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ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on February 27, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(4):509-513; doi:10.1093/icesjms/fsn014
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© 2008 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Growth and biochemical responses of the offspring of mussels directly affected by the "Prestige" oil spill

Laura G. Peteiro, Ramón Filgueira, Uxío Labarta and María José Fernández-Reiriz

CSIC, Instituto de Investigaciones Marinas, Eduardo Cabello 6, 36208 Vigo, Spain

Correspondence to M. J. Fernández-Reiriz: tel: +34 986 231930; fax: +34 986 292762; e-mail: mjreiriz{at}iim.csic.es

Peteiro, L. G., Filgueira, R., Labarta, U., and Fernández-Reiriz, M. J. 2008. Growth and biochemical responses of the offspring of mussels directly affected by the "Prestige" oil spill. – ICES Journal of Marine Science, 65: 509–513.

We investigated whether perturbations to growth and biochemistry, detected in Mytilus galloprovincialis mussel seed cultured after the "Prestige" oil spill (2003), were evident in its offspring (2004). Sublethal effects in the 2003 mussels or, alternatively, direct exposure to remobilization of fuel on the seabed, might have detrimental effects on mussel juveniles in 2004. However, the absence of differences in lipid composition and growth performance between mussel seed gathered from the area most affected by the spill (Pindo) and the reference population (Miranda) seems to indicate the absence of sublethal effects related to hydrocarbon exposure in the offspring of mussels directly exposed to the "Prestige" oil spill.

Keywords: growth performance, lipid composition, Mytilus galloprovincialis, mussel raft cultivation, "Prestige" oil spill, sublethal effects

Received 11 July 2007; accepted 16 January 2008; advance access publication 27 February 2008.


   Introduction
Top
 Introduction
Material and methods
 Results and discussion
 References
 
The "Prestige" oil spill (~60 000 t of a Russian heavy fuel oil) in November 2002 affected a large area (~800 km of the NW Spanish coast) and a variety of habitats (González et al., 2006). During the first few days after the spill, the oil floated on the sea surface and might also have been mixed within the water column. Owing to the nature of the oil (type M–100), it deposited in particulate and aggregate form on the seabed (Sánchez et al., 2006). Therefore, the evolution of PAH concentration in seawater, sediment, and mussel tissues showed a similar pattern, with high concentrations during the first few days after the spill, followed by a depuration period when hydrocarbon concentration diminished close to background levels in seawater and mussel tissues (Nieto et al., 2006; Soriano et al., 2006). In the winter following the spill, there was a slight increase in hydrocarbon concentration in the sea and mussel tissues, probably through subtidal remobilization during winter storms (Nieto et al., 2006; Soriano et al., 2006). However, Laffon et al. (2006) suggested that the environmental impact of the oil spill persisted until June 2004. Mytilus galloprovincialis larval stages or embryos, which are the most sensitive stages in the life cycle of Mytilus (Martin et al., 1981), might be directly exposed to such incidental increases of hydrocarbons in seawater.

Bivalves, particularly mussels, are widely distributed sessile filter-feeders that may react to environmental changes through easily measurable physiological responses (Dame, 1996). Therefore, mussels are commonly used as sentinel organisms to identify the status and trends of chemical exposure and to establish pollution gradients in a variety of environments. In addition, the industry farming mussels (M. galloprovincialis) is a cornerstone of the Galician (NW Spain) economy and requires viable mussel seed for economic success. Although significant quantities of spilled oil did not enter the inner part of the estuaries where commercial raft culture of mussels takes place, there was a significant impact on an extensive area where mussel seed is gathered for cultivation. Several sublethal effects have been observed in mussels directly exposed to the "Prestige" oil spill, such as DNA damage (Laffon et al., 2006), lysosomal disturbances, and alterations of the digestive gland (Marigómez et al., 2006), diminished survival rate in air, and changes in lipid and fatty acid compositions (Labarta et al., 2005). In addition, an experimental culture following industrial procedures was carried out to assess the progress of growth and biochemical composition of individual mussels from seeding to harvest (Peteiro et al., 2006, 2007). Those studies pointed out several sublethal effects for mussel seed from the impacted area, as both short-term (alterations in lipid composition) and long-term effects (slower growth rates). Natural stress and stress related to pollution are often linked with reduced growth rates (Salazar and Salazar, 1991; Dame, 1996) and with changes in biochemical composition, specifically in fractions that involve changes in the cycle of accumulation and use of energy reserves (Patel and Eapen, 1989; Capuzzo, 1996; De Coen and Janssen, 1997; Smolders et al., 2004). Several surveys have reported either decreases or increases in total carbohydrates or proteins related to pollution (Patel and Eapen, 1989; De Coen and Janssen, 1997; Smolders et al., 2004). Nonetheless, studies on exposure to lipophylic organic contaminants such as PAHs or PCBs primarily focus on the impairment of lipid metabolism, mainly in the distribution and concentration of polar and neutral lipids (Capuzzo and Leavitt, 1988; Capuzzo, 1996; Ferreira and Vale, 1998; Bergen et al., 2001), because of the greater sensitivity of this fraction (De Coen and Janssen, 1997). Stress in Mytilus edulis adults affects their eggs (Bayne et al., 1978), so the offspring of mussels affected by a spill might also show sublethal effects even without direct exposure to the oil.

Sublethal effects in the 2003 mussels or, alternatively, direct exposure to remobilization of fuel on the seabed, might have had detrimental effects on mussel juveniles in 2004. The aim of this study was to assess whether perturbations in mussel seed growth (slower growth rates; Peteiro et al., 2006) and biochemistry (changes in lipid content; Peteiro et al., 2007) observed in the first mussel seed cultured after the "Prestige" oil spill (2003) from an impacted area are evident in its offspring (2004).


   Material and methods
Top
 Introduction
 Material and methods
Results and discussion
 References
 
Mytilus galloprovincialis seed was gathered from two locations along the Galician coast, Pindo and Miranda (Figure 1), in February 2004. The mussel seed gathered is considered to be the offspring of mussels evaluated the previous year as a consequence of the reproductive cycle of M. galloprovincialis in Galicia (Villalba, 1995). Although the larval dispersion pattern in these areas is not known, the mussels we gathered were the offspring of mussels settled in the same area the previous year or the offspring of mussels settled nearby which were similarly exposed to the spill (González et al., 2006). The Pindo location was considered to be the area impacted by the spill, according to the mussel seed physiological and biochemical response the previous year (Labarta et al., 2005; Peteiro et al., 2006, 2007) and according to Soriano et al. (2006), who considered as "hotspots" of the spill those locations with total concentrations of 13 parent PAHs in wild mussel tissues >500 µg kg–1 dry weight and reported 4134 µg kg–1 dry weight at a station nearby in February 2003. Miranda is outside the main impacted area (González et al., 2006), values of total concentrations of 13 parent PAHs in wild mussel tissues at a station nearby in February 2003 being 268 µg kg–1 dry weight (Soriano et al., 2006); mussels from that location did not display sublethal effects the previous year (Labarta et al., 2005; Peteiro et al., 2006, 2007), so are considered to be a reference population. Both mussel seed populations were transplanted from their original locations to the Lorbé area in the Ría de Ares-Betanzos, to maintain both under equal environmental conditions for the evaluation of growth performance. Two ropes were used for each population, with a density of ~15 kg of mussel seed per rope. Initial shell lengths (mean ± s.d.) were 15.98 ± 1.146 and 16.77 ± 0.602 mm (F1,4 = 2.234, p = 0.209), and total dry weights were 0.16 ± 0.027 and 0.14 ± 0.009 g (F1,4 = 0.467 p = 0.532) for mussels from Pindo and Miranda, respectively. The experiment, which lasted until April 2005, employed a raft system (500 m2) and commercial protocols and techniques.


Figure 1
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  		Figure 1. Map of Galicia (NW Spain) showing the exposed (Pindo) and reference (Miranda) mussel seed sites (in squares), the location of the experimental culture (underlined) and the location of the wreck of the tanker "Prestige".

 
Gross biochemical composition (proteins, carbohydrates, and total lipid content) and lipid composition (phospholipids, sterol esters + waxes, sterols, free fatty acids, and triacylglycerols) were analysed at the onset of the experimental culture in February 2004. Growth performance [rates of growth in length and weight, adjusted growth curves, and length classification (<50, 50–70, and >70 mm) at harvest] was evaluated monthly from seeding to harvest. Sampling protocol and data analysis followed (Peteiro et al., 2006, 2007).


   Results and discussion
Top
 Introduction
 Material and methods
 Results and discussion
References
 
At the onset of the experiment, no differences in total lipid content (p > 0.05; Table 1) or lipid class composition (p > 0.05; Table 1) were detected between populations. In the previous year at the start of the culture, the seed from Pindo had a higher total lipid content, particularly of triacylglycerols, and lower phospholipid and free fatty acid concentrations than seed from areas not impacted by the oil spill (Labarta et al., 2005; Peteiro et al., 2007). Changes in lipid metabolism as sublethal effects of exposure to organic contaminants such as PAHs or PCBs are well documented (Capuzzo and Leavitt, 1988; Ferreira and Vale, 1998; Bergen et al., 2001; Smolders et al., 2004; Orbea et al., 2006), and most surveys have stressed impairments in the distribution and concentration of polar and neutral lipids, which are commonly reflected by increases in triacylglycerol content (Capuzzo and Leavitt, 1988; Bergen et al., 2001). In terms of gross biochemical composition, differences in protein and carbohydrate concentrations between populations were observed here (Table 1; p < 0.05). Although levels of proteins and carbohydrate could be used as indicators of the impact of environmental contamination (Patel and Eapen, 1989; De Coen and Janssen, 1997; Smolders et al., 2004), studies of exposure to lipophylic organic contaminants such as PAHs and PCBs have primarily focused on the impairment of lipid metabolism, mainly in the distribution and concentration of polar and neutral lipids, owing to their sensitivity (Capuzzo and Leavitt, 1988; De Coen and Janssen, 1997; Bergen et al., 2001). Therefore, the lack of response in the lipid fraction likely indicates that the variability in protein and carbohydrate content between the two populations was related to local environmental heterogeneity in temperature, food availability, and quality.


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  		Table 1. Gross biochemical composition, lipid composition, and growth rates of the exposed (Pindo) and reference (Miranda) populations (mean ± s.d.), and MANOVA comparisons between locations.

 
Growth performance integrates the physiology of bivalve molluscs and, therefore, is a widely used indicator of pollution and environmental quality (Salazar and Salazar, 1991; Dame, 1996). Here, no differences were detected between populations in any of the values of growth curve parameters (Figure 2; p > 0.05) or growth rates (Table 1; p > 0.05). Differences in mussel size between populations [percentage of mussels below the minimal commercial length (<50 mm), small mussels (50–70 mm), and large mussels (>70 mm)] were not observed (Figure 3; p > 0.05). As commercial classification of mussels is based on the number of mussels per kg, the same classification applies to both populations. In an earlier experimental culture (Peteiro et al., 2006), the Pindo population showed a lower asymptotic value in the weight growth curve and slower weight growth rates than populations from unpolluted areas. Additionally, in the earlier year’s harvest, a lesser percentage of Pindo mussels were classified as large mussels than in other populations, resulting in an inferior commercial classification, with obvious economic consequences.


Figure 2
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  		Figure 2. Growth curves for the two mussel populations cultivated (February 2004/April 2005) in terms of (a) shell length, and (b) total dry weight, both adjusted to the Gompertz model (Yt = Y{infty}(e–e(–k (t—t'))). All parameters are statistically significant (p < 0.001) and are compared between populations using an extra sum-of-squares (Motulsky and Christopoulos, 2004).

 


Figure 3
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  		Figure 3. Percentage of mussels <50, 50–70, and >70 mm obtained for each population at harvest (April 2005). Frequency values of these mussel sizes among experimental populations were compared using contingency tables and {chi}2 statistics. Lines drawn at equal levels represent no significant differences (p > 0.05).

 
Cajaraville et al. (2006) also observed signs of recovery in mussel health 2 years after the "Prestige" oil spill, related to lysosomal membrane stability and cell composition in digestive gland epithelia. In addition, PAH concentrations detected in sediments showed no effects in bivalve embryogenesis bioassays (Beiras and Saco-Álvarez, 2006; Franco et al., 2006). Those authors suggested that the fraction of weathered fuel which accumulated in the sand as solid particles and tar balls lacked toxicity to water column organisms as a result of evaporation, dissolution, and photodegradation of toxic components of low molecular weight during initial weathering. Similarly, Page et al. (2005) concluded that hydrocarbons from residues of the "Exxon Valdez" oil spill that remained buried in shoreline sediments for several years had limited bio-availability to mussels.

In summary, the absence of differences in biochemical composition and growth performance between the reference (Miranda) and spill-impacted area (Pindo) may indicate an absence of the effects of hydrocarbon exposure in the offspring of mussels directly affected by the "Prestige" oil spill.


   Acknowledgements
 
We thank PROINSA mussel farm and their employees, especially H. Regueiro, M. García, C. Brea, and O. Fernández-Rosende, for technical assistance. We also thank A. Ayala, B. González, and L. Nieto for conducting the biochemical analyses. The study was supported by the contract project PROINSA, Code CSIC 2004448, Galicia PGDIT03RMA13E.


   References
Top
 Introduction
 Material and methods
 Results and discussion
 References
 

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This Article
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