How does the greater white-toothed shrew, Crocidura russula, responds to long-term heavy metal contamination? — A case study

Abstract

Heavy metals accumulation in parallel with the evaluation of physiological and biochemical effects resulting from continued metal exposure were considered here using for the first time the great white-toothed shrew Crocidura russula as an in vivo model. Shrews were originated from an abandoned lead/zinc mining area and from a reference area, both in Alentejo, southern Portugal. Hepatic contents of nickel, copper, zinc, cadmium, mercury and lead were quantified by Inductively Coupled Plasma Mass Spectrometer (ICP-MS). Haematological parameters (white blood cells, red blood cells, haemoglobin and haematocrit) were obtained in a Coulter Counter Analyser and biochemical markers of the redox balance (glutathione S-transferase, glutathione peroxidase, and glutathione reductase) activities were measured spectrophotometrically using a Duo-50 spectrophotometer. Compared with control animals, significantly higher concentration of hepatic cadmium (9.29 vs. 1.18 μg/g dry weight) and nickel (1.56 vs. 0.343 μg/g dry weight) were detected in the shrews collected in the mining area. However, no significant changes were observed on haematological or enzymatic parameters in animals exposed to metal pollution. The obtained results show that shrews are good bioaccumulators of toxic heavy metals, but very tolerant to their effects, revealing an interesting long-term adaptation to polluted environments. In addition, this study provides reference values for haematological parameters and antioxidant enzymes levels in C. russula, which may be relevant for comparative purposes in further studies.

Introduction

Mining wastes remaining after the extraction of target metals are referred as important sources of environmental contamination, reaching in some cases levels that might become toxic to wildlife and an environmental risk to human health. Portugal has a legacy of about 85 old mines deactivated for economical reasons. Most of these mines were deactivated without any previous environmental recovery plan. As a consequence, tones of metal residues are still circulating in their surroundings (Santos Oliveira et al., 2002). Preguiça, a lead/zinc mine located in Alentejo, southern Portugal was deactivated 40 years ago, being a fine illustration of this reality. Over the last decades, the area once occupied by the mine has been covered by vegetation, hiding all the tailings and scoria produced and accumulated in the soil.

Several studies have confirmed that insectivores may accumulate superior amounts of heavy metals in their tissues, suggesting their major role as biomonitors (e.g. Talmage and Walton, 1991, Ma et al., 1991, Ma, 1996, Pankakoski et al., 1993, Pankakoski et al., 1994, Komarnicki, 2000, Ma and Talmage, 2001). The potential interest of ground-living insectivores as in situ models, such as shrews, is explained by their widespread occurrence; limited home range; small body size; high metabolic rate; and invertebrate-based diet, especially because invertebrates are known to accumulate high levels of metals (Hunter and Johnson, 1982, Scanlon, 1987, Ma et al., 1991, Shore, 1995). In the present study, the greater white-toothed shrew, Crocidura russula, a widely distributed species in western and southern Europe, including Portugal (ICN/CBA, 1999), is tested as a model of environmental long-term mining contamination.

Ecotoxicological surveys usually focus on bioaccumulation but rarely determine biological effects of long-term exposure to mining residues. So, only a few studies report morphological, biochemical, haematological, or genetic alterations for metal-exposed insectivores (e.g. Ma, 1989, Dodds-Smith et al., 1992, Hendricks et al., 1995) or other small mammals (Nunes et al., 2001, Viegas-Crespo et al., 2003). In this study, in addition to hepatic heavy metal accumulation, haematological and biochemical effects are investigated in C. russula inhabiting an abandoned mine area. Haematological values (white and red blood cells, haemoglobin and haematocrit) can be indicative of the physiological status of wild animals (Marques et al., 2006). Biochemical parameters, such as antioxidant enzyme activities (glutathione S-transferase, glutathione peroxidase and glutathione reductase) are often used as markers of oxidative stress, considering the active role they play in the detoxification of deleterious compounds produced by several metals and other environmental pollutants (Cnubben et al., 2001).

The obtained results will also allow i) to assess the role of the white-toothed shrew as a bioindicator of heavy metal pollution, ii) to determine haematological and biochemical reference values for this species and at last iii) to confirm the potential environmental risk of abandoned mines.