Sea-level change as a critical factor

A number of potential mechanisms might have caused staghorn corals to become a dominant reef builder during the Middle Pleistocene in all reef provinces, including species diversification, nutrient availability, global cooling, and sea-level fluctuations. The temporal incongruence between increasing diversity and increasing dominance, coupled with the occurrence of staghorn coral–dominated reefs in the low-diversity Caribbean (fig. S1) (20), excludes diversification as the main driving force. During the Early to Middle Pleistocene, carbonate production at Caribbean reefs increased strongly, following oligotrophication of the Caribbean Sea (20, 21). In contrast, reefs in the Central Indo-Pacific are exposed to terrestrially derived nutrients as the result of increased relief. These opposite regional trends, in contrast to the global rise of staghorn coral dominance, make changes in nutrient availability an unlikely driver. Similarly, global cooling is also unlikely to have played a major role because staghorn coral dominance is most pronounced in lower latitudes (14, 22), and the onset of global cooling at 2.73 million years ago (Ma) (23) occurred before the shift in staghorn coral dominance.

Following a period of relative sea-level stability during the Late Miocene and Pliocene, the world shifted into a regime, atypical of most of Earth’s history (22, 23), that comprised up to 50 pronounced glacial-interglacial cycles, including the first major Northern Hemisphere glaciation (FMG) at 2.15 Ma. These cycles resulted in pronounced sea-level fluctuations, with amplitudes of sea-level change increasing from 60 to 80 m to over 100 m after MPT around 0.8 Ma (23, 24). Extremes in the rate of sea-level change did not top 8 m/ky before the FMG but since then increased to >8 m/ky, with extremes of up to 15 m/ky (fig. S2). The increase in amplitude was not associated with an increase in the rate of sea-level rise during deglaciations (fig. S2).

Sea-level cycles affect coral reef habitat in three ways. First, extensive shelf systems where coral reefs develop are confined to less than 100-m water depth, so that habitat is restricted during sea-level lowstands. For example, a sea-level fall of 60 m reduces the amount of habitat available for coral reefs by 69%, and during the most recent glacial maximum (Last Glacial Maximum) available space was reduced by up to 88% (2, 25, 26). Second, habitat differentiation is reduced during lowstands. For example, the loss of shelf area of less than 100-m water depth limits reef development to nearshore fringing reefs (27). These fringing reefs face the open ocean, so they experience higher wave energy than present-day high–sea-level coastal reefs that develop behind offshore barrier reefs. Third, as a consequence of the sea-level cycles, reefs were repeatedly forced to relocate across the shelf to track rising and falling levels (28). Especially in large shelf reef systems, the nearest potentially habitable area could have been tens to hundreds of kilometers away from their highstand location.

Rates of sea-level change increased substantially during the Quaternary so that during post-FMG deglaciations, sea-level rose by up to 15 m/ky (fig. S2) (29). We find a statistically significant relationship between the proportion of staghorn corals in coral assemblages and the rate of sea-level change during the Cenozoic (Fig. 4). In addition to the striking increase in dominance during the Quaternary (Fig. 3), abundant staghorn corals have been reported from some units in the Caribbean (16) and Tethyan realms (15, 17) of the Late Oligocene age, a time interval that also has elevated rates of sea-level change compared to the Middle to Late Miocene (22). Staghorn corals have a combination of two life history characteristics that make them particularly well suited to high rates of sea-level change: high growth rates and asexual fragmentation. Branches of staghorn coral colonies can achieve skeletal extension rates that are an order of magnitude higher than extension rates observed in other taxa (7) (fig. S3). Calcification rates in staghorn corals can be two times faster than in other corals (30). Acropora can reach these high linear extension rates because of a differentiation in calcification rate along the branch, and translocation of photosynthetic products: In Acropora, there is a distinct gradient along branches so that calcification rates observed 2 to 3 cm from the branch tip are only two-thirds of the rate obtained at the tips of branches (31). Photosynthesis by endosymbionts increases rates of calcification (32); however, the axial corallites of Acropora do not generally contain abundant zooxanthellae (33). Instead, the high rate of calcification at the apical polyp is maintained by the efficient translocation of photosynthetic products from the radial polyps via a complex gastrovascular system (34, 35). Recent models for the relationship between calcification, respiration, and photosynthesis suggest that calcification rates are promoted by the spatial partitioning of these processes within the coral colony (33). High rates of calcification are translated into high rates of extension via a two-stage mineralization mechanism in which a thin scaffolding develops first and then is subsequently in-filled by secondary deposits (36, 37).

Fig. 4 Relationship between inferred rates of sea-level rise and the global proportion of Acropora among global coral genus occurrences. Positive values among modeled rates of sea-level change (22) are averaged over Bartonian and younger Cenozoic subepochs and compared with the proportion of Acropora plus Isopora occurrences among all coral genus occurrences reported from the same subepochs in the Paleobiology Database. Error bars denote 95% binomial confidence intervals of proportions. R = 0.86, P = 0.001 (Pearson) and ρ = 0.59, P = 0.08 (Spearman). Solid squares, Eocene-Pliocene; open circles, Pleistocene and Holocene.

To cope with the challenges of sea-level changes, sessile organisms have the ability to disperse over large distances, settle, and rapidly occupy large areas. Branching corals can disperse over large distances during sexual reproduction and subsequently expand rapidly as the result of asexual fragmentation (38–40), thus filling habitat space more rapidly than massive corals (41). As long as environmental conditions allow, modern staghorn corals are among the fastest to recover from environmental disturbances (42). We suggest that fast growth rates, rapid recovery, and asexual fragmentation enabled staghorn corals to dominate Quaternary reefs.