Crude Oil and Its Burnt Residues Induce Metamorphosis in Marine Invertebrates

Abstract

Metamorphosis is a critical process in the life cycle of most marine benthic invertebrates, determining their transition from plankton to benthos. It affects dispersal and settlement and therefore decisively influences the dynamics of marine invertebrate populations. An extended period of metamorphic competence is an adaptive feature of numerous invertebrate species that increases the likelihood of finding a habitat suitable for settlement and survival. We found that crude oil and residues of burnt oil rapidly induce metamorphosis in two different marine invertebrate larvae, a previously unknown sublethal effect of oil pollution. When exposed to environmentally realistic oil concentrations, up to 84% of tested echinoderm larvae responded by undergoing metamorphosis. Similarly, up to 87% of gastropod larvae metamorphosed in response to burnt oil residues. This study demonstrates that crude oil and its burned residues can act as metamorphic inducers in marine planktonic larvae, short-circuiting adaptive metamorphic delay. Future studies on molecular pathways and oil-bacteria-metamorphosis interactions are needed to fully understand the direct or indirect mechanisms of oil-induced metamorphosis in marine invertebrates. With 90% of chronic oiling occurring in coastal areas, this previously undescribed impact of crude oil on planktonic larvae may have global implications for marine invertebrate populations and biodiversity.

Keywords: benthic recruitment; crude oil; metamorphosis; planktonic larvae; pollution.

Figure 1

Survival and metamorphosis of gastropod (Rissoa sp.) veliger larvae after 3 days of exposure to oil burning byproducts (soot and burnt oil). (a) Experimental setup used to obtain soot and residues of burnt oil in the mesocosms (1: crude oil burning, 2: soot emissions collected, 3: rain simulation, 4: deposition of soot on the mesocosm). (b) Plankton net sample with high concentration of gastropod larvae (left) and individual gastropod larva (right), scale bar = 100 μm. (c) Effect of oil burning byproducts 1 day after burning on survival and metamorphosis of gastropod veliger larvae. (d) Effect of oil burning byproducts 6 days after burning on survival and metamorphosis of gastropod veliger larvae (Ctrl= control without pollutants, Soot, Oil= burnt oil). Lowercase italic letters (a, b) indicated different statistical groups (p < 0.05).

Figure 2

Effect of burnt oil on survival (left panel) and metamorphosis (right panel) of gastropod (Rissoa sp.) veliger larvae after 3 days of exposure to water collected from the mesocosms (10 days after burning) with or without the addition of food ad libitum (Isochrysis galbana, 50000 cells mL^–1) (Ctrl= control without pollutants, Oil= burnt oil). Lowercase italic letters (a, b) indicated different statistical groups (p < 0.05).

Figure 3

Survival and metamorphosis of competent sand dollar (Dendraster excentricus) larvae after 3 days of exposure to crude oil. (a) Schematic of the normal life cycle. (b) Effect of crude oil on metamorphosis (Amb = ambient temperature treatment (13 °C), HW = heat wave treatment (18 °C)). Data are presented as means (n = 3) with standard deviations. Lowercase italic letters (a, b, c) indicate different statistical groups (p < 0.05) and refer to the color-matching temperature treatment. (c) Effect of crude oil on survival at ambient temperature (left panel) and in the heat wave treatment (right panel).

Figure 4

Development of competent sand dollar (Dendraster excentricus) larvae after 3 days of exposure to crude oil. (a) Fraction of larvae with malformations (Amb = ambient temperature treatment (13 °C), HW = heat wave treatment (18 °C)). Data are presented as means (n = 3) with standard deviations. Lowercase italic letters (a, b, c) indicate different statistical groups (p < 0.05) and refer to the color-matching temperature treatment. (b–e) Images of larvae at the end of exposure: (b) competent larva that has not metamorphosed, (c) metamorphosed larva, and (d, e) malformed larvae. Scale bar = 200 μm.

Figure 5

Schematic of the normal life cycle of gastropods with planktonic larvae (left side) and the potential impact of oil pollution on this process (right side). After hatching, larvae swim in the plankton and disperse. Once they reach competence, they can react to chemical cues indicating suitable settlement substrates, undergo metamorphosis, and settle. Oil pollution can trigger metamorphosis and settlement in the absence of appropriate cues and result in settlement in unsuitable habitats.