The role of local and global human stressors
Although climate change is currently imperiling reef ecosystems globally [49], the early timing of the initial declines in CaribbeanAcropora corals suggests that climate change was not responsible for this first phase of Caribbean coral community transformation. In the Caribbean, anthropogenic ocean warming did not become significant until the 1970s [50-51] and warming-related coral bleaching was not observed until the late 1980s [52]. Our recent analysis of long-term trends in the dominance of A. cervicornis and A. palmatashowed that initial declines in the 1950s and 1960s were unrelated to regional or global stressors (i.e., anthropogenic temperature stress or hurricane exposure; ref 13).
Instead, the early timing of initial changes in Caribbean coral communities implicates long-standing local stressors such as fishing and land-based pollution. However, the paucity of long-term data on fishing effort/reef fish abundance or reef water quality precludes a quantitative assessment of the role of these activities in recent Caribbean-wide reef ecosystem change. Consequently, despite the well-established relationships between hermatypic coral persistence and abundant herbivorous reef fish populations and low-sediment, low-nutrient waters [3,53-55], historical fishing and land clearing have been largely ignored in most analyses of Caribbean coral declines [56]. Fortunately, a few longer-term datasets on water quality at various Caribbean reefs provide valuable insights into the role of land-based runoff in coral community change. An analysis of seawater and macroalgae nitrogen content since the 1990s from the Florida Keys implicates land-based nutrients from agriculture and development in the decades-long coral declines within that reef tract [57]. Studies based on historical and paleontological data also suggest that early reef ecosystem declines in Barbados and Panama may be attributed to increases in coastal runoff from historical land clearing for agriculture [17,58-59].
In contrast to the early transformation of Caribbean coral communities following the initial loss of Acropora in the 1950s/1960s, more recent changes since the 1980s/1990s demonstrate the heightened effects of local stressors and climate change acting on reefs simultaneously. Although our study suggests that White Band Disease was not the cause of initial Acropora declines, it confirms that it has unequivocally contributed to the loss of this genus: the second significantAcropora decline observed in our time series in the early 1980s immediately followed the first instances of this disease reported in the late 1970s [9]. Land-based runoff has been shown to exacerbate coral bleaching and disease [57,60-61], suggesting that reef eutrophication played a role in the emergence of these morbidities. Similarly, the region-wide declines in stress-tolerant and weedy corals we observed since the 1980s/1990s reveal that local and global stressors are making Caribbean reef environments unsuitable even for those corals with the hardiest of life history strategies. Indeed, recent monitoring efforts have documented declines in several stress-tolerant taxa from bleaching and disease that were initiated two decades ago [62-63] and show that several stress-tolerant species are currently rapidly succumbing to the highly lethal Stony Coral Tissue Loss Disease that does not affect Acropora [64-66]. Monitoring efforts are also documenting declines in weedy corals such as Agaricia due to recent Caribbean-wide bleaching events [67]. Thus, the shifts documented in our 131,000-year record indicate a long history of increasingly stressful environmental conditions on Caribbean reefs that began with local human disturbances and have culminated in the combined effects of local and global change.