Honest signals to maintain a long-lasting relationship: floral colour change prevents plant-level avoidance by experienced pollinators

Abstract

Honest signals prevail when those signals manipulate receivers to benefit the senders more than deceptive signals do. Floral colour change (FCC), reported in hundreds of species, is a well-known example of honest signalling in plant–pollinator interactions. It occurs in fully turgid flowers, and usually correlates with a cessation of reward production in individual flowers. This trait has been considered a plant strategy that enhances distant pollinator attraction by extended displays, while minimizing visits to non-reproductive flowers by honest colour signals. Here, we propose an additional, overlooked benefit of FCC, which emerges when we consider the spatial learning ability of pollinators to avoid unprofitable plants. If a plant retains rewardless flowers without FCC, it is difficult for pollinators to visually locate the rewarding flowers. Although the enhanced display initially attracts more pollinators, its low profitability for foraging may cause plant-level avoidance by them. The avoidance resulting from rewardless flower retention may be prevented by FCC because it helps pollinators to find rewarding flowers. To test this hypothesis, we observed the behavioural changes of bumblebees foraging in an array of artificial plants. We found that rewardless flowers without FCC could initially attract bees by increasing the plant's display size, but their lack of reward resulted in plant-level avoidance by those bees with spatial memories. The FCC in rewardless flowers, in contrast, encouraged bees to return by helping them to find rewards on plants. Consequently, honest plants with FCC received more visits than those dishonest plants that did not display colour change. Floral colour change thus can prevent plant-level avoidance by pollinators that use spatial memory when choosing plants. The spatial learning ability of pollinators may, therefore, be one of the keys to understanding why both colour-changing and non-colour-changing plant species occur among angiosperms. A lay summary is available for this article.