Elsevier

Environmental Pollution

Volume 257, February 2020, 113612
Environmental Pollution

Foraminifera as bioindicators of water quality: The FoRAM Index revisited

https://doi.org/10.1016/j.envpol.2019.113612Get rights and content

Highlights

  • FoRAM Index is a powerful water quality management tool in coral reefs.

  • FoRAM Index must be modified to suit location-specific assemblages.

  • Methodological modifications will ensure usability of the index worldwide.

Abstract

Coral reefs worldwide are degrading at alarming rates due to local and global stressors. There are ongoing needs for bioindicator systems that can be used to assess reef health status, the potential for recovery following destructive events such as tropical storms, and for the success of coral transplants. Benthic foraminiferal shells are ubiquitous components of carbonate sediment in reef environments that can be sampled at minimal cost and environmental impact. Here we review the development and application of the FoRAM Index (FI), which provides a bioindicator metric for water quality that supports reef accretion. We outline the strengths and limitations of the FI, and propose how it can be applied more effectively across different geographical regions.

Introduction

Across the globe, coral populations and reef accretion have declined as the environmental conditions upon which they depend have been degraded by anthropogenic activities. As a result, reef management agencies are faced with the challenge of managing resources to increase the resilience of local reefs to the broader-scale environmental changes. Because long-term trends in physical and chemical parameters of reef environments can be subtle and masked by diurnal, seasonal and interannual variability, the necessity for bioindicators that integrate environmental conditions was widely recognised by the mid-1990s (e.g. Crosby et al., 1995, Jackson et al., 2000).

Evidence for both subtle changes and dramatic losses in coral reef communities emerged in the 1970s. Around the Caribbean, growing human populations were clearing uplands for agriculture and coastlines for urban and tourist development (e.g. Rogers, 1990, Ogden, 1996). With increased fishing pressure on reef fish, the sea urchin (Diadema antillarum) populations exploded, increasing reef bioerosion (e.g. Hay, 1984, Sammarco, 1982), while minimising macroalgal growth; followed by the disease outbreak and massive dieoff of the urchins in 1983, that has allowed unchecked macroalgal proliferation (Lessios, 2016). On the clearest offshore reefs, white-band disease was destroying stands of Acropora spp. (Antonius, 1977, Bruckner, 2016). In the Pacific, Crown-of-Thorns starfish (Acanthaster planci) outbreaks were being documented (e.g. Sapp, 1999, and references therein). In Kaneohe Bay, Oahu, Hawai’i, in the 1960s and 1970s, coral reefs were being taken over by macroalgae such as Dictyospheria. Concern for the reefs prompted a ground-breaking study of the influence of nutrient pollution on the reef communities (e.g. Laws and Redalje, 1979, Laws and Redalje, 1982, Smith et al., 1981). These studies found, while monitoring sewage discharge into the bay, dissolved inorganic nitrogen was rapidly taken up by phytoplankton, and that chlorophyll a, and particulate nitrogen were much more sensitive and widely applicable indices of nutrient enrichment than inorganic nutrient concentrations. Moreover, because the time frame for influence on benthic biomass and community structure is much longer than for responses within the water column, Laws and Redalje (1982) concluded that the benthos must be considered when assessing the impact of sewage pollution.

At about the same time, changes in assemblages of benthic foraminiferal shells in sediments were recognised as indicative of nutrient pollution in tropical coastal waters (e.g. Hirshfield et al., 1968, Seiglie, 1968, Seiglie, 1971). Benthic foraminifera are protists, many of which build calcium carbonate shells, and are a crucial component of the benthos (Murray, 2014). While assessing impacts of atomic testing at Enewetak Atoll in the central Pacific, Hirshfield et al. (1968) observed that foraminiferal assemblages were dominated by larger benthic foraminifera, except in the vicinity of the research laboratory outfall, where other, fast-growing, smaller, heterotrophic foraminiferal taxa dominated. In subtropical and tropical reef environments, reef-associated larger benthic foraminifera are generally dominant, as they utilise algal endosymbionts, and have environmental requirements similar to those of reef-building corals (e.g. Hallock, 1999, Prazeres and Renema, 2019). More intense anthropogenic activities, such as agricultural and sewage pollution in inshore bays and lagoons, can produce more extreme conditions that benefit a few stress-tolerant foraminiferal taxa (e.g. Seiglie, 1968, Seiglie, 1971, Culver, 1990, Culver and Buzas, 1995). Therefore, foraminiferal abundances, diversity and assemblage-level sensitivity to shifts in water transparency and food sources, combined with their production of sand-sized shells that accumulate in the sediments, make foraminifera natural bioindicators of water quality in coastal environments (Alve, 1995, Schaffer, 2000).

These observations of changes in foraminiferal assemblages with the gradient of available organic matter provided the basis of the Foraminifera in Reef Assessment and Monitoring (FoRAM) Index of Hallock et al. (2003). The FoRAM Index (FI) was based on studies of northwest Atlantic and Caribbean foraminiferal assemblages in sediment samples, especially Puerto Rico and the Florida Reef Tract. The FI was designed to provide a relatively simple, low-cost metric to assess the potential for associated hard-bottom benthic environments to support calcifying organisms that host algal symbionts, including reef-building corals. This index is based on sediment samples, in which proportions of shells of three functional groups of foraminifera are determined: (1) the larger benthic foraminifera (LBF), (2) fast-growing, smaller heterotrophic taxa that require well-oxygenated conditions (OSF), and (3) stress-tolerant taxa (STF) that can tolerate intermittent hypoxia. The FI was developed to be a coral-independent measure to provide resource managers with a means of assessing whether water quality is sufficient to support reef growth or recovery after major stress or coral-mortality event. Therefore, the FI is not applicable in environments dominated by mud or very fine sand particles (<125 μm), such as estuaries, where STF would likely dominate (Hallock et al., 2003).

Since its publication in 2003, the FI has been applied to reef environments worldwide and has also been utilised in marginal and non-reefal environments (e.g. Hallock, 2012, and references therein). However, modifications of the original methods make comparisons across studies challenging and, in some cases, impossible. Moreover, the FI thresholds proposed for sediments from the Caribbean region cannot be assumed to be appropriate under modified methods or in other biogeographic regions, such as the Pacific Ocean or southwest Atlantic. Therefore, we propose further standardisation of the FI, and provide recommendations that will allow the broad application of this index as a powerful tool in assessment and monitoring programs in reef environments worldwide. At the same time, we note that some variations in methods can provide useful data for local studies, and we further explain why the FI is not appropriate in some subregions and reef environments.

The objective of this paper is to clarify and facilitate the use of the FI in reef assessment programs worldwide. Our goals are to: (1) discuss examples of the use and application of the FI, (2) address important considerations on the use of the FI such as size range of specimens examined as a function of sieve-mesh size used in sample processing, replicate sampling and numbers of specimens counted, live (stained) versus total assemblages, sediment textures, depth of sample collection, and ultimately, interpretation of resulting data; and (3) propose standardised protocols for the FI with the goal to improve its applicability for coral reefs in the Pacific Ocean and other reef areas, and to produce comparable data that will lead to wider applicability of the FI in assessment of water quality and monitoring programs.

Section snippets

The need for bioindicators in shallow coral reef environments

In the 1960s into the 1990s, local impacts such as increased terrigenous sedimentation associated with land clearing, and nutrient input from agricultural runoff and ever-increasing human populations in coastal regions, as well as overfishing, were considered the major causes of reef degradation (e.g. Pandolfi et al., 2003, Ramos-Scharrón, 2010, Burke et al., 2011). Widespread coral bleaching events associated with strong El Niño conditions occurred in 1982–83 and 1987, but the consequences of

Challenges in developing suitable bioindicators

A key categorical aspect of a marine bioindicator is its resilience and fitness towards short and/or long terms environmental changes. Bonanno and Orlando-Bonaca (2018) clearly articulated that a bioindicator must be able to capture the accumulated effects of pertinent stressors before biological functionality is altered, which ultimately would hinder an organisms capacity to respond predictably to environmental disturbances. This resonates with major challenges in developing a bioindicator in

The development of the FoRAM Index

In reef ecosystems, benthic foraminifera are particularly useful because their life spans (a few weeks up to ∼2 years) are relatively short when compared to reef-building corals. As such, the response to changes in nutrient flux, for example, can be detected in shorter time frames (Crevison et al., 2006) when compared to the potential multi-year response of coral populations. For example, a change in water quality that is not detectable in adult reef-building corals but that reduces larval

Application of the FoRAM Index

Since its publication in 2003, the FI has been applied to reef environments in biogeographic regions nearly worldwide. The FI has also been utilised in marginal and non-reefal environments in the subtropical north- and southwestern Atlantic, the Mediterranean, and Indo-Pacific (e.g. Barbosa et al., 2009, Dimiza et al., 2016). Notes on methods utilised and notable observations in a variety of pertinent papers are summarised in Table 1.

As noted by Hallock (2012), because LBF taxa differ between

Technical issues while applying the FI

Sampling design: The FI was originally developed using samples from depths of ∼3–15 m. For detailed comparisons of reefs within an area, the strategy employed by Pisapia et al. (2017) can be recommended. Additionally, Pisapia et al. (2017) successfully integrated the utilisation of the FI with pre-existing monitoring programs without any compromise. They selected locations of interest based on the management status of the adjacent island, and then collected three samples at ∼50 m intervals from

Towards a standardised protocol

The original goal of the FI was to provide a rapid and cost-effective assessment tool of water quality in coral reef ecosystems (Fig. 2, Fig. 3). Modified approaches applied by some researchers have demonstrated how the FI can be used to reveal local gradients or temporal changes (e.g. Koukousioura et al., 2011, Carilli and Walsh, 2012, Kelmo and Hallock, 2013), which are legitimate applications. In other cases, regional characteristics of the reefs can result in FI values that are not useful,

Assessment of foraminiferal populations and global climate change

An approach more suitable to monitoring on seasonal scales is to assess the responses of key taxa, with respect to absolute abundances and “condition”, through visual and molecular tools using the “omics” approach, if available. For example, Hallock (1996) and Hallock et al. (2006) proposed the possibility of differentiating between long-term water quality decline and the effects of photo-oxidative stress (i.e. from elevated water temperature or photic stress) by analysing populations of

Conclusions

Managing local water quality in coastal-marine environments is fundamental for the long-term protection of diversity and to maintain carbonate accretion in reef ecosystems (Hughes et al., 2003, Wooldridge and Done, 2009). Establishing biological time series based on foraminifera is a relatively straightforward and cost-effective way to evaluate changes in the environment over time (Hallock et al., 2003). The use of benthic foraminifera provides a simple tool for assessment of local and global

Acknowledgements

Dr. T. Edward Roberts for illustrating the specimens of foraminifera in Fig. 1, Fig. 2. Dr. Willem Renema for his comments on early versions of the manuscript. This work was partially supported by the Puerto Rico Sea Grant (grant number R/104-1-18) awarded to MM-C.

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