Millennial‐scale change in the structure of a Caribbean reef ecosystem and the role of human and natural disturbance

Abstract

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 3000-yr 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 yr 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.

Millennial-scale change on a Caribbean reef system that experiences hypoxia

“…from ~1800 to 1000 yrs BP. Accretion rates in sites sampled in this and previous studies (Cramer et al 2017(Cramer et al , 2020. Recent samples with important trends are indicated by the black rectangle.…”

“…Notwithstanding, one of these studies (Cramer et al 2020) reported an increase in the proportion of infaunal deposit-and suspension-feeding bivalve communities over the last 1000 years and suggested this may be evidence for a gradual decrease in oxygen levels within the reef sediments over time.…”

Caribbean mangrove forests act as coral refugia by reducing light stress and increasing coral richness

“…However, based on observations in the area of phase shifts to algae and increased land clearing activities, it is likely to be linked to land‐based runoff and algal overgrowth. Observed elevated sea surface temperatures, increased nutrients, and overexploitation of herbivorous reef fishes in the area could all promote algal growth (Cramer et al 2020).…”

The transformation of Caribbean coral communities since humans

“…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].…”