Abstract
Intraspecific floral colour polymorphism is a common trait of food deceptive orchids, which lure pollinators with variable, attractive signals, without providing food resources. The variable signals are thought to hinder avoidance learning of deceptive flowers by pollinators. Here, we analysed the cognitive mechanisms underlying the choice of free-flying stingless bees Scaptotrigona aff. depilis trained to visit a patch of artificial flowers that displayed the colours of Ionopsis utricularioides, a food deceptive orchid. Bees were trained in the presence of a non-rewarding colour and later tested with that colour vs. alternative colours. We simulated a discrete-polymorphism scenario with two distinct non-rewarding test colours, and a continuous-polymorphism scenario with three non-rewarding test colours aligned along a chromatic continuum. Bees learned to avoid the non-rewarding colour experienced during training. They thus preferred the novel non-rewarding colour in the discrete-polymorphic situation, and generalized their avoidance to the adjacent colour of the continuum in the continuous-polymorphism situation, favouring thereby the most distant colour. Bees also visited less flowers and abandoned faster a non-rewarding monomorphic patch than a non-rewarding polymorphic patch. Our cognitive analyses thus reveal that variable deceptive orchids disrupt avoidance learning by pollinators and exploit their generalization abilities, which make them favour distinct morphs.
Highlights
Many insects act as efficient pollinators because of their remarkable capacities to learn and memorize flower features associated with nectar and pollen reward[1]
Our experimental situation was inspired by the interaction between the neotropical deceptive orchid Ionopsis utricularioides (Sw.), which presents intraspecific floral colour variation[12], and the stingless bee Scaptotrigona aff. depilis Moure 1942 (Meliponini), which is a floral visitor of this orchid[12] and which can be trained to visit artificial feeders offering sucrose solution[13,14]
The flowers of I. utricularioides varied from white to purple to the human eye (Fig. 1b) and did not reflect in the range of ultraviolet (300–350 nm; Fig. 1c). They occupied the blue-green area of the colour hexagon (Fig. 1d). and presented a continuous floral colour polymorphism, where the more distant points in that space were separated by distances larger than 0.1 hexagon units (HU), which corresponds approximately to a discrimination level of 60% in bees[21]
Summary
Many insects act as efficient pollinators because of their remarkable capacities to learn and memorize flower features associated with nectar and pollen reward[1]. These theoretical conclusions require experimental analyses to determine how pollinators perceive and make decisions in a food-deceptive scenario presenting either continuous or discrete polymorphic signals Achieving this goal is difficult as the only way to study decision making by foraging bees under laboratory conditions ensuring proper stimulus control, including the setting of artificial polymorphic colour scenarios, consists in luring the insects with sucrose solution. We reproduced colours available in I. utricularioides and trained bees to choose a rewarded neutral grey colour vs non-rewarded orchid colours ( CS+ and CS−, respectively), all presented on artificial flowers This situation corresponds to a case of differential conditioning in which animals learn to discriminate stimuli with distinct outcomes[15,16]. We provide a cognitive laboratory analysis of the deceptive interaction between orchids and pollinators and uncover the perceptual and associative mechanisms underlying this ecological situation
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