Abstract
Fear can have strong ecosystem effects by giving predators a role disproportionate to their actual kill rates. In bees, fear is shown through foragers avoiding dangerous food sites, thereby reducing the fitness of pollinated plants. However, it remains unclear how fear affects pollinators in a complex natural scenario involving multiple predator species and different patch qualities. We studied hornets, Vespa velutina (smaller) and V. tropica (bigger) preying upon the Asian honey bee, Apis cerana in China. Hornets hunted bees on flowers and were attacked by bee colonies. Bees treated the bigger hornet species (which is 4 fold more massive) as more dangerous. It received 4.5 fold more attackers than the smaller hornet species. We tested bee responses to a three-feeder array with different hornet species and varying resource qualities. When all feeders offered 30% sucrose solution (w/w), colony foraging allocation, individual visits, and individual patch residence times were reduced according to the degree of danger. Predator presence reduced foraging visits by 55–79% and residence times by 17–33%. When feeders offered different reward levels (15%, 30%, or 45% sucrose), colony and individual foraging favored higher sugar concentrations. However, when balancing food quality against multiple threats (sweeter food corresponding to higher danger), colonies exhibited greater fear than individuals. Colonies decreased foraging at low and high danger patches. Individuals exhibited less fear and only decreased visits to the high danger patch. Contrasting individual with emergent colony-level effects of fear can thus illuminate how predators shape pollination by social bees.
Highlights
The impacts of predation cascade through an ecosystem: predators can influence prey and affect primary producers [1,2,3]
We focused on bees because they are important pollinators in a wide variety of ecosystems [25], influence plant fitness [6,14,15], are prey for multiple predators [15,22,26], and exhibit antipredator avoidance
The 4 fold more massive hornet species, V. tropica, posed a threat that elicited a 4.6 fold stronger defensive response from colonies. Hunting at flowers Both hornet species attempted to attack A. cerana foraging on natural flowers (Fig. 1B)
Summary
The impacts of predation cascade through an ecosystem: predators can influence prey and affect primary producers [1,2,3]. Over 90% of flowering plant species in terrestrial ecosystems use animal pollinators to assist their reproduction [4], and 67% of flowering plants use insect pollinators [5]. Indirect top-down effects, mediated by predation of pollinators may be common [6] and have strong ecosystem effects [3]. Predation can directly reduce pollinator numbers, and exerts an important non-lethal effect, fear, which alters prey spatial distribution and foraging frequency [7,8,9,10]. We use a functional definition of ‘‘fear’’ as prey exhibiting wariness and avoiding a predator [12]
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