 – 92% in 24 h) found at the Great Barrier Reef (Hoey and Bellwood 2010). Padina consumption fell broadly within the ranges previously found (Humphries et al. 2015; Plass-Johnson et al. 2015). It seems that despite widely varying species compositions across broad geographic scales, realized browsing pressure at unfished reefs is quite comparable (Tebbett et al. 2020), highlighting the role local drivers can play in determining browsing pressure. Interestingly, consumption at the fish-depauperate and macroalgae-dominated study site 3 was also relatively high. This result contrasts with previous studies where higher densities of macroalgae were associated with lower browsing rates, supposably through feeding dilution (Chong-Seng et al. 2014) or predator avoidance (Hoey and Bellwood 2011). The combination of both low fish and urchin biomass, the absence of browsing recorded on RUV, but relatively high macroalgae consumption at this structurally-eroded and macroalgae-dominated site is indeed surprising. It should be noted, however, that the high consumption was mainly driven by removal of Padina, the macroalgae which appeared overall more palatable in this and other experiments (Humphries et al. 2015), compared to Sargassum, the macroalgae which dominated this reef and is most often associated with phase shifts (Hughes et al. 2007). Still, the organism responsible for the high removal of Padina at this site remains unidentified and could possibly include overlooked species such as nocturnal crabs (Francis et al. 2019). At the two fished study sites, consumption was higher compared to reports of other overfished or macroalgae-dominated reefs. For example, Sargassum sp. removal rates of only 2% in 4.5 h were found on macroalgae-dominated reefs in the Seychelles (Chong-Seng et al. 2014). At the heavily fished zones of this study, despite the low biomass of browsing fish, macroalgae removal is possibly still realized by small-bodied grazers and sea urchins.
The possibility that small-bodied grazers can endure high fishing pressure and control macroalgal establishment could be seen as hopeful (Cernohorsky et al. 2015; Knoester et al. 2019; Müller et al. 2021), yet there are several reasons to be cautious. First, small herbivorous fish are likely to be targeting leaves or epiphytes only, without removing the holdfasts of macroalgae (Streit et al. 2015). Second, small herbivorous fish appear more vulnerable to bleaching events and the ensuing habitat loss of branching coral (Nash et al. 2016). In addition, when bleaching events open up large areas of space, macroalgal settlement and growth is likely to overwhelm the grazing capacity of small herbivores, increasing chances of a phase shift (Williams et al. 2001). We suppose this could have happened at study site 3 during the strong 1998 El Niño (McClanahan et al. 2001), despite the implemented partial fishing restrictions (Williams et al. 2019). Lastly, while increasing numbers of sea urchins can partially compensate for the loss of herbivorous fish (McClanahan 2014), the intensity of their scraping feeding method can undermine long-term reef development through bioerosion (Carreiro-Silva and McClanahan 2001) and hinder coral settlement (Humphries et al. 2020). In addition, as illustrated by the negative correlation between sea urchin abundance and macroalgae consumption in this study, browsing pressure by urchins (at overfished reefs) appears to be relatively small compared to the browsing pressure by herbivorous fish (at protected reefs). Hence, at overfished reefs, small-bodied fish and sea urchins may partially take over the role of larger herbivorous fish in controlling macroalgal growth, but such a change in control is likely to undermine reef resilience.
The apparent limited functional redundancy of browsers at the studied protected reefs may also have implications for reef resilience, as the loss of key species can have large detrimental impacts on ecosystem functioning (Cheal et al. 2013; Nash et al. 2016). In accordance with reports from numerous preceding studies using macroalgae buffet assays, browsing in this study was dominated by a few species only (Puk et al. 2016) and with marked variation in dominant species across sites (Cvitanovic and Bellwood 2009). Naso elegans was among the dominant browsers in this study and closely-related species have been identified as dominant browsers across the Indo-Pacific (Hoey & Bellwood, 2009; Plass-Johnson et al., 2015; Welsh & Bellwood, 2015), highlighting the importance of this genus in macroalgal control across broad geographic scales. Browsing was not only performed by those classified as browsers and this supports several studies that suggest plasticity in functional roles exists (Bellwood et al. 2006; Chong-Seng et al. 2014; Tebbett et al. 2020). Indeed, scraping parrotfish were recorded taking substantial amounts of bites as has been found in previous studies (McClanahan et al. 1994), but are more likely to have been targeting epiphytes (Lefèvre and Bellwood 2011; Clements et al. 2017). Interestingly, Siganus spp. and Kyphosus spp., species frequently identified as dominant browsers at the Central Indo-Pacific and Great Barrier Reef (Michael et al. 2013; Puk et al. 2016) were not recorded biting in this study despite their presence in nearby seagrass habitat and at the reef crest. Instead, Siganus spp. in the Western Indian Ocean have been shown to target more delicate and turf algae (Humphries et al. 2015; Ebrahim et al. 2020). Kyphosus spp., situated higher in water column, might have been feeding on drifting algae instead (Carpenter 1986). Altogether, these results align with other browsing studies in the Indo-Pacific in that they identify only a select and sometimes surprising group of species responsible for macroalgal removal from the diverse assemblage of potential browsers present. This variability may in part explain the finding that the reef with the highest herbivore biomass in this study did not bolster the highest browsing pressure, and especially consumption of Sargassum was relatively low here. Thus, in addition to the biomass of herbivores present, realized browsing pressure is likely also depending on many more factors such as spatial restrictions (Puk et al. 2016), behavioural variation (Bennett and Bellwood 2011) as well as temporal variation (Lefèvre and Bellwood 2011; Seah et al. 2021).
The variation in browsing pressure found can be indicative of divergent resilience between the studied reefs and their fisheries management (Nyström et al. 2008). Holbrook et al. (2016) experimentally identified a coral to macroalgae tipping point when herbivore biomass dropped below about 50 kg ha-1 in Moorea. This experimental biomass threshold corroborates field observations from reefs in Indonesia, where a lack of macroalgal removal was observed at herbivorous fish biomass levels below 50 kg ha-1 (Plass-Johnson et al. 2015). Three of the six Kenyan reefs included in the current study harboured an herbivore biomass that was just above this threshold. On two of these reefs, coral is still dominant over macroalgae. This finding is in agreement with data from Singaporean (Bauman et al. 2017), Indian (Cernohorsky et al. 2015) and Indonesian (Plass-Johnson et al. 2015) reefs, where macroalgae removal and coral dominance are still realized with herbivorous fish biomasses as low as 80 kg ha-1. Nevertheless, reefs like these might be pushed to macroalgae dominance through an external disturbance such as bleaching (Williams et al. 2001). The minimum herbivore biomass needed to absorb such increasingly common disturbances remains unknown for the Indo-Pacific (Roff and Mumby 2012), but could possibly lie around 200 kg ha-1 at our study sites as above this threshold browsing pressure was found to level off. In the marine reserve, a coral-dominated and a macroalgae-dominated reef co-exist under roughly equal browsing pressure. This co-existence could be indicative of alternative steady states (Holbrook et al. 2016) and illustrates that shifts to alternative stable states can be difficult to reverse even when ambient browsing pressure is relatively high (Schmitt et al. 2019). In such cases, the protection of herbivorous fish could be reinforced by removing macroalgae manually in an effort to push the ecosystem back to coral dominance (Ceccarelli et al. 2018; Williams et al. 2019). More effective, however, would be to keep herbivore levels well above phase-shift thresholds and prevent macroalgal dominance in the first place (Anthony et al. 2015). Our results indicate that fisheries management through marine reserves and no-take zones in particular, even small-scale and community-managed, have the potential to safeguard the diversity and biomass of functionally important herbivorous fish. Following effective management, a high level of macroalgal control is realized as large-bodied browsing and scraping fish seem to benefit markedly from fisheries protection. Although gains in browsing pressure appear to level off with increasing herbivore biomass and reasonable levels of browsing were still realized at fished study sites, the long-term resilience of these fished reefs is uncertain given the eroding nature of urchin browsing (Carreiro-Silva and McClanahan 2001), the high susceptibility of small-bodied herbivorous fish to coral loss (Nash et al. 2016) and their limited capacity to control sudden increases in macroalgae (Williams et al. 2001; Streit et al. 2015). Therefore, we recommend to continue the establishment of a network of community managed no-take zones to allow for the recovery of herbivorous fish biomass well above potential phase-shift thresholds, increase ecosystem resilience, promote local stewardship and move towards sustainable use of coral reefs (Topor et al. 2019). Such local management could help restore and maintain coral dominance and provide heightened resilience against large-scale disturbances during the Anthropocene.