Xenobiotic Effects on Intestinal Stem Cell Proliferation in Adult Honey Bee (Apis mellifera L) Workers

Abstract

The causes of the current global decline in honey bee health are unknown. One major group of hypotheses invokes the pesticides and other xenobiotics to which this important pollinator species is often exposed. Most studies have focused on mortality or behavioral deficiencies in exposed honey bees while neglecting other biological functions and target organs. The midgut epithelium of honey bees presents an important interface between the insect and its environment. It is maintained by proliferation of intestinal stem cells throughout the adult life of honey bees. We used caged honey bees to test multiple xenobiotics for effects on the replicative activity of the intestinal stem cells under laboratory conditions. Most of the tested compounds did not alter the replicative activity of intestinal stem cells. However, colchicine, methoxyfenozide, tetracycline, and a combination of coumaphos and tau-fluvalinate significantly affected proliferation rate. All substances except methoxyfenozide decreased proliferation rate. Thus, the results indicate that some xenobiotics frequently used in apiculture and known to accumulate in honey bee hives may have hitherto unknown physiological effects. The nutritional status and the susceptibility to pathogens of honey bees could be compromised by the impacts of xenobiotics on the maintenance of the midgut epithelium. This study contributes to a growing body of evidence that more comprehensive testing of xenobiotics may be required before novel or existing compounds can be considered safe for honey bees and other non-target species.

Field-relevant doses of the systemic insecticide fipronil and fungicide pyraclostrobin impair mandibular and hypopharyngeal glands in nurse honeybees (Apis mellifera)

“…Given that the bees were provided with a generally favourable environment with sufficient food resources, we hypothesize that pesticides reduced nutrient digestion and absorption in nurses, contributing to improper glandular development. Indeed, such effects have been reported in insects 27 , 28 with studies demonstrating that exposure to pesticides affect the honeybee midgut 23 – 25 , including some that demonstrate that fipronil induces death of digestive midgut epithelial cells 26 . Further studies are necessary to explore the connection between nutrition and pesticides exposure and the glandular development of bees in greater detail.…”

Honey Bee Workers That Are Pollen Stressed as Larvae Become Poor Foragers and Waggle Dancers as Adults

“…High levels of pesticides in brood comb during larval development reduce adult longevity [ 105 ], which would likely be compounded by larval pollen stress because pesticides are more toxic to protein-deficient workers [ 106 ]. Furthermore, pesticide exposure of cells in the midgut, the site of nutrient adsorption, increases cell death in both adult and larval workers [ 107 , 108 ], but the effects are especially pronounced for larvae. Susceptibility to economically damaging brood pathogens is also worsened when larvae are undernourished [ 72 , 109 , 110 ].…”

“…Finally, adults infected with the gut parasite Nosema exhibit many of the same symptoms that we generated with larval pollen limitation alone (reduced longevity, early onset of foraging; [ 111 , 112 ]), so these two stressors may act synergistically, even though exposure occurs during different stages of life. Unfortunately, the symptoms of larval pollen stress reported here mimic the negative effects on workers of these environmental stressors that also impair workers’ access to nutrients [ 107 , 108 , 113 – 115 ]. Together, multiple stressors may coalesce into a perfect storm of conditions that make it difficult for workers to acquire the nourishment that they need to function as efficient foragers and dancers.…”

Understanding the Effects of Sublethal Pesticide Exposure on Honey Bees: A Role for Probiotics as Mediators of Environmental Stress

“…Systemic infections in honey bees could be exacerbated by acaricide, neonicotinoid, or fungicide exposure, which reduces intestinal stem cell proliferation (Forkpah et al, 2014) and increases midgut apoptosis (Gregorc et al, 2018;Carneiro et al, 2019), potentially weakening the gut barrier. Hemocytes also function as phagocytic cells in the honey bee hemolymph; however exposure to neonicotinoids reduces hemocytes phagocytic activity (Walderdorff et al, 2018) and hemolymph antimicrobial activity (Brandt et al, 2016).…”