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Around 4,000 plant species from different parts of the world secrete nectar outside their flowers, such as on their stems or leaves, through secretory glands known as extrafloral nectaries. Unlike floral nectar, extrafloral nectar does not attract pollinators; rather, it attracts insects that defend plants, such as ants. These insects feed on the sweet liquid and, in return, protect the plant from herbivores. However, this protection comes at a cost.

A study in the Journal of Ecology points out that the presence of ants can reduce the frequency and duration that bees visit the flowers of plants with extrafloral nectaries.

Pollination is only impaired when extrafloral nectaries are close to the flowers. Plants with these glands in other locations, such as on their leaves or branches, had increased reproductive success, likely due to the protection against herbivores provided by ants.

On the other hand, butterflies, another group of pollinators, are not affected by ants. This may be due to the way these two groups feed. Butterflies use a long, straw-like organ called a proboscis to suck nectar from a distance, keeping them safe from ants.

"Bees, on the other hand, need to get very close to the flower to collect pollen and floral nectar, but ants don't allow them to stay for long. Not surprisingly, our analysis showed that the presence of ants is detrimental to pollination when extrafloral nectaries are close to flowers, but has a positive effect on plant reproduction when they're located further away," explains Amanda Vieira da Silva, who conducted the study as part of her doctoral research in the Graduate Program in Evolution and Diversity at the Federal University of ABC (PPG-EvoDiv-UFABC) in São Bernardo do Campo (state of São Paulo, Brazil).

The conclusions are the result of an analysis of data from 27 empirical studies on the relationships between ants, pollinators, and plants with extrafloral nectaries. The articles were selected from an initial screening of 567 studies after applying inclusion and exclusion criteria. The data were compiled and analyzed with computational tools.

Multiple mutualisms

"Studies have typically focused on the effect of only one isolated interaction on plants. For example, they quantify how much ants favor the defense of plants against herbivores or how much pollinators favor plant reproduction. But these interactions can occur at the same time. So, to understand how these interactions influence plant growth and reproduction, we need to look at them in an integrated way," explains Laura Carolina Leal, a professor at the Institute of Environmental, Chemical, and Pharmaceutical Sciences at the Federal University of São Paulo (ICAQF-UNIFESP) in Diadema. Leal supervised Silva's doctoral studies and is also a co-author of the paper.

Evolutionary analyses of plant genera with extrafloral nectaries indicate that this trait can be easily acquired or lost over time. Therefore, the interference of ants in bee visits to flowers may have acted as a decisive selective pressure in the evolutionary trajectory of extrafloral nectaries in plants.

"If ants visiting extrafloral nectaries harm plant reproduction by scaring away bees, maintaining these nectaries can become disadvantageous for plants, and the glands may be lost over time," Leal explains.

Not coincidentally, of the nearly 1,000 genera with extrafloral nectaries, only 46 depend exclusively on bees for pollination. The authors have a hypothesis for the simultaneous occurrence of plant interaction with defensive ants and pollinating bees, at least in some cases.

"We know that in some groups of plants with extrafloral nectaries and flowers pollinated by the vibration of bees, new leaves with active extrafloral nectaries and flowers are produced in different seasons throughout the year, which would avoid conflict between the two," says Anselmo Nogueira, a professor at the Center for Natural and Human Sciences (CCNH) at UFABC, Silva's co-advisor, and co-author of the study.

The research group is developing new studies to understand whether a third interaction can stabilize ant interference in the pollination of plants with extrafloral nectaries.

"If the resource is very good for the bee in the flower and for the ant on the leaf, perhaps they'll never meet. In addition, some plants with extrafloral nectaries, such as certain legumes, harbor nitrogen-fixing bacteria in their roots, which promote plant productivity and may enable the plant to invest in high-quality resources for both animal partners," comments Nogueira.

The researcher coordinates a project that investigates the evolution of multiple mutualisms in the same plant lineage. In a previous study, his group showed that the interaction between a species of legume and nitrogen-fixing bacteria increases the attractiveness of these plants to pollinating bees.