Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences

Abstract

Predators of pollinators can influence pollination services and plant fitness via both consumptive (reducing pollinator density) and non-consumptive (altering pollinator behaviour) effects. However, a better knowledge of the mechanisms underlying behaviourally mediated indirect effects of predators is necessary to properly understand their role in community dynamics. We used the tripartite relationship between bumblebees, predatory crab spiders and flowers to ask whether behaviourally mediated effects are localized to flowers harbouring predators, or whether bees extend their avoidance to entire plant species. In a tightly controlled laboratory environment, bumblebees (Bombus terrestris) were exposed to a random mixture of equally rewarding yellow and white artificial flowers, but foraging on yellow flowers was very risky: bees had a 25 per cent chance of receiving a simulated predation attempt by 'robotic' crab spiders. As bees learnt to avoid 'dangerous' flowers, their foraging preferences changed and they began to visit fewer yellow flowers than expected by chance. Bees avoided spider-free yellow flowers as well as dangerous yellow flowers when spiders were more difficult to detect (the colour of yellow spiders was indistinguishable from that of yellow flowers). Therefore, this interaction between bee learning and predator crypsis could lead flower species harbouring cryptic predators to suffer from reduced reproductive success.

Honey bees selectively avoid difficult choices

“…Previously it has been shown that bees responded to variation in task difficulty or task risk by slowing down to improve accuracy (18,26), and in an ethological setting bees responded to a cryptic predation risk by shifting their foraging strategy, perhaps akin to opting out of difficult discriminations in our assay (27). These findings raise the question of how bees are doing this.…”

Rules and mechanisms of punishment learning in honey bees: the aversive conditioning of the sting extension response

“…Their behavioral responses to these disturbances were then measured. For instance, free-flying bees foraging for sucrose solution learned to avoid flower patches infested with real or robotic crab spiders (Dukas, 2001;Dukas and Morse, 2003;Ings and Chittka, 2008;Ings and Chittka, 2009), or artificial flowers when penalized either with quinine (Chittka et al, 2003;Avarguès-Weber et al, 2010) or a puff of compressed air (Gould, 1986). Aversive treatments given in a context in which a sucrose reward is also delivered induce an increase in choice accuracy in difficult perceptual discriminations (Chittka et al, 2003;Ings and Chittka, 2008;Avarguès-Weber et al, 2010).…”

Net neutral effects of a generalist vertebrate predator on seed production result from simultaneous suppression of plant antagonists and mutualists

“…In particular, a single predator species may simultaneously suppress both herbivores and pollinators. For example, crab spiders can capture various flower visiting insects, including flower herbivores such as beetles and moths, as well as pollinators such as honeybees and even bumblebees (Dukas & Morse 2003;Suttle 2003;Dukas 2005;Robertson & Maguire 2005;Ings & Chittka 2009), and many birds and reptiles known as predators of phytophagous insects also consume insect pollinators (Suttle 2003;Muñoz & Arroyo 2004;Meehan et al 2005). These examples imply that a single generalist predator species may have contrasting effects on plant fitness (Romero & Koricheva 2011).…”