Flora - A Twist of Fate

A Floral Twist of Fate - New Zealand mistletoes
Natural History,  Sept, 2000  by Laura A. Sessions

New Zealand mistletoes that bear strange, sealed flowers depend on savvy native pollinators to thrive.
Every year in December, the beginning of the austral summer, the green temperate rainforests in parts of New Zealand come alive with bright-red mistletoe flowers. One of my favorite places to see this natural display of Christmas color is a thirty-acre fragment of southern beech forest on the shore of South Island's Lake Ohau. This turquoise glacial lake lies in the shadow of the central Southern Alps' snowy peaks. Nearly every southern beech in this patch of forest is host to one or more large mistletoe plants. Botanists categorize mistletoes as hemiparasites--plants that can make food through photosynthesis after siphoning water and mineral nutrients from a host plant via rootlike structures that penetrate the host's bark and vascular system. The mistletoes that grow on the Ohau beeches can reach nine feet in both length and width and can virtually envelop a tree, but unlike their European and North American counterparts, they do not damage their hosts. When the mistletoe flowers mature, they drop from the plant and form red piles on the forest floor, like confetti from a holiday party.

A visitor to the Ohau forest who examines these fallen blossoms will notice that many of them have opened upside-down. While the petals of most other flowers are joined at the bottom and fold back from each other at their tips, these mistletoe petals are fused at the top and detached at the base. The stigma, or pollen-receiving structure, stays sealed within the flower tip, hidden from any pollinators that might fertilize the bloom and thus stimulate fruit and seed production, leading to a new generation of mistletoes. Why would a plant produce hundreds of flowers if they remain inaccessible to pollinators? In 1969, referring to these sealed flowers, botanist Job Kuijt declared, "We cannot even guess at the meaning of this bizarre performance."

Thanks to a research project that began in 1992 and continues today, we can offer more than a guess at the significance of the fallen and unfertilized mistletoe flowers. We now know that these mistletoes have a pollination system unique in New Zealand and that the unpollinated blooms dying on the forest floor represent a breakdown of the system. Led by Dave Kelly and Jenny Ladley, of the University of Canterbury in Christchurch, the project, which I joined in 1996, has gradually been transmogrified into a ten-person field effort. Every December, as other people prepare to celebrate the holidays, we gather our ladders and video cameras, sort through piles of tiny colored wires, mesh bags, batteries, chemicals, and microscope slides, and head out to the field. We now monitor more than 200 plants throughout New Zealand to determine changes in their size, health, and rates of pollination and fruiting. We also take more than 100 hours of video footage each year to record which pollinators visit plants and how they behave.

While mistletoes grow in temperate and tropical regions worldwide, New Zealand is home to eight species that occur nowhere else and one that is also found only on Norfolk Island in the Tasman Sea, between New Zealand and Australia. Our research has focused on two of these species, red mistletoe (Peraxilla tetrapetala) and scarlet mistletoe (P. colensoi).
In one of their first experiments, Kelly and Ladley attempted to learn more about New Zealand mistletoe reproduction by putting mesh bags over branches bearing unripe buds. The flowers could then be hand-pollinated, and the potential fruit production could be estimated. Or so Kelly and Ladley thought. After several weeks of close monitoring, the buds had ripened but failed to open. Eventually they began to split from the bottom, as Kuijt had noted, and to fall off the branches. This occurrence and a knowledge of the ways in which certain African and Indian mistletoes achieve pollination gave the researchers clues to what might be going on. On Christmas Eve of 1992, Ladley watched from just a few feet away as a tui, a native honeyeater (a nectar-eating bird), moved deftly among the nearby unbagged flowers on the tree. Using its beak, the bird reached for a bud and gave it a quick twist, which released the four petals. Within a second after the bud sprang apart, pollen was catapulted onto the tui's head as the bird sipped a pool of nectar.
Until this revelation, no one had known that any New Zealand mistletoes--or any other New Zealand flowers--relied on this unusual pollination mechanism. Flowers that can be popped open in this way by animals are called explosive. Various plant families from different parts of the world have such flowers, many of which are easily tripped by the touch of an insect or even by the wind. But flowers that require forceful opening are rarer and must attract pollinators that know the trick. From the bird's perspective, explosive twist-top buds unequivocally signal the presence of a sweet fast food (nectar) wrapped in a tamperproof package. The mistletoe also benefits from this setup. Sealed buds protect pollen against rain and mist until a pollinator is available, and once it is, the miniexplosion effectively showers the bird with pollen. The mistletoe usually ceases to produce nectar within the flower once it is opened, thereby encouraging birds to concentrate on opening new flowers rather than revisiting old ones.

In addition to the tui, another New Zealand species of honeyeater, known as the bellbird for its clear, bell-like call, commonly opens mistletoe flowers. Of the 170 species of honeyeaters in Australia and the Pacific Islands, only three--the tui, the bellbird, and the stitchbird (the latter surviving only on offshore islands)--are found in New Zealand. For their mutually beneficial relationship to have evolved, the honeyeaters and the mistletoes with explosive flowers presumably have been coexisting for thousands or perhaps millions of years. Introduced birds, such as blackbirds and finches (which are casual nectar feeders), rarely twist the flowers open. Perhaps these exotic species have not been living long enough with mistletoes in New Zealand to learn the opening maneuver. Occasionally we have seen bellbirds trying unsuccessfully to hasten the opening of the flowers of yellow mistletoe, or Alepis flavida, which open on their own. This suggests that explosive opening in red and scarlet mistletoe flowers might have evolved as the birds sought to be the first to reach an untapped nectar source.

Two years after their discovery of the exploding mistletoe flowers, the team found that birds were not the only animals that had learned how to access mistletoe riches. Several species of native solitary bees (Hylaeus agilis and various Leioproctus species) are barely one-fifth the size of a red mistletoe bud, but with persistent gnawing and heaving, they occasionally manage to pry one open with their mandibles. The bees are not interested in nectar; instead, they harvest pollen and haul it back to their nests to feed their larvae. In contrast to the birds' instant twist-and-sip method, the tiny bees often take more than a minute just to release the petals. On average, they succeed in opening one bud in every four they attempt to spring. But their efforts are generously rewarded. A bee that manages to jimmy open a mistletoe bud gets first access to an untapped store. The New Zealand red mistletoe is the only plant in the world with bird-pollinated explosive flowers that are also opened by insects. This challenges the common notion that plants usually have only one guild of pollinators--for example, either birds or butterflies, but not both.
As is the case with the honeyeaters, only native bees seem to have had time to learn how to unlock the mistletoe blossoms; the insects' introduced counterparts--exotic honeybees and wasps--have not yet discovered the trick. The native bees may be playing a role that in other parts of the world is likely to be adopted by other types of animals. New Zealand has relatively few pollinators. There are no mammalian pollinators, and only seven bird, one bat, sixteen butterfly, and about forty native solitary bee species serve New Zealand's flowers. (Australia, in contrast, is home to about 3,000 bee species and 110 bird species that are active pollinators.) Consequently, most New Zealand flowers either attract a range of pollinators (a variety of insects, for example) or are self-fertile (that is, able to produce fruits without pollen from another plant). Red and scarlet mistletoes' dependence on a few savvy pollinators came as a surprise.

Also unusual is the flower structure of red and scarlet mistletoes, which allows for visits by pollinators of vastly different sizes. A solitary bee weighs only one three-thousandth as much as a bellbird. When a tui or a bellbird pops open a bud, all four petals spring back, and as the bird inserts its beak into the corolla to drink nectar, its head often brushes pollen onto the receptive stigma. If the flower reacted the same way to a bee's probings, the insect could easily gather pollen from the anthers (the pollen-producing structures) without ever touching the stigma, and pollination would be unlikely. But bees seldom "detonate" flowers the same way birds do. Instead the bee makes a small slit in the end of the bud, creating just enough room to push its way inside. In such cramped quarters, the bee is more likely to touch the stigma--and pollinate the mistletoe--as it harvests pollen from the anthers. Our experiments show that on average, and despite their size, bees deposit about the same number of pollen grains during a single visit as birds do.

Still, bees are probably not as important to these mistletoes as native honeyeaters are, because the bees enter far fewer flowers. In addition, red and scarlet mistletoes depend on birds for seed dispersal. Peraxilla seeds are small and green even when ripe. In order for the seeds contained within the fruit to germinate and to become established on a new host tree branch, the fruit skins must be removed. The birds devour and digest the fruit and its skin, then defecate the seeds, often onto a branch of another tree. The pulpy seed is surrounded by a sticky layer that glues it to the surface on which it lands. Germinating immediately, the seed sends out "rootlets" to tap into the host tree's water supply.
Because of the mistletoe's reliance on honeyeaters for both pollination and dispersal (in addition to the honeyeaters, only one other bird, the waxeye, frequently eats the fruit), mistletoe plants are particularly subject to reproductive failure if their avian partners become scarce or disappear, as has happened with other indigenous birds. Plants that maintain less specialized relationships with their pollinators can reproduce with the help of many different insects or various birds; for them, the loss of any one species of pollinator is not so significant. But red and scarlet mistletoe flowers cannot open without the help of specific native bird and bee species, and unopened flowers have only a 5-10 percent chance of forming seeds through self-pollination. Unfertilized flowers end up as mysterious bottom-opened remnants on the forest floor.

At the turn of the last century, botanists reported forests ablaze with the scarlet blooms of native mistletoes, but today few areas of New Zealand support profuse growth. In most places, unpollinated dead blooms littering the ground are more common than flowers twisted open by birds and bees. Our experiments have shown that at several sites in the central Southern Alps of South Island, mistletoe plants produce no more fruits than plants that have been placed inside cages to keep out pollinators. This means that birds and bees are visiting flowers so infrequently--or that the birds are becoming so scarce--that essentially there is no increase at all in pollination over the low rate of self-pollination. (Birds may also be dispersing fewer seeds, although this may be less of a problem than the decline in pollination; ripe fruits can wait six weeks for a bird's visit, while buds last only six days.) A potential cycle of decline could begin if pollination drops to the point at which these mistletoes become rare and individual birds lose the twisting habit or if, over time, the bird species "forget" how to access flowers.

The decline of New Zealand mistletoes is one of a series of ecological changes stemming from the introduction of land mammals into plant and animal communities that evolved without such creatures. Rats, stoats, ferrets, cats, and possums have decimated native animals that were unaccustomed to mammalian predators. Native birds in particular have drastically declined, and some have been forced to seek refuge on mammal-free offshore islands. One mammal I have studied, the Australian brush-tailed possum, harms mistletoe in a direct way, by devouring it. But another cause of the gradual disappearance of mistletoes throughout New Zealand is the elimination of avian pollinators by mammals. This chain of ecological events may already have doomed a close relative of the red and the scarlet species, the mistletoe known as Trilepidia adamsii, which has been extinct since the mid-1950s. New Zealand has risen to the challenge, however, and measures are being taken to control exotics and to conserve native species, including honeyeaters and the remaining mistletoes. No longer a mystery, the fallen flowers of Ohau have proved to be the warning sign of a disruption in a long-standing ecological relationship. That partnership must be revived if the newfound pollination phenomenon itself is to survive in New Zealand.

A Virginia native, Laura A. Sessions ("A Floral Twist of Fate" page 38) traveled to New Zealand in 1996 as a Fulbright scholar. She earned her master's degree in botany at New Zealand's University of Canterbury in Christchurch, studying the effects of introduced brush-tailed possums on New Zealand mistletoes. Along the way, Sessions notes, "I realized that I enjoy learning and writing about science more than I like actually doing it." She is currently pursuing a doctorate in science communication and the media, as well as continuing work on the effects of introduced animals in New Zealand. An "introduction" herself, Sessions says she has come to love New Zealand's "beautiful landscapes and relaxed pace of life."

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