Catching the thief: Nectar robbing behaviour by bumblebees on naturalised Fuchsia magellanica in Ireland

Fuchsia magellanica (Ongaraceae) is a plant with a traditionally ornithopholous pollination system, pollinated primarily by hummingbirds in its native range. As a naturalised alien plant in Ireland, F. magellanica is visited largely by bumblebees, with evidence for nectar robbing behaviour of the long-tubed flowers. We aimed to investigate nectar robbing behaviour of bumblebees on F. magellanica, and in particular whether floral and pollinator traits (size) determined likelihood of nectar robbing. While F. magellanica was visited by a number of bumblebee species, only two with shorter tongue lengths were observed to rob nectar from flowers. Although there was no observed relationship between intra-specific bee body size and nectar robbing behaviour, nectar robbing was observed most frequently in the site with the highest number of bees. Proportions of robbed flowers were low overall and varied between populations, but there was a significant relationship between flower size and whether it was nectar robbed with larger flowers robbed more often. Our work suggests that floral size determines whether a flower-visitor will choose to nectar rob or not in this system. Nectar robbing may also be related to bee density which could suggest this behaviour is driven by competition for resources, or that it is learnt by observing other bees.

The Sensory and Cognitive Ecology of Nectar Robbing

Animals foraging from flowers must assess their environment and make critical decisions about which patches, plants, and flowers to exploit to obtain limiting resources. The cognitive ecology of plant-pollinator interactions explores not only the complex nature of pollinator foraging behavior and decision making, but also how cognition shapes pollination and plant fitness. Floral visitors sometimes depart from what we think of as typical pollinator behavior and instead exploit floral resources by robbing nectar (bypassing the floral opening and instead consuming nectar through holes or perforations made in floral tissue). The impacts of nectar robbing on plant fitness are well-studied; however, there is considerably less understanding, from the animal’s perspective, about the cognitive processes underlying nectar robbing. Examining nectar robbing from the standpoint of animal cognition is important for understanding the evolution of this behavior and its ecological and evolutionary consequences. In this review, we draw on central concepts of foraging ecology and animal cognition to consider nectar robbing behavior either when individuals use robbing as their only foraging strategy or when they switch between robbing and legitimate foraging. We discuss sensory and cognitive biases, learning, and the role of a variable environment in making decisions about robbing vs. foraging legitimately. We also discuss ways in which an understanding of the cognitive processes involved in nectar robbing can address questions about how plant-robber interactions affect patterns of natural selection and floral evolution. We conclude by highlighting future research directions on the sensory and cognitive ecology of nectar robbing.

Effects of the availability of floral resources and neighboring plants on nectar robbery in a specialized pollination system

Many plants pollinated by nectar-foraging animals have to maintain a balance between legitimate visitor attraction strategies and mechanisms that minimize illegitimate visits. This study investigated how floral display and neighboring species composition influences nectar robbing in the tropical ornithophilous herb Heliconia spathocircinata. We tested the role of inflorescence display, flower abundance, and neighboring species in the reduction of nectar robbing in H. spathocircinata. Our results indicate that nectar robbing hummingbird activity was higher in moderately large inflorescence displays and that the frequency of nectar robbing in H. spathocircinata decreases with increased flower abundance and the presence of neighboring plant species. Neighboring non-ornithophilous plants decreased the frequency of nectar robbing in H. spathocircinata flowers to a greater extent than ornithophilous ones. These results suggest that nectar robbing hummingbirds are attracted to similar conditions that attract legitimate visitors, and that spatial aggregation and mixed-species displays may represent a mechanism to dilute nectar robbing effects at an individual level.

Corolla Abscission Triggered by Nectar Robbers Positively Affects Reproduction by Enhancing Self-Pollination in Symphytum officinale (Boraginaceae)

Nectar robbers, which affect plant fitness (directly or indirectly) in different degrees and in different ways, potentially constitute a significant part of mutualistic relationships. While the negative effects of nectar robbing on plant reproductive success have been widely reported, the positive effects remain unknown. The target of our study was to evaluate the effects of nectar robbers on the reproductive success of Symphytum officinale (Boraginaceae). We observed the behavior, species and times of visitors in the field, and we assessed the effect of nectar robbers on corolla abscission rate and time. To test the fitness of corolla abscission, we detected the changes in stigma receptivity, pollen viability, pollen amount and appendage opening size along with the time of flower blossom. The flowering dynamics and floral structure were observed to reveal the mechanism of self-pollination. Finally, pollen deposition seed set rate and fruit set rate were determined to estimate the effect of nectar robbers on reproduction success. We observed 14 species of visitors and 2539 visits in 50 h of observation; 91.7% of them were nectar robbers. The pressure and nectar removal of nectar robbers significantly promoted corolla abscission during a period when pollen grains are viable and the stigma is receptive. In addition, corolla abscission significantly increased the pollen deposition and seed setting rate. Our results demonstrate that nectar robbing contributes to enhancing seed production and positively and indirectly impacts the reproductive success of S. officinale. This mechanism involved the movement of anthers and indirect participation by nectar robbers, which was rarely investigated. Considering the multiple consequences of nectar robbing, understanding the impact of nectar robbers on plant reproduction is essential to comprehend the evolutionary importance of relationships between plants and their visitors.

A Reference Genome for the Nectar-robbing Black-throated Flowerpiercer (Diglossa brunneiventris)

Black-throated Flowerpiercers (Diglossa brunneiventris) are one species representing a phenotypically specialized group of tanagers (Thraupidae) that have hooked bills which allow them to feed by stealing nectar from the base of flowers. Members of the genus are widely distributed in montane regions from Mexico to northern Argentina, and previous studies of Diglossa have focused on their systematics, phylogenetics, and interesting natural history. Despite numerous studies of species within the genus, no genome assembly exists to represent these nectivorous tanagers. We described the assembly of a genome sequence representing a museum-vouchered, wild, female Diglossa brunneiventris collected in Peru. By combining Pacific Biosciences Sequel long-read technology with 10X linked-read and reference-based scaffolding, we produced a 1.08 Gbp pseudochromosomal assembly including 600 scaffolds with a scaffold N50 of 67.3 Mbp, a scaffold L50 of 6, and a BUSCO completeness score of 95%. This new assembly improves representation of the diverse species that comprise the tanagers, improves on scaffold lengths and contiguity when compared to existing genomic resources for tanagers, and provides another avenue of research into the genetic basis of adaptations common to a nectivorous lifestyle among vertebrates.

The flowerpiercers interactions with a community of high Andean plants

Background Flowerpiercers (Diglossa) are traditionally considered as “parasites” of the pollination processes, as they can access the nectar without entering in contact with the reproductive structures of the plants. Nevertheless, the effect of flowerpiercers seems to vary according to their behavior and the flower’s traits. So, in this work, we aimed to explore the floral characteristics that may determine the susceptibility to robbing and pollen transport by flowerpiercers. Also, we identified the potential types of interactions and studied interaction network properties. Methods We collected the information of 16 ornithophilic plants regarding their floral traits and robbing frequency. Also, we captured 4 species of flowerpiercers and evaluated pollen transport (frequency and loads). We tested the correlation between floral traits, robbing frequency, and pollen transportation. Later, we used these variables in a cluster and principal component analyses to identify the potential types of interactions. Finally, we analyzed and compared the structure of the plants-flowerpiercers interaction network. Results Nectar production significantly influenced both nectar robbing and pollen transportation. While the corolla length was only correlated to the robbing susceptibility. Also, we found that particular flowerpiercers species transported higher loads of some plant pollen, which can be related to the differences in behavior and morphometric traits. We proposed the classification of five different types of plant-flowerpiercer interactions, that showed different potential mutualist or antagonist relations based on the affectation of nectar robbing and the service of pollen transportation. The interaction networks consisted of 49 links, with 2.4 links per species, and presented indicators of a medium to high resilience, stability, and resistance (nestedness, connectance, and robustness). Also, the network presented medium to low specialization and substantial niche overlap. Conclusions The ecological role of the flowerpiercers goes beyond its classic assignation as “parasites” as they can actively transport pollen of several Andean plants, affecting its evolutionary history and the stability of the systems.