CHAPTER 15 CHAPTER 15 Lead in the Environment
15.3 INTAKE AND UPTAKE OF LEAD
Amounts of lead entering and being assimilated by plants and animals from the atmosphere, soil, and water are not always directly related to environmental concentrations. Lead intake and uptake depends upon many factors including its chemical and physical form, exposure route, and the biology of the exposed organism. Lead reaches plants via wet and dry deposition onto plant surfaces, including road and soil splash, and by uptake from roots. Inorganic lead reaches terrestrial animals mainly via inhalation and ingestion, and absorption through the skin or gills is important for aquatic animals. Organic lead may be absorbed through the skin of all animals, although such uptake is generally insignificant.
15.3.1 Plants
15.3.1.1 Aquatic Plants
The availability of lead (and other metals) for uptake by aquatic plants is related to a wide range of chemical and physical variables, including the chemical form of lead, the pH of water, the presence and quantity of calcium and magnesium ions (water hardness) and nutrients, and the quantity and nature of suspended material. Lead from water usually enters plants in an ionic form, and uptake by aquatic plants can be from water, soil, air, or a combination of the three depending upon the type of plant (rooted/submerged, etc.). Crowder54 reviewed lead uptake by plants. Of wetland plants, the submergent macrophytes generally tend to have the highest lead concentrations, although uptake is species-specific. Subterranean parts tend to accumulate the highest lead concentrations, and senescent foliage can contain higher lead concentrations than live foliage. Under certain conditions lead concentrations in aquatic plants have been correlated with sediment lead concentrations, and plant lead concentration may be negatively correlated with water pH. Under experimental conditions, pH and electrode potential (Eh) interact to influence lead uptake.54
In experimental studies with rooted macrophytes, lead was rapidly taken up from solution containing 1.0 mg Pb2+/L via passive mechanisms.55 A large proportion of lead taken up within one hour by shoots of Elodea canadensis was released within 2 weeks of transfer to clean water, although 10% appeared to remain irreversibly bound.
There has been concern over the uptake of lead deposited as gunshot by aquatic and terrestrial plants. Plants can take up large amounts of lead from spent gunshot deposited in acidic soils and sediments (maximum of 24,892 àg/g d.w. — T. Elkington, pers. comm.). However, most wetland sites are not particularly acidic, and Behan et al.56 found similar lead concentrations in plants collected from heavily hunted wetlands and from refuges. In spite of this some lead from deposited shot may become available for uptake, and these authors found that 3 years after seeding a 0.17-ha pond with 227 kg lead shot, the roots and shoots of aquatic plants had significantly higher lead concentrations than controls. However, this amount of shot is at least an order of magnitude higher than that found in most heavily shot-over wetlands. The exception to this is the fall zone from shotgun target ranges, where lead shot density ranged from 4.15 x 106 to 3.70 x 109 pellets/ha.57
15.3.1.2 Terrestrial Plants
Quantities of lead accumulated on plant surfaces are related to atmospheric concentrations, particle size, topography, climate, and surface characteristics of plants. Little is known of the movement of aerosol lead following deposition on plant surfaces or in stomata, although it appears that most deposited lead is immobile, perhaps being embedded in the cuticle. Although foliar transport of aerosol lead appears limited in most species, Rule et al.,58 using a solution of 210Pb, illustrated foliar absorption and translocation of lead to the youngest leaves of lettuce and the storage roots of white icicle radish plants. Translocation of atmospherically derived lead within some species has been confirmed using similar 210Pb tracer studies.59
The contribution of atmospheric lead to total plant lead may be high both in areas of low soil and low atmospheric lead concentrations as well as in areas with high atmospheric lead concen- trations. Tjell et al.60 found that > 90% of total lead in grass in rural areas of Denmark resulted from atmospheric deposition. Plants with rough foliar surfaces tend to retain more lead than those with smooth or waxy surfaces,61 and surface characteristics may also influence the amount of lead removed by precipitation. Large seasonal fluctuations in the lead concentrations of foliar parts of plants have been recorded, with values sometimes an order of magnitude higher in winter than in summer months. Increased concentrations in winter are thought to be related to higher deposition rates resulting from increased thermal stability in winter,62 possible higher lead uptake by dead and decaying material due to cuticular breakdown increasing permeability and facilitating lead access,63 and slower winter pasture turnover rates.
The availability of soil lead for uptake by plant roots depends upon physical and chemical soil characteristics. Lead is generally strongly adsorbed onto solid soil components with high organic matter cation exchange capacity and high percentage silt or clay. Under such conditions little ionic lead is available in the aqueous phase for uptake by plant roots. When soils are low in the components described and under conditions of poor drainage, low soil pH, and low concentrations of iron oxides and phosphorus, the availability of lead to plant roots increases. The application of calcium or phosphate to soils can reduce lead availability to plants through the formation of lead hydroxide, carbonate, or phosphate compounds of low solubility.64 Lead uptake by roots can be passive65 or active,66 and uptake is influenced by species, cultivar, age, and growth rate. Metal uptake by roots can be accelerated in species in which roots release solubilizing agents or carriers into the rhizosphere, as some of these may act as ligands or chelate metals.54 Transport of lead between roots and foliar parts of plants tends to be limited, and it has been suggested that lead may be precipitated in vesicles that fuse with cell walls in roots, immobilizing and inactivating it.66 However, although most lead taken up from soil appears to accumulate in roots, Rolfe67 found that significant concentrations of lead also accumulated in the leaves and stems of eight tree species within one growing season in soils of high lead content.
The high binding capacity of soil for lead, its limited transport from roots, and the tendency for lead to accumulate at xylem sites within the plant all act as natural barriers against the movement of lead to foliar parts.68 Although total plant lead concentrations are generally higher with high soil lead concentrations, the increase in plant lead is generally small proportional to that in soils. The Ministry of Agriculture, Food and Fisheries (MAFF)69 investigated lead concentrations in plants grown in a variety of soils and found that, in soils with up to 25 times background lead concen- trations, plant lead concentrations did not more than double.
15.3.2 Animals
15.3.2.1 Aquatic Animals
Lead uptake by aquatic organisms is via water (absorption through skin, gills, intestine, etc.) and food. The chemical form of lead and other elements present both in water and diet, along with
species and other biological and environmental factors, influences lead uptake. Lead uptake by certain freshwater fish, such as the pumpkinseed sunfish (Lepomis gibbosus) and rainbow trout (Salmo gairdneri), has been shown to increase as water pH decreases.70,71 As in many terrestrial animals, calcium appears to have an important influence on lead transfer. Lead uptake and retention in the skin and skeleton of coho salmon (Oncorhynchus kisutch) was reduced when waterborne or dietary Ca was increased.72
Organic lead compounds, which accumulate in lipids, tend to be taken up and accumulated by freshwater teleosts more readily than inorganic lead compounds. Organic lead compounds are generally more toxic than inorganic compounds to aquatic organisms, and toxicity increases with the degree of alkylation.73 A wide range of aquatic organisms can absorb and accumulate very high lead concentrations, and the residence time of lead appears to be related to the route of administration.74
15.3.2.2 Terrestrial Animals
Ingestion and inhalation are the most important exposure routes of lead to terrestrial animals.
The relative contributions of those routes to total body burden will vary according to environmental concentrations, other environmental factors, and biological considerations such as species, age, sex, and diet.
15.3.2.2.1 Inhaled Lead
Most atmospheric lead is present as particulate inorganic salts, which, following inhalation, may be exhaled, deposited in the lungs and lower respiratory tract, or deposited in the windpipe and subsequently swallowed. Maximum lung retention occurs when particle sizes are 1.5 to 2.5 àm aerodynamic diameter.75 Although deposition rates vary in relation to air lead concentration, particle size, and respiration rates, approximately 50% of inhaled lead is deposited in the lungs, even when atmospheric lead concentrations are relatively high.76 Practically all lead deposited in the lungs is absorbed into the bloodstream. Half-lives of removal of lead from the lungs have been estimated at 6 h for humans77 and 12 h in dogs.78 Very little lead is thought to remain in the lungs after 3 days. Although most atmospheric lead is inorganic, a similar proportion of organic lead may be absorbed.79
15.3.2.2.2 Ingested Lead
Lead is usually ingested along with food and water but may be ingested independently. Examples of nonfood ingestion include the ingestion of spent lead gunshot and anglers weights by waterfowl and ingestion of paint chips and soil by children and other young animals, known as “pica” (the compulsive active ingestion of nonfood objects). Contaminated sediments adhering to food items not only contribute to the body burden but may reach toxic levels when sediment distribution is restricted but lead content is high. Sediments in the Coeur d’Alene river system have been implicated in numerous lead poisoning instances in tundra swans.45
Following the ingestion of lead in the diet, a large proportion is eliminated directly with the feces. The proportion of ingested lead absorbed from the intestine is small relative to the proportion of inhaled lead absorbed and varies according to a wide range of factors, primarily dietary.
Absorption of ingested lead is reduced when ingestion occurs along with food or if food is already present in the intestine.80 It is believed that certain dietary constituents may either inhibit lead absorption through the intestinal wall or stimulate the excretion of lead into feces, or both.81 The strong influence of dietary and other factors on intestinal lead absorption is such that values given in the literature for intestinal lead absorption in humans vary by up to an order of magnitude.
However, the majority of studies have found an 8 to 18% absorption of ingested lead, and 10% is most frequently quoted.16,82,83 In other animals gastrointestinal absorption efficiencies are different, and even within species large variations are recorded.
15.3.2.2.2.1 Factors Influencing Lead Absorption in the Intestine — The amount of lead absorbed from the intestine depends upon a range of factors including the chemical form of lead ingested. As early as 1923 Hanzlik and Presho84 illustrated experimentally that metallic lead was more toxic to pigeons than similar amounts of lead as lead chloride, iodide, sulfide, carbamate, or acetate. They suggested that this might result from reduced lead solubility and, consequently, reduced intestinal uptake when other elements were present along with the lead. The physical as well as chemical form of lead also influences absorption, and smaller lead particles (<180 àm) may be absorbed from the intestine more rapidly than larger ones.1
As discussed, only a small proportion of inorganic lead ingested is absorbed into the body. This is considered to account for approximately 10% of ingested lead in humans83 and may be as low as 1 to 2% in cattle and sheep.85 Studies in which animals have been fed various forms of lead have shown widely different tolerances between species. Absorbed lead normally bypasses the soft tissues and is sequestered in the bones; nutritional status also plays an important role in this process.86 Differences in response are probably attributable to interspecific differences in abilities to absorb, store, detoxify, and excrete lead. These factors appear to be largely related to diet as well as physiological and environmental factors. Age differences in susceptibility to lead poisoning have been widely studied. Although uptake and storage of lead does vary in many species with age, increased toxicity of lead to young animals is related more to an increased lead sensitivity of certain body systems during early stages of development. In some young birds increased storage of lead by juveniles in the developing bones may serve to reduce the toxic effects of a given lead exposure over those of adults. In addition, the bones of female birds exposed to lead frequently have more elevated concentrations than those of males.87,88 This is related to an increased calcium metabolism and turnover in bones of females, necessitated by eggshell production.
In a nationwide survey of lead-poisoned waterfowl, hepatic lead levels were independent of age and sex; lead-poisoned ducks tended to have higher hepatic lead levels than geese or swans, but the difference could be attributed to differences in body weight rather than kinetic differences between species.89 Differential absorption and sensitivity to lead may be genetically based as well.
Black ducks (Anas rubripes) and mallards (A. platyrhynchos) were not different in their response to dosing with lead shot, and there was no seasonal effect.90 However, there was a significant difference in vulnerability; the wild-caught birds exhibited greater mortality and weight loss, probably due to captive-related stress. Lead accumulation in bone and blood of smelter workers was varied and apparently related to the allele they carried for delta-aminolevulinate dehydratase (ALAD).91 Further analysis has linked response and accumulation to alleles not only for ALAD but also the vitamin D receptor gene and the enzyme aminolevulinic acid.92
A considerable amount of research related to lead absorption has been carried out in laboratory studies using the rat. As early as 1939 a component of apples — probably pectin — inhibited lead assimilation in growing rats.93 Researchers also found higher lead retention in growing than adult rats. Milk in the diet has been found to influence lead absorption in rats. Dietary calcium appears to be one of the most important factors influencing lead absorption and toxicity. Lead uptake, toxicity, and soft tissue storage are increased in lead-exposed animals fed low-calcium diets. This has been illustrated in a wide range of birds and mammals including waterfowl, rats, dogs, horses, and sheep.94–97 In sheep low-calcium diets adequate in other minerals fed to lambs along with 400 mg Pb/kg resulted in death within 5 weeks. With adequate dietary calcium, lambs survived for up to 10 months.98 Other dietary factors that have been shown to influence lead uptake or toxicity are phosphorus, zinc, iron, ascorbic acid, vitamin D, and protein. Iron-, calcium-, phosphorus-, zinc-, and protein-deficient diets tend to result in increased lead uptake and toxicity, and dietary supple- ments of these constituents tend to decrease lead uptake or alleviate signs of lead poisoning in
many species.8,95–99 However, the interactions between lead and other dietary constituents are very complex, and under certain circumstances, and in some species, dietary excess of many elements, including those listed above, may exacerbate lead toxicity.
In some animals there appears to be a seasonal peak in lead poisoning. In children, cattle, and dogs, lead-poisoning cases are most common in spring or summer months.97,100,101 Although this remains largely unexplained, it is thought that this might be related to increases in vitamin D levels, stimulated by increased sunlight. Vitamin D appears to be associated with intestinal lead absorption, and increased levels of dietary vitamin D tend to increase lead absorption and retention in some animals.102 The seasonal incidence of lead poisoning in some animals may also be related to other physiological factors such as dehydration102 or differential access to lead-contaminated dietary material.
When nonfood ingestion of lead occurs, similar factors will influence absorption and retention, although most animals usually rapidly egest large lead objects. However, this is not the case with waterfowl and other birds ingesting lead shot or anglers weights. Waterfowl actively ingest grit, which is retained in their muscular gizzard to help grind up and breakdown ingested material.
Small ingested lead objects may be similarly retained and ground down within the gizzard. The retention and absorption of ingested shot by waterfowl is related to the quantity of food ingested and its physical characteristics as well as its chemical characteristics, as described above. Smaller, softer foods, especially those low in fiber, generally pass more rapidly through the intestine,103 possibly increasing the expulsion rate of ingested shot and any lead particles eroded from the shot’s surface. However, an increased shot expulsion rate does not always imply decreased absorp- tion. Mourning doves (Zenaida macroura) fed a seed diet had lower shot retention rates but higher tissue lead concentrations than those on a pelleted diet, probably due to differences in lead absorption related to the chemical constituents of the diets.104 Lead absorption rates from ingested gunshot are lowest when physical characteristics of diet facilitate the rapid passage of lead through the intestine and chemical components reduce lead absorption. Large-scale avian mortality has occurred due to shot ingestion.105,106