Colony Failure Linked to Low Sperm Viability in Honey Bee (Apis mellifera) Queens and an Exploration of Potential Causative Factors

Abstract

Queen health is closely linked to colony performance in honey bees as a single queen is normally responsible for all egg laying and brood production within the colony. In the U. S. in recent years, queens have been failing at a high rate; with 50% or greater of queens replaced in colonies within 6 months when historically a queen might live one to two years. This high rate of queen failure coincides with the high mortality rates of colonies in the US, some years with >50% of colonies dying. In the current study, surveys of sperm viability in US queens were made to determine if sperm viability plays a role in queen or colony failure. Wide variation was observed in sperm viability from four sets of queens removed from colonies that beekeepers rated as in good health (n = 12; average viability = 92%), were replacing as part of normal management (n = 28; 57%), or where rated as failing (n = 18 and 19; 54% and 55%). Two additional paired set of queens showed a statistically significant difference in viability between colonies rated by the beekeeper as failing or in good health from the same apiaries. Queens removed from colonies rated in good health averaged high viability (ca. 85%) while those rated as failing or in poor health had significantly lower viability (ca. 50%). Thus low sperm viability was indicative of, or linked to, colony performance. To explore the source of low sperm viability, six commercial queen breeders were surveyed and wide variation in viability (range 60–90%) was documented between breeders. This variability could originate from the drones the queens mate with or temperature extremes that queens are exposed to during shipment. The role of shipping temperature as a possible explanation for low sperm viability was explored. We documented that during shipment queens are exposed to temperature spikes (<8 and > 40°C) and these spikes can kill 50% or more of the sperm stored in queen spermathecae in live queens. Clearly low sperm viability is linked to colony performance and laboratory and field data provide evidence that temperature extremes are a potential causative factor.

Immunosuppression in Honeybee Queens by the Neonicotinoids Thiacloprid and Clothianidin

“…Although reports of colony losses due to high rates of queen failure exist, only few studies address direct or indirect physiological effects in queens caused by pesticide exposure 2, 5, 29, 30 . Most studies focused on only three neonicotinoid insecticides, clothianidin, imidacloprid, and thiamethoxam, which are currently subject to a moratorium in the European Union 31 .…”

Assessment of ecological risks of agrochemicals requires a new framework.

“…This is the case of the lady beetle Hippodamia variegata exposed to sublethal concentrations of thiamethoxam [80]. Neonicotinoids can also negatively affect honeybee drone sperm quality [81,82] while fipronil affects drone fertility by inducing a decrease in spermatozoa quantity that is associated with an increase in spermatozoa mortality [83], so these insecticides may ultimately lead to colony failure [84].…”

Honey bee queens are vulnerable to heat-induced loss of fertility

“…Climate change is threatening biodiversity around the globe [1][2][3] , and one potential driver is through heatinduced reductions in fertility [4][5][6] . The impact of heat on fertility is far-reaching in the animal kingdom, affecting mammals [7][8][9][10][11] , birds 12 , fish 13 , nematodes 14 , and insects 4,[15][16][17][18][19][20][21] . At temperatures of 40-43 ͦ C, spermatogenesis is compromised 22 , sperm viability drops 4,18,19 , sperm are less competitive 4 , and motility is compromised 15,23,24 .…”

“…The impact of heat on fertility is far-reaching in the animal kingdom, affecting mammals [7][8][9][10][11] , birds 12 , fish 13 , nematodes 14 , and insects 4,[15][16][17][18][19][20][21] . At temperatures of 40-43 ͦ C, spermatogenesis is compromised 22 , sperm viability drops 4,18,19 , sperm are less competitive 4 , and motility is compromised 15,23,24 . Extreme weather events such as heatwaves are increasing in frequency and severity [25][26][27] , which could have widespread effects on populations via reduced reproductive output [4][5][6] .…”

“…Like other insects, individual honey bees are ectothermic, but their colonies (which are mainly composed of tens of thousands of sterile workers) are able to thermoregulate remarkably well 46 . However, female and male reproductive individuals (queens and drones, respectively) could be vulnerable to temperature extremes during mating flights or in poorly ventilated colonies, and queens are especially vulnerable during routine shipments 18 . The queen breeding industry depends on shipping live, newly mated queens across long distances to deliver them to beekeepers, and temperature stress while in transit could undermine the industry.…”