Bees eavesdrop upon informative and persistent signal compounds in alarm pheromones

Abstract

Pollinators such as bees provide a critical ecosystem service that can be impaired by information about predation. We provide the first evidence for olfactory eavesdropping and avoidance of heterospecific alarm signals, alarm pheromones, at food sources in bees. We predicted that foragers could eavesdrop upon heterospecific alarm pheromones, and would detect and avoid conspicuous individual pheromone compounds, defined by abundance and their ability to persist. We show that Apis cerana foragers avoid the distinctive alarm pheromones of A. dorsata and A. mellifera, species that share the same floral resources and predators. We next examined responses to individual alarm pheromone compounds. Apis cerana foragers avoided isopentyl acetate (IPA), which is found in all three species and is the most abundant and volatile of the tested compounds. Interestingly, A. cerana also avoided an odor component, gamma-octanoic lactone (GOL), which is >150-fold less volatile than IPA. Chemical analyses confirmed that GOL is only present in A. dorsata, not in A. cerana. Electroantennogram (EAG) recordings revealed that A. cerana antennae are 10-fold more sensitive to GOL than to other tested compounds. Thus, the eavesdropping strategy is shaped by signal conspicuousness (abundance and commonality) and signal persistence (volatility).

Poison and alarm: The Asian hornetVespa velutinauses sting venom volatiles as alarm pheromone

“…We used the same instruments and protocol as Number of hornet responses (colony treated as unit of replication). Wang et al (2016). In brief, a custom EAD system was coupled to the HP7890B GC.…”

“…Alarm pheromones can play dual roles, by activating nest defence and serving as a warning that allows foragers to avoid dangerous sites. For example, honeybee alarm pheromone can attract guards to the nest entrance for nest defence (Boch and Shearer, 1971;Roubik, 1989) and repel foragers from foraging sites with predators (Li et al, 2014;Wang et al, 2016). In social wasps and hornets, nest guards can also release alarm pheromones to recruit nest defenders (Bruschini et al, 2008).…”

Foragers of sympatric Asian honey bee species intercept competitor signals by avoiding benzyl acetate from Apis cerana alarm pheromone

“…Theoretically, they could intercept alarm signal information 14 . As predicted, A. cerana can use olfactory eavesdropping to detect and avoid an alarm pheromone component in the sympatric Apis dorsata that A. cerana does not possess 15 .…”

“…In the context of foraging, bees are not defending their colony but rather fleeing from danger and marking a location as dangerous 26 . For example, GOL and DA are most effective at repelling A. dorsata and A. cerana foragers, even though GOL is not found in A. cerana 15 . This example of A. cerana intercepting an alarm pheromone component of another bee species illustrates the complexity of forager responses to alarm pheromones 15 .…”

“…Isopentyl acetate (IPA) is the major component of sting alarm pheromone in all honey bee species 19 . The main other previously-reported sting alarm pheromone components (>10% by mass) of each species are benzyl acetate (BA, in A. mellifera ) 20 , octyl acetate (OA, in A. mellifera , A. cerana , A. florea and A. dorsata ) 21 , ( E )-oct-2-en-1-yl acetate (OEA, in A. mellifera ) 22 , ( E )-dec-2-en-1-yl acetate (DA, in A. cerana, A. dorsata , A. laboriosa and A. florea ) 15 , 20 , 21 , 23 , ( Z )-eicos-11-en-1-ol (EH, in A. mellifera and A. cerana ) 24 , 25 , and gamma -octanoic lactone (GOL, in A. dorsata and A. laboriosa ) 26 , 27 .…”