Environmental contamination has profound consequences for ecosystem processes, activities, and services, as well as human health [1,2,3]. Heavy metals infiltrate both terrestrial and aquatic ecosystems, impacting the element flow, the diversity and population of flora and fauna, and even ecosystem security [4,5,6,7]. For example, lead (Pb) moves to the soil, where it then enters the roots of crops, accumulating significant amounts of Pb within the stems, leaves, and grains [8]. The consumption of substances with elevated heavy metal concentrations by an organism might result in immune system suppression, weight loss, and potentially lethal outcomes. Mercury infiltrates aquatic habitats and builds up to significant amounts in fish [9]. Consuming fish that contain high amounts of mercury poses a significant health risk to people. Cadmium (Cd) is a common heavy metal that is mostly present in its natural form in the soil and lithosphere. Human activities have also led to the buildup of Cd in the atmosphere, water, and soil [10,11]. The root uptakes Cd from the soil and concentrates it in various plant tissues, with a particular affinity for the reproductive organs. When Cd accumulates in pollen and nectar, it poses a possible risk to the safety of pollinators, particularly bees [12,13].

There is a global decline in the richness of pollinators [14]. Evidence shows that the percentage of managed honey bee colonies decreased by 43% in the US between 2019 and 2020 [15]. Various factors influence the richness and abundance of pollinators [16]. Cadmium, a widespread contaminant, has a significant impact on pollinator life cycle, richness, and abundance [6,12,17,18]. For example, the accumulation of Cd in pollen and nectar hinders bee larvae’s normal growth and interferes with their usual transition into pupae [12,17,19]. Several studies have extensively shown the effects of Cd on different aspects of pollinating insects, such as the development, lifespan, gut microbiota, brain networks, and cognition of bumble bees and honey bees [12,13,20].

Plants that thrive in soil with low levels of cadmium only transmit a small quantity of Cd to their pollen and nectar. However, pollen contains a substantially higher amount of Cd compared to honey, because bees can partially purify nectar by removing heavy metals during honey production [21]. For example, the Cd and Pb content in honey is decreased by 75% and 73% compared to that in the nectar [22]. Bogdanov found that metal contamination levels are lower in honey compared to those in the bodies of bees [23]. Thus, rather than the honey, the level of Cd in pollen is the decisive component for the development of bees. Moreover, when exposed to low levels of soil Cd, the amount of nectar influences bees’ foraging behavior [24]. At high levels of exposure, bees are unable to effectively eliminate the substantial amounts of this poisonous chemical present in the nectar [21]. As a result, cadmium accumulates in both pollen and honey. This mutually impacts bee growth and foraging behavior. For example, Gekière found that high concentrations of Cd induce severe gut melanisation of bumble bees and reduced sucrose consumption [25]. Once the pollen and honey exceed a specific Cd threshold, larvae’s growth and pupation are hampered [12,17]. However, there is a dearth of studies regarding the specific association by which the impact on bee growth and foraging behavior fluctuates in relation to the Cd dosage of pollen or nectar. Herein, we speculate that the relationships by which soil cadmium affects bee growth and foraging behavior vary with the dose of cadmium in the soil. The soil in Sichuan has a significantly elevated Cd concentration compared to other regions in China. In Sichuan, the average background value of cadmium is 5.6 times higher than in other regions due to the parent materials, mining, and industrial activities [26]. Herein, we test the effects of low or high soil Cd concentrations on the honey bee growth and foraging behavior in Sichuan, China. Our findings shed a new light on the effects of Cd on pollinator growth and foraging behavior and the global decline of pollinators.

The level of cadmium in pollen and nectar directly affects the richness, abundance, and foraging behavior of honey bees [12,17,19]. Research indicates a substantial correlation between soil cadmium concentration and the decline in both bee populations and diversity [6,18]. Moroń et al. [6] demonstrate a direct correlation between Cd levels in pollen and the reduction in bee abundance and diversity. Increased levels of Cd-contaminated pollen can impede larval development and disrupt the normal pupation process of bees [46]. Moreover, the presence of cadmium in nectar directly influences the growth and foraging behavior of bees [13,17]. Increased Cd concentrations in nectar extend developmental duration and diminish the body size of bees [19,47]. Our findings suggested that cadmium concentrations in nectar and pollen affected the growth and development of honey bees, while the specific impacts varied based on the concentration of soil cadmium. The exposure of honey bees to low levels of soil cadmium (Cd) revealed that the Cd concentration in pollen was the principal factor influencing honey bee body mass. As cadmium concentration in pollen increases, there is a notable decline in the body mass of larvae, pupae, and worker bees. A recent study has shown that honey bees may extract heavy metal ions from nectar [21]. In settings of low soil cadmium content, we observed that honey bees efficiently eliminated around 50% of cadmium from the nectar. The presence of cadmium in honey did not influence larval growth, as honey bees can remove cadmium ions from the honey. Nonetheless, the concentration of Cd in honey was markedly elevated in soil environments exhibiting moderate to high amounts of Cd. Borsuk et al. [21] assert that honey bees possess an optimal capacity for the removal of heavy metal ions. The quantities of cadmium in honey rose in the medium and high concentration treatments, and the cadmium levels in worker bees similarly elevated. We propose that the cadmium content in nectar inversely correlates with honey bees’ ability to remove cadmium. When a particular threshold is exceeded, the ability of bees to remove cadmium decreases. Thus, in soils with moderate to high Cd concentrations, the levels of Cd in nectar and pollen had a synergistic effect on the body mass of honey bees.

The quantity and quality of nectar and pollen significantly influence the foraging behavior of bees [30,48,49,50]. Increased levels of heavy metals in nectar and pollen reduce visitor frequencies [20]. Liu et al. [24] established that 4 mg·kg⁻¹ Cd in soil resulted in a higher nectar yield and an enhanced rate of floral visits compared to the 8 mg·kg⁻¹ Cd treatment. The nectar is hypothesized to include higher levels of Cd, resulting in a reduced frequency of honey bee visits to flowers. Xun et al. [13] found that the presence of heavy metals, such as copper, zinc, nickel, and lead, in nectar reduced the feeding duration of pollinators on specific flowers. The results demonstrate that the increasing concentration of soil cadmium is associated with a notable decline in the incidence of bees foraging on flowers. In our study, the factors affecting the frequency of honey bee visits to flowers fluctuated based on the Cd concentration in the soil. Low soil cadmium concentrations, on one hand, led to a single flower producing more nectar [24]. In contrast, honey bees may remove Cd [21], hence reducing the Cd concentration in nectar. The nectar quantity in each flower affected the frequency of honey bee visits when the soil exhibited low cadmium levels. As the plant grows in situations with moderate to elevated soil cadmium concentrations, the nectar volume per flower decreases. The concentration of cadmium in pollen and nectar increased concurrently. Nonetheless, honey bees often choose flowers with lower cadmium contents in their nectar and pollen [24]. Consequently, honey bees are compelled to reduce their floral visits and intentionally avoid collecting nectar with high cadmium contents.

The content of cadmium in pollen and nectar is correlated with its levels in various plant tissues [51,52]. The plant’s exposure to low cadmium (Cd) concentrations shows a positive correlation between Cd levels in pollen and those in the roots, stems, leaves, and flowers. The quantity of Cd in pollen, nectar, and honey exhibits a positive correlation with the Cd concentration in the roots, stems, leaves, and flowers of plants subjected to medium and high levels of Cd. A significant positive correlation was identified between Cd concentrations in roots, stems, leaves, and flowers and the Cd concentrations in the soil, regardless of treatment concentration. These findings indicate that the soil Cd permeates the aerial parts of plants through their roots, potentially disseminating to the stems and leaves, finally affecting the reproductive structures, including flowers. As a result, Cd accumulates in the nectar and pollen. The content of cadmium in pollen much exceeds that in nectar, suggesting that bees may remove Cd²⁺ from nectar [21].

The plasticity of floral traits influences pollinators’ foraging behavior and their selection of food resources [48]. Research indicates that soil heavy metals might alter the dimensions and abundance of flowers, thereby affecting the foraging behavior of pollinators [20]. Yet, we have not conducted any research on floral morphology at different Cd concentrations. Thus, it is unclear whether variations in flower size, plant height, and other characteristics influence the frequency of honey bee visits to the flowers. Moreover, our trials indicated a notable occurrence of dead honey bees around beehives located in environments with moderate to high concentration levels. The number of colonies was observed during the study to decrease by approximately one-third (observed by J. Liu). Therefore, more real-world evidence is needed to find out exactly how changes in cadmium content affect the death rate of honey bees. This project exclusively examined the mechanism by which different amounts of cadmium affect bee body mass and foraging behavior through field studies. However, it does not prove, through targeted feeding studies, how changing the amount of cadmium in nectar and pollen affects honey bees’ health, longevity, memory, and ability to think and reason, as well as their gut microbiome and their ability to reproduce and maintain a healthy population. Future endeavors necessitate increased empirical validation.