Photosymbiosis: The Driving Force for Reef Success and Failure

Abstract

Photosymbiosis has been an important process in the evolution of ancient reef systems and in reef success today. Modern reefs and many of those in the geologic past inhabited nutrient-depleted settings. The complete collapse of some ancient reef ecosystems may be attributed to the breakdown of the ecologic and physiologic relationships between symbiont and host. Many algal groups developed symbioses with calcifying metazoans and protists and live with them, but the most common of these today are dinoflagellates in the genus Symbiodinium, sometimes called zooxanthellae. This photosymbiotic relationship conferred important metabolic advantages to both partners, allowing exploitation of tropical, shallow-water oligotrophic settings. In addition to improved metabolism, a by-product was rapid calcification which increased the growth of reefs and provided advantages to the hosts through larger and stronger skeletal support. Strong evolutionary pressures exerted by the symbiont-host relationship created bonds and favored longevity and adaptive novelty. Photosynthesis accounts for the remarkable reef growth and carbonate sedimentation in the tropics. Photosymbiosis gave reef organisms an adaptive edge to develop new life strategies that could not be developed by organisms which did not foster this relationship. Many living calcified organisms harbor many different photosymbionts and likely a variety of ancient calcified organisms did too (foraminifera, calcified sponges, corals, brachiopods and bivalve mollusks). Symbiodinium now a dominant symbiont apparently appeared in the Eocene and so was probably not utilized by earlier reef organisms, although the fossil record of dinoflagellates most closely related to Symbiodinium extends back to the Triassic. Today Symbiodinium inhabits a wide variety of unrelated host organisms from protists to mollusks. While the identity of more ancient photosymbionts is unclear, indirect evidence suggests photosymbiotic ecosystems existed as far back as the Proterozoic and possibly even earlier.Assessment of photosymbiosis in ancient reef ecosystems requires recognition of specific characteristics possessed by the calcifying reef organisms. Since the symbionts do not fossilize, the presence of photosymbiosis in fossils is a working hypothesis based on modern symbioses and best confirmed by a set of specific morphologic adaptations and isotopic analyses. Important among these is the thin tissue syndrome—the modification to achieve the “solar panel” effect. Large size and unusual or complex morphology also may indicate photosymbiosis. In the case of colonial organisms such as corals, high levels of corallite integration, where corallites are modified for increasing cooperation, may assist because most colonial photosymbiotic organisms today, such as corals, are exclusively photosymbiotic.Analysis of organisms and reefs through geologic time permits assessment of the strength of photosymbiosis as a driving force. Reef ecosystems revealing the strongest assessment for photosymbiosis are those of the mid-Paleozoic (Late Ordovician to Devonian), late Paleozoic, early Mesozoic and Neogene. The Early Cambrian archaeocyathan (sponge) reefs indicate photosymbiosis but perhaps with different ancient symbionts such as cyanobacteria, also contained in some modern sponges. Reef ecosystems of the late Paleozoic and early part of the Jurassic indicate the presence of some photosymbiosis. The extinction of many photosymbiotic reef ecosystems during critical intervals of mass extinctions may have been driven by the failure of the symbiosis or demise of the symbionts. Reef gaps in the geologic record reflect the absence of photosymbiosis. The present-day reef crisis involves disturbance of photosymbiosis, and study of future reef declines will benefit by application of data from the fossil record.

Harnessing stratigraphic bias at the section scale: conodont diversity in the Homerian (Silurian) of the Midland Platform, England

“…Large size and high degree of colony integration in favositids are commonly taken as indicator of their photosymbiotic mode of growth (e.g. Stanley & Lipps ) and large colonies suggest a position within the photic zone. The boundary between PS1 and PS2 corresponds to a relative sea‐level fall that equates to the basal Much Wenlock Limestone Formation sequence boundary.…”

From rolling stones to rolling reefs: a Devonian example of highly diverse macroids

“…) and, more interestingly, photosynthesis efficiency (Stanley & Helmle ). For Palaeozoic rugose and tabulate corals, these effects are not easy to test but it is commonly admitted that they shared similar physiology as suggested by similar growth and colony integration (Coates & Jackson ; Stanley & Lipps ), or stable isotopes of the coral skeleton (Zapalski ; Zapalski et al . , and reference therein).…”

Polymorphic adaptations in metazoans to establish and maintain photosymbioses

“…Together with sponges, corals are the main contributors in establishing reefs (Stanley & Lipps, ; Lipps & Stanley, ) and the diversity of species that harbour photosymbionts is comparable between these two taxa. Yet, cnidarians are either photosymbiotic with chlorophytes (Kovacevic, ) or dinoflagellates (Muller‐Parker et al, ); in rare cases even with both (Fig.…”

“…; Verde & McCloskey, ). Their photosymbiosis with Symbiodinium is thought to underlie the ability of corals to form massive reefs: more than 95% of the energy required is provided by the symbiont's photosynthetic activity (Muscatine, Pool & Trench, ; Stat et al, ; Harii, Yamamoto & Hoegh‐Guldberg, ; Stanley & Lipps, ). This energetic boost provides the energy needed for light‐enhanced calcification (Goreau, ; Muscatine et al, ; Roth, ).…”

“…The host shelters the symbiont or the kleptoplasts against predators and environmental fluctuations, and supplies sufficient inorganic compounds, such as CO 2 , for photosynthesis (Pearse & Muscatine, ; Stat, Carter & Hoegh‐Guldberg, ; Yellowlees, Rees & Leggat, ), although CO 2 limitation in the host can occur (Rädecker et al, ). In turn, the host receives photosynthates, mainly in the form of fixed carbon, which can meet at least 50% of their overall nutritional requirements (Fitt, Fisher & Trench, ; Klumpp & Griffiths, ; Stat et al, ; Hernawan, ; Stanley & Lipps, ). In comparison, kleptoplasts are probably only able to supply their host slugs with between 1% (Rauch et al, ) and 60% (Raven et al, ) of their nutritional requirements.…”