Tipping Points and Indicators Fact Sheet - Lead
Authors
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47906
LEAD IN A NUTSHELL:
• Lead is a poisonous metal, exhibiting neurotoxicity in mammals and a host of physiological and behavioral changes in fish
o Chronic lead exposure results in decreased production of delta-aminolevulinic acid (ALA-D), a critical enzyme in the blood, altered osmoregulation, and severe physical abnormalities in fish such as black tails, lordoscoliosis, muscular atrophy, caudal fin degeneration, and paralysis
o Neurological damage and behavioral changes include increased prey spitting, hyperactivity, and decreased reaction capabilities
• While fish may be able to adapt to chronic exposures of other metals, for example copper, by producing certain proteins such as metallothioneins, studies have shown that fish do not produce these same physiological adaptive responses to lead, and instead tend to simply increase their body burden of lead
Lead is a poisonous metal that is known to damage nervous connections, and cause blood and brain disorders in mammals (ATSDR 2006). Metallic lead occurs in nature but is rare, and usually found in ore with copper and occasionally zinc and silver (Samans 1949). Lead pollution in waterways is a consequence of anthropogenic activities, deposited by industrial effluents and mining. It is one of the metals of highest concern in terms of its effects on physiology (Heath 1995).
Lead is known to inhibit the activity of the enzyme delta-aminolevulinic acid dehydrase (ALA-D), which catalyzes the first reactions of heme synthesis, which leads to the ultimate formation of hemoglobin (Heath 1995). Heme is a component of hemoglobin, the iron-containing red blood cell protein, whose functions are critical to the survival of all red-blooded vertebrates, as well as some invertebrates (Maton et al. 1993). Hemoglobin transports oxygen (which binds to the heme groups of the hemoglobin) from the lungs to the rest of the body where it releases oxygen for cell use, while picking up and delivering carbon dioxide to the lungs for exhalation (Hsia 1998). While mercury may also cause slight inhibition of ALA-D, other metals do not have measurable effects on this enzyme, which makes it a great diagnostic indicator of chronic or acute lead poisoning in humans (DeBruin 1976).
Similarly, when fish are exposed to lead, the ALA-D enzyme is inhibited. Studies show that a 60-day chronic exposures of a freshwater fish—a cyprinid, Barbus—to 47ug/L lead resulted in a severe reduction (12-31%) of red-blood cell counts, hematocrit (the percentage of blood volume occupied by red blood cells), hemoglobin concentration, and mean corpuscular volume (MCV, a measure of the average red blood cell volume reported as part of a standard complete blood count) (Tewari et al. 1987). Trout exposed to varying concentrations of waterborne lead (10, 75, 300ug/L Pb) exhibited a dose-dependent inhibition of ALA-D in their red blood cells and spleen. The highest concentration of lead (300ug/L) caused some trout to become anemic. The mechanisms that propagated anemia in the trout are predicted to be similar to that in mammals. In mammals, lead is shown to cause anemia (a condition in which the body does not have enough healthy red blood cells) by inhibiting ALA-D, which in turn prevents hemoglobin production, and shortens the lifespan of circulating red blood cells. Recovery of ALA-D activity of these exposed trout in lead-free water was extremely slow.
However, a review of biomonitoring studies of ALA-D levels in fish show that organic lead has little effect on the enzyme, and only inorganic lead is able to inhibit ALA-D (Hodson et al. 1984). Therefore, high blood levels of lead in fish but little ALA-D inhibition would indicate greater concentrations of organic lead in an aquatic environment, while inhibition of ALA-D would indicate higher concentrations of the inorganic form. Fortunately, fish contamination by inorganic lead is rarely severe enough to generate significant ALA-D inhibition. However, a study of the combined effects of various metals (cadmium and zinc) with lead shows that these two metals act synergistically with lead, and together become very powerful inhibitors of ALA-D; it is important to note that cadmium and zinc by themselves or together without lead do not impact ALA-D (Berglind 1986). Since natural systems are always a heterogeneous mixture of various pollutants, including heavy metals, this could mean that the ‘safe’ amounts of organic lead previously thought to cause little ALA-D inhibition, may actually significantly affect ALA-D function as a result of interacting with other contaminants, such as zinc and cadmium. Furthermore, regardless of lead source, the physiological and psychological effects of lead on fish can be rather severe.
Lead negatively effects osmoregulation in fish. An experiment that exposed various concentrations of lead (10/75/300ug/L) to rainbow trout in slightly hypotonic brackish water for 30 days showed a dose-dependent elevation in plasma potassium (Haux and Larson 1992). In vitro studies show that mammalian red blood cells (erythrocytes) leak potassium into plasma when exposed to lead. Increased plasma potassium in mammals is also associated with heart failure and cirrhosis (Rose 1999, Stepien and Miller 1994). However, it is unknown if these phenomena hold for fish (Hasan and Hernberg 1966). Even if increased potassium plasma in fish does not directly lead to heart disease and cirrhosis, it clearly upsets the osmoregulatory balance that fish must maintain in order to survive in their brackish or freshwater environments. Waterborne lead exposures in freshwater fish may actually be more detrimental, considering they expend more energy on osmoregulation—up to 50% of their resting metabolic rate—than saltwater species.
A study conducted on fish from a lead-contaminated lake showed a decrease in plasma sodium but no change in plasma potassium (Haux et al. 1985). It is possible that previous or chronic lead exposure has led to physiological adaptations over the generations of fish who have lived in this contaminated environment (Heath 1995).
However, a different chronic test that exposed various life stages of rainbow trout to lead showed that lead-exposed trout eggs and sac fry were more sensitive to the detrimental effects of lead than fish from non-exposed eggs (Davies et al. 1976). This suggests that chronic and multi-generational exposures to lead do not necessarily confer physiological adaptations. To support this notion, a study by Mebane et al. (YEAR) on the effects of chronic lead exposure on a midge’s life cycle suggest that these tolerant aquatic benthic macroinvertebrates are unable to regulate and develop tolerances to nonessential metals, such as lead.
Additionally, lead has not been shown to induce the production of Metallothioneins (MTs) (Juedes and Thomas 1984), which are low molecular weight polypeptides (i.e. proteins) that contain abundant sulfhydryl groups which bind to heavy metals which help provide protection against metal toxicity (Heath 1995).
Chronic exposure also exacerbates the lead body burden of fish by decreasing mucus production and secretion, which may serve as a way of decreasing metal uptake rate and inhibiting diffusion of the toxic chemicals (Miller & MacKay 1982, Handy & Eddy 1990, Part & Lock 1983). Another study by Somero et al. (1977) suggests that binding to mucus may be a critical mechanism by which fish depurate. Therefore, these studies suggest that chronic exposures result in dangerous body burdens. In fact, lead poisoning was found to result from resorption of lead through the gills, which gradually functionally damage their inner organs (Haider 1964).
Several physical abnormalities in fish have been documented as a result of chronic lead exposure. At relatively low concentrations, lead induces hyperactivity in freshwater fish such as largemouth bass (Atchinson et al. 1987). With increasing and chronic exposures to lead, physical abnormalities such as black tails, lordoscoliosis (spinal curvature), paralysis, muscular atrophy, and caudal fin degeneration have been observed in rainbow trout, and at times were so severe as to make spawning impossible. These abnormalities are strongly speculated to be associated with direct neurological damage due to chronic lead exposure (Davies et al. 1976).
Not surprisingly, lead is linked to neurological damage and behavioral changes in fish. For example, a feeding experiment in Zebrafish (with Daphnia) demonstrated an increase in handling time (time from capture until prey is swallowed) and a decrease in reaction distance (the distance between prey and point at which predator begins pursuit) after a 14-day exposure to 100ug/L Pb (Nyman 1981). Prey lost to predators after capture (prey spitting) was generally more pronounced in lead-exposed fish than those in control groups. A classical conditioning experiment in goldfish found learning impairments more prevalent in fish exposed to 70ug/L lead for 48 hours (Weir & Hine 1970). Other behavioral changes in fish due to lead exposure result from histological effects to lateral line organs, which ultimately affect olfactory organs. The lateral line organs of fish are primarily used to detect water movements, shifting pressure changes, and hydrodynamic activities in the immediate surroundings. Therefore, lead impairs reaction capabilities of fish, which in turn affects survival by predation and other environmental factors (Heath 1995).
The toxicity of waterborne lead, however, is also affected by the chemical and physical conditions of the water, as well as whether the lead is in dissolved form. Studies have shown that pH, water hardness, and the partial pressure of CO2 (gaseous) largely affect the toxicity of lead. Water that is lower in pH (more acidic) increases the uptake of lead, because acidification increases lead’s availability (Campbell and Stokes 1985). Water hardness has a large effect on lead’s toxicity (Spehar & Flandt YEAR); lead was found to be more toxic in soft water over hard water. This was partially demonstrated by how lead-induced physical abnormalities in fish occurred faster in softer water (Davies et al. 1976). Davies et al. attributed decreased toxicity of lead in harder water to how a larger proportion of it is partially tied up or complexed into non-toxic chemical compounds. Considering that the dissolved fraction of lead is directly toxic to fish in an aquatic environment (Berglind 1986), this makes sense. Water hardness also affects gill permeability to water and ions. Because lead does not biomagnify (i.e. concentrate up the food chain), a primary mechanism by which fish obtain lead is not through the ingestion of prey, but by simply breathing, or ventilating their gills. Harder water makes gill tissue less permeable, and therefore lead uptake via gill ventilation is reduced in these conditions (Hunn 1985). Additionally, the calcium ion, which is a major cation contributing to water hardness, also binds to gill surfaces, giving them a positive charge which repels other cations (McWilliams & Potts 1978), such as lead.