Acute sublethal exposure to toxic heavy metals alters honey bee (Apis mellifera) feeding behavior

Overview

Burden and colleagues tested whether worker honey bees detected, rejected, or changed sucrose responsiveness after acute exposure to cadmium-, copper-, and lead-contaminated sucrose. This is in-scope a4 toxicology and animal-feeding exposure evidence for metals in pollinator food resources, not honey occurrence data.

Key numbers

The paper tested cadmium chloride and lead chloride at 0.001 mg/L, 0.01 mg/L, 0.1 mg/L, 1 mg/L, and 10 mg/L in 1 M sucrose. Copper chloride was tested at 0.002 mg/L, 0.02 mg/L, 0.2 mg/L, 2 mg/L, and 20 mg/L in 1 M sucrose. The authors state these concentrations were comparable to or lower than concentrations found in contaminated environments and measured in floral parts of plants grown in contaminated soils.

Assay sample sizes were:

For cadmium, antennal stimulation showed no difference between sucrose and sucrose plus cadmium for any tested concentration (SOLUTION: chi2 = 0.384, p = 0.535; CONCENTRATION: chi2 = 15.975, p = 0.003). Proboscis stimulation also showed no significant concentration effect on consumption of sucrose and sucrose plus cadmium (CONCENTRATION: chi2 = 2.033, p = 0.730; SOLUTION: chi2 = 2.315, p = 0.128), although the authors describe a non-significant reduction at 1 mg/L and 10 mg/L.

For copper, antennal stimulation showed significant rejection of sucrose plus copper at every tested concentration. The paper reports pairwise p < 0.001 for 0.002 mg/L, 0.02 mg/L, 0.2 mg/L, 2 mg/L, and 20 mg/L compared with uncontaminated sucrose. Proboscis stimulation did not show an effect of copper on contaminated-sucrose consumption (CONCENTRATION: chi2 = 2.003, p = 0.730; SOLUTION: chi2 = 2.315, p = 0.128).

For lead, antennal stimulation showed a significant concentration effect and solution-by-concentration interaction (CONCENTRATION: chi2 = 51.733, p < 0.001; SOLUTION: chi2 = 4.915, p = 0.027; CONCENTRATION x SOLUTION: chi2 = 16.011, p = 0.003). At 0.001 mg/L, the percentage of bees exhibiting proboscis extension reflex to lead-contaminated sucrose was lower than to uncontaminated sucrose (p = 0.016), while 0.01 mg/L, 0.1 mg/L, 1 mg/L, and 10 mg/L did not differ from sucrose-only trials (all p = 1.000).

For lead proboscis stimulation, concentration and solution both affected consumption (CONCENTRATION: chi2 = 10.169, p = 0.038; SOLUTION: chi2 = 32.415, p < 0.001). Consumption of lead-contaminated sucrose was lower than uncontaminated sucrose at 0.001 mg/L (p < 0.001), 0.01 mg/L (p = 0.019), 0.1 mg/L (p < 0.001), and 1 mg/L (p < 0.001), but did not differ at 10 mg/L (p = 1.000).

In the sucrose-response-threshold assay, cadmium pretreatment did not significantly change sucrose discrimination (CONCENTRATION: chi2 = 7.367, p = 0.195). Copper pretreatment also did not significantly change sucrose responsiveness (CONCENTRATION: chi2 = 5.405, p = 0.368). Lead pretreatment produced a significant concentration-by-sucrose interaction (CONCENTRATION x SUCROSE%: chi2 = 43.731, p = 0.012); bees pretreated with 0.01 mg/L and 1 mg/L lead showed higher responsiveness at 1% sucrose (p = 0.041 and p = 0.032, respectively).

The paper cites major agricultural-region soil concentration ranges in the United States as cadmium < 0.01-2 mg/kg, copper < 0.06-495 mg/kg, and lead < 1.0-135 mg/kg.

Methods (brief)

The study collected pollen-forager worker honey bees at colony entrances, anesthetized them in an ice-water bath, restrained them in harnesses, fed them 1 M sucrose, and held them about 24 h before assays. Antennal assays recorded proboscis extension reflex after stimulation with water, sucrose, water, and sucrose plus metal, repeated across increasing metal concentrations. Proboscis assays recorded whether bees consumed a 0.6 microliter droplet after antennal stimulation. Sucrose-response-threshold assays fed bees 20 microliters of sucrose or sucrose plus metal 2 h before testing response to increasing sucrose concentrations from 0.1% to 30%. Analyses used logistic and multinomial logistic generalized estimating equations in IBM SPSS version 23.

Related evidence

• Cadmium
• Copper
• Lead

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