Isn't It a Bloomin' Crime?

Nectar robbers might really be misunderstood helpers

"I hate to contradict Darwin," says evolutionary biologist Joan Maloof. Yet the great man may have been a little quick to declare something a crime.

Both Maloof, now at Salisbury State University in Maryland, and Charles Darwin puzzled over creatures that make off with nectar or pollen from a flower but don't do any pollination.

The bumblebees that Maloof monitors, for example, often ignore the front-door entry to the flared corydalis blooms. That approach would direct them near enough to dust the stigma a female part of the flower, with pollen the bee had picked up from the male parts, anthers, of another flower.

These chubby bees have short tongues, however, and can't push deep enough into the bloom to sip the nectar. Rather than give up the prize, they alight on the outside of the flower and bite a hole near the nectar reservoir. The bees get their nectar all right, but the flower is left unpollinated.

In one of the earliest accounts of such behavior, Darwin borrowed the language of crime. "[A]ll plants must suffer in some degree when bees obtain their nectar in a felonious manner ...," he wrote in an 1872 treatise.

"I think he was brilliant," says Maloof. Yet she and her colleague David Inouye of the University of Maryland in College Park question whether such larceny necessarily harms the plant. Might such bees in fact be doing flowers favors? Last October, the researchers reviewed 18 studies of nectar robbing and found only six documented negative effects on the flowers. Six studies found no effect either good or bad, and the other six reported that flowers actually benefited from the so-called robbery.

"Now, we've opened our eyes a bit," says Inouye, who has followed the study of floral larceny for decades. "We've realized you can't assume that it's all bad or all good." This sense of complexity didn't exist 18 years ago, when he wrote the last review on the subject, he recalls. However, "all of a sudden, there seems to be a renewed interest," he says. Too bad Darwin's missing the fun.

In his botanical police reports, Inouye separates the robbers from the thieves. Nectar robbers are "breaking and entering," he explains. Maloof's bees fall into this crowd, cutting holes into flower tissue like bank robbers drilling their way into a safe.

In contrast, thieves just pick the treat-filled pockets of a flower without performing the business of pollination. A butterfly, dipping its long proboscis into a flower that's better shaped for short-tongued bees, might hang back so far from the floral sex organs that nothing happens except the removal of nectar--no pollen in, no pollen out. Such visitors could just as well be called incompetent pollinators as nectar thieves.

Whatever their mode of crime, the perpetrators come in a variety of shapes and sizes. They can be small, such as ants and rice-grain-size Trigona bees. The larger carpenter bees, with their wood-boring equipment, readily nip holes in flowers. For a creature as big as a hummingbird or the tropical Diglossa birds called flowerpiercers breaking into a flower presents little problem.

There's a lot of nectar crime out there, says Rebecca Irwin, soon to be of the University of Georgia in Athens. For tubular flowers or ones that dangle nectar-filled sacs, she estimates that just about all species fall prey to some kind of larceny. Anyone strolling through a garden or some wild spot can probably pick out small holes on flowers already attacked Irwin says. Check around the base of the blooms, and crime may not seem so rare. "You'll be surprised," she predicts.

Maloof and Inouye likewise report high crime rates. The 18 studies they reviewed report robbery in at least a third of the plants surveyed, and in some cases, rates reached 100 percent. And there's a lot of repeat crime. In one study of bluebells, half the visits to individual plants ended in robbery of nectar. In a study of a fuchsia species, that figure was 80 percent.

These alleged crimes deserve more attention, argues Irwin. For more than a century, biologists have puzzled over the ways that the pollinators could shape the evolution of flowering. Shouldn't the larcenists have effects, too?

Nobody's saying that nectar crimes are victimless. Irwin's studies of scarlet gilia (Ipomopsis aggregata) in the Rocky Mountains offer a good example of ill effects for the plants. Hummingbirds pollinate the long, slim tubular flowers that flare brilliant red around the top of the plant stem. However, Bombus occidentalis, one of the short-tongued bumblebees native to western North America, robs nectar. In one of the rare research projects in which the scientists manipulated flowers, Irwin turned to crime herself. She figured out how to mimic a bee nip by snipping a hole the right size with sharp-pointed scissors and pilfering the nectar. "It took a lot of experimenting," she says. "But you learn, and then you can rob hundreds of flowers just like a bee."

When she cut a robber's hole in 80 percent of the flowers on a single gilia plant, she found that it yielded only half the number of seeds produced by plants in which she attacked just 10 percent of the blossoms. Since a gilia blooms only once in its lifetime, rampant stealing at the high rate Irwin sees in nature cuts total reproductive potential in half, she says. That's indeed bad news for a robbery victim.

The seed shortfall, Irwin says, doesn't seem to have anything to do with the physical trauma of robbery. When she cut a nectar hole, stole the nectar, and then dusted pollen onto the female organs, the flower set seed perfectly well.

Instead, Irwin blames the plunge in seed number on robbery somehow rendering the blooms unappealing to the pollinating hummingbirds. "They're pretty amazing," Irwin explains. "They have to be really good choosers." A hummingbird needs nectar from hundreds of flowers a day in order to fuel its high-revved daytime metabolism and still live through the night.

So how do hummingbirds know a flower's been robbed? Orinthologists don't think the birds sniff out nectar, so do they check for holes? Irwin snipped holes in one set of flowers and left another intact. She removed nectar from all the blossoms via a syringe put down the flower's tube, then replaced it in a fraction of both the snipped and the unsnipped blooms. When hummingbirds cruised the array, they picked out the flowers with nectar, regardless of holes. This coming summer, Irwin says, she hopes to test the possibility that the buzzing wings of the bird set a nectar-filled flower vibrating at a different rate from a robbed flower.

This tale fits the pattern of birds-and-bees conflicts. Trigona bees in the tropics take some 20 minutes to chew a single hole in a flower and then defend their handiwork fiercely, she says. Observers report them chasing away even birds. In work not yet published, Irwin and her colleagues reviewed the larceny literature and found overall "a strong negative effect" for bird-pollinated plants with bee trouble.

Now for some good news about crime. Maloof hasn't found that robbery harms seed production in the rare Rocky Mountain wildflower she studies, Corydalis caseana.

Bees pollinate the fragrant, pink-and-white tubular blooms, which cluster atop waist-high plants. Bees also rob the flowers. B. occidentalis, the same species that taps gilia, also drills into about 80 percent the corydalis blooms, Maloof will report in an upcoming issue of the AMERICAN JOURNAL OF BIOLOGY. "You can actually hear them crunch a little hole in the back" of the flower, Maloof says.

To tease out what the robbers do, Maloof enlisted volunteers from the research-assistance program Earthwatch. They helped her monitor the comings and goings of bees that flew into the study patch. Volunteers tracked individual bees, calling out their movements a transcriber. They differentiated their charges by picking a female code name. At peak visiting hours, Maloof says, "you had to get creative: 'I've got um ... um ... Henrietta!'"

The group found evidence for one of several benefits--yes, that's benefits--that some botanists have proposed for plant-robbery victims. In the Corydalis studies, bumblebees doing real pollinating flew longer distances between stops when working a robbed flower patch, compared with a relatively unmolested one. Researchers of bee behavior have long known that nectar and pollen foragers encountering skimpy rewards tend to fly farther before trying again, as if the added distance could get them out of a patch of dud flowers. From the plant's point of view, that distance bonus might mean pollen ends up far from close relatives, resulting in crosses that create vigorous offspring.

Considering other robbery studies, Maloof points out that robbed flowers with scant rewards may drive bees to visit more blooms in a given time, thus spreading pollen to more potential parents. "Ideally, you want to keep the bees harried and moving around," Maloof says. "You don't want them to get a long drink and then take a nap."

Also, that high tally of individual blooms might be scattered among an unusually large number of plants, Maloof says. Other work has revealed that pollinating bees tend to give up after sampling just a few blossoms if rewards fall below a threshold. They just move on to the next plant, a great scenario for reducing botanical inbreeding.

Sarah Richardson found a different bonus for robbed plants when she studied the three bee species that buzz around the desert willow. An inhabitant of arid land, the Chilopsis linearis dangles narrow leaves like a willow's, yet it bursts out in stubby trumpet blooms like its relative, the catalpa.

Richardson, of the University of Arizona in Tucson, monitored visitors to the showy white blooms and found that a plump carpenter bee quickly turns to robbery. For the first 4 or 5 days of the flowering season, carpenter bees approach the flowers from the legitimate end, the flare of the trumpet. However the bees pack a lot of bulk, and "they really have to strain themselves," Richardson says. They try other approaches too, including poking the long sharp tube projecting from their mouths into the side of the flower and slicing a slit. "After that, they never touch the anthers and stigma again," Richardson says.

Her analysis of the carpenter bees' effect depends on two other species, one of them a honeybee that frequents the blooms. For this plant, "they're really bad pollinators," Richardson says. Their small bodies often wriggle to collect pollen or nectar without touching the stigma. Honeybee saliva and perhaps exposure to sun, ruin the potency of the pollen they pick up from the flowers.

Brushing such dud pollen onto a stigma can ruin a flower's chances for future pollination. The flower collects pollen on the two upright flaps of the stigma. When a bee brushes them, they press together in a matter of seconds. "They're like praying hands," Richardson says. Sometimes, they stay closed for days, preventing further pollen deposits.

As the honeybee does just about everything wrong, from the flower's point of view, the other species in the tale, the Bombus sonorus bumblebee, does just about everything right. It carries fully potent pollen and almost always brushes it onto the stigma of the flower.

This wonder bee doesn't even seem to avoid robbed flowers, Richardson found. Yet honeybees do. Thus, robbery boosts a flower's chances of hosting the better bee.

F or other bee-pollinated plants, the whole distinction between robbers and pollinators may fall apart. Luis Navarro of the University of Santiago de Compostela in Spain blurred that difference in his analysis of a pea relative he studied in the northwest of his country.

One long-tongued bee pollinates the blossoms of lady's fingers, Anthyllis vulneria, without any illicit chewing. Two other bees, however, nick holes in the blooms and suck nectar, he reported last year in THE AMERICAN JOURNAL OF BOTANY. In the course of this safecracking, the big-bodied robbers sometimes blunder into the pollen and brush against the female parts of the plant. Their inelegant maneuvers thus provide extra chances of pollination. Navarro argued that they made the difference in the higher probability of pollination he observed in robbed flowers: 71.7 percent setting fruit versus 55.4 percent of unrobbed ones.

Even if robbers don't bumble onto the flower's sex organs, the interlopers may still come back later for a legitimate visit. William Morris of Duke University in Durham, N.C., has monitored bees crawling over Mertensia paniculata bluebells. On the first day a flower opens, its pink tube presents pollen to visitors. When a bloom reaches the age of 3 to 5 days, the tube darkens to blue and secretes nectar. Morris reports that two bumblebee species act as honorable pollinators when they collect pollen from the pink youngsters but turn to nectar robbery on the old, blue flowers. An individual bee frequently switches to and from crime. Is that bee a really a robber? Such muddles inspire Maloof and Irwin to talk about "robberlike pollinators."

Effects of the criminal element could extend far beyond the individual plant, Irwin says. She and her colleagues have recently received a National Science Foundation grant to look into larceny's effect on plant communities. In preliminary studies, Irwin's team found that scarlet gilia set more seed when mixed with another robbery target, butter-and-eggs or Linaria vulgaris, than when gilias grow alone. The researchers suspect that the alternative sources of illicit nectar protect the usual target of robbers.

Moving the discussion to an even broader level, Anurag Agrawal of the University of Toronto sees the questions of nectar robbing as intriguing issues marking the fine line between parasites and so-called mutualists--organisms of two species that both enjoy benefits. That is, assuming the line exists. "[A]re mutualisms simply reciprocal parasitisms between individuals of two interacting species?" Agrawal asks in a commentary on robbery in the March TRENDS IN ECOLOGY AND EVOLUTION.

Nick Waser has another question. A longtime iconoclastic theorist at the University of California, Riverside, Waser wants to know if flowers and their pollinators are really as tightly coordinated as biologists once thought.

Waser sighs at the thought of textbooks that expound on long, red trumpet flowers that fit hummingbirds or blooms that seep nectar at just the right depth for a certain moth's unfurled proboscis. "What you learned is a cartoon of pollination," he says. "It's much messier than that."

Supposedly specialized flowers often host a great diversity of insects and birds, whose impacts vary. A slightly bumbling bee might provide vital services when better pollinators aren't around but then become a nuisance, essentially a thief, in better times.

To sort out these complicated systems, researchers need to be vigilant in designing the next wave of experiments, Irwin cautions. For example, previous workers often compared the fates of naturally robbed flowers with unrobbed ones. But suppose the robbers attack mostly the weaklings and losers? Low seed set for robbed plants would thus make robbing look artificially destructive. Or suppose the robbers prefer plants bursting with vigor. These primo plants might absorb the losses and still outdo weakling plants.

To resolve such matters, Irwin argues for researchers to rob some flowers themselves in a carefully random way. "Take heart, students looking for projects," she says. "There is plenty to do."