It was the week before Christmas, and mistletoe in full flower wrapped the upper branches of a regal old beech tree in a blaze of scarlet. The spiky blooms jutted out from the dark green foliage like red coronets, and at the foot of the tree the ground was a carpet of fallen jewels.
I had spotted the tree from the turnoff to Blackball, inland from Greymouth, on the South Island’s West Coast. Blackball is a town normally associated with coal, salami and a quaint old hotel called Formerly the Blackball Hilton (see New Zealand Geographic, Issue 47). But none of these features had drawn me there. I was in the South Island to find out why our native mistletoes are in decline—a puzzle which has turned out to be the ecological equivalent of a murder mystery.
New Zealand has eight native mistletoe species, seven of them endemic and one found also on Norfolk Island. A ninth species, also endemic, was last seen in the 1950s and is presumed extinct (see sidebar, page 88). Three of our mistletoes—the red, scarlet and yellow mistletoes—bear flowers that are among the most vivid and spectacular in our native flora. Indeed, a spray of scarlet mistletoe, Peraxilla colensoi, was chosen to grace our former $2 note—the only time a threatened plant has been depicted on our currency. That note is now a relic, and scarlet mistletoe, in common with several other of our native mistletoes, is in danger of following suit.
Mistletoes are partial parasites, or hemiparasites, in that they carry out their own photosynthesis but rely on their hosts for water and minerals. Seed dispersal is thus a critical phase of their life cycle: unless a mistletoe seed lands on an appropriate host, it will not develop into a new plant.
Tui, bellbirds and silvereyes are the main dispersers of the pea-sized fruits of Peraxilla mistletoes—the main focus of this story—although kereru, blackbirds and yellowheads have also been observed eating the berries. During its passage through a bird’s gut, the fruit’s tough outer skin is removed, exposing a gluey layer surrounding the seed, which sticks to whatever the seed lands on. If that happens to be a young branch of a suitable host, the seed is in luck. It sends out a specialised rootlet which penetrates the bark and taps into the host’s vascular system.
Unlike many overseas mistletoe species, New Zealand mistletoes do not generally harm their hosts, probably because they grow extremely slowly. For example, the stems of two-year-old plants are rarely longer than 15 mm. Such glacial growth means mistletoes are especially vulnerable to herbivore browsing and other physical damage in their early years, but should a plant survive this period it could live for decades.
However, few mistletoes now get that chance. To appreciate the extent of the decline, one need only read the accounts of 19th-century botanists. In 1884, Henry Claylands Field, an amateur plant collector, wrote that near Raetihi, on the Central Plateau, red mistletoes, Peraxilla tetrapetala, “form large bushes in tops of trees, and blossoms are so abundant as to almost hide the foliage. Fully 10 per cent of the large trees have one or more Loranthus [mistletoe] growing on them. When cutting a line for the Wanganui–Taupo road, in September and October 1882, my men felled many trees on which the plant was growing.”
Today, only a few dozen stands of red mistletoe endure in this vast area, and each stand supports only a handful of plants. What can account for such a dramatic reduction in numbers? Until recently, the prime suspects in the disappearance of mistletoe were possums, habitat loss and over-collecting. Each, without doubt, has been partly to blame, but studies by a team of researchers including Jenny Ladley and Dave Kelly from the University of Canterbury and Alastair Robertson from Massey University suggest other villains are implicated in the plants’ demise.
I looked up at the handsome crown of scarlet mistletoe in the branches of the Blackball beech tree, then down at the fallen flowers lying strewn across the moss-covered roots. Most people would not have noticed anything amiss in this floral red carpet, but I had been alerted to a true botanical oddity lurking there. In the flowers, I had been told, was a clue to the demise of mistletoe—a clue that had baffled investigators for years.
I knelt down to look more closely, and noticed that in many of the fallen blooms the petals had opened from the bottom upwards rather than the top downwards (see photograph opposite). As a result, the stigma—the receptacle for pollen—had not been exposed to the outside world and had thus been unable to be pollinated. For pollination to occur (and hence fertilisation and the propagation of the species), mistletoe flowers must open from the top, exposing the stigma and pollen-coated anthers. But only one in 10 of the flowers I saw had opened in this way.
Why would a plant put so much energy into producing flowers which, nine times out of 10, exclude pollinators? “We cannot even guess at the meaning of this strange performance,” admitted international mistletoe expert Job Kuijt, of British Columbia, in his 1969 book on mistletoes of the world.
Little real progress had been made toward solving this puzzle before Jenny Ladley started to study the Peraxilla mistletoes for her master’s thesis in 1992. “I wanted to find out what was pollinating these mistletoes, and whether the pollination was successful,” she told me.
First, she set up a control experiment in which she put mesh bags over unripe scarlet mistletoe buds, to exclude pollinators such as insects or birds. She intended to hand-pollinate the flowers as they ripened and then estimate seed production.
To her surprise, the buds ripened but failed to open, preventing her from gaining access to the stigma and thus foiling her experiment. “I was sitting under the tree on Christmas Eve, asking myself what I was doing wrong, when I noticed a tui in the mistletoe. The penny dropped. The flowers were being opened—and probably pollinated—by birds.”
But how? To see the process for myself, I rigged up a rope and jumar and hoisted myself into the beech branches. I didn’t have long to wait before a tui arrived. From just metres away, I watched it jump from twig to twig, checking the ripeness of the mistletoe flowers. (Researchers believe the birds can tell which flowers are ripe by their colour. When a flower is ripe, a bulge at the end turns pink.)
When it found a ripe flower, the tui grabbed the tip in its beak and gave it a squeeze. The four petals instantly sprang open, flicking pollen from the ripe anthers on to the tui’s head and giving the bird access to a pool of nectar inside the base of the flower.
Ladley says that when a tui reaches in for its nectar “reward” it usually brushes against the anthers and gets even more pollen on its head. When it visits another flower, some of this pollen is transferred to the stigma, at the tip of the pistil, which sticks up from the centre of the flower like an aerial. This contact initiates the process of fertilisation and fruit formation.
Ladley realised that the top-opened flowers she was seeing on the ground had been sprung by birds, while bottom-opened and unopened flowers had not been visited or pollinated.
The discovery was unexpected because none of the other Australasian mistletoes, nor any other New Zealand in this vast area, and each stand supports only a handful of plants. What can account for such a dramatic reduction in numbers? Until recently, the prime suspects in the disappearance of mistletoe were possums, habitat loss and over-collecting. Each, without doubt, has been partly to blame, but studies by a team of researchers including Jenny Ladley and Dave Kelly from the University of Canterbury and Alastair Robertson from Massey University suggest other villains are implicated in the plants’ demise.
Native flower, shares this method of pollination, which relies on the tripping of a spring-loaded petal arrangement. Several hundred African mistletoe species have such flowers, which botanists refer to as “explosive” because of the way they burst open and catapult pollen on to the head of the visiting bird, but the phenomenon was unknown in this part of the world.
Bird pollination itself is not unusual in New Zealand. Our three species of honeyeater—tui, bellbird (korimako) and stitchbird (hihi)—all pollinate a range of flowering native plants, including pohutukawa, flax, kaka beak, fuchsia and kowhai. (The stitchbird, however, is now extinct on the mainland and confined to offshore islands—see New Zealand Geographic, Issue 53). Despite the presence of these birds, New Zealand is not well supplied with pollinators, notes Laura Sessions, another member of the Canterbury mistletoe research group. “Only seven bird, one bat, 16 butterfly and about 40 native solitary bee species serve New Zealand’s flowers,” she wrote in an article in Natural History magazine. “Australia, in contrast, is home to about 3000 bee species and 110 bird species that are active pollinators.
“Consequently, most New Zealand flowers either attract a range of pollinators . . . or are self-fertile (that is, able to produce fruits without pollen from another plant). Red and scarlet mistletoes’ dependence on a few savvy birds came as a surprise.”
Why would a plant develop such specialised pollination? “This isn’t known for sure,” Kelly told me, “but there could be an advantage to the plant in having flowers which remain shut until the right pollinator comes along. A closed flower will protect pollen and nectar from wind, rain and the wrong kind of nectar gatherer—the sort that could take the nectar without doing the job of pollination. For the right kind of pollinating bird—a tui or bellbird—a sealed flower is a tamper-proof container holding an assured reward: a sip of high-energy nectar. For the birds, triggering sealed flowers is an efficient way of foraging—they learn not to waste their time on already opened flowers, where the nectar may have been taken.”
From my perch in the branches I noticed that tui weren’t the only creatures working the mistletoe flowers. Bellbirds were there, too—a surprise, because I had been told that bellbirds are not generally found in the same tree as tui, as the latter chase them away. The bellbirds were so well camouflaged and secretive I hadn’t noticed their presence, even after two days of tree-sitting.
Once I knew bellbirds were around I started looking for signs that would give them away. I began to notice isolated twigs jerking or plant debris falling inexplicably out of dense foliage. Bellbirds seemed to be hiding in the denser parts of the tree and avoiding exposed edges; probably keeping out of sight of tui.
One morning, after enduring five consecutive cold, damp, overcast days, I awoke to crisp, clear conditions. I climbed to my observation perch and waited for the first bird of the day to show itself. As the air warmed I noticed tiny native bees biting the tips of the mistletoe flowers and occasionally triggering the explosive mechanism.
I had read that several species of native bee had been observed opening the smaller red mistletoe flowers, but that scarlet mistletoe flowers were too stiff and large to be activated by bees. Yet here it was happening right in front of me.
In the intervals between bird visits I turned my attention to the bees. Their method of opening the flowers was to pry the petals apart until the gap was just wide enough for them to slip inside. This action triggered a partial release, with about a third of the flower being exposed.
According to Kelly and Ladley, this partial opening may be another of Peraxilla’s adaptations to its pollinators. If bees popped the petals wide open, as birds do, pollination would be a hit-and-miss affair because the bees are so small (less than 10 mm in length) they might gain access to the pollen without necessarily touching the stigma. A partial opening provides a gap just wide enough for a bee to push into, but narrow enough to make it likely that the bee will brush against the stigma while harvesting pollen from the anthers. A bee-triggered flower usually opens fully somewhere between a few seconds and several hours after the initial visit.
It can take a native bee several minutes to pry a mistletoe flower open, and bees succeed in opening only about one flower in 20 they visit. These bees do not make honey, so they are not interested in collecting nectar though they may sip some to supply their own energy needs. They gather the protein-rich pollen to feed their larvae.
Introduced bees have not learned the trick of opening Peraxilla flowers, and neither have most introduced birds, although chaffinches and silvereyes have been observed opening mistletoe flowers, and bumblebees trip the occasional flower by accident. A hailstone or twig striking the tip of a flower may also be enough to trigger the opening mechanism.
From experiments conducted by the Canterbury group, it seems that a native bee visiting a mistletoe flower will deposit about the same number of pollen grains on the stigma as a bird will in a single visit. But because bees open far fewer flowers than birds do, they are thought to be less important pollinators than birds.
On the other hand, if bird numbers are low, bees may provide enough pollination to maintain seed production. And when they do succeed in opening a flower, that flower can be visited later by other insects and birds, providing a pollination benefit to the plant.
In the new year, I joined Kelly and Ladley in Craigieburn Forest Park, in the foothills of the Southern Alps, site of their ongoing investigation into mistletoe pollination. The floral litter beneath red mistletoe bushes in the beech forest here indicated that these plants were suffering a level of pollination failure similar to that of the scarlet mistletoe at Blackball.
Tui are absent from Craigieburn, so bellbirds are the prime pollinators. But are they present in sufficient numbers to service the area’s mistletoes? As Kelly remarked, “Most of us assume bellbird populations are in good health because we see the birds regularly, but no one has really examined what state they are in.”
During the summers of 1999–2001, the group began testing the hypothesis that low bellbird numbers were contributing to mistletoe decline. Experiments conducted at seven sites in the central Southern Alps showed that plants exposed to birds and bees produced scarcely more fruit than plants from which pollinators were excluded, implying that the pollinators were either so scarce or doing such a bad job that they could not lift the pollination rate above that of self-pollination. (Between 2 and 20 per cent of flowers set fruit by self-pollination, while bird pollination lifts fruit set to 35–60 per cent.*)
Self-pollination in Peraxilla is thought to occur when a bottom-opened flower, detached from its base, slides off the plant. The stamens, attached to the petals, will be pulled past the stigma, which remains on the plant, perhaps allowing pollen transfer and fertilisation. Self-pollination is likely to produce fewer, less viable seeds than cross-pollination, and, over time, may have negative genetic consequences for a population.
A third possibility, that the pollinating birds were choosing other foods that are energetically more valuable to them than mistletoe flowers, was tested by another member of the team, David Murphy. He examined bellbird diets and found that during the flowering and fruiting seasons bellbirds favoured mistletoe over other food sources. “So we can say that low bellbird numbers are the likely cause of pollination failure in mistletoe in Craigieburn,” he said.
Is this reduction in bird numbers a recent phenomenon, wondered the Canterbury researchers? Alastair Robertson decided to go back to Henry Field’s 1884 report on mistletoe on the Central Plateau. “Crucially,” Robertson says, “the report notes that ‘P. tetrapetala [red mistletoe] open very peculiarly. A small proportion (certainly less than a tenth) open from the apex downwards, whereas the rest open from the bottom.’
“We know the bottom-opened flowers have not been visited by a pollinator, and thus we can infer that even in the early 1880s, over 90 per cent of P. tetrapetala flowers were not being pollinated. This pollination failure coincided with a major decline in bird densities on the mainland at that time.”
Bird decline in the late 19th century was widely reported. Sir Walter Buller noted that bellbirds virtually disappeared from the North Island between 1860 and 1870. Tui suffered similar depletion. Thirty years later, a comparable decline took place in the South Island. Buller reported that the decline in tui and bellbirds coincided with the spread of ship rats and stoats. Although both birds have recovered to a certain extent, high-density populations are today associated only with areas free from predators, such as offshore islands.
The Canterbury researchers began to suspect that by killing bellbirds, these predators were having as great an impact on mistletoe as browsers such as possums were having. The depredations of possums on mistletoe are well known, but are thought to vary in seriousness from place to place.
“In the North Island there is no doubt that possums cause extensive damage to mistletoe,” said Kelly. “Undertake possum control and the mistletoe bounces back. But in the South Island there are a lot of sites where, for some reason, mistletoes don’t seem to be as high on the possums’ list of preferences. They get nibbled now and then but they don’t get obliterated. Some dense mistletoe populations exist in areas long inhabited by possums, while other mistletoe populations have declined in the absence of possums.”
How do predators fit in to this picture? To study the effect of stoats, a suspected predator of bellbird chicks, Kelly’s group set up two study sites during the summer of 2000–2001. At one, near Broken River, stoats were trapped, while at Mt Cheeseman no trapping was carried out. At the Broken River site 22 stoats were caught and there was an 84 per cent nest success rate. At Mt Cheeseman, only 18 per cent of nests were successful.
“We started trapping in September, and by January there were 80 per cent more bellbirds in the treated area,” says Kelly.
Despite the increase in bellbird numbers, however, mistletoe pollination in the area did not improve. “That was a really low-flowering year,” said Kelly, “and even a small number of birds could have got around all the flowers.
“We repeated the study in 2001–2002 and caught 11 stoats. But I don’t think we are going to be able to show statistically that increased bellbird numbers have led to increased pollination this time either, even though it was a much higher-flowering year than last year.”
While Kelly and his crew await the results that will prove the link between predation and pollination, other researchers are convinced that poor seed dispersal is at least as important in explaining mistletoe decline. In the central North Island, for example, mistletoe fruits have been known to fall to the ground and rot for want of dispersing birds.
Peter de Lange, a botanist with the Department of Conservation, and Brian Molloy, of Landcare Research, argue that, low as it is, self-pollination is sufficient to maintain an adequate seed supply, and that dispersal is the bigger issue. But even dispersal, they say, is primarily a problem in deep forest. “Around the edges of forests, as well as in many rural and urban areas, such as around Dunedin, and along roads—the Arthur’s Pass road is a classic example—introduced birds are spreading mistletoe very effectively, and in these places red and scarlet mistletoe are on the increase,” says de Lange.
“What it comes down to,” says Suzan Dopson, writer of DoC’s mistletoe recovery plan, “is that several things—habitat loss, the loss of native pollinators and dispersers and the effects of herbivores—are causing mistletoe decline, but they vary in importance around the country. The long-term survival of mistletoe requires us to address all these problems.”
My last day in Craigieburn held a surprise. I wanted to get an early start, so I climbed to my observation point at about 6 A.M. Soon after settling down I heard the familiar screech of a kea. Nothing much was happening in the mistletoe so I was glad of some kea entertainment.
Two kea flew into the tree and began biting through some brittle twigs with their secateur-like beaks and dropping them on me. Unlike the shy bellbirds, these noisy parrots seemed unconcerned by my presence.
One of them dropped into the mistletoe at my eye level. Then, to my surprise, it took the end of a flower in its beak. Instead of biting hard, it squeezed gently. Using its tongue, it rolled the flower forward and back against the inside upper curve of its bill, instantly triggering the explosive mechanism. It then inserted its tongue into the pool of nectar.
The kea’s method of opening the flower was quite different from that of the bellbirds and tui, which twist and tug the flower tip to release the petals. After opening a dozen or so flowers in leisurely fashion, the kea looked up and knocked its head into a small bunch of mistletoe blossoms. This seemed to amuse it, because it repeatedly butted the flowers as if heading a soccer ball.
Tiring of the game, the bird went back to opening flowers. It opened at least 20 in two minutes before flying off. Was pollination happening here? It was hard to tell, but I couldn’t help wondering how many more surprises our mistletoes might have in store.
Nor could I avoid a feeling of concern over the future of these extraordinary plants. Of our remaining native mistletoes, it is the bird-pollinated ones—the two Peraxilla species and Alepis flavida, the yellow mistletoe which have suffered the greatest decline. They are not yet considered endangered, but over much of their former ranges, where once they were plentiful, these plants are now rare.
Studies of historical paintings and herbarium sheets of the extinct Trilepidea adamsii suggest to Kelly that its flowers were explosive and even more specialised than those of Peraxilla. “Perhaps Trilepidea was even more sensitive to the drop in native bird numbers that occurred from the late 19th century onwards,” he says.
Yellow mistletoe has proved less vulnerable to bird decline because its flowers are less specialised: they open unassisted, allowing many different birds and insects to distribute their pollen. Also, they routinely self-pollinate if no birds or bees come to visit, so at least some seeds are always produced.
Peraxilla mistletoes, however, are more susceptible to fluctuations in the populations of tui and bellbirds. Every day in Blackball, as I watched hundreds of unopened or bottom-opened buds drift to the ground, it was obvious that the remaining birds were just not up to the pollination task.
Kelly, Ladley and their colleagues have clearly implicated predators of birds—especially stoats—as important suspects in the case of the disappearing mistletoes. We have known for a long time that such predators were responsible for the decline of our endemic fauna, but their role in the decline of plants has been less obvious. Now it is clear that controlling these pests will not just bring back the birds and their songs, but also help keep mistletoe’s brilliant blooms in the forest canopy.