Pamela Hallock

Nutrient excess and the demise of coral reefs and carbonate platforms

Growth rates of corals on Holocene reefs indicate that carbonate platforms should easily keep pace with long-term subsidence and sea-level changes, yet drowned reefs and platforms are common in the geologic record. Recognition of the negative influence of nutrients on reef communities provides a clue to that paradox. The primary carbonate-sediment producers of the coral reef community are highly adapted to nutrient-deficient environments. Input of nitrates and phosphates stimulates growth of plankton, which reduces water transparency, limiting depth ranges of zooxanthellate corals and calcareous algae and thereby reducing carbonate production. Higher nutrient concentrations and plankton densities also stimulate growth of fleshy algae and ahermatypic suspension-feeding animals in the benthos. Besides displacing hermatypic algae and corals, many of these fastgrowing competitors are bioeroders that actively destroy thze reefal structure. Because rates of carbonate production and bioerosion are similar, even modest increases in nutrient availability can shift a reef community from net production to net erosion. In the geologic record, drowned reefs and carbonate platforms typically exhibit evidence of nondeposition, bioerosion, and reduced redox potential, which indicate excess nutrient availability during drowning. Drowned reefs overlain by shales are possible victims of nutrients in terrestrial runoff that suppressed reef growth before arrival of siliciclastic sediments. Other drowned platforms may have succumbed during rapid pulses of sea-level rise that flooded previously subaerial platforms. Nutrients in the soils of the flooding platform were mixed into surface waters, suppressing reef growth. The reef drowned if submergence proceeded beyond the critical depth before the excess nutrients were exported from the system. Other mechanisms for reef drowning by excess nutrients include changes in local or regional upwelling patterns or mid-ocean overturn.

The role of nutrient availability in bioerosion: Consequences to carbonate buildups

Abstract Zooxanthellate organisms, which are among the major carbonate producers on coral reefs, are highly adapted to nutrient-deficient conditions and tend to be outcompeted by filamentous or fleshy algae if nutrients are abundant. Reef-dwelling bioeroding organisms, on the other hand, seem to increase in abundance with increasing availability of nutrient and food resources. Maximum rates of calcium carbonate production in a reef system are comparable in magnitude to maximum rates of bioerosion. The dynamic interplay between accretion destruction of coral reefs is therefore likely to be strongly influenced by nutrient availability. Nutrient availability may also influence development of carbonate facies. In reef systems that develop in oligotrophic waters, skeletal sands and framework should dominate carbonate buildups. In systems that develop in mesotrophic waters, enhanced bioerosion should reduce much of the skeletal material to carbonate muds, increasing the prevalence of mud-rich facies. Eutrophic conditions should result in bioeroded hardgrounds and carbonate depositional hiatuses. When carbonate accumulation rates fail to equal or exceed rates of local relative sea-level rise, reefs drown. Bored and lithified pavements with crusts of ferromanganese oxides, phosphates, or glauconite often separate shallow-reef from overlying deeper-water deposits. Nondeposition, bioerosion, and evidence for low redox potentials at the sediment-water interface all implicate excess nutrient availability as a factor in reef drowning. Some carbonate depositional hiatuses and bioerosional surfaces are local phenomena, evidence of responses to local increases in nutrient availability resulting from submergence of soils, runoff, or topographic upwelling. Others appear to reflect regional or worldwide events. Because many carbonate-producing organisms have life history strategies specialized to nutrient-deficient conditions, they are unable to compete when nutrients become plentiful. Events that triggered ocean turnover or sharp increases in the rate of deep ocean circulation would have increased sea-surface nutrient availability worldwide. Such eutrophication could have caused widespread extinctions in reef communities. Because eutrophication promotes bioerosion, details of the fossil records of those events are probably lost in bioerosional hiatuses.

Large foraminifera; a tool for paleoenvironmental analysis of Cenozoic carbonate depositional facies

Previous studies of test shape and distribution trends of reefassociated Foraminiferida provide the basis for a model of foraminiferal distribution in Cenozoic carbonate depositional facies. The model predicts distributions offoraminifera in Wilsons Standard Carbonate Facies. Basinal sediments from above the calcium carbonate compensation depth will contain predominantly low latitude planktonic foraminifera with a minor component of deeper benthic species. Open shelf and toe of reef slope sediments from euphotic zone depths will be visually dominated by very large, flat, rotaliine foraminifera. Larger foraminifera of carbonate foreslope environments are of intermediate thicknesses; total foram faunas of foreslope and ecologic reef are typically diverse. Shelf edge sands are often concentrations of tests of large, robust, subspheroid rotaliine species. Open carbonate platform sediments are characterized by robust to intermediate rotaliines and soritids. Lagoons and other restricted carbonate shelf environments of normal or hypersalinity are dominated by miliolids, peneroplids and small rotaliines. This model, when tested on thin sections cut from lower Miocene carbonate cores from four Philippine wells, enhanced the paleoenvironmental analysis and interpretation developed using standard petrographic techniques. The model is based upon recognition of three major groups of easily recognizable foraminifera: 1) thin, larger, rotaliineforaminifera plus planktonics, 2) ovate, larger rotaliines, and 3) miliolines and smaller rotaliines. The relative percentages of these environmentally diagnostic foraminifera, when plotted on triangular diagrams, provide graphic indication of paleoenvironment.

Why are larger Foraminifera large

Delayed maturation and growth to large sizes are only advantageous under stable environmental conditions where food resources are limited. Specialization to algal symbiosis is also highly advantageous under those conditions if sunlight is available. The coevolution of these two characteristics has occurred many times in many foraminiferal lineages. These traits are sometimes associated with increased embryon size and suppression of sexual reproduction, which are also characteristics most advantageous under stable environmental conditions. Specialization for these traits, ensuring success in warm, shallow, stable, oligo- trophic environments, often dooms the species or lineage to extinction when conditions change.

Foraminifera as Bioindicators in Coral Reef Assessment and Monitoring: The FORAM Index

Coral reef communities are threatened worldwide. Resource managers urgently need indicators of the biological condition of reef environments that can relate data acquired through remote-sensing, water-quality and benthic-community monitoring to stress responses in reef organisms. The “FORAM” (Foraminifera in Reef Assessment and Monitoring) Index (FI) is based on 30 years of research on reef sediments and reef-dwelling larger foraminifers. These shelled protists are ideal indicator organisms because:• Foraminifers are widely used as environmental and paleoenvironmental indicators in many contexts;• Reef-building, zooxanthellate corals and foraminifers with algal symbionts have similar water-quality requirements;• The relatively short life spans of foraminifers as compared with long-lived colonial corals facilitate differentiation between long-term water-quality decline and episodic stress events;• Foraminifers are relatively small and abundant, permitting statistically significant sample sizes to be collected quickly and relatively inexpensively, ideally as a component of comprehensive monitoring programs; and• Collection of foraminifers has minimal impact on reef resources.USEPA guidelines for ecological indicators are used to evaluate the FI. Data required are foraminiferal assemblages from surface sediments of reef-associated environments. The FI provides resource managers with a simple procedure for determining the suitability of benthic environments for communities dominated by algal symbiotic organisms. The FI can be applied independently, or incorporated into existing or planned monitoring efforts. The simple calculations require limited computer capabilities and therefore can be applied readily to reef-associated environments worldwide. In addition, the foraminiferal shells collected can be subjected to morphometric and geochemical analyses in areas of suspected heavy-metal pollution, and the data sets for the index can be used with other monitoring data in detailed multidimensional assessments.

Similarities between planktonic and larger foraminiferal evolutionary trends through Paleogene paleoceanographic changes

Abstract The Paleogene evolutionary records of planktonic foraminifera and larger benthic foraminifera show parallel patterns in development that may, in part, reflect changes in nutrient flux to surface waters. Following the terminal Cretaceous extinctions, faunas were dominated by a few cosmopolitan opportunistic species. More specialized k-strategists in both groups diversified during the Paleocene, dominating into the early Eocene, consistent with he globally mild climatic regime and probable limited rates of nutrient flux to surface waters. High-latitude cooling intensified in the middle Eocene, promoting diversification of less specialized taxa characteristic of cooler and deeper waters, higher latitudes, meridional upwelling zones, and boundary currents. Geographic ranges of warm-water taxa diminished and fragmented, yet many species survived. Thus, global diversities during the middle Eocene were the highest in the Cenozoic. As cooling and increased rates of nutrient flux further intensified in the late Eocene, extinction rates of warm-water planktonic and larger benthic species exceeded origination rates of cooler water and less specialized forms, so diversity dropped to intermediate levels where it remained through the late Eocene and Oligocene. Previous observations that planktonic foraminiferal faunas dominated by warm-water taxa are often replaced by cool-water faunas, even though oxygen isotopes only recorded relatively minor cooling, can be reconciled by the explanation that the biotic communities responded to changes in trophic resources and euphotic habitats that accompany the temperature reduction, as well as to temperature change itself.

Symbiont-bearing Foraminifera

Of approximately 150 extant families of Foraminifera, less than 10% harbor algal endosymbionts (Lee and Anderson, 1991a). Nevertheless, these families are responsible for much of the carbonate produced by the Foraminifera, because symbiosis is prevalent in tropical larger foraminifers and planktonic foraminifers, the two groups that are the most prolific carbonate producers. Globally, Milliman and Droxler (1995) estimated carbonate production at 5.7 billion tons per year, of which larger foraminifers produce about 0.5% and planktonic foraminifers produce about 20% (Langer, 1997). Lee and Anderson (199 l a ) , in their review of the biology of symbiosis in Foraminifera, listed four miliolid, three rotaliid, and five globigerinid families as hosts of algal symbionts belonging to three divisions and five classes of the algae. A few members of several families of smaller rotaliid foraminifers (e.g. Asterigerinidae) appear to host endosymbionts, but those relationships await study. In addition, members of several families are able to sequester chloroplasts, which are harvested from algal food, for days to weeks after ingestion (Lopez, 1979; Cedhagen, 1991; Lee and Anderson, 1991a). While this is not a true symbiosis, chloroplast sequestering does enable these protists to benefit directly from photosynthesis. Algal symbiosis appears to have arisen independently in most of these lineages of Foraminifera, as well as in several now extinct lineages. Evidence for independent origins is strongest for the miliolid families and subfamilies. The ornamented Peneroplidae (Fig. 8.1.A) host symbionts belonging to the red algae (Division Rhodophyta) (Fig. 8.2.A), while the unornamented Peneroplidae (Fig. 8.1.B) and the Archaiasinae (Family Soritidae) (Fig. 8.1.C) host symbionts belonging to the green algae (Division Chlorophyta) (Fig. 8.2B). The Soritinae (Family Soritidae) (Fig. 8.1.D) host dinoflagellate symbionts (Division Chromophyta, Class Pyrrophyceae) (Fig. 8.2.C), and the Alveolinidae I Fig. 8.1.E) host diatom symbionts (Division Chromophyta, Class Bacillariophyceae). Among the planktonic Foraminifera (Fig. 8.3), both dinoflagellate (Fig. 8.2.D) and chrysophyte (Division Chromophyta, Class Chrysophyceae) (Fig. 8.2.E) symbionts are common. Recent isotopic studies (Norris, 1996a) indicate that within

Algal symbiosis: A mathematical analysis

Host and algal symbion growth can be described by an iterative model which incorporates utilization efficiencies of host and symbiont. This model predicts that, with input of organic matter to the host and at very low host and algal utilization efficiences coupled with efficient recycling of nutrients between the host and symbionts, production of organic matter by the system can be increased by 2–3 orders of magnitude over that of a system comprised of only autotrophs and heterotrophs. Energy available for growth and respiration by the host is 1–2 orders of magnitude over that available to a heterotroph without symbionts. Algal symbiosis is highly advantageous in oligotrophic environments where radiant energy is abundant, growth-limiting nutrients are scarce and only concentrated in organic matter, and much energy must be expended to capture that organic matter.

Platforms of the Nicaraguan Rise: Examples of the sensitivity of carbonate sedimentation to excess trophic resources

The Nicaraguan Rise is an active tectonic structure in the western Caribbean. Carbonate accumulation on its platforms has not kept pace with relative Holocene sea-level rise, despite a tropical location remote from terrigenous sedimentation. Trophic resources apparently exceed levels favoring coral-reef development because sponge-algal communities dominate the drowning western platforms, in contrast to mixed coral-algal benthos on Pedro Bank and well- developed coral reefs along the north coast of Jamaica. Concentrations of biotic pigments in sea-surface waters show a corresponding west-east gradient; oceanic waters flowing over the western banks carry nearly twice as much biotic pigment as oceanic waters north of Jamaica. Sources enriching the western Caribbean are terrestrial runoff, upwelling off northern South America, and topographic upwelling over the Nicaraguan Rise. That relatively modest levels of trophic resources can suppress coral-reef development holds important implications for understanding carbonate platform drownings in the geologic record.

Coral Reefs, Carbonate Sediments, Nutrients, and Global Change

As the 21st century begins, studies of coral reefs, carbonate sediments, and limestones will continue to be fundamental to understanding the past, present, and future of marine ecosystems and global climate. An intellectually challenging aspect of carbonate research is the plethora of paradoxes associated with the biology of carbonate-secreting organisms, carbonate geochemistry, and carbonate depositional ecosystems. Discovering new paradoxes, deciphering existing ones, and deepening understanding of old ones undoubtedly will continue to engage carbonate researchers well into the new century.