Erica Giarratano

Seasonal variation in biomarkers in blue mussel (Mytilus edulis), Icelandic scallop (Chlamys islandica) and Atlantic cod (Gadus morhua)—Implications for environmental monitoring in the Barents Sea

In the Barents Sea, the limited data on biological relevant indicators and their responses to various anthropogenic stressors have hindered the development of a consistent scientific basis for selecting indicator species and developing practical procedures for environmental monitoring. Accordingly, the main aim of the present study was to develop a common set of baseline values for contaminants and biomarkers in three species, and to identify their strengths and limitations in monitoring of the Barents Sea. Blue mussel (Mytilus edulis), Icelandic scallop (Chlamys islandica) and Atlantic cod (Gadus morhua) were sampled from a north Norwegian fjord in March, June, September and December 2010. Digestive glands from the bivalve species and liver from Atlantic cod were analysed for biomarkers of oxidative stress (catalase [CAT], glutathione peroxidase [GPX], glutathione-S-transferase activities [GST], lipid peroxidation as thiobarbituric reactive substances [TBARS] and total oxyradical scavenging capacity [TOSC]), biotransformation (ethoxyresorufine-O-deethylase activity [EROD]) and general stress (lysosomal membrane stability [LMS]). Concentrations of polycyclic aromatic hydrocarbons (PAHs) and metals in the bivalves and PAH metabolites in fish bile were quantified. Finally, energy reserves (total lipids, proteins and carbohydrates) and electron transport system (ETS) activity in the digestive gland of the bivalves and liver of Atlantic cod provided background information for reproductive cycle and general physiological status of the organisms. Blue mussel and Icelandic scallop showed very similar trends in biological cycle, biomarker expression and seasonality. Biomarker baselines in Atlantic cod showed weaker seasonal variability. However, important biological events may have been undetected due to the large time intervals between sampling occasions. Physiological biomarkers such as energy reserves and ETS activity were recommended as complementary parameters to the commonly used stress biomarkers, as they provided valuable information on the physiological status of the studied organisms. Interpretation of the seasonality in oxidative stress biomarkers was in general difficult but TOSC and lipid peroxidation were preferred over the antioxidant enzyme activities. This study is the first reporting seasonal baseline in these three species in a sub-Arctic location. Overall, the Icelandic scallop was considered the most adequate organism for environmental monitoring in the Barents Sea due to the interpretability of the biomarker data as well as its abundance, ease to handle and wide distribution from the southern Barents Sea to Svalbard.

Biomarkers and heavy metal bioaccumulation in mussels transplanted to coastal waters of the Beagle Channel.

Mussels coming from a mussel farm at Brown Bay (Beagle Channel) were transplanted to four sites inside Ushuaia Bay for 2 and 4 weeks. The objective of this study was to assess the quality of coastal waters of Ushuaia Bay by measuring catalase activity, lipid peroxidation, total lipid content, bioaccumulation of heavy metals and condition index in transplanted mussel Mytilus edulis chilensis. Biomarkers except condition index showed significant differences among exposure times as well as among tissues. Digestive gland presented the highest catalase activity, malondialdehyde level and total lipid content. Digestive gland also was the main target tissue of accumulation of iron and copper, while gill accumulated the highest levels of zinc. A principal component analyzes with the whole set of data allowed to separate stations based on physicochemical conditions and biochemical responses of each studied area.

Heavy metal concentrations and biomarkers of oxidative stress in native mussels (Mytilus edulis chilensis) from Beagle Channel coast (Tierra del Fuego, Argentina).

The aim of this study was to evaluate the usefulness of oxidative stress biomarkers of pollution in native mussels Mytilus edulis chilensis from the Beagle Channel. Spatial and seasonal variations of catalase, glutathione-S-transferase and lipid peroxidation in gills and digestive gland were analyzed in relation to environmental parameters, heavy metals in sediment and in tissue. Four sites with anthropogenic impact and a control site were selected and monitored during the four seasons of 2007. We found significant differences among sites in concentrations of dissolved nutrients and heavy metals in sediments, with the highest values recorded at sites with anthropogenic pressure. Different patterns were observed between concentrations of metals in tissues and in sediments suggesting differences in bioavailability. There were also significant differences in biomarker responses among sites, despite the strong seasonal variability. Our results showed relatively moderate levels of pollution in the study area as a result of urban influences.

Seasonal and pollution-induced variations in biomarkers of transplanted mussels within the Beagle Channel.

The occurrence of biomarker variations linked to environmental factors makes it difficult to distinguish the effect of pollution. In an attempt to evaluate spatial and seasonal effects of environmental parameters on biomarker responses, mussels Mytilus edulis chilensis coming from an aquaculture farm were transplanted to several points within Ushuaia Bay (Beagle Channel) for 6 weeks in summer and winter. Activities of superoxide dismutase, catalase, glutathione-S-transferase and levels of lipid peroxidation were measured in gills and digestive gland. Cu, Zn, Fe, Cd and Pb concentrations were also assessed. Results indicated a significant effect of seasons on biological responses as well as in metal bioaccumulation showing the influence of natural factors such as dissolved oxygen, temperature and food availability. The interdependence of those environmental factors is important for the homeostasis of thermoconformers, especially regarding their oxidative metabolism and should also be taken into consideration to distinguish natural from pollution-induced variations.

Heavy metals monitoring in the southernmost mussel farm of the world (Beagle Channel, Argentina).

Water quality surrounding the mussel farm of Mytilus edulis chilensis at Brown Bay (Beagle Channel) was evaluated. The levels of five heavy metals in sediment and in gill and digestive gland of mussels were examined to consider potential risks to human health. Cd showed the highest enrichment factor in relation to its level in Earth crust (3.85-21.58), which could be related to an upwelling phenomenon. A seasonal trend was found regarding metal bioaccumulation, being higher in winter than in summer. The bioaccumulation pattern in gill was Zn>Fe>Cu>Cd, meanwhile in digestive gland was Fe>Zn>Cu>Cd. Despite Pb was measured in sediment (15.59-23.91 microg/g dw), it was not available for being incorporated by mussels. In all cases it was below the detection limit (2.37 microg/g dw). With regard to human consumption of mussels from Brown Bay, none of the elements analyzed should cause concern for consumers. Values measured in tissue mussels were below the limit of 10 microg/g dw for Cd and Pb established by SENASA for molluscs. Considering that studied mussels are for human consumption and the relatively high levels of metals in sediment may vary their availability if physical parameters changes, periodical monitoring must be carried out to avoid human risks and to produce food in a responsible manner that complies with the food safety standards.

Biomarkers of environmental stress in gills of ribbed mussel Aulacomya atra atra (Nuevo Gulf, Northern Patagonia)

In this study, we assessed in gills of native ribbed mussels Aulacomya atra atra from three sites within Nuevo Gulf (Northern Patagonia) several biomarkers such as reactive oxygen species (ROS), lipid radicals (LR), malondialdehyde (MDA), superoxide dismutase (SOD), catalase (CAT), glutathione S-transferase (GST) and metallothionein (MT). Furthermore, concentrations of main trace metals (Fe, Al, Zn, Cu, Cd and Pb) were quantified in mussel tissue. Results showed significant induction of SOD, GST, MT and MDA, as well as, higher concentration of Fe, Al and Cd in winter than in summer. The high MDA content measured in mussels from Folías Wreck seemed to be caused by the very high levels of Fe that would come from the corrosion of the vessel. Mussels from the control site Punta Cuevas presented the lowest levels of Cd and the highest of Al in winter. Despite positive correlations were found between Al and GST and MT, no spatial differentiation was detected in those biomarkers. On the other hand, MT was only related to Al been most likely influenced by environmental variables than by the trace metals. It has to be highlighted that the relationship detected among water temperature, nutrients and antioxidant responses in gills is probably related to the fact that this tissue is in direct contact with water and it is sensitive to its fluctuations. Taking into account that mussel gill is a tissue actively proliferating and the first target of contaminants present in water, so that changes in its antioxidant system can provide an earlier warning signal than in other tissues.

Trace metal content in sediments and autochthonous intertidal organisms from two adjacent bays near Ushuaia, Beagle Channel (Argentina)

The aim of this work was to monitor levels of Cd, Cu, Pb, Zn and Fe in sediments, mussels (Mytilus edulis chilensis) and limpets (Nacella magellanica) from the Industrial zone (IZ); fuel dock (FD) and Ushuaia Peninsula (UP) on the Beagle Channel. In sediments, seasonal variations showed high values of Cu and Pb in spring and Zn in autumn. Comparing among sites, Cd concentration was superior in UP (2.07 μg/g); while Pb was maximum in FD (41.00 μg/g). In mussels, a higher bioaccumulation in winter was found. Mussels from UP showed the highest bioaccumulation of Cu (5.95 μg/g) and those from FD presented the highest of Zn (170.15 μg/g). A seasonal trend was not found for limpets, while differences among sites were observed for Cd being the highest at IZ (3.02 μg/g). Although pollution level found was low, anthropic activities at the studied sites could result in deterioration, further monitoring is recommended.

Assessment of antioxidant responses and trace metal accumulation by digestive gland of ribbed mussel Aulacomya atra atra from Northern Patagonia

Seasonal and spatial variability of trace metal concentrations and of a battery of antioxidant parameters were evaluated in digestive gland of the ribbed mussel Aulacomya atra atra. Fe, Al and Cu accumulated in tissue exhibited maximum values in winter, coinciding partially with the highest labile concentrations of Fe and Cu in sediment. Metals, as other pollutants, are known to influence the oxidative status of organisms and antioxidant enzymes have been often proposed as biomarkers of contaminant effects. Seasonal variations of trace metals did not appear to influence those of biochemical parameters, which generally showed an opposite trend with higher enzymatic activities in summer when trace metal concentrations were lower. Organisms from Punta Cuevas (control site) showed higher induction of reactive oxygen species production than those from both considered impacted sites, suggesting the possibility of some biochemical adaptation in organisms or a higher modulation of environmental and physiological factors on antioxidant responses than levels of trace metals. This study, which is the first in the area in this matter, showed that seasonal variations of potential biomarkers should be incorporated into interpretation of long-term biomonitoring studies in this marine coastal ecosystem.

Metals from mine waste as potential cause of oxidative stress in burrowing crab Neohelice granulata from San Antonio bay.

The Natural Protected Area San Antonio bay is of particular importance for its congregation of migratory shorebirds and it has been declared one of the Western Hemisphere Shorebird Reserve Network International site (WHSRN). Present study represents the first assessment of variation on oxidative stress biomarkers in male crab Neohelice granulata from San Antonio bay (Río Negro, Argentina) under field conditions, associated mainly to metal contamination coming from passive mining wastes. Three sites were sampled once every three months from November 2012 to August 2013 within this sea inlet (Pile, Fishery and Port) and a control site at the southeast of the bay (Punta Perdices). Accumulation of Ni, Zn, Cr and Al varied only with seasons although without a constant trend, meanwhile Cd, Cu and Pb also varied among sites being highest in Pile and Port. Biochemical results indicated that variations in catalase activity was only site specific being maximum in Pile; meanwhile lipid radical, α-tocopherol and metallothioneins were only seasonal specific being higher in autumn and winter. Seasonal variation was also found for total thioles, being the content higher in summer and autumn than in winter. Correlation analysis revealed that malondialdehyde and α-tocopherol have a positive association with Al and negative with Ni, meanwhile GST has a positive association with Fe. Crabs from the closest area to the waste pile did not exhibit a differentiated oxidative pressure despite the higher accumulation of metals. It is possible that crabs from contaminated areas have developed a tolerance to metals, indicating a strong ecotoxicological selective pressure. More studies are needed to assess whether there is a transfer of metals through the food chain.

Baseline levels of biomarkers of oxidative damage in Odontesthes nigricans (Pisces, Atherinopsidae) from two coastal areas of the Beagle Channel, Argentina

Se evaluaron diversos biomarcadores de dano oxidativo en el pejerrey Odontesthes nigricans proveniente de las bahias Varela y Golondrina, ubicadas sobre la costa norte del Canal Beagle (Tierra del Fuego, Argentina), y se trataron de relacionar las respuestas observadas a los datos ambientales. Bahia Varela es principalmente visitada por pescadores locales y turistas durante la temporada de primavera-verano, por otro lado Bahia Golondrina es un area de escaso impacto humano, a pesar del crecimiento poblacional registrado en sus inmediaciones. Los peces de Bahia Golondrina mostraron una mejor condicion en comparacion a aquellos provenientes de Bahia Varela. La actividad de los antioxidantes enzimaticos y el contenido de los antioxidantes no enzimaticos fueron mas bajos en las branquias que en el higado, independientemente del sitio de muestreo. No se encontraron diferencias significativas en las branquias entre sitios de muestreo. Sin embargo, se observo un aumento en la actividad de la catalasa y la superoxido dismutasa y una disminucion en la relacion GSH/GSSG en el higado de los peces de Bahia Varela, posiblemente debido a mayores niveles de estresores ambientales naturales, principalmente metales en los sedimentos. Este estudio indica una respuesta organo-dependiente y establece diferentes niveles basales de parametros bioquimicos para cada bahia que pueden ser considerados como valores normales de homeostasis de pejerreyes salvajes.