Flowers with poricidal anthers and their complex interaction networks—Disentangling legitimate pollinators and illegitimate visitors

Abstract

In flowers with poricidal anthers, pollen is not freely accessible and legitimate access is restricted to bees capable of vibrating the anthers. Despite the protection of pollen provided by poricidal anthers, numerous illegitimate, non‐buzz‐pollinating flower visitors rob pollen. We aimed to quantify the influence of functional groups of floral visitors and illegitimate interactions on the network structure to disentangle the flower visitor network into its mutualistic and antagonistic components. We delimited three functional groups of bees based on their pollen collection behaviour in poricidal flowers: large bees that vibrate entire flowers in a single buzzing position (flower buzzing), bees vibrating single anthers in different positions (anther buzzing) and non‐vibrating flower‐damaging or gleaning bees (non‐buzzing). Moreover, we characterized legitimate and illegitimate interactions of co‐occurring and co‐flowering plants and their flower visitors based on the stigma contact during a visit. Since we independently assessed the type of interaction with bee–plant species combinations, we were able to include the behavioural variations of each bee species across different flowers. The networks were modular, with stronger interactions within subsets of species than among the subsets. All modules included a combination of flower‐, anther‐ and non‐buzzing bees, and mutualistic and antagonistic networks were intermingled. Seven bee species shifted their roles across plant species. Specialization in the subset of interactions with pollinators was higher than the overall visitation network. Flower‐buzzing bees were more specialized than anther‐buzzing and non‐buzzing bees, which used virtually all poricidal flowers similarly. Although plants with poricidal anthers shared a specialized mechanism of pollen release, their pollinators were highly dissimilar and formed compartments of interacting species. The interaction‐level approach taken in our study confers a high specificity to the pollinator network, leading to a more complex and realistic picture of mutualistic webs versus its embedded florivory, which are otherwise confounded in pooled networks across flower visitors. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13204/suppinfo is available for this article.

Buzz pollination: studying bee vibrations on flowers

“…Despite buzz pollination being known for more than a 100 yr (Teppner, ), we are still at the early stages of understanding how floral and bee characteristics, including their biomechanical properties as well as the behaviour of bees, influence the release and collection of pollen, and ultimately plant and pollinator fitness (De Luca & Vallejo‐Marín, ). Recently, there has been a surge of interest in the study of buzz pollination, from documenting the macroevolution of buzz‐pollinated floral morphologies (Dellinger et al ., ) to characterising buzz pollination ecology and behaviour in both field (Corbet & Huang, ; Switzer & Combes, ; Mesquita‐Neto et al ., ) and laboratory settings (Russell et al ., ; Whitehorn et al ., ; Arroyo‐Correa et al ., ). More generally, buzz pollination provides the opportunity to investigate basic evolutionary questions including the origin and demise of complex floral adaptations (Dellinger et al ., ), the convergent evolution of flower form and function across disparate plant families (De Luca & Vallejo‐Marín, ), evolutionary biomechanics, the evolutionary ecology of pollen rewards (Larson & Barrett, ), the balance between antagonistic and mutualistic interactions between plants and pollinators (Mesquita‐Neto et al ., ), as well as to address fundamental questions on learning and cognition of complex motor routines in invertebrates (Russell et al ., ).…”

Bee and floral traits affect the characteristics of the vibrations experienced by flowers during buzz-pollination

“…Our study focused on bumblebees (Bombus spp. Latreille), which are well known for their ability to buzz pollinate and are important buzz pollinators in both temperate and tropical regions (De Luca et al, 2014;Mesquita-Neto et al, 2018;Rosi-Denadai et al, 2018). There are approximately 250 species of bumblebees (Bombus: Bombini) worldwide, comprising bees of medium to very large size (9-22 mm long) (Michener, 2000).…”

Nectar Secretion of Floral Buds of Tococa guianensis Mediates Interactions With Generalist Ants That Reduce Florivory

“…The myrmecophytic ant-domatia interaction of Tococa guianensis is a well-known example of obligatory and specialised mutualism (Davidson and Mckey, 1993) because the plants provide all the food needs of resident ants, and the ants protect the plant against herbivore attack (Davidson and Mckey, 1993;Heil et al, 1998). However, during a previous study on pollination and pollinators (Mesquita-Neto et al, 2018), we noted that flower buds of T. guianensis exude a sugary solution that attracts ants. The flowers of T. guianensis are visited exclusively by pollencollecting bees (Ranieri et al, 2013;Mesquita-Neto et al, 2018).…”