TROPICS: 30-year Follow-up and Analysis of Mangroves, Invertebrates, and Hydrocarbons

Few tropical oil spill studies have focused on long-term effects, most dealing with cleanup, restoration, and damage assessment. In the process, researchers have assembled a list of short- and medium-term effects (e.g., Lewis, 1983, RPI, 1987, Dodge et al., 1995). As shown in Table 1, details exist for acute and chronic, early stages, but not for long-term (10+ year) stages.

The TROPICS treatments were designed to simulate a severe, but realistic scenario of oil release in shallow, low energy coastal waters, and in close proximity to sensitive mangrove, seagrass, and coral habitats, explore the short-, mid-, and long-term effects (Figure 1).

The long-term duration of effects at the TROPICS oil spill in Panama was published through 25 years, as shown in Table 2. Descriptions of effects refer to percent changes in organisms over time, relative to baseline or previous years' data.

Reports on the three years following the TROPICS spills were produced by RPI (1987) and Ballou et al. (1989). In the first year following the spills severe impacts were seen on mangroves at the non-dispersed oil site and invertebrates at the dispersed oil site. After two years the non-dispersed oil site showed severe effects on mangroves and associated sea life. Relatively minor effects were seen on seagrass and coral communities. Inversely, dispersed oil negatively affected sea life in tropical communities but had relatively few effects on their habitats: seagrasses and mangroves. Effects appeared to stabilize in 2.5 years and the study was discontinued. In contrast, Dodge et al. (1995) reported on research done ten years after the 1984 spills which showed an increase in Site O effects but apparent recovery at the Site D.

The TROPICS studies contained intensive hydrocarbon sampling and analyses in the first 2.5 years and in the 10-year follow-up study (1994). Total petroleum hydrocarbons (TPH) were low or non-detectable after 10 years but changing forms of polycyclic aromatic hydrocarbons (PAH via EPA 8270, Florida Spectrum Environmental) were detected through 25 years (2009).

The present research was conducted at the same sites located on two islands in Bahia Almirante near Bocas del Toro, on the Caribbean coast of Panama. The original sites were chosen on the basis of presence and condition of mangrove forest, seagrass bed, and coral reef. Since these were experimental spills, baseline pre-spill studies of these sites were conducted numerous times in 1983 and 1984.

Three 900m² sites were selected at separate locations: Reference (R), Non-Dispersed Crude Oil (O), and Dispersed Crude Oil (D). Three habitats were available for study within each 30m × 30m site (900m²): mangrove forest, seagrass bed, and coral reef. However, since the focus of the present research was mangroves and component invertebrates, methods and detailed results are provided herein for mangrove forest (with invertebrates) only, as well as basic hydrocarbon sampling. The methods follow those used in 1984 and 1990, briefly as follows:

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  Mangrove parameters – adult tree (>2m) height (m), seedling (<2m) height (m), tree diameter at breast height (DBH, 1.3 m high, in cm), canopy density (Forestry Suppliers™ crown densitometer, recorded in percent); all of these were taken at nine stratified (three tidal elevation strata: high, medium and low), random tree plots within each site.

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  Invertebrates – mangrove tree snails (Littorina angulifera and other species) counted in vertical height classes and determined for nine stratified, random tree plots within each site.

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  Invertebrates – mangrove oysters (Crassostrea rhizophorae), flat tree oysters (Isognomon alatus), and pearl oysters (Pinctada margaritifera), counted on five prop roots extending below mean high tide on each of three trees along the seaward edge (lowest stratum) of each site.

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  Hydrocarbons – three sub-surface cores taken randomly from each mangrove zone (high, medium, and low elevations) at each site, using pre-cleaned glass containers provided by a certified laboratory. These were kept refrigerated and deposited in the laboratory two days after sampling, after which they were analyzed for PAH via EPA 8270 (Florida Spectrum Environmental).

Summaries of biological data collected over 30 years are given in Table 3 and Figures 1-3 for mangrove trees and seedlings. Statistical analyses are summarized in Table 7.

As shown, notable effects were detected at Site O: significant declines in trees and increases in seedlings (i.e., plants < 2m tall) were seen by year 10. The 1985 one-year data are included to show the rapid loss of trees which was believed to have stabilized by 7 months after treatment (RPI, 1987, Ballou et al., 1989). The 1994 (10-year) re-visit showed that this was not correct since a continuation or new “wave” of tree mortality had occurred. By 17 years trees had been essentially restored from seedlings at Site O. The opposite occurred at Sites D and R which experienced losses of mangrove trees before 25 years, dropping from baseline by 72% (25 years) and 76% (20 years), respectively. Tree counts at these sites have increased since then. Seedlings showed high recent increases over baseline at Sites O and R. It has been reported that seedling production peaks in October/November (the period sampled in 2013) and sometimes, researchers have avoided sampling then, and if they do sample, seedlings are scored (and counted) on the basis of node (joint) classes (e.g., Keller and Jackson, 1993). Due to time constraints, this method of viable seedling verification was not used in the present study.

A breakdown of mangrove forest characteristics from baseline vs. long-term (10 years and 29 years) is given in Table 4 (statistics for mangrove measures and invertebrate counts are presented later in Table 7). Tallest trees were at Sites O and D; all trees showed highest diameter at breast height (DBH, 1.3m) in 2013, led by Site D; canopy cover was highest in 1984; most trees were at Sites O and D in 2013; and most seedlings were at all sites in 2013, led by Sites R and O.

The issue of seedling and small tree deformities at Site O arose in 10 years and reached high levels of incidence in 17 years, continuing through 29 years (Fig. 2). Deformities seen were mainly curling and distortions of prop roots in small trees and seedlings. Likely causes relating to PAH effects are discussed later.

Data for mangrove invertebrates (mangrove tree snails, mangrove oysters, flat tree oysters, and pearl oysters) were assembled for pre-spill (1984), spill study dates (1984-1986), 10 years (1994), and 29 years (2013). Mangrove tree snail (Littorina angulifera, etc.) results are given in Table 5 and Figure 3.

As shown, all sites showed dramatic increases at the end of year 1 with upward trends at Sites R and D in 10 years post spill, and peaking at Site D in 29 years. Site O remained in downward trends, never reaching baseline.

Focusing on the three years of main collection efforts for tree snails simplifies the results, as shown in Figure 3. Data were log-transformed from percent of baseline. As shown, all sites showed an increase by ten years, although only Site D continued to increase.

Prop root bivalve (oyster) counts are given in Table 6 and Figure 4. Summaries are given for mangrove oysters (Crassostrea rhizophorae), flat tree oysters (Isognomon alatus), and pearl oysters (Pinctada margaritifera).

Prop root oyster counts for three main study years are illustrated in Figure 4. Summaries are given for mangrove oysters (Crassostrea rhizophorae, top) and flat tree oysters (Isognomon alatus bottom). Pearl oysters (Pinctada margaritifera) are not included because they were very rare in the early studies (pre- and 1984-1986 post-). As shown, both oysters had similar growth curves, for Site O: peaking 10 years after the spill and then declining (precipitously for flat tree oysters). In contrast, both oysters showed gradual upward trends with no declines at Sites D and R.

Comparisons were made between years and sites using two-way analysis of variance (ANOVA) and appropriate post-hoc tests (Sigma Stat ver. 3.1, Aspire Software, Ashburn, VA). The Holm-Sidak method was selected as the post-hoc test because of its power in analysis of two-way ANOVAs. Results are given in Table 7 for the main years 0 (1984), 1 (1985), 2 (1986), 10 (1994), 20 (2004), 25 (2009), and 29 (2013), for the three sites. As shown, mangrove tree counts, heights, and flat tree oysters were not significant. All other parameters were significant for years and/or sites.

Analytical results of all sites for the previous collections indicate that hydrocarbon levels as Total Petroleum Hydrocarbons (TPH) have continued to drop over the last 10± years until they are undetectable. Polycyclic Aromatic Hydrocarbons (PAH) peaked in 2009 (year 25), with the two-ringed naphthalenes making up 94 percent of the total. The change in PAH composition between 1994 (year 10) and 2009 shows a progressive molecule size reduction (seemingly the opposite of convention, discussed later) going from four-ringed chrysenes, fluoranthenes, and pyrenes, to three-ringed phenanthrenes and anthracenes, and ending with two-ringed (lightest) naphthalenes. However, no PAH was detected in 29 years (all components were undetectable at the lowest detection level).

The effects of non-treated and dispersed crude oil at the TROPICS site, specifically the short- and long-term ecosystem disruptions, have been documented and continue to be short- and long-term for various parameters. While dispersant (Site D) showed serious and immediate effects on fauna, these effects were short-lived, and the site returned to pre-dose conditions, without long-term, ecological disruptions. In contrast, Site O has undergone considerable long- term changes as the oil contamination has resulted in ecological disruptions at that site. The Site O mangrove forest lost a significant portion of trees which were slowly replaced by “waves” of seedlings (early ones did not survive to produce trees). The seven-fold appearance of seedlings in year 10 (1994) was believed to be due to the effect of canopy opening as well as to nutrient production by the weathering oil (Dodge et al., 1995). At 29 years, the Site O and Site D mangroves were restored by over 100% while Site O and Site R seedlings maintain their presence by approximately 1,200 percent of the original counts. The long-term (post-ten-year) affects on mangrove fauna at the sites have been explored and have raised questions about invertebrate productivity at Site O.

Pearl oysters were relatively new to the sites, having first appeared in high numbers 10 years after the spills, and increasing in much higher numbers at all sites such that percent of increase could not be graphed with trees. Since pearl oysters cannot be mistaken for other oysters it is unlikely that they were misidentified for 10 years, and their increased numbers appear to be a natural phenomenon.

Mangrove deformities have been seen and photo-documented at Site O (and no others) for many years. Recent incidents, such as deformed prop roots arising from otherwise normal looking plants, indicate that the situation is continuing. Since PAHs are known to be mutagenic, and since they have been present at Site O for some 25 years, it is likely that high levels found at Site O early in this study may be responsible. Mutagenicity of PAHs in mangroves has been documented and is the subject of environmental monitoring (e.g., Klekowski et al., 1994;Proffitt and Travis, 2005). Since propagules are being produced at Site O it would be important to know if they might be transferring these deformities (i.e., mutations) to subsequent generations, on site and elsewhere.

The change in PAH appeared to go from heaviest to lightest compounds, culminating with two-ringed naphthalenes which were the last seen after 25 years, making up 94% of the PAH. This sequence is generally the reverse of what is commonly seen in spills, where light aromatics such as benzene and naphthalene are removed first and heavy PAH such as asphaltenes (e.g., tars) and resins remain the longest (NAP 1985). However, the anaerobic, tropical, low flushing, organically rich, marine sediments in the study sites have analogs in groundwater, landfill, laboratory bacterial studies, and creosote contamination sites which may apply; however, discussion of these is beyond the scope of the present research.

DeMicco et al. (2011) detailed the Net Environmental Benefits Analysis (NEBA) for nearshore dispersant use on mangroves, seagrass, corals, and hydrocarbons, based on a previous 25 years at the TROPICS sites. The present study focused on invertebrates, mangroves, and hydrocarbon presence. By analyzing the data collected during this study and combining it with information carried out at the sites previously, a number of observations confirm the NEBA for dispersant use at this site:

1. 1)

   at 10 years, live mangrove trees suffered severe mortality at Site O (54% survival) but very little at Site D (97% survival)

2. 2)

   earlier high seedling production (now over 1,000 %) resulting from open space provided by high mortality at Site O led to the present, albeit excessive re-growth of trees (now at 144%); in contrast is the near baseline tree count at Site D (107%).

3. 3)

   mutations were seen on trees at Site O during the past 20 years but none were ever detected at Sites D or R

4. 4)

   at 10 years, mangrove tree snail populations were near baseline (115%) at Site O but experienced natural increases at Sites O (232%) and R (208%), and this trend continued through the present

5. 5)

   in contrast, 10-year mangrove oyster populations increased tremendously (481%) at Site O but were near baseline at Sites D (176%) and R (152%)

6. 6)

   aromatic hydrocarbons were detected for 25 years (but not at 29 years) at Site O but were not detected after 3 years at Sites D or R

7. 7)

   at 28 years, oyster populations receded (325%) at Site O but continued increasing at Sites D (458%) and R (297%)

Almost thirty years have passed since non-dispersed and dispersed crude oil was released into the tropical ecosystem marking the beginning of the TROPICS study. Over this time, reports and papers have documented the trade-offs in dispersant use in shallow-water tropical ecosystems. Although the scale of the experiment or the failure to use replicates could be debated, there are some conclusive results of this study that should be taken into account for management of oil spills on water.

Relative to oil spills in mangroves, it is apparent that:

• Long-term (e.g., 10-30 year) negative effects of non-dispersed oil in a mangrove forest are real and measurable

• Long-term effects include keystone floral and faunal components of the ecosystem

• Medium-term (e.g., 10 years) and long-term, negative effects can be reduced by the appropriate use of dispersants in nearshore environments

• Medium- and long-term, dispersed oil spill effects are similar to conditions at the control site

The authors thank Clean Caribbean and Americas (CCA) for financial support, and Joseph Baca and Hector Carrillo for field support. Mangrove research conducted since 1994 is dedicated to mangrove team leader Dr. Sam Snedaker (1938 – 2005).