View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Crossref Ecotoxicology (2013) 22:486–505 DOI 10.1007/s10646-013-1042-4 Marine ecosystem health status assessment through integrative biomarker indices: a comparative study after the Prestige oil spill ‘‘Mussel Watch’’ Ionan Marigo´mez • Larraitz Garmendia • Manu Soto • Amaia Orbea • Urtzi Izagirre • Miren P. Cajaraville Accepted: 19 January 2013 / Published online: 23 February 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com Abstract Five integrative biomarker indices are com- integrative indices based on biomarkers show different pared: Bioeffects Assessment Index (BAI), Health Status sensitivity, resolution and informative output, all of them Index (HSI), integrated biological response (IBR), eco- provide coherent information, useful to simplify the inter- system health condition chart (EHCC) and Integrative pretation of biological effects of pollution in marine pol- Biomarker Index (IBI). They were calculated on the basis lution monitoring. Each others’ advantages, disadvantages of selected biomarker data collected in the framework of and applicability for ecosystem health assessment are the Prestige oil spill (POS) Mussel Watch monitoring discussed. (2003–2006) carried out in Galicia and the Bay of Biscay. According to the BAI, the health status of mussels was Keywords Ecosystem health assessment Á Mussels Á severely affected by POS and signals of recovery were Prestige oil spill Á Integrative indices Á Biomarkers evidenced in Galicia after April-04 and in Biscay Bay after April-05. The HSI (computed by an expert system) Abbreviations revealed high levels of environmental stress in 2003 and a AChE Acetylcholinesterase activity recovery trend from April-04 to April-05. In July-05, the ADDU DNA adducts health status of mussels worsened but in October-05 and AOX Acyl-CoA-oxidase activity April-06 healthy condition was again recorded in almost all BAI Bioeffect Assessment Index localities. IBR/n and IBI indicated that mussel health was CAT Catalase activity severely affected in 2003 and improved from 2004 CI Cumulative intensity onwards. EHCC reflected a deleterious environmental CIIR Cumulative intensity of inflammatory responses condition in 2003 and a recovery trend after April-04, CIPI Cumulative intensity of parasitization although a healthy ecosystem condition was not achieved CRI (Sub)cellular Response Index in April-06 yet. Whereas BAI and HSI provide a basic DRI Disease Response Index indication of the ecosystem health status, star plots ECHH Ecosystem health condition chart accompanying IBR/n and IBI provide complementary ERI Epithelial Response Index information concerning the mechanisms of biological EROD Ethoxyresorufin-O-deethylase response to environmental insult. Overall, although the GST Glutathione-S-transferase activity HSI Health Status Index IBI Integrative biomarker index IBR Integrated biological response I. Marigo´mez (&) Á L. Garmendia Á M. Soto Á A. Orbea Á IRI Inflammatory response index U. Izagirre Á M. P. Cajaraville LMS Lysosomal membrane stability CBET Ikerketa-Taldea, Zoologia eta Biologia Zelularra Saila, LP Labilization period of lysosomal membrane Plentziako Itsas Estazioa (PIE), Universidad del Paı´s Vasco/ LPF Accumulation of lipofuscins Euskal Herriko Unibertsitatea, Areatza Z/G, 48620 Plentzia- Bizkaia, Basque Country, Spain LRI Lysosomal Response Index e-mail: [email protected] MAD Malonyl dialdehyde 123 Integrative biomarker indices for marine ecosystem health assessment 487 MET Mean epithelial thickness (digestive gland mechanistic information to scientists, albeit the full epithelium) potential of using biomarkers in biological monitoring MLR Mean luminal radius (digestive gland programs has been limited by the scarcity of integrated epithelium) statistical analysis (Beliaeff and Burgeot 2002). During the MMCs Melanomacrophage centers recent last years, however, biomarkers have been inte- MN Induction of micronuclei grated in ecosystem health indices for simplicity purposes. MRI Molecular/Metabolic Response Index The use of these indices provides comprehensive infor- MT Methallothioneins mation about the biological effects of pollution in marine NL Intracellular accumulation of neutral lipids organisms and may therefore serve as useful tools for PII Parasitic Infestation Index environmental managers (Broeg and Lehtonen 2006). POS Prestige oil spill The bioeffects assessment index (BAI; Broeg et al. SFG Scope-for-growth 2005), a modification of the ‘‘Health Assessment Index’’ SOS Stress-on-stress (HAI; Adams et al. 1993), was designed for the assessment SRI Systemic Response Index of multifactorial contamination in coastal areas using fishes S/VL Lysosomal surface-to-volume ratio as sentinels (Broeg et al. 2005). BAI is defined as a TBARS Thiobarbituric acid reactive substances ‘‘general health’’ index because it comprises biomarkers of TRI Tissue Response Index non-specific toxic effects and responds to a variety of VvBAS Volume density of basophilic cells different contaminants (Broeg et al. 2005). BAI was first VvL Lysosomal volume density applied for the long-term study of the biological effects of pollution in the German Bight using flounders (Platichthys flesus) as sentinels, and included deleterious effects at different levels of biological complexity, say: changes in Introduction EROD activity, LMS, NL and macrophage aggregates in liver, as well as diversity of parasitic fauna (Broeg et al. The key objectives in the assessment of marine ecosystem 2005). BAI was also satisfactorily applied in the Baltic Sea health are to provide information necessary to ensure (Broeg and Lehtonen 2006), as a part of the EU-BEEP maintenance of biodiversity and the integrity of marine project, where biomarkers had been recorded in sentinel P. communities, to limit human influences on living resour- flesus, eelpouts (Zoarces viviparous) and blue mussels ces, to protect critical habitats and to safeguard human (Mytilus edulis). In mussels, the selected biomarkers for the health. Changes in community structure and measures of calculation of BAI were LMS, NL and MN in digestive chemical contamination are often used to indicate ecosys- gland (Broeg and Lehtonen 2006). tem health status but, regrettably, these responses are The Health Status Index (HSI) is computed by an expert manifestations of damage rather than prognostic indices system (ES) designed and developed within the BEEP (Knap et al. 2002). Changes at simplest levels of biological framework to evaluate and integrate (effect and exposure) complexity (molecular, cellular, tissue-level), which responses of biomarkers (recorded at different levels of underlie effects at complex biological levels and for which biological organization in mussels) to natural and con- causality can be established (Cajaraville et al. 1993; Knap taminant-induced stress (Viarengo et al. 2000; Dagnino et al. 2002), may provide early warning of ecosystem et al. 2007). The expert system was first applied using 11 health deterioration. Biomarkers are responses at such biomarkers measured in caged mussels deployed along a simple levels that indicate the presence of pollutants pollution gradient near the Genoa Harbour (Dagnino et al. (exposure biomarkers) or the magnitude of the biological 2007). Later on, it was satisfactorily applied in several field response to pollutant exposure (effect biomarkers; and laboratory studies. In the field, HSI was computed to McCarthy and Shugart 1990). Effect biomarkers give a integrate seven biomarkers recorded in mussels caged general picture of the health status of the environment along a copper pollution gradient in the Visnes fjord whereas exposure biomarkers have specificity of reaction (Norway) (Dondero et al. 2006). The expert system was (McCarthy and Shugart 1990). Marine pollution monitor- also successfully applied to a set of 8 biomarkers data from ing programs are increasingly including molecular, cell and a biomonitoring study carried out about 20 years ago in the tissue-level biomarkers, applied in combination, for the pollution gradient along the Langesundfjord (Norway) assessment of the biological effects of pollutants (Den (data from GESAMP workshop (Oslo 1986); Dagnino et al. Besten 1998; Cajaraville et al. 2000; Viarengo et al. 2000; 2007). Under laboratory conditions, the expert system was Knap et al. 2002; Marigo´mez et al. 2006; Orbea et al. 2006; employed to integrate the responses elicited in 6 bio- Zorita et al. 2007; Hylland et al. 2008; Garmendia et al. markers recorded in mussels exposed to crude oil, alkylated 2011a, b, c). Thus, biomarkers have provided useful phenols and PAHs for 21 days in the RF Rogaland 123 488 I. Marigo´mez et al. Research Institute (Stavanger, Norway) (Dagnino et al. 2011c); (b) (sub)Cellular Response Index (CRI), measured 2007). In all cases, HSI computed by the expert system in terms of LRI (Izagirre and Marigo´mez 2009, Garmendia provided a clear indication of the stress syndrome in et al. 2011a); (c) Tissue Response Index (TRI), measured mussels, although the batteries of biomarkers employed in terms of VvBAS (Garmendia et al. 2011b); (d) Systemic differed in the type and number of biomarkers. Response Index (SRI), in terms of cumulative intensity of The Integrated Biological Response (IBR; Beliaeff and inflammatory responses (Garmendia et al. 2011b, c); and Burgeot 2002) index is based on biochemical biomarkers, (e) Disease Response Index (DRI)) in terms of