Millennial-scale change in Caribbean coral reef ecosystem structure and the role of human and natural disturbance

Caribbean coral reefs have transformed into algal-dominated habitats over
the past half-century, but the role of specific anthropogenic drivers is
unresolved due to the lack of ecosystem-level data predating human
disturbance. To better understand the extent and causes of long-term
Caribbean reef declines, we produced a continuous 3,000-year record of the
ecosystem state of three reefs in Bocas del Toro, Caribbean Panama. From
fossils and sediments obtained from reef matrix cores, we tracked changes
in reef accretion rates and the taxonomic and functional group composition
of fish, coral, urchin, bivalve and benthic foraminifera. This dataset
provided a comprehensive picture of reef community and environmental
change. At all sites, reefs shifted from systems with greater relative
abundance of herbivorous fish, epifaunal suspension feeding bivalves, and
Diadema urchins to systems with greater relative abundance of
micropredator fish, infaunal bivalves, and Echinometra urchins. These
transitions were initiated a millennium ago at two less-degraded reefs
fringing offshore islands and ~250 years ago at a degraded patch reef near
the continental coast. Ecosystem shifts were accompanied by a decline in
reef accretion rates, and at the patch reef, a decline in water quality
since the 18th century. Within all cores, synchronous increases in
infaunal bivalves and declines in herbivorous fish regardless of water
quality suggest a loss of hard substrate and increasingly hypoxic sediment
conditions related to herbivore loss. While the early timing of ecosystem
transitions at the fringing reefs implicates large-scale hydrological
change, the more recent timing of change and loss of water quality at the
patch reef implicates terrigenous runoff from land-clearing. Our
whole-ecosystem reconstruction reveals that reef ecosystem deterioration
appears to follow a predictable trajectory whether driven by natural or
anthropogenic disturbances and that historical local human activities have
quickly unraveled reefs at a scale similar to longer-term natural
environmental change.