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.

Funding: This work was supported by the Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, and the CAS 135 program (XTBG-T01) of Chinese Academy of Science, China National Research Fund (31260585) to Ken Tan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2013 Tan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

The impacts of predation cascade through an ecosystem: predators can influence prey and thus affect primary producers [1]–[3]. Predator effects on pollinators are particularly important. 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 therefore be common [6] and have strong ecosystem effects [3]. Predation can directly reduce pollinator numbers, but also exerts an important non-lethal effect, fear, which alters prey spatial distribution and foraging frequency [7]–[10]. Fear results from the anticipation or awareness of danger [11]. We use a functional definition of “fear” as prey exhibiting wariness and avoiding a predator [12].

The ecological consequences of fear can be as strong as actual predator consumption [13]. Fear is an effective pollinator deterrent, disrupting plant pollination and thereby affecting plant fitness. Crab spider presence, for example, resulted in fewer pollinator visits for shorter durations and decreased a measure of plant fitness, seed production in Leucanthemum vulgare [6]. Artificial crab spider models that could not kill insects similarly reduced insect pollinator visits to Rubus rosifolius flowers, resulting in 42% reduced seed set and 50% fruit mass decrease [14]. Fruit production of western monkshood, a bumble bee pollinated plant, significantly decreased at sites with high beewolf hornet activity [15]. In this case, 32% of attacks ended in successful predation, but, overall, studies demonstrate that predator effects are largely non-consumptive and result from fear of predators [16].

Studies that examine the effects of multiple predators upon prey behavior remain less common than single-predator studies. To understand how prey manage multi-level risk [17], we therefore need more data on how prey show vigilance [18] to multiple predators. Researchers studying pollinators have generally examined responses to a single predator species at a time [14], [19]–[24]. However, animals often face danger from multiple predator species that are differentially dangerous.

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 anti-predator avoidance. Bumble bees (Bombus ternarius) visited milkweed patches with spiders at a significantly lower rate compared to patches without spiders [20]. Honey bees (Apis mellifera) preferred safe over dangerous feeders (with a dead bee or a dead spider) and avoided revisiting sites where they experienced a predation attempt [21]. Honey bees also avoided flowers with crab spiders and flowers that had recently held spiders [22]. Dukas and Morse [19] compared pairs of milkweed patches and found that A. mellifera visited spider-infested patches less often, though not when natural spider densities were low [27]. However, it is not known how social bees will respond when presented with a naturally occurring situation of multiple predator species corresponding to different danger levels at food patches. Such information is important because understanding the size and strength of indirect effects in trophic cascades requires detailed knowledge of how prey respond to predators [28].

Bee predation studies have focused on sit-and-wait predators, like crab spiders, that wait on an inflorescence for pollinators. However, aerial predators may also be important and have a larger hunting area per predator. For example, Wilson and Holway [29] provided evidence that wasp (Vespula pensylvanica) presence elicited avoidance in Hylaeus bees. The “beewolf” wasp (Philanthus spp.) preys only on bees and its presence reduces bumble bee abundance and monkshood fruit set within a 50 km2 area around a hornet aggregation [15]. Hornets can also affect bee pollination by directly competing for nectar resources. Bumble bees avoid competing Vespula hornets on milkweed flowers [30]. Vespula pensylvanica presence reduces floral visitation by bees and decreases fruit set [31]. The effects of aerial predators like hornets upon bee foraging and pollination therefore deserves greater attention.

Finally, fear-driven systems are traditionally described in terms of fierce vertebrate carnivores, in which fierceness is measured by prey responses [8]. The bee-hunting hornets are also fierce predators and are important because they prey upon key pollinators. In Asia, hornets within the genus Vespa are major honey bee predators and can lead to colony attrition and absconding [32], [33]. The big Asian hornet, Vespa tropica, will rob honey by first killing guard honey bees until the colony absconds [32]. Seeley et al. [34] reported that V. tropica could cause an A. florea colony of approximately 6000 bees to abscond after just three hours of fighting. The hornet, V. velutina, although smaller in body size than V. tropica, is similarly damaging [26], [35], [36]. Researchers have previously studied these hornets as honey bee nest predators, but we also observed them flying over flowers hunting for foraging A. cerana. Because V. tropica is four-fold more massive than V. velutina (Fig. 1), we predicted it would present a greater threat.

The Asian honey bee species, A. cerana, evolved with these Vespa predators and therefore has special defenses: a shimmering behavior that repels hornets [26], [37] and, as a final defense, surrounding the well-armored hornet with a ball of bees that kill with their intense body heat [38]. Apis cerana is also an important native pollinator [39], [40]. We therefore chose this species to test the hypothesis that a valuable pollinating insect would exhibit differential vigilance when presented with multiple food patches simultaneously containing different predator species. Bee predators can prefer patches containing high quality food that is more attractive to prey [41], [42]. In one experiment, we therefore matched food quality to danger, testing how bees respond when given choices among patches that were higher in quality (more concentrated nectar) and also higher in danger.

We measured both colony- and individual-level responses because honey bees are superorganisms and thus foraging decisions occur at individual and colony levels [43]. Like A. mellifera, A. cerana can recruit nestmates to floral resources [44], thus potentially amplifying the effects of vigilance at the colony level. For example, A. mellifera recruit less for a nectar resource that is perceived to be dangerous when a recently dead bee is placed on the resource [45].