Detecting Photosymbiosis in Fossil Scleractinian Corals

Chiara Tornabene, Rowan C. Martindale, Xingchen T. Wang, Morgan F. Schaller
2017 Scientific Reports  
The evolutionary success of reef-building corals is often attributed to photosymbiosis, a mutualistic relationship scleractinian corals developed with zooxanthellae; however, because zooxanthellae are not fossilized, it is difficult (and contentious) to determine whether ancient corals harbored symbionts. In this study, we analyze the δ 15 N of skeletal organic matrix in a suite of modern and fossil scleractinian corals (zooxanthellate-and azooxanthellate-like) with varying levels of diagenetic
more » ... alteration. Significantly, we report the first analyses that distinguish shallow-water zooxanthellate and deepwater azooxanthellate fossil corals. Early Miocene (18-20 Ma) corals exhibit the same nitrogen isotopic ratio offset identified in modern corals. These results suggest that the coral organic matrix δ 15 N proxy can successfully be used to detect photosymbiosis in the fossil record. This proxy will significantly improve our ability to effectively define the evolutionary relationship between photosymbiosis and reef-building through space and time. For example, Late Triassic corals have symbiotic values, which tie photosymbiosis to major coral reef expansion. Furthermore, the early Miocene corals from Indonesia have low δ 15 N values relative to modern corals, implying that the west Pacific was a nutrient-depleted environment and that oligotrophy may have facilitated the diversification of the reef builders in the Coral Triangle. Through photosymbiosis, dinoflagellates, called zooxanthellae, live within the tissue of many modern scleractinian corals. Zooxanthellae photosynthesize within the coral tissue providing corals with most of their energy, while the coral hosts in turn live in shallow, clear waters where zooxanthellae have optimal exposure to sunlight for photosynthesis 1-3 . Although both zooxanthellate and azooxanthellate scleractinians exist and can build reefs, a symbiotic relationship with zooxanthellae is an obvious advantage. Zooxanthellae provide corals with photosymbiotic byproducts (e.g., oxygen and glucose), which allow the corals to calcify at an expedited rate, making zooxanthellate corals more efficient reef-builders than azooxanthellate corals in shallow, oligotrophic conditions 2, 4, 5 . Photosymbiosis is, therefore, considered a key aspect of modern corals and thought to be the main driver of the Triassic expansion and diversification of shallow-water scleractinian corals 1, 6-10 . Nevertheless, since zooxanthellae live within the soft tissue of corals, they are not directly preserved in the fossil record, making it difficult to determine whether fossil corals had symbionts, when photosymbiosis originated, or how this relationship evolved through time. Morphological characteristics of coral skeletons (corallite size, growth form, and level of corallite integration 11 ) are frequently used to infer photosymbiosis in the fossil record and are often used in Phanerozoic compilations of coral-zooxanthellae symbiosis 8, 11-13 . For example, zooxanthellate corals tend to be colonial and have small, highly integrated corallites whereas azooxanthellate corals tend to have solitary growth forms and larger polyps 11 . Additionally, some coral colony morphologies are influenced by the presence of zooxanthellae and are used in the fossil record to demonstrate dependence on sunlight 14 . A delicate plate-like or platy coral morphology, for example, is common in quiet, deep, poorly-lit waters where corals need to maximize their exposure to sunlight for zooxanthellae photosynthesis 14 . Morphological characteristics, however, are not definitive and can be misleading when trying to identify whether extinct species, rather than coral assemblages, were symbiotic 13, 15 . More recently, macroscopic and microscopic growth bands have been used to infer photosymbiosis in corals 9, 10 . Macroscopic density bands, which are inferred to be annual growth bands, have been used to estimate fossil coral growth rates as a proxy for ancient photosymbiosis because modern zooxanthellate corals can grow faster than their azooxanthellate counterparts 9 . Alternatively, the regularity of microscopic skeletal growth bands in the fibrous aragonitic fibrous bundles of coral skeletons has also been proposed as a signature of photosymbiosis 10, 16, 17 . Published: xx xx xxxx OPEN www.nature.com/scientificreports/ 2 SciEntific REPORTS | 7: 9465 |
doi:10.1038/s41598-017-09008-4 pmid:28842582 pmcid:PMC5572714 fatcat:zp5lp6rw5nbfvot3y7zvn5dgma