The transformation of coral communities from pre-human period to present
Our 131,000-year record of coral community composition reveals that since humans arrived in the Caribbean, coral reefs throughout this region have transformed from systems dominated by competitiveAcropora corals typified by fast growth, large and structurally complex colonies, and high rates of reproduction via fragmentation and lower tolerance to human disturbances to systems dominated by stress-tolerant and weedy corals with relatively slower growth, lower-relief colony forms, and higher tolerance to human disturbances (Figures 2,3). Initial significant declines in Acropora occurred by the 1960s, a decade before the first recorded instances of White Band Disease and two decades before the die-off of the Diadema urchin and widespread coral bleaching. These early Acropora declines were related to local human stressors but not regional stressors including climate change [13], although more recent outbreaks of White Band Disease since the 1990s have been linked to climate change [42]. The initial mid-20th century loss ofAcropora was followed by a lagged increase in the prevalence of stress-tolerant and weedy corals that began in the 1970s and 1980s. By 2005-2011, these community shifts culminated in previously subdominant stress-tolerant and weedy coral taxa being present at 2-3 times more sites than Acropora , the genus which had continuously dominated shallow reef zones across the Caribbean throughout the Pleistocene and Holocene up until the mid-20th century [13,18,29]. The loss of Acropora also appears to have facilitated an increase in the prevalence of Millepora , a non-framework building hydrozoan with a competitive life history strategy (Figures 2a,3a).
Although initial declines in Acropora predate regional disturbances, subsequent changes bear a clear imprint of anthropogenic climate change. For instance, while the prevalence of stress-tolerant and weedy corals is significantly higher today than the pre-human period, increases generally leveled off or reversed beginning in the late 1980s. The slowdown of increases in these corals is likely a response to the rapid explosion in benthic macroalgae following the die-off of the keystone herbivore Diadema antillarum and increases in bleaching-related mortality from anthropogenic temperature stress. The more marked declines in Agarcia compared toPorites likely reflect the greater sensitivity of Agariciato thermal stress: Agaricia experienced widespread bleaching episodes during thermal anomalies in the 1980s and 1990s [43-45]. The post-1980s declines/plateaus in stress-tolerant and weedy species shown in this study are also a reflection of the increasingly frequent epizootics affecting these corals over the past 2-3 decades and that are linked to a combination of local and global anthropogenic stressors [46].
Our time series suggests that the Caribbean-wide loss of Acroporacorals opened up both physical substrate and niche space for formerly subdominant corals with stress-tolerant and weedy life history strategies to occupy. The uniform rarity of Acropora and consistently high prevalence of weedy and stress-tolerant species (particularly Siderastrea , Agaricia , and Porites ) have greatly reduced the distinctiveness of modern coral communities at larger geographic scales, resulting in a Caribbean-wide homogenization beginning in the 1960s at the midslope zone and in the 1980s at the reef crest zone (Figures 2-4). The homogenization of reef coral communities following the loss of Acropora and Orbicella has been reported for the Florida reef tract [47] and Belize and Panama [15]. However, our study shows that coral communities have become more homogeneous across the entirety of the Caribbean. Although overall community distinctiveness has declined since the baseline historical period (1500-1959), this trend leveled off by the 1990s as increases in the prevalence of stress-tolerant and weedy corals were halted following climate change-related bleaching and disease (Fig 4).
Although broadly similar compositional changes occurred in coral communities at the reef crest and midslope zones, subtle distinctions in the trajectories of change between zones provide insight into their varying susceptibilities to different stressors. Declines in community dissimilarity were more striking at the midslope, reflecting the more precipitous decline of A. cervicornis at this zone compared to the decline of A. palmata at the reef crest (Figures 2a,3a). This pattern may reflect declines in reef water quality from runoff, as increased turbidity would most likely have a greater effect on deeper reef zones due to increasing light attenuation with depth. However, the significant post-1980s declines in the prevalence in stress-tolerant and weedy corals that occurred at the reef crest (but not midslope) zone may reflect higher coral mortality from (1) anthropogenic bleaching in shallower zones that experience greater thermal stress and/or (2) the die-off of the Diadema urchin that prefers shallower reef zones [48].