A newly described leaf-biting behavior could help bumble bees mitigate the effects of climate change

By Alison McAfee

August 1st, 2020

Bumble bees are surprisingly smart. They can master complex tasks like learning to roll a ball onto a target to get a sugar reward — a task similar, in principle, to using tools. They can even recognize objects in the dark, which they have previously only seen through a window, just by feeling their shape. But new research shows that bumble bees aren’t just intelligent, they’re also manipulative.

Researchers at the Swiss Federal Institute of Technology Zurich (ETH Zurich) have found that worker buff-tailed bumble bees (Bombus terrestris, one of the species managed for commercial pollination) manipulate plants to flower earlier than they normally would, particularly when the bees are starved for pollen. The bees do this by biting holes in the plants’ leaves, which stimulates the plants to bloom early and gives the desperate bees their pollen.

A bumblebee (Bombus terrestris) worker damaging a plant leaf. Bee-inflicted leaf damage leads to accelerated flowering. Bumble bees make incisions with their mandibles and appear to widen them with their proboscis. Photo by Hannier Pulido, courtesy of the De Moraes and Mescher Laboratories.

“It always surprises me how, even in systems we think we know so much about, there are still so many things we don’t know,” says Dr. Consuelo De Moraes, the study’s senior author. “That’s one of the most fascinating things about science, there is still so much to discover.”

Initially, the researchers were working on a project on butterfly egg laying, but while some students were working in the greenhouse, which was also home to a bumble bee colony, they noticed this bizarre behavior. They saw bumble bees landing on leaves and perforating them, but why? They called in Harriet Lambert, a PhD student and one of the lead authors on the study, to take a look.

“Initially, I think we all assumed that something was wrong with the colony,” Lambert says. They purchase bumble bee colonies from commercial suppliers, and the colonies could have varying degrees of health. But over time, they observed this behavior in colonies they obtained from many different sources, so it wasn’t just an aberration.

“It soon became clear that under the right conditions, every hive we worked with, both inside and outside, would damage the leaves of plants,” says Lambert. Either the bees were acquiring some kind of resource from the leaves, or something else was going on.

But unlike some other bee species, bumble bees do not use pieces of leaves in their nests. And while some plants secrete nectar from their leaves or stems through extra-floral nectaries, these particular plants (tomato and mustard varieties) do not. When Lambert combed through the literature to learn more about this curious leaf-perforating habit, though, she found nothing — the behavior had not yet been described. They had accidentally stumbled on something new.

And when the researchers followed what happened to bee-bitten and unbitten plants over time, they found that the tomato plants flowered a full month earlier than their unassaulted counterparts, corresponding to 38 days after the bees perforated their leaves. The mustard plants responded similarly, flowering about two weeks early, or 17 days after biting.

“There are a lot of studies on pathogens and mostly abiotic stresses, like drought, inducing flowering,” says De Moraes. “That’s where the hypothesis came from.” Not very much is known about insect herbivores changing the timing of flowering, she explains, but that was the first thing that came to her mind: Maybe the bees were manipulating the plants to flower early.

Many plants have evolved to accelerate their flowering time when they become stressed. This is because when growing conditions are poor, their future is uncertain, often making it more advantageous for the plant to invest in reproduction sooner rather than later. “It’s possible that the bees are tapping into those internal signalling mechanisms,” says Dr. Mark Mescher, one of the study’s coauthors, making the plants flower earlier than they normally would.

And it looks like there is something uniquely special about the bite of a bee — simply punching holes in the leaves with tweezers had very little effect. When tomato plants were mechanically damaged by humans, they flowered only 5 days earlier than normal, compared to 30 days when bitten by bees. But it’s still not clear why.

“We tried to replicate the bee’s damage as closely as possible,” says De Moraes, including doing the mechanical damage at the same time the bees were damaging other plants, and matching the sizes and shapes of the holes. “We tried our best, but it’s possible that we’re not replicating the damage in the same way.”

The other, more interesting possibility is that there is something in the bees’ saliva — a cue — that the plant perceives, and it’s this cue that induces flowering. Indeed, the bees not only bite the leaf, creating a hole — they also can be seen sticking their proboscis through the hole, apparently licking it. What that cue is, if it does exist, remains unknown.

The initial observations of leaf biting were made in a greenhouse, and subsequently confirmed to be linked to pollen deprivation in laboratory experiments. But in these kinds of artificial conditions, there was still the possibility that this leaf-punching was just a maladaptive behavior induced by living in a more stressful environment. The next step, therefore, was to take the experiments outside.

Over the course of two years, the researchers conducted rooftop experiments to see if the bees would still do the behavior when they were under more natural conditions. In the first experiment, they showed that bumble bees do indeed perform the behavior even when they have broader foraging options, and that their propensity to punch leaf holes on experimental plants declines as the surrounding forage sources increase during the spring.

In another experiment, bumble bee colonies were placed on two different rooftops — at both sites, the bees had patches of flowerless plants nearby, but on one roof, there was also a wildflower garden. As predicted, the bees without the wildflower garden punched more holes than the bees with access to flowers. And when the garden was cut down, hole punching ensued on that rooftop, too.

These outdoor observations also revealed that leaf-biting behavior isn’t restricted to buff-tailed bumble bees. During the course of their studies, the researchers also saw wild red-tailed and white-tailed bumble bees (B. lapidarius and B. lucorum, respectively) punching leaf holes. Honey bees also visited the study sites, but never even landed on a flowerless plant — they only visited flowers. This hole-punching behavior may have evolved in bumble bees, specifically, because they are more vulnerable to resource scarcity.

Unlike honey bees, who pack away all the pollen and nectar they can for hard times ahead, bumble bees don’t store much food. They keep some surplus nectar and pollen in wax pots within their nests, but it is not enough to sustain the colony for long periods of time.

“Workers can only supply the energy requirements of the nest if there is a continuous seasonal succession of suitable flowering plants,” Lambert explains. This means that the timing of bumble bee brood rearing depends on near-synchronous forage availability. And forage isn’t always available, so maybe instead of stocking their pantry during a flow, like honey bees do, their approach is to order a future supply during dearth.

Like honey bees, bumble bees also need to collect nectar to survive. But surprisingly, nectar deprivation does not stimulate the leaf-biting behavior. One reason, the researchers speculate, is because in the complete absence of nectar, the colony is probably not going to survive long enough to receive the early flower reward anyway. Pollen, though, is only fed to developing larvae, meaning that it is not always an essential resource. Brood rearing can expand and contract as resources permit — or, in the case of leaf-biting, as resources are coerced — and the colony will live on.

But this leaf-biting behavior might also come with a cost to the plant. Accelerating the time to flowering could mean that the plant will have fewer resources to invest in its flowers than it normally would, which could result in a lesser quality forage source for the bees and lower attractiveness to other pollinators. When you’re starving, though, low quality forage is better than nothing, and getting it as soon as possible is better than getting high quality forage later, when it may be too late.

However, Mescher cautions that we don’t yet know if there is a cost to the plant at all. Instead, the plants might also benefit from this seemingly coercive relationship. “It’s possible that this is not actually manipulation,” Mescher says, “it could be communication. It’s an open question.”

That’s because pollinators are also resources to the plants, and plants are sometimes in competition for pollinators’ services. This leaf-damaging behavior may serve as a signal to the plant that pollinators are around and open for business, allowing the plant to better time its flowering with when there are actually bees around to pollinate them.

This kind of mutually beneficial communication might occur in other systems, too. According to a review published by Dr. Dani Lucas-Barbosa, a postdoctoral fellow also at ETH Zurich, insect herbivory can either accelerate or delay plant flowering, depending on the insect species, plant species, and at what developmental stage the plant incurs the damage.

For example, two different butterfly species — the small and large white cabbage butterflies — also induce early flowering in specific contexts. While the adult white butterflies are beneficial pollinators, their caterpillars eat the leaves and flowers of plants and can cause significant damage. Mustard plants can perceive when large white butterfly eggs have been laid on its leaves, though, likely also through some kind of chemical cue. In this context, the plant responds by accelerating its seed production so that it can reproduce before the eggs hatch and the caterpillars eat its flowers. But the small white butterfly can also delay flowering, as do some other leaf-eating insects, so this phenomenon appears not to be as consistent as with the bumble bees.

Many plants have evolved inducible chemical defenses in response to herbivory, whether by ungulates or insects. Tomato plants, for example, can release chemical signals into the air when they are attacked by insect herbivores, which stimulates neighboring tomato plants to produce herbivore-deterring chemicals, despite never having contacted the leaf-munching pests themselves. But the plant’s chemical defenses can also include antimicrobial agents, which occasionally make their way into nectar. We don’t yet know if the plant interprets the bees’ leaf holes like herbivory, but some researchers have suggested that bumble bees and monarch butterflies self-medicate on nectar containing antimicrobial compounds to help them fight disease.

However, if self-medication is going on here, and it’s not clear if it is, it is probably only a secondary benefit. The primary driver behind this crafty bumble bee behavior is most likely to regain synchrony between flowering plants and pollinators, which depend on each other to survive. The potentially mutually beneficial interactions between bumble bees and plants could make ecosystems better able to withstand environmental disturbances, including one of the greatest disturbances in recent history: climate change.

Climate change is expected to alter the suitability of some regions to support bee forage, and to change the habitable ranges of the bees themselves. In an ever-changing environment, it would be an asset for the bees to be able to coax their environment, to a degree, to better suit their chronological needs.

“Environmental disturbances and climate change might tend to disrupt synchrony between bees and the plants,” Mescher says. “This direct information transfer [between species] could make ecosystems more resilient.” While the bumble bees’ manipulative tendencies may at first appear cunning, it is likely not an entirely selfish act.

“Whenever I spot the typical bee holes, or see workers damaging leaves, I still feel awestruck at their social complexity,” says Lambert. These bees are not only smart, they are environmental engineers.

This article originally appeared in American Bee Journal.

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