44.6.1 Diet and Lead Shot Ingestion in Waterfowl
Jordan205 concluded after controlled experiments with mallards, lesser scaup (Aytha affinis), and Canada geese (Branta canadensis) that diet was the most important variable modifying the toxic effects of ingested lead-shot pellets. A corn diet resulted in 50% mortality and 34% net weight loss by 25 days, following a dose of four No. 6 lead shot (Table 44.3). However, commercial duck food in the form of pellets was the most effective in lessening these toxic effects, followed by aquatic plants and grains. Corn is deficient in essential minerals, including calcium, several vitamins, and low in protein, hence enhancing the effects of lead. However, the author concluded that these nutritional factors alone were not entirely responsible. The size and hardness of the diet was also a factor. The physical form of the diet appeared to determine the rate of food intake of captive waterfowl, where commercial duck pellets were taken in greatest amounts, followed by small grains and wild seeds, with rice more so than mixed grains, and corn the least. The smaller softer feeds, including duck pellets, which essentially became mash after ingestion, were more easily reduced to a softer form in the gizzard and hence passed along more readily to the intestine, hastening the rate of elimination of lead. Thus, both nutritional benefits and movement of a greater volume of food are likely to facilitate the elimination of lead removed from the surface of ingested lead shot.
Others have also reported greater toxicity of lead-shot ingestion in conjunction with a corn diet.206, 207
44.6.2 Calcium and Lead Shot Ingestion
Carlson and Nielsen208 studied the role of dietary calcium on lead-shot poisoning in adult mallards. In this study, there were three dietary groups consisting of: Group I, fed pelleted calcium- supplemented corn (1.2% Ca); group II, fed a pelleted commercial duck ration with 1.2% Ca; and Group III, fed cracked corn (0.03% Ca). Ten ducks from each group were given four No. 4 lead shot via an esophageal tube, and five ducks from each group were kept as pair-fed controls. Anorexia and weight loss were most severe in the lead-shot-dosed Group III ducks. Group III had a maximum reduction in food consumption of 87%, followed by a slight improvement in appetite but a loss of 35% of the initial body weight. Group I treated ducks had a reduction in food consumption of 64%
that eventually returned to the quantities consumed at the start of the experiment; Group I ducks lost 18% of their initial body weight. Group II treated ducks maintained healthy appetites during the experiment and had a weight gain of 2% of their initial body weight. The number of ducks that became moribund and were euthanized differed significantly among the treated groups, with 100%
of Group III, 50% of Group I, and 0% of Group II treated ducks becoming moribund.
© 2003 by CRC Press LLC
Table 44.3 Interactive Effects of Nutritional Factors and Other Elements on Lead Toxicity in Birds
Species, Age
Form of Pb,
Dose or Dietary Concentration Interactive Factor
Observation
Period Effects Ref.
Mallard, Lesser scaup Canada goose
(adults)
Four No. 6 lead shot pellets Commercial feed vs. corn and other diets
25 days post dosing
Lead-shot ingestion most toxic with corn diet and least toxic with softer diets with respect to mortality and weight loss
205–207
Mallard, adult Four No. 4 lead shot pellets Dietary calcium supplementation
9 weeks Calcium supplementation of a corn diet decreased lead- related mortality by one half and decreased weight loss as well as histopathological lesions
208
Mallard, adult Lead contaminated mining sediment (1000 ppm Pb in diet)
Ground corn diet vs.
commercial diet
15 weeks Ground corn diet containing lead sediment resulted in 80% mortality, greatest weight loss, lowest hemoglobin concentration, and threefold greater hepatic lead accumulation than with commercial diet containing lead sediment
209
Mallard, ducklings Lead contaminated mining sediment (830 ppm Pb in diet)
Two thirds ground corn/one third commercial diet mixture vs. commercial diet
6 weeks Ground corn diet mixture containing lead sediment resulted in highest blood lead concentration, reduced growth, most oxidative stress, and increased prevalence of acid-fast inclusion bodies in the kidney compared to commercial diet containing lead sediment
210–212
Japanese quail, young adults
Lead acetate in drinking water at
100 or 400 àg/mL Poultry feed vs. ground corn
7 days Corn diet resulted in lead-related mortality, greatest weight loss and suppressed antibody-mediated immunity
214
Zebra finch 10 àg/mL of lead as lead acetate and of cadmium as cadmium chloride in drinking water
0.3 vs. 3% calcium 51 days Low dietary calcium enhanced hepatic and renal accumulation of lead (~400%) and cadmium (~200%), increased metallothionein production, and inhibited ALAD the most compared to controls
215
Ringed turtle dove 50 ppm of lead as lead acetate, 20 ppm cadmium as cadmium chloride, and 1500 ppm aluminum as aluminum sulfate
0.4 vs. 2% calcium 6 months Low dietary calcium enhanced the accumulation of lead and cadmium but not aluminum, increased
metallothionein production, and inhibited ALAD the most compared to controls
215
All three groups of treated ducks had increased protoporphyrin IX concentrations compared with controls. Groups I and III lead-treated ducks had significant reductions in erythrocyte counts, PCV, hemoglobin concentrations, and mean corpuscular hemoglobin concentrations as compared with controls. Group II had reduced hemoglobin concentration and mean corpuscular hemoglobin concentration compared with controls. However, none of the above changes differed statistically among the three dietary groups of lead-poisoned ducks. Gross pathologic lesions of treated ducks (pectoral muscle atrophy and green discoloration of gizzard mucosa) were most pronounced in Group III, followed by Group I and Group II, in that order. Histopathologic lesions consisting of neuropile vacuolization, intranuclear inclusion bodies, neuronal degeneration, and myocardial and pectoral muscle degeneration, necrosis, and atrophy occurred most frequently in the Group III treated ducks, less in the Group I treated ducks, and least in the Group II treated ducks. These findings suggested that the addition of calcium to the corn diet had an ameliorating effect, but other nutrients found in the Group II commercial duck diet were also important in mollifying lead absorption and metabolism in mallard ducks.
44.6.3 Diet and Lead-Contaminated Mining Sediment in Waterfowl
A series of experiments was conducted to measure the toxicity of lead-contaminated mining sediment from the Coeur d’Alene River basin (CDARB) in Idaho to waterfowl, including mallards, Canada geese, and mute swans (Cygnus olor), under optimal and less-than-optimal nutritional conditions.
44.6.3.1 Adult Mallards
In adult mallards, mortality of 80% occurred from lead poisoning within 15 weeks when fed a less than optimal diet of ground corn containing 24% CDARB sediment (with 3954 àg/g lead in this sample of sediment), but none died when 24% CDARB sediment was mixed into a nutritionally balanced commercial duck diet.209 Birds fed the corn diet containing 24% CDARB sediment lost weight. Mallards fed 24% CDARB sediment in the commercial diet and corn diet had elevated levels of protoporphyrin (424 and 689 àg/dl) compared to controls fed the commercial diet and corn diet (45 and 25 àg/dl). Four of five mallards fed 24% CDARB sediment in a commercial diet and all five fed the contaminated sediment in a corn diet had renal intranuclear inclusion bodies.
Lead accumulation was higher in the livers of mallards fed 24% lead-contaminated sediment in the corn diet (38 àg/g) than in the commercial diet (13 àg/g). These laboratory findings with mallards demonstrated that ingestion of realistic amounts of sediment from the Coeur d’Alene River Basin caused lead poisoning in waterfowl, as had been reported in the field, and a less-than- optimal diet such as corn could severely intensify many aspects of these effects.
44.6.3.2 Duckling Growth and Survival
Other studies were conducted to assess the effects of the same sediment on posthatching development of mallard ducklings for 6 weeks.210–212 Day-old ducklings received untreated control diet, clean-sediment-supplemented (24%) control diet, or CDARB-sediment-supplemented (3449 àg/g lead) diets at 12% or 24%. The 12% CDARB diet resulted in a blood lead concentration of 1.4 ppm (wet weight) with over 90% depression of red blood cell ALAD activity and over a threefold elevation of free erythrocyte protoporphyrin concentration. The 24% CDARB diet resulted in blood lead of 2.6 ppm with over sixfold elevation of protoporphyrin. In this group, the liver lead concentration was 7.9 ppm (wet weight), and there was a 40% increase in hepatic reduced glu- tathione concentration. The kidney lead concentration in this group was 8.0 ppm and acid-fast inclusion bodies were present in the kidneys of four of nine ducklings. When ducklings were on a less-than-optimal diet (two thirds corn and one third standard diet), CDARB sediment was more
toxic; blood lead levels were 1.7-fold higher, body growth and liver biochemistry (TBARS) were more affected, and the prevalence of acid-fast inclusion bodies increased.
In addition, significant effects on the brain were seen due to lead accumulation and included oxidative stress, altered metabolites, and decreased brain weights.211,212 Significant increases in brain-reduced glutathione (GSH), calcium, and triglyceride concentrations occurred, with signifi- cant decreases in brain protein, ATP, and brain weights. Nutrient level of the diets significantly affected brain GSH, triglyceride, inorganic phosphorus, and protein concentrations, acetylcholinest- erase activity, and brain and body weights. Nutrient levels marginally affected lead accumulation in the brain. The incidence and duration of ten behaviors was recorded (resting, standing, moving, drinking, dabbling, feeding, pecking, preening, bathing, and swimming). Contaminated sediment significantly affected the proportion of time spent swimming yet did not significantly affect any of the other recorded behaviors. There were also signs of disruption of balance and mobility.
Nutrient level affected the amount of time spent in water-related behaviors.
44.6.3.3 Mute Swans
In another study with captive mute swans, CDARB sediments were combined with either a commercial avian maintenance diet or a less optimal diet of ground rice and fed to captive mute swans for 6 weeks.213 Experimental treatments consisted of maintenance or rice diets containing 0, 12 (no rice group), or 24% lead-contaminated (3950 àg/g lead) sediment or 24% uncontaminated (9.7 àg/g lead) sediment. Swans fed the less optimal rice diet containing 24% lead-contaminated sediment were the most severely affected, experiencing a 24% decrease in mean body weight, including three birds that became emaciated. All birds in this treatment group had significant reduc- tions in hematocrit and hemoglobin concentrations, nephrosis, and abnormally dark, viscous bile.
This group also had the greatest mean concentrations of lead in blood (3.2 àg/g), brain (2.2 àg/g), and liver (8.5 àg/g). These birds had significant increases in mean plasma ALT, cholesterol, and uric acid concentrations and decreased plasma triglyceride concentrations. This study revealed that mute swans consuming environmentally relevant concentrations of CDARB sediment developed severe sublethal lead poisoning and that toxic effects were more pronounced when the birds were fed lead- contaminated sediment combined with rice, which closely resembles the diet of swans in the wild.
44.6.4 Diet and Acute Lead Exposure on Immunity of Quail
Grasman and Scanlon214 investigated the interacting effects of acute lead exposure and different diets on antibody and T-cell-mediated immunity in 9-week-old male Japanese quail. The treatments were: (1) a positive control group fed 20 àg/g corticosterone, (2) a negative control group given no lead or corticosterone, (3) a low-lead group, and (4) a high-lead group. The low- and high-lead groups received 100 and 400 àg/mL lead as lead acetate in drinking water for 7 days. The two diets were poultry feed and ground corn. Control quail fed corn lost 13–14% of initial body mass, but lead-dosed quail fed corn lost 23–24%. All quail fed poultry feed gained body mass. On the corn diet, three high-lead and one low-lead quail died of lead poisoning. Corn increased the percentage of heterophils in white blood cells and decreased lymphocytes and monocytes. There was marginal evidence that lead increased the heterophil/lymphocyte ratio in corn-fed quail. Corticosterone sup- pressed this response more than lead. In corn-fed quail, lead suppressed the primary total antibody response to immunization with chukar partridge (Alectoris graeca) erythrocytes. However, lead suppressed antibody-mediated immunity only at dosages that also caused clinical lead poisoning.
44.6.5 Interactive Effects of Calcium on Lead, Cadmium, and Aluminum in Finches and Doves
Scheuhammer215 examined the influence of low dietary calcium on the accumulation and effects of dietary lead, cadmium, and aluminum in zebra finches (Taeniopygia guttata) and ring doves
(Streptopelia risoria). In zebra finches fed a diet containing low Ca (0.3%), the hepatic and renal accumulation of lead was enhanced approximately 400% and of cadmium about 150–200%, compared to birds fed a 3.0% Ca diet. Low dietary calcium also caused bones of female finches to lose an average of about 60% of their normal calcium content. Loss of bone-calcium was also observed in male finches but was less than in females. In reproductively active ring doves, low (0.4%) dietary calcium enhanced the accumulation of lead and cadmium but not of aluminum, compared with accumulation in doves consuming a 2.0% Ca diet. Enhanced accumulation of lead and cadmium was accompanied by an increased synthesis of the metal-binding protein metallothio- nein and by a greater inhibition of delta-aminolevulinic acid dehydratase activity. These results indicated that under conditions of reduced dietary calcium availability, such as can occur in acid- impacted environments, wild birds risk increased uptake of certain toxic metals more rapidly.