Herbivory is one of the strongest drivers of coral reef community structure (Burkepile and Hay 2006; Holbrook et al. 2016). Reductions in herbivory, often driven by overfishing, are a common cause of coral decline, loss of resilience, and phase-shifts to algae dominated states (Bellwood et al. 2004; Rasher et al. 2012; Holbrook et al. 2016). We found that herbivorous fish biomass and grazing potential were significantly lower at Varadero than nearby Rosario. In turn, Varadero had significantly higher cover of Halimeda spp., whereas the benthic community at Rosario was dominated by closely cropped turf and CCA, groups typically associated with more resilient, coral dominated reefs (Fig. 3b). Yet, despite the limited herbivore community, high sedimentation, and greater Halimeda abundance at Varadero, an extensive coral community persists between 1–12 m (Pizzarro et al. 2017; this manuscript). Total coral cover was over 2x higher at Varadero than Rosario (Fig. 3a) and among the highest levels reported in the Caribbean (Jackson et al. 2014). Thus, our results suggest herbivorous fishes played a minimal role in maintaining coral cover on Varadero.
Relatively few studies to date have examined herbivory on highly turbid reefs. Those that have, report limited herbivore communities and very low rates of herbivory (e.g. Cheal et al. 2013; Guest et al. 2016; Bauman et al. 2017). This limited herbivory can likely be ascribed to the greater attenuation of light which, when studied across depth gradients, reduces algal productivity (Tebbett and Bellwood 2021). In turn, this lower productivity may in turn support fewer grazers and lead to concurrent declines in the biomass, diversity, and grazing rates of herbivorous fishes (Brokovich et al. 2010; Cooper et al. 2019). For instance, algal productivity on the Great Barrier Reef was ~ 3–5x lower and herbivore biomass ~ 2–7x lower at 15 m than at 3 m (Russ 2003). On Varadero, the annual average daily integrated irradiance at 3.5 m between 2016–2017, when our study took place, was roughly equivalent to light levels nearly 10 m deeper on Rosario (López-Londoño et al. 2021). Thus, reductions in light due to turbidity at Varadero likely limited algal productivity and reduced the need for strong top-down control.
Because our study only involved a single sampling period it is unclear if the patterns we observed hold year-round. Herbivory is typically stronger during warmer periods and relaxes during cooler seasons (Lefèvre and Bellwood 2010). However, water temperatures are similar at both Rosario and Varadero throughout the year, with slightly cooler conditions at Rosario (López-Londoño et al. 2021). Thus, any temperature-driven fluctuations in grazing rates should be the same at both sites and not influence our overall patterns. Similarly, while seasonal upwelling influences algal cover on some Colombian reefs (Diaz-Pulido and Ferreira 2002) both Rosario and Varadero are south of the major Colombian upwelling zone in Guajira (Gomez Gaspar and Acero 2020). Accordingly, while a more in-depth evaluation of the seasonal dynamics at both sites would be valuable, we do not anticipate that it would change the overall patterns in herbivory or coral cover recorded here.
The turbid conditions at Varadero also appear responsible for maintaining the coral community. Turbidity can limit harmful interactions between high temperatures and irradiance that promote coral bleaching (Cacciapaglia and van Woesik 2016). Furthermore, turbid systems often have greater amounts of suspended particulate matter that some corals species can consume to maintain a positive energy balance, survive bleaching, and reestablish symbiosis (Anthony and Fabricius 2000; Grottoli et al. 2006; Tremblay et al. 2016). As a result, turbid reefs are garnering attention as potential refuges from thermal stress. Our study occurred at the end of a 3-year global coral bleaching event (Eakin et al. 2019). The dramatically higher bleaching frequency we recorded at Rosario (nearly one-in-ten corals still bleached) versus Varadero (fewer than one-in-fifty) suggests that protection from bleaching had substantial impacts on preserving Varadero’s coral community. Interestingly, in the early 2000’s Rodríguez-Ramírez et al. (2010) reported coral cover was dominated by Agaricia spp. and Orbicella spp. were abundant. However, both these coral groups are sensitive to bleaching and during our surveys Agaricia spp. accounted for only 6% of benthic cover, and Oribcella spp. <1.5% (Fig. 4). Accordingly, as climate change has caused increasingly frequent bleaching events, the unique abiotic conditions at Varadero that help corals survive bleaching appear to be more important for community structure than the absence of strong top-down pressure.
Yet the turbid outflow and pollution from the Dique canal also appears to make Varadero’s existence precarious. Nutrient enrichment promotes coral diseases (Vega Thurber et al. 2014) and coral microbial communities at Varadero display increased microbial diversity that is indicative of stress (Roitman et al. 2020). Further, the average disease prevalence on Varadero, while highly variable, was > 2x greater than Rosario (Fig. 4) and at depths below 10 m the reef is dominated by coral rubble and the skeletons of dead Orbicella and Agaricia spp. (Pizarro et al. 2017; López-Londoño et al. 2021). This coral mortality at depth was absent at Rosario and suggests light limitation has killed corals in the deeper zones of Varadero (> 12 m), and that further declines in water clarity could endanger shallower corals. Therefore, Varadero appears to be narrowly situated where the Dique canal’s sediment plume helps shallow corals persist under low herbivory levels, but the pollution and light limitation still threaten the reef by promoting disease and truncating the depth range where corals can survive.
Many reefs have experienced substantial declines in coral cover due to increasing pollution and coastal development but in the past decade numerous reports of robust coral communities in turbid systems have surfaced (reviewed by Zweifler et al. 2021). Results from our study and other investigations of turbid reefs suggest that rates of herbivory are low and the importance of herbivores in maintaining coral dominance on these reefs is reduced (Cheal et al. 2013; Guest et al. 2016b; Bauman et al. 2017). However, the safe operating space for these turbid reefs may also be reduced. Corals that survive in these environments must be resilient to sedimentation and either capable of tolerating low light or proficient in heterotrophic feeding. Such species typically constitute only a small portion of reef communities and as a result, expanding urbanization is likely to lead to the loss of diversity and structural complexity on most coastal reefs (Heery et al. 2018). Further, while herbivory does not appear to be essential for maintaining coral cover, the low rates of herbivory on turbid reefs could retard recovery when corals die in these turbid environments (Heery et al. 2018). Thus, while our study suggests that high rates of herbivory are not essential for maintaining coral cover on turbid coral reefs, their impacts on the resilience of these ecosystems warrants further attention. Likewise, as anthropogenic impacts on the planet increase, studying reefs in suboptimal conditions like Varadero will continue to provide insight into how future reefs will function and helps us understand processes that are important for maintaining reefs in human-dominated habitats.