Date Published: June 27, 2019
Publisher: Public Library of Science
Author(s): Ana M. Chicas-Mosier, Christopher W. Dinges, Jose L. Agosto-Rivera, Tugrul Giray, Devrim Oskay, Charles I. Abramson, Wolfgang Blenau.
Aluminum is increasingly globally bioavailable with acidification from industrial emissions and poor mining practices. This bioavailability increases uptake by flora, contaminating products such as fruit, pollen, and nectar. Concentrations of aluminum in fruit and pollen have been reported between 0.05 and 670mg/L in North America. This is particularly concerning for pollinators that ingest pollen and nectar. Honey bees represent a globally present species experiencing decline in Europe and North America. Region specific decline may be a result of differential toxicity of exposure between subspecies. We find that European honey bees (Apis mellifera mellifera) may have differential toxicity as compared to two allopatric Mediterranean subspecies (Apis mellifera carnica and Apis mellifera caucasica) which showed no within subspecies exposure differences. European honey bees were then used in a laboratory experiment and exposed to aluminum in their daily water supply to mimic nectar contamination at several concentrations. After approximately 3 weeks of aluminum ingestion these bees showed significantly shorter captive longevity than controls at concentrations as low as 10.4mg/L and showed a possible hormetic response in motility. We also compared European honey bees to Africanized/European hybrid bees (Apis mellifera mellifera/scutellata hybrid) in short-term free-flight experiments. Neither the European honey bee nor the hybrid showed immediate foraging deficits in flight time, color choice, or floral manipulation after aluminum exposure. We conclude that European honey bees are at the greatest risk of aluminum related decline from chronic ingestion as compared to other subspecies and offer new methods for future use in honey bee toxicology.
Pollinator stress is attributed to three primary factors: 1) habitat fragmentation, 2) chemical application and 3) introduced pathogens [1–4]. These factors can be cooperative and can create unmanageable stress and reduce population survival. For example, insecticide application may decrease immunity, allowing pathogens to more easily incapacitate pollinators [5, 6]. Stress caused by pathogens may then be exacerbated by poor foraging from contaminant exposure or environmental factors. Inefficient foraging is a documented result of neonicotinoid insecticide exposure through reduced olfactory senses and the cholinergic system [7–10]. As a result of the stress placed on pollinators, some neonicotinoids have been banned in Europe [11, 12]. Unfortunately however, virtually identical mechanisms of action and consequences of other toxicant exposure, such as from metals, are not as well studied and may have similar negative impacts on pollinators. This article seeks to determine how aluminum affects the choice-making, motility, circadian rhythmicity and lifespan of honey bee subspecies in free-flight and captive laboratory conditions.
The effects of aluminum were tested using two experimental paradigms. The first, a free-flight cap-pushing experiment, compared two subspecies of honey bee Apis mellifera mellifera (OK-M) and an Apis mellifera mellifera/ scutellata hybrid (PR-S) from Oklahoma, USA and Puerto Rico, USA, respectively (Table 1). The cap-pushing experiment investigated how floral manipulation and disorientation are affected by aluminum as well as color preference when blue and yellow flowers are available. The second experimental paradigm, the monitor system, examined how aluminum affects motor activity, circadian rhythmicity, and survival. The monitors are a laboratory-based incubator experiment and included three subspecies of honey bee, OK-M, Apis mellifera carnica (T-Car) and Apis mellifera caucasica (T-Cau, Table 1). The latter two subspecies are allopatric and indigenous to the Mediterranean and were at a common apiary in Tekirdağ, Turkey.
Aluminum does not immediately limit foraging capabilities at low doses. It does not cause immediate disorientation and may only minimally change color preference in some subspecies of honey bee. Aluminum does however drastically affect OK-M bees in lifespan, circadian adherence, and motility at the concentrations used in this study. This subspecies of honey bee occurs in two regions where population decline has been a concern; North America and Europe . The OK-M subspecies may be at severe risk as a result of acidification combined with stressors such as pathogens and food limitation and this may be cause for further investigation of aluminum toxicity [4, 30, 34].