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].