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Ecology

Selective hosts

Flowers exploit color and odor to hide from or attract specific bees

The broad landscapes of rocky, highland meadows host a mosaic full of biodiversity

Maria Gabriela Camargo

When a bee flies across a meadow, it sees, at a distance, compositions in shades of green. Color is only revealed at close range, except for red, which is invisible to it. Birds, however, have a larger range of structures in their eyes that allow them to see red. Colors are the main mode of communication between plants and pollinators, but the perceptions of human eyes aren’t enough to understand the complexity of this relationship. From these sensory differences comes the antiquated notion that flowers pollinated by birds tend to be red, while those that benefit from the activities of bees usually have yellow flowers. However, there is more to it than attracting pollinators, according to the research group led by biologist Patrícia Morellato, from São Paulo State University (UNESP) in Rio Claro. The latest news is that selective invisibility can have actual benefits, by excluding unwanted visitors.

Ecologist Maria Gabriela Camargo, during her postdoctoral work at Morellato’s laboratory, arrived at this conclusion after analyzing the colors of flowers (283 species) pollinated by animals (244 species of bees and 39 hummingbird species) in the rocky meadows of the Cipó Mountains in Minas Gerais. She measured the spectra of light reflected by the flowers and other parts of plants, then associated them with their principal pollinators, according to an article published in partnership with colleagues from Germany and São Carlos, in the April issue of the journal New Phytologist.

Back in the lab, Camargo perceived that differences in the light reflected by flowers depended on their typical pollinator, reiterating the importance of color in attraction. Those visited by hummingbirds emit longer wavelengths, invisible to bees. She made diagrams representing the visual space of birds and bees and plotted the flowers on them according to their pollinators, mapping how animals see the flowers. The results indicate that most flowers pollinated by hummingbirds are not seen by the bees as having color, whether they are red (more often), yellow, or white. Hummingbirds see all colors, and contrary to the dogma that they like red, are particularly attracted by strong contrasts. “Red flowers are not easily detected by bees, and we saw that evading them can be important because in the hummingbird-pollinated flowers bees can steal the nectar without pollinating,” Camargo observes.

Maria Gabriela Camargo Flowers with large openings, such as this Luxemburgia, are typical of those pollinized by beesMaria Gabriela Camargo

Researchers also found that markings known as nectar guides—lines, dots, or spots not always visible to the human eye that function like marked trails—appear in 52 percent of bee flowers and 26 percent of those pollinated by hummingbirds. “The guides optimize the manipulation because they allow bees to direct their activity and spend less time moving through the flower,” says Camargo, explaining why the markings would be advantageous for both the insects and the flowers.

A color that obscures the flower instead of attracting, thus selecting the visitor, represents a change in how these ecological relationships are viewed. “It was a spectacular finding, that colors can act as a floral filter,” says German biologist Klaus Lunau of the University of Düsseldorf, a specialist in pollination and a coauthor of the study. “That attracting pollinators is just one of the functions of flower colors, which can also serve to frighten herbivores and other unwanted visitors, is something new,” he adds.

Three particular qualities of the highland meadows make their short-statured vegetation—and its curious survival strategies in the poor, stony soil it grows in —ideal for this study of pollinator communities. It is an ecosystem characterized by a great diversity of plant life, where the plants use bees and hummingbirds as their principal pollinators, and where, due to the open vegetation, the flowers are visible at a distance and provide good contrast to the background, favoring visual communication. The UNESP researchers hope to repeat the same kind of analysis for other environments, such as forests, with another repertoire of different species and conditions, to verify if their conclusions are maintained.

For Camargo, one distinct feature of the study was to confirm, in nature, the hypothesis of bee exclusion and patterns of coloration—described above—to attract them. Morellato adds that it will now be possible to further advance our understanding of how these interactions in the highland meadows function.

Maria Gabriela Camargo Nectar at the bottom of Augusta longifolia’s elongated flower, a color invisible to bees, can only be reached by hummingbirdsMaria Gabriela Camargo

Night vision
Besides affirming that the revised outlook on pollination could bring innovation in future studies, Klaus Lunau highlights the importance of Brazilian diversity. “Many questions go unanswered because most studies have been conducted using European honeybees and two species of bumblebees, ignoring the great diversity not only of these genera, but also of stingless and solitary bees.” Lunau has contributed to reducing this lack of knowledge by partnering with biologist Isabel Alves-dos-Santos, from the Institute of Biosciences of the University of São Paulo (IB-USP), in experiments conducted in the apiary. “Here, the conditions are good for doing experiments because we can train, feed, and manipulate the bees,” she says. “Two of Klaus’s students came over from Germany, and by the end of the study period the bees were following them back and forth through the garden!” They examined two species of stingless bees, Partamona helleri and Melipona bicolor, and found that their preferences are not homogeneous. The first species tended to choose bluish colors, while the latter did not appear to have a preference for specific colors, as reported in a September 2018 article published in PLOS ONE. Although color is the main form of flower signaling, apparently other senses may be more important to Melipona.

In recent years, the USP group has begun to explore the nightlife of bees. With no light to be reflected, at night colors fail to fulfill their role. Alves-dos-Santos became interested in the subject when his student Guaraci Duran Cordeiro, studying the cambuci (Campomanesia phaea, a common tree of the Atlantic Rainforest), realized that the flowers had already been visited by six in the morning. He found four species of nocturnal bees active in the flowers as soon as they opened at 4:30 a.m. Nocturnal species of bees have been largely ignored until now. “Bee snoops don’t go out at night,” the researcher jokes.

More recently, the USP researchers have been studying guarana flowers (Paullinia cupana), which open around two in the morning, and have documented various species of nocturnal pollinators. In dark orchards, where researchers can’t even see the flowers, bees follow chemical trails using their antennae and guide themselves perfectly to what interests them. In partnership with biologist Stefan Dötterl of the University of Salzburg, Austria, the USP group is chemically analyzing these odors, as shown in a July 2018 article in Frontiers in Plant Science. The ratio of chemical components could be crucial to filtering the attracted bee species, thus cultivating a more productive relationship. “Bees from the Apis genera tend to visit flowers on the same plant, which isn’t useful for species that require cross-pollination,” notes the researcher, referring to the need for pollen from one plant to fertilize another. “Other species of bees range between plants more.”

Projects
1. Combining new technologies to monitor phenology from leaves to ecosystems (nº 13/50155-0); Grant Mechanism Partnership for Technological Innovation (PITE); Microsoft Research Agreement; Principal Investigator Leonor Patrícia Cerdeira Morellato (UNESP); Investment R$1,842,134.97 (FAPESP).
2. Floristic diversity and seasonal patterns in rocky highland meadows and the Cerrado (nº 10/51307-0); Grant Mechanism Partnership for Technological Innovation (PITE); Vale-FAPEMIG-FAPESP Agreement; Principal Investigator Leonor Patrícia Cerdeira Morellato (UNESP); Investment R$441,438.71 (FAPESP).

Scientific articles
CAMARGO, M. G. G. de et al. How flower colour signals allure bees and hummingbirds: a community-level test of the bee avoidance hypothesisNew Phytologist. Vol. 222, no. 2, pp. 1112–22. Apr. 2019.
KOETHE, S. et alSpectral purity, intensity and dominant wavelength: Disparate colour preferences of two Brazilian stingless bee speciesPLOS ONE. Vol. 13, no. 9, e0204663. Sept. 28, 2018.
CORDEIRO, G. D. et al. Pollination of Campomanesia phaea (Myrtaceae) by night-active bees: a new nocturnal pollination system mediated by floral scentPlant Biology. Vol. 19, no. 2, pp. 132–9. Mar. 2017.
KRUG, C. et al. Nocturnal bee pollinators are attracted to guarana flowers by their scentsFrontiers in Plant Science. Vol. 9, 1072. July 31, 2018.

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