Marine snow formation during oil spills: additional ecotoxicological consequences for the benthic ecosystem

The Deepwater Horizon (DWH) oil spill in the Gulf of Mexico in 2010 was one of the largest oil spills in history. For three months, oil leaked from the Macondo well at 1,500 m depth into the Gulf. As one of the spill responses, an unprecedented amount of dispersants were applied, both at the sea surface and, for the first time ever, directly injected into the wellhead. During the spill, unusually large amounts of marine snow, including Extracellular Polymeric Substances (EPS), were formed. Oil-contaminated marine snow aggregates were formed by aggregation of EPS with suspended solids, phytoplankton cells due to the spring bloom, and the dispersed oil droplets. The marine snow sank through the water column and settled on the ocean floor. This process was named MOSSFA: Marine Oil Snow Sedimentation and Flocculent Accumulation. MOSSFA was an important pathway of transferring oil to the deep-sea, and 14-21% of the total discharged oil is estimated to have settled on the sediment, where it impacted the benthic ecosystem. This thesis focused first on the mechanism of EPS snow formation, and then more in depth on the additional ecotoxicological consequences of marine snow formation during oil spills for the benthic ecosystem. Chapter 2 describes the role of chemical dispersants in the presence of phytoplankton in the formation of EPS, one of the main ingredients of marine snow. Results show that phytoplankton-associated bacteria were responsible for the EPS formation, and the symbiosis between the phytoplankton and its associated bacterial community provided the bacteria with energy to produce the EPS. The microcosm experiment in Chapter 3 investigated the effect of marine snow on oil biodegradation in microcosms without benthic macroinvertebrates. Results showed that marine snow hampers oil biodegradation: the presence of marine snow reduced the depletion of oil alkanes by 40%, most likely due to the high biodegradability of marine snow organics compared to the oil. Biodegradation of marine snow resulted in anaerobic conditions in the top of the sediment layer. This reduced the oil biodegradation. Marine snow thus prolongs the residence time of oil in the benthic ecosystem. The next microcosm experiment, described in Chapter 4, investigated the effects of oil-contaminated marine snow on benthic macroinvertebrates, and the effect of macroinvertebrates on oil biodegradation. Bioturbation by the invertebrates increased the oxygenated top layer of the sediment and partly counterbalanced the inhibition of oil biodegradation due to oxygen consumption by marine snow. Survival of three benthic invertebrate species was reduced by (oil-contaminated) marine snow. Oxygen depletion near the sediment surface seemed to be the main reason for the observed adverse effects of the marine snow. In addition, indications were found that some species used the marine snow as food source, even when it was oil-contaminated. In the last microcosm experiment, described in Chapter 5, two benthic invertebrate species were monitored over a period of 42 days after which new animals were introduced and observed for an additional period of 22 days. Marine snow degradation again resulted in lower dissolved oxygen concentrations in the water column, which inhibited oil biodegradation on the sediment compared to oil in combination with clay. The oxygenated top layer of the sediment disappeared, and recovered after ~20 days. At the end of the experiment, mudsnails from the treatments with oiled marine snow had higher PAH concentrations in their tissues than the animals from the treatments with the same amount of oil in clay only, confirming the use of marine snow as food source. Overall, oil-contaminated marine snow on the ocean sediment can negatively affect benthic ecosystems, and can hamper oil biodegradation and ecosystem recovery. The additional consequences of MOSSFA during oil spills and spill responses should be taken into account in oil spill response planning.