Article: Batista, D.; Tellini, K.; Nudi,A.H.; Massone, T.P.; Scofield, A.; Wagener, A. (2013) Marine sponges as bioindicators of oil and combustion derived PAH in coastal waters. Marine Environmental Research. 92:234-243. doi: 10.1016/j.marenvres.2013.09.022
If you drove a car today, charred your steak on the grill, or warmed yourself by the fireplace, you were producing polycyclic aromatic hydrocarbons, or PAHs. This is a class of compounds with more than 100 different forms, each with a different configuration and number of conjugated planar carbon rings (Figure 1). These persistent organic pollutants (POPs) are found naturally in petroleum products (known as a petrogenic source), but are also produced from the incomplete combustion of organic matter (pyrogenic source), such as fossil fuels and wood. Obviously, this means we are still actively, and increasingly, emitting these pollutants to the environment where they are either directly released into the marine ecosystem, or are transported there through the atmosphere.
More than 30 PAHs have been identified as carcinogenic, mutagenic, and genotoxic; 16 of these are now priority pollutants for the US EPA. They are among the most frequently detected persistent organic pollutants in marine coastal areas, and as such, warrant consistent monitoring. One way scientists have found to conduct such studies is with biomonitoring. Biomonitoring employs the kind assistance of local organisms, referred to as bioindicators, which are collected and analyzed to determine their level of exposure to pollutants. PAHs have low water solubility, and therefore prefer to accumulate on particulate matter in the water column. These particulates effectively transport PAHs to the benthic sediment where they are ingested and accumulate in the lipids (fatty tissue) of filter feeders, like mollusks and sponges.
Brown mussels (Perna perna) (Figure 2) have been the filter feeder of choice for biomonitoring assays along the Brazilian coast because these bivalves have economic importance and a wide geographical distribution. Additionally, researchers tend to use invertebrates as bioindicators because they have a higher capacity to accumulate contaminants than vertebrates do. However, brown mussels are limited in their habitats and cannot indicate pollution levels at depth because they live in shallow coastal waters. The ideal bioindicator would have a wide range of habitats at different depths and temperatures, be easy to collect, accumulate a variety of the target compounds, and have a high tolerance for pollution so it can live in contaminated environments long enough to effectively represent the surrounding water. Researchers in Brazil think they have found such an organism.
Hymeniacidon heliophila, or the sun sponge (Figure 3), is an easily identifiable massive sponge found all the way from North Carolina to southern Brazil. Sponges are among the most abundant benthic animals, able to live in tropical zones, coral reefs, rocky shores, and even artificial structures. Additionally, sponges can filter a great volume of water: one kilogram of sponges can process over 24,000 liters per hour. Even though sun sponges are typically found in shallow waters on the continental shelf, they can be found at depths of 7000 meters. They also have the special ability to withstand polluted habitats thanks to the help of ammonia oxidizing microorganisms. Previous studies have already demonstrated the efficacy of sponges to accumulate other pollutants.
In order to determine their suitability as an in situ monitoring tool for PAHs, a survey was conducted in both the dry (August and September) and wet (February and March) seasons of 2010 in the coastal Rio de Janeiro region of Brazil (Figure 4). Sampling sites included the heavily polluted Guanabara Bay, the less impacted coastal area of Itaipu, and three islands in the Cagarras Archipelago just offshore. In the open water sites, sponges were collected at two different depths (0.5 and 7-8 meters) in order to compare PAH concentrations throughout the water column. For comparison to established sampling methods, brown mussels and water were also collected concurrent with the sun sponges. PAH concentrations were determined for both individual sponges and homogenized composites of 10 specimens. The pollutants were extracted from the samples using strong organic solvents, and then 33 individual PAHs were measured using gas chromatography/mass spectrometry.
Not surprisingly, the greatest concentrations were found in samples from Guanabara Bay, the largest urban estuary in the Brazilian coast. Concentrations were lowest in specimens from Itaipu, indicating less impact from petrogenic inputs. The primary PAHs found in sponges and mussels alike were signatures of diesel: dibenzothiophene (DBT) and phenanthrene, as well as their alkylated homologs. At all stations, DBT compounds were dominated by the weathered form, indicating that not only were all sites contaminated by oil, but the pollution was from persistent shipping traffic. In the bay, this maritime transport is largely due to shipping to and from urban areas as well as increasing offshore oil exploration; whereas, petrogenic PAHs in the Cagarras Archipelago are derived mainly from the traffic of recreational and fishing boats.
If you are only concerned with petrogenic PAHs, both mussels and sponges appear to reveal the same relative distributions between sampling areas. However, when it comes to pyrogenic PAHs – those derived from combustion and generally more harmful to biota – sponges give you a sampling advantage. Pyrogenic PAHs are higher molecular weight compounds and generally bind to small particles. Unfortunately, brown mussels tend to accumulate larger particles (>100 micrometers), perhaps excluding pyrogenic compounds from their filtering and therfore biasing their PAH accumulation toward petrogenic molecules. Sun sponges, on the other hand, mainly retain particles <1 micrometer and can be used to indicate influences from both leaked oil and burned fuel. This signature was found in sponges from sites with intense vehicle traffic.
Depth profiles were able to show contrasts between the surface and bottom waters, but the differences were generally not significant. The concentration of total PAHs was higher at depth in the bay, possibly due to higher concentrations of particles enriched in organic matter, acting as vehicles for PAH transport to greater depths. Likewise, differences between the wet and dry seasons were negligible, except at Itaipu, where PAH concentrations were significantly higher in the wet season, possibly due to increased runoff carrying more PAHs from the land. Since Itaipu typically has lower PAH concentrations, it is more susceptible to seasonal changes in source intensity.
Conclusions and implications:
The sun sponge appears to be a good candidate to replace, or at least supplement, brown mussels as important PAH biomonitors. They are able to accumulate both petrogenic and pyrogenic PAHs; they can withstand high levels of pollution, changes in habitat conditions and seasons; and they appear to have a body chemistry that does not favor the biotransformation of pollutants. All of these attributes make them ideal bioindicators for persistent pollutants. Regular sampling of the sun sponge along the Rio de Janeiro coasts will provide a more holistic and detailed profile of PAH contamination than the brown mussel as offshore oil exploration in the region continues to grow.