Climatic and biotic thresholds of coral-reef shutdown

Climate change is now the leading cause of coral-reef degradation and is altering the adaptive landscape of coral populations1,2. Increasing sea temperatures and declining carbonate saturation states are inhibiting short-term rates of coral calcification, carbonate precipitation and submarine cementation3–5. A critical challenge to coral-reef conservation is understanding the mechanisms by which environmental perturbations scale up to influence long-term rates of reef-framework construction and ecosystem function6,7. Here we reconstruct climatic and oceanographic variability using corals sampled from a 6,750-year core from Pacific Panamá. Simultaneous reconstructions of coral palaeophysiology and reef accretion allowed us to identify the climatic and biotic thresholds associated with a 2,500-year hiatus in vertical accretion beginning ∼4,100 years ago8. Stronger upwelling, cooler sea temperatures and greater precipitation—indicators of La Niña-like conditions—were closely associated with abrupt reef shutdown. The physiological condition of the corals deteriorated at the onset of the hiatus, corroborating theoretical predictions that the tipping points of radical ecosystem transitions should be manifested sublethally in the biotic constituents9. Future climate change could cause similar threshold behaviours, leading to another shutdown in reef development in the tropical eastern Pacific. Climatic and oceanographic variability have played a dominant role in the development of reefs throughout the Phanerozoic eon10, and the recent past is no exception. In Panamá and several other locations in the Pacific, coral reefs stopped accreting vertically for 2,500 years, beginning ∼4,100 cal yr BP (ref. 8; calibrated 14C calendar years before 1950; Fig. 1a). Correlations with regional palaeoclimate proxies suggest that enhanced variability of the El Niño/Southern Oscillation (ENSO) was the ultimate cause of reef shutdown in the tropical eastern Pacific8 (TEP). Climatic shifts at that time led to environmental and cultural impacts on a global scale11,12. In this study we investigated the long-term impacts of environmental variability on coral physiology and reef development in the TEP to ascertain the climatic, oceanographic and biotic controls on ecosystem state in the past. We quantified the range of environmental conditions that corals experienced during the past ∼6,750 years to determine whether significant changes in climate or oceanography were associated with changes in coral physiology or reef accretion. We then evaluated the environmental and physiological thresholds that characterized the catastrophic phase shift to the hiatus. In Pacific Panamá, El Niño-like periods are characterized by a warm, dry climate and a reduction in seasonal upwelling. Those conditions are reversed during La Niña-like periods (Supplementary Discussion and Supplementary Fig. 1). Contemporary environmental variability is high at Contadora Island, a site in Pacific Panamá that is exposed to intense seasonal upwelling and the interannual impacts of ENSO. We extracted a 2.68-m, vertical pushcore, designated EP09-28, from the uncemented reef framework at Contadora. The framework is built of branch fragments of Pocillopora spp. corals packed in fine sediment (Supplementary Fig. 3). Through geochemical analysis of the coral skeletons, we reconstructed reef palaeoenvironments and changes in coral physiology during the entire Holocene history of the Contadora reef, from its initiation ∼6,750 cal yr BP to present (Supplementary Table 4 and Supplementary Fig. 7). To constrain environmental conditions before and after the hiatus we measured the elemental ratios and isotopic compositions of 133 diagenetically unaltered Pocillopora skeletons distributed throughout the core (Supplementary Fig. 4). Our palaeoclimatic reconstructions are based on temperature calibrations for Sr/Ca and oxygen isotopes (δ18O) using modern Pocillopora damicornis colonies from Contadora (Fig. 2 and Supplementary Figs 5 and 6). Whereas Sr/Ca in coral skeletons is primarily driven by temperature, δ18O reflects a combination of temperature and seawater δ18O (δOsw), which generally tracks hydrologic variability13 (Fig. 2).We identified a significant relationship between Sr/Ca and temperature (Fig. 2a), and between coral-reconstructed δOsw and local precipitation (Fig. 2c), in the modern corals. The modern-day calibration confirmed that Sr/Ca and δ18O records from pocilloporid corals capture the seasonal range in climate characterized by intensewinter-time upwelling of coolerwater (high Sr/Ca and high δ18O) accompanied by dry conditions (high δOsw). At each sampled horizon in the core, we used multiple coral fragments to reconstruct: palaeotemperature and palaeosalinity from Sr/Ca and δ18O (ref. 13); oceanic palaeoproductivity (upwelling), primarily from the local reservoir correction 1R (=114C; ref. 8; Supplementary Methods) and to a lesser extent from Ba/Ca (ref. 14); and coral physiology from δ13C and B/Ca (refs 15–18). Although there has been much debate over the interpretation of δ13C in coral skeletons, its variability is generally assumed to be driven by metabolic processes in the