Researchers at AAAS Pacific Division Meeting Explore the Startling Decline of a Hawaiian Native Bird

WAIMEA, Hawaii—The Hawaii akepa is a tiny bird, about the size of a small finch, and where its scarlet cousin the I'iwi is spectacular and another cousin, the akohekohe, is an amazing blend of black, red, and orange, the akepa's beauty is more humble. While the males are brilliant orange, the females feature more muted colors that blend into mountain forests.

For scientists who spoke at the recent annual meeting of the AAAS Pacific Division here, the akepa is nonetheless more remarkable for its unusual breeding cycle, the large size of its nestlings and other evolutionary traits. But the genius of evolution may not be enough to save the akepa.

The loss of forest habitat, attacks by introduced predators, competition from non-native birds, increased disease and parasites—in the past few years, some of these threats to Hawaii's native birds seemed to hit critical mass for the akepa. Leonard Freed and Rebecca Cann, who have spent almost 20 years studying birds on the slopes of the dormant Mauna Kea volcano, at a half-day symposium described scenes of avian desperation:

They found one male so weak that he needed oxygen to recover. Females foraged frantically in the mountain-forest canopy, then begged their mates for food until their voices failed. The gender of young akepas skewed strongly to males. Mortality rates among both fledglings and older birds spiked.

"Where have all the young girls gone?" asked Cann, a professor in the Department of Cell and Molecular Biology at the University of Hawaii at Manoa, trying to understand why young female akepa were suddenly in very short supply.

Further, asked Freed, where were the fledglings? "It wasn't due to chance that we didn't catch them," he said. "They simply weren't there." And among the few captured during later years, why were most underweight and exhibiting signs of stunted growth?

The case of the declining akepa is complex, but to Hawaiian researchers, it fits a familiar pattern: Though native birds, plants, and sea animals evolved and thrived in an isolated paradise for millions of years, the arrival of humans—and the resulting loss of habitat and introduction of new predators, competitors, and diseases—has put them in danger.

It was a recurring theme during the Pacific Division's annual meeting, attended by more than 330 researchers, educators and others from 15-20 June on the Island of Hawai'i (the Big Island) at the Hawaii Preparatory Academy. The meeting featured dozens of symposia, workshops, talks, and poster sessions, ranging across fields—from anthropology and biology to nanotechnology, pharmacology, and science education.

But much of the meeting focused on the health of Hawaii and other Pacific islands, and how they serve as an environmental barometer for the rest of the earth. There were sessions on the remote Palmyra Atoll, an outpost of biodiversity in the Central Pacific Ocean; the conservation of endangered Hawaiian land snails; the uncertain future of anchialine pools, the brackish shoreline waters that are home to rare plants and animals; and the impact of disease on Hawaiian corals, turtles, and other native species.

The akepa is not suffering alone, but to Freed, Cann and their colleagues, its demise is a conundrum of historic importance. If it succumbs to extinction, that's yet another sign that Hawaii's diverse ecosystems are approaching a tipping point that could, in time, point to dangers for a variety of other species, perhaps even humans.

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The Hakalau Forest National Wildlife Refuge was established in 1985, a 33,000-acre tract of rain forest extending from about 6000 down to 3000 feet on the windward slopes above the coastal city of Hilo. Cann and Freed, a wife-and-husband research team, first worked there in 1987; they built a field station there in the 1990s, to cooperate with the U.S. Fish & Wildlife Service in research and education. The akepa nests in the cavities of the large ohia and koa trees there, and it feeds on a variety of insects and spiders found in the forest canopy.

The refuge offers a close-up view of the struggles faced by Hawaii's native flora and fauna. Four endangered bird species live there, in addition to several species of endangered plants. But it is the only national wildlife refuge in the country in which endangered predators feed on endangered prey. Feral pigs and other destructive, non-native invaders have lived there, too.

Because the Island of Hawaii is only half a million years old, and most organisms on the refuge have relatives on older islands, Hakalau also affords researchers a view back in time, a perspective on how birds and other animals have evolved in the islands.

In her talk at the symposium, Cann said that the first ancestors of the Hawaii honeycreepers arrived around 5 million years ago, soon after the oldest main island of Kauai developed suitable habitat from colonizing plants, insects, and spiders. In time, the birds evolved and developed new species, adapting to the islands' many ecosystems and microclimates. Fifty-four separate species and subspecies of historically known honeycreeper emerged—including the akepa. The fossil record in Hawaii shows many more honeycreepers, including a relatively large one appropriately named the King Kong finch.

The honeycreepers are marvels of evolution to rival the finches that Charles Darwin studied on the Galapagos Islands. They come in a rainbow of colors. Some eat nectar; some eat seeds. Some eat snails, and most consume insects and spiders in every conceivable way. Their heads and bills have evolved to enable these feeding habits, which for the insectivorous species include insects on leaves, on bark, and inside of wood. Where some honeycreepers have bills that are long and curved or blunt as a parrot's, the akepa has a short bill that is laterally asymmetrical for prying open leaf-buds and seed pods in search of the prey within; their bills can also be used to glean insects and spiders on foliage and small twigs. Like the other honeycreepers, it settled into a niche where any competition it faced from other native species was sorted out long ago as part of the adaptive radiation.

But the arrival of Polynesians around 500 C.E. began an inexorable disruption of the natural balance that, over the next 1500 years, gave rise to a plague of threats to the native birds. The Polynesians captured some of the most brilliant birds and used their feathers for clothing and artwork, Cann said. Europeans arrived in the late 1700s, and over the years their farming, ranching, and logging operations leveled the forests. They brought rats and then, to control the rats, they brought in mongooses, which also dine on birds. They brought mosquitoes, which would eventually transmit avian malaria from introduced birds; they brought in pigs which escaped, and armies of feral pigs made wallows where more mosquitoes could breed. Then they brought in non-native birds such as the Japanese white-eye to control the bugs. In all, they brought in more than 150 species of non-native birds, for a range of purposes.

The cumulative effect: "Half of the native birds that we know of historically are extinct," Cann said at the symposium. "Of the half that remains, half are endangered. That's the bottom line."

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The Hawaii akepa was listed as endangered in 1970, but for a long time, not much was known about it. Cann, Freed and their colleagues at the Hakalau Forest Biological Field Station have done much to shed light on the life of the akepa and other native birds—and the impact of climate change, non-native intruders, parasites and disease.

They were the first to document an increase in avian malaria at upper elevations in birds, a glimpse into what might become more common with global warming. They also showed, with their student Jaan Lepson, that bright orange akepa males do not acquire that plumage until they are three years old. (They are interested in why males advertise their youth and inexperience to females for two years.)

Every year through July 2006, they used mist nets to catch and study birds in the research area; they banded them, examined them and sometimes took blood samples. In addition, they track the birds and study their nests.

What they've learned about the akepa's breeding cycle offers insight into the ingenious working of evolution.

The akepa produces one brood of 2 eggs per year. Reproduction and molting are times of high energy demand for birds; natural selection has especially guided birds to reproduce at times when the most food is available, and to molt following breeding. But in his presentation at the symposium, Matthew Medeiros, a graduate student and biologist at the Whitney Harris World Ecology Center at the University of Missouri-St. Louis, said the akepa defies that pattern: It reproduces at a time when its meal of choice—insects and spiders living in the forest canopy foliage—are declining. That, Medeiros said at the symposium, is "unprecedented."

But the Hakalau researchers found more surprises. The akepa nestlings weigh more than their parents. And the heaviest fledglings with the most fat have survival rates that match those of adult birds. Another secret of akepa's success was in the timing, Medeiros said: The young birds were making the transition to independence just as the population of young spiderlings in the canopy was at its height. They also found that the parents were molting most of their primary flight feathers while fledglings were still growing and food was at its seasonal low level. The hypothesis is that parents are banking their care in the bodies of their nestlings during a time of relative plenty for use by growing fledglings, while parents are molting during leaner times.

Beginning in 2000, the researchers began to see dramatic changes in the akepa's condition. From 2000 to 2003, the bird had lower nesting success, lighter weight nestlings, and no fledglings were captured in mist-nets, said Freed, an associate professor of zoology at the University of Hawaii at Manoa. Fledglings were observed but died months before the normal termination of parental care in 2002-2003. Of the few fledglings caught in 2004-2005, he said, most were underweight. Older akepas, too, seemed to be slowly disappearing, because there were too few young birds to replace the adults that died at the normal rate

In the same period, researchers noted another sign of trouble. Before 2003, ectoparasites such as mites and lice had been almost unheard of in 12 species of native and introduced birds in the area. But that changed beginning in 2003: Chewing lice were becoming rampant—it was "the most explosive increase of any parasite documented worldwide," said Gustav Bodner, a graduate student in zoology at the University of Hawaii. Many of the affected birds had "fault bars," or visible lines of weakening across their feathers. He also showed that for most species of native birds, individuals with lice were less likely to be recaptured in mist-nets.

The number of young females declined precipitously: Before 2000, 57% of the fledglings and second-year birds had been female; between 2000 and 2006, the number was 13%. Only the females in best condition were breeding successfully, and in the bird's evolutionary course, the researchers say, the most well-fed females tend to produce male offspring. The less well-fed females would be favored to produce daughters, which are smaller and less demanding to raise. Without a closer male-female balance, the bird would move steadily toward extinction.

In 2006, the akepa population in the Hakalau research area crashed. It was in that summer that the researchers saw clear signs of desperation among the birds—the loss of body fat, frantic foraging, spiking mortality. It got worse in 2008. When female akepa beg for food, Freed said, their call usually has two notes. But in that spring, the call sometimes reduced to one note. Most of the females were too weak to beg at all. Never before had they observed the akepa attempt to breed in almost total silence.

Hunger could help explain the increasing impact of parasites. "If birds are in poor condition for other reasons," Bodner said, "they might not be able to deal with lice." Similarly, he said, fault bars in a bird's wings indicate nutritive stress. Because the lice degrade body plumage, the birds require more food to replace the heat that is lost through that plumage.

Studies of two tracts on the Hakalau research sites showed the cumulative impact of these threats. In the long-term study site at 1900 meters (about 6200 feet), 71 adult akepa were banded or otherwise recognizable in 2005, but only 19 total birds were detected in 2008, a decline of 73%. In a second tract at an elevation of 1770 meters (about 5800 feet), 24 akepa were banded in 2005; by 2008, Freed said, only two were detected, a decline of over 90%.

Two other endangered Hawaiian birds—the akiapolaau and the Hawaii creeper—also were under severe stress between 2000 and 2008. The creeper disappeared from the 1770 m site and the akiapolaau disappeared from the 1900 m site in 2008. But among the akepa, the evidence suggested that it was on a one-way street to incipient extinction over a larger area.

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What was causing this destruction?

It wasn't the weather, Bodner and Freed agreed—temperatures and rainfall were not out of the ordinary in the years after 2000. It couldn't have been ectoparasites, Freed said, because half of the akepa that crashed didn't have them. And it wasn't pox virus, which causes a bird's bill to disintegrate at the base or for toes to fall off, because levels in 2005-06 were no different than in previous years.

But according to Cann and Freed, there was another critical factor at work: the Japanese white-eye.

A pretty yellow-green bird with a distinctive white ring around each eye, the white-eye is about the same size as akepa, and its beak is similarly suited for finding insects and spiders in the foliage. In fact, it had had been introduced in Hawaii in 1929 to help control insects. "Little did the people who brought it here know how well it could control insects," Freed said at the symposium. .

Beginning in 2000, Cann said, researchers noted a "substantial and steady" increase in the numbers of white-eye in the study areas. They had been present all along, while the akepa population was healthy. In a matter of a few years, Freed added, their numbers increased by 30%. And that meant that a niche occupied for millennia by the Hawaii akepa and its ancestors, with no competitors, suddenly had to be shared.

Circumstances favored the white-eye. They nest earlier than the akepa, and by the time they were done raising their young, Cann said, the akepa and its brood had only forest "leftovers" to eat.

The evidence, Freed said, pointed to one conclusion: "The white-eye are replacing the akepa."

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Hakalau Forest National Wildlife Refuge was created to protect native birds and plants, but ironically, the refuge has been taken over by a non-native bird and chewing lice. This may be a synergistic problem that will lead to extinction of many birds, because the lice increase food requirements while the white-eye makes less food available. And because the white-eye's feeding range and patterns overlaps with that of every other native bird species, its advances may also be involved with the decline of the endangered akiapolaau and Hawaii creeper.

While many introduced birds are taken for granted in Hawaii, Freed said that the plight of the akepa shows that introduced species can eventually cause major damage.

Now researchers are working to develop strategies for controlling the threats to akepa and other endangered birds, but options appear to be limited.

Bodner, for example, said that organic insecticides could be employed to control lice and mites with little impact on the environment. But this requires capturing individual birds in mist-nets and dusting them. Meanwhile, the akepa is being bred in captivity at a Hawaiian center affiliated with the San Diego Zoo.

Freed worries that it may be too late, but he sees some signs of hope.

In the three-year-study of akepa populations during 2004-2006, researchers found that fledglings at lower elevations—where there were fewer white-eye—weighed more. In other words, getting the akepa healthy requires getting rid of the white eye, or reducing its numbers to reduce competition for food.

The key, he says, will be to get federal wildlife officials to take action to control the white-eye population in the ecosystems that host the akepa.

After the AAAS Pacific Division's annual meeting closed last month, he said, the U.S. Fish and Wildlife Service indicated that it will convene a meeting soon on supporting the akepa. Success, Freed said, will require a perennial commitment to conserve native species. "At minimum," he said, "birds need to be in good nutritive condition to be able to mount immune defenses against diseases like malaria that are expected to increase in importance in the future."

One of the things Freed hopes to discuss at that meeting is how the captive breeding program—especially the breeding of females—could be critical to the akepa's long-term survival in Mauna Kea's forests. Captive females should be kept on a restricted diet. If they're allowed to eat as much as they want, "then their two-egg clutch will likely be all sons," he explained.

"Until the situation in nature improves with white-eye control, the population of female akepa will get older and more vulnerable to chronic food shortage. Young akepa females released from captive breeding could provide new blood and new energy for reproduction while we're working to restore the forest's natural balance."

Edward W. Lempinen

18 July 2008