FORAMINIFERA AS BIOINDICATORS IN CORAL REEF ASSESSMENT AND MONITORING

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. Since coral reef communities are subject to a myriad of stresses, it is critical to have an indicator of water-quality conditions that will support reef development, even in the absence of healthy coral populations following mass mortality events. Cockey et al. (1996) argued that larger foraminiferal populations, which are immune to coral-specific diseases and recover much more quickly from physical impacts than long-lived coral populations, are sensitive indicators of water-quality conditions that support reef development.

Numerous researchers have used foraminiferal studies in environmental investigations. Foraminifera play a significant role in global geochemical cycles of inorganic and organic compounds. Their tremendous taxonomic diversity and cosmopolitan occurrence make them potential bioindicators for different types of pollution. Their hard tests are readily preserved, and can record evidence of environmental stress over time. Many other factors favor their use as bioindicators: (1) they are ubiquitous to marine environments; (2) they live on and in sediment, which can act as a sink for pollution; (3) 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; (4) the relatively short life spans of foraminifers as compared with long-lived colonial corals facilitates differentiation between long-term water-quality decline and episodic stress events; and (5) reef-building, zooxanthellate corals and foraminifers with algal symbionts have similar water-quality requirements. Hallock et al. (1995) and Williams et al. (1997) have conducted detailed studies of the key taxon Amphistegina gibbosa. Comparisons of living or total assemblages between impacted and unimpacted "reference" sites (e.g., Angel et al., 2000), comparisons of assemblages from different kinds or degrees of pollution (e.g., Alve, 1995; Yanko, 1994;1998), and comparisons of assemblages in surface samples over time (e.g., Cockey et al., 1996) can be made. Because the shells of these small protists are commonly preserved in marine sediments, perhaps the most important potential advantage may be the use of sediment cores to determine if and how much assemblages have changed at sites of interest (Hallock, 2000; Ishman, 2000).

After more than a century of study, a great deal is known about the basic biology of foraminifera. Benthic foraminifera are classified into orders based on their shell structure. Murray (1973) showed that relative proportions of the three most common benthic groups, when plotted on a ternary diagram, provide clues to the environments in which these organisms live. These three groups include the porcelaneous Miliolida; the calcareous perforate taxa that are now classified in several orders, the most important of which are the Rotaliida and the Buliminida; and the agglutinated taxa, which include the Lituolida, Trochamminida, and Textulariida. The Miliolida have been important environmental indicators from the Carboniferous onward. They secrete imperforate shells of high magnesium calcite, which are most easily produced in warm, shallow, hypersaline waters saturated with CaCO3 (Haynes, 1981). The agglutinated taxa, particularly those that produce organic or ferrigenous adhesives, generally dominate environments where sea water is undersaturated with respect to CaCO3, such as estuarine, polar and deep-sea habitats. Finally, the perforate taxa have been able to adapt to a great range of environments. This order not only includes exceptionally eurytopic, opportunistic taxa, including Ammonia spp., but also highly specialized taxa such as algal symbiont-bearing forms (Hallock, 2000).

For the purpose of this CD, foraminiferal taxa have been further divided into six functional groups based not only on taxonomy, but also the environments to which they give us clues: symbiont-bearing miliolids, symbiont-bearing rotaliids, opportunists, smaller miliolids, miscellaneous smaller perforate taxa, and agglutinated taxa. Symbiont-bearing foraminifera are indicative of more pristine environments and can be thought of as coral analogues because symbiont-bearing foraminifera and corals require similar environmental conditions, i.e., warm, clear, low-nutrient water with normal marine salinities. Symbiont-bearing miliolids typically inhabit back-reef areas, whereas symbiont-bearing rotaliids inhabit the fore reef. Smaller miliolids and other smaller perforate taxa are heterotrophic and can take advantage of relatively abundant food resources. Opportunistic taxa can take advantage of a wide range of stressful environmental conditions, and are notable for their tolerance of low oxygen environments and anthropogenic pollution. Finally, the agglutinated taxa create their tests from tiny particles they pick up from the environment and cement to themselves, and are common in estuaries or brackish environments. Be mindful that the placement of foraminiferal taxa into these functional groups is somewhat arbitrary because some taxa have species in more than one category. For example, Quinqueloculina, which is a smaller miliolid, has agglutinated species. More than 300 species of foraminifera have been identified in subtropical coastal regions of the the western Atlantic and Caribbean. Common examples of foraminifera belonging to each of these functional groups defined above are presented in the CD.

The "FORAM" (Foraminifers in Reef Assessment and Monitoring) Index, presented in the "Methods" section, is based on 30 years of research on reef sediments and reef-dwelling larger foraminifers and utilizes foraminiferal assemblages from surface sediments of reef-associated environments. The index can provide 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. It involves simple calculations that require limited computer capabilities and therefore can be readily applied 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.

The FORAM Index and this CD were developed under support from the U.S. Environmental Protection Agency Office of Research and Development's National Center for Environmental Research "Science to Achieve Results" Program (STAR-GAD-R825869).



References

Alve, E., 1995, Benthic foraminiferal responses to estuarine pollution: a review. Journal of Foraminiferal Research, v. 25, no. 3, p. 190-203.

Angel, D. L., Verghese, S., Lee, J. J., Saleh, A. M., Zuber, D., Lindell, D., and Symons, A., 2000, Impact of a net cage fish farm on the distribution of benthic foraminifera in the northern Gulf of Eilat (Aqaba, Red Sea). Journal of Foraminiferal Research, v. 30, p. 54-65.

Cockey, E. M., Hallock, P. M., and Lidz, B. H., 1996, Decadal-scale changes in benthic foraminiferal assemblages off Key Largo, Florida. Coral Reefs, v. 15, p. 237-248.

Hallock, P., 2000, Larger foraminifera as indicators of coral-reef vitality, in Environmental Micropaleontology, v. 15, p. 121-150.

Hallock, P., Talge, H. K., Cockey, E. M., and Muller, R. G., 1995, A new disease in reef-dwelling foraminifera: implications for coastal sediment. Journal of Foraminferal Research, v. 25, p. 280-286.

Haynes, J. R., 1981, Foraminifera. Macmillan Publishers, London, 433 pp.

Ishman, S. E., 2000, Benthic foraminifera distributions in South Florida, in Environmental Micropaleontology. Kluwer Academic Press, p. 371-383.

Murray, J. W., 1973, Distribution and Ecology of Living Benthic Foraminiferids. Cran, Russak and Co., New York, 274 pp.

Williams, D. E., Hallock, P., Talge, H. K., Harney, J. N., and McRae, G., 1997, Responses of Amphistegina gibbosa populations in the Florida Keys (U.S.A.) to a multi-year stress event (1991-1996). Journal of Foraminiferal Research, v. 27, p. 264-269.

Yanko, V., Kronfeld, J., and Flexer, A., 1994, Response of benthic foraminifera to various pollution sources: implications for pollution monitoring. Journal of Foraminiferal Research, v. 24, no. 1, p. 1-17.

Yanko, V., Ahmed, M., and Kaminski, M., 1998, Morphological deformities of benthic foraminiferal tests in response to pollution by heavy metals: implications for pollution monitoring. Journal of Foraminiferal Research, v. 28, no. 3, p. 177-200.

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