AS our dugout canoe floats silently down a tributary of the Orinoco river in the llanos, the central plains of Venezuela, I realise we are being observed. The unblinking eyes of a large cayman rise above the muddy waters to study our boat, which carries six scientists and me. I shift uneasily, aware that our only defences are a catapult and plant clippers. But I鈥檓 in good company. Fabian Michaelangeli of the Venezuelan Institute of Scientific Investigations (IVIC) is a naturalist and experienced wildlife photographer. His colleagues, Maria-Gloria Dominguez-Bello and the ebullient American phytochemist Eloy Rodri麓guez, now of Cornell University, are also adept at life in the tropics.
Suddenly, pandemonium erupts as our canoe slips beneath overhanging branches. It is raining stinky cow birds. Unable to fly, chicks are dive- bombing into the river from nests overhead and swimming underwater, pulling themselves back onto the bank and up the trees monkey-style with pairs of clawed wing tips. One bird, however, parachutes directly into our canoe. I scoop the captive up and hold it at eye level.
The hoatzin (pronounced 鈥渨hat-seen鈥) chick 鈥 aka stinky cow bird or stinking pheasant 鈥 resembles a pubescent punk rocker, with a tiny mohican and a stubble of blue feathers beginning to fill in the face and neck. When the chick grows up, its body, from the neck down, will resemble a cross between a pheasant and a turkey, and its brown eyes will have turned red. But right now, its five tiny black tail feathers are splayed out indignantly like a miniature Indian headdress.
Advertisement
The chick does have one distinctive adult trait 鈥 the faint scent of cow manure. The source of this perfume is a pocket-like crop and oesophagus similar to the foregut of a cow. The crop serves as a fermentation 鈥渧at鈥, full of rich bacterial porridge that breaks down fibrous plant leaves into smelly, but nutritious volatile fatty acids that are absorbed in the intestine. This little detoxification tank allows the bird to do something extraordinary: it can digest plants that other birds 鈥 or mammals 鈥 would find poisonous.
From cuckoo to cow bird
The hoatzin (Opisthocomus hoazin a relative of the cuckoo) became an overnight celebrity in 1989 when a group of researchers, including Dominguez- Bello, reported in Science that it is the only known bird with foregut fermentation. This trait was previously confined to mammals such as ruminants, colobus monkeys, kangaroos and tree sloths. But little is known about the hoatzin or how it evolved from mere cuckoo to 鈥渃ow bird鈥. Hence the reason for capturing our two-week-old stinky cow bird, which has now buried its little mohican in my shirt pocket.
We head back to our headquarters at Hato Pin~ero, a cattle ranch and bird watching reserve, located in the state of Cojedes. Parrots parade up and down the TV antenna of the Pin~ero hotel, where researchers and bird- watchers mingle and swap tales about jaguars and capybaras, rodents the size of pigs. Down the road, a separate scientific research station is being built. Meanwhile, we make do with an abandoned souvenir shop, equipped with a dissecting table, specimen tubes, and an incubator to culture crop samples.
I reluctantly hand over the captive to be weighed and photographed, returning later to eye a test tube full of the leafy-green 鈥済oop鈥, fermented juices from the chick鈥檚 autopsied crop. 鈥淭his contains powerful bacterial degraders,鈥 exclaims Rodri麓guez, waving the test tube of fermented leaf matter in one hand, and in the other, a branch of partially nibbled leaves from nearby the hoatzin鈥檚 nest. The fibrous leaves belong to the poison ivy family, and contain nasty-tasting tannins and other compounds which are notoriously hard to break down. 鈥淟ook,鈥 points out Rodri麓guez, 鈥渋t reduced them to a liquid pulp just like a kitchen blender鈥.
Rodri麓guez, professor of environmental biology at Cornell University, is best known for his work in the field of zoopharmacognosy, the study of how animals use pharmacologically active plants. Michaelangeli is chief of the IVIC鈥檚 gastrointestinal laboratory; his associate researcher, Dominguez-Bello, is a rumen microbiologist. The rest of the IVIC crew includes a botanist, a biologist and a digestive physiologist.
As the sun disappears over the hilltop and our working light fades, the discussion continues over dinner. In spurts of Spanish and English, the group explains the importance of the hoatzin goop; if these bacterial and enzyme degraders could be identified, they could be cultured or genetically manipulated for a variety of purposes such as mopping up oil spills or 鈥渆ating鈥 toxic industrial by-products.
Livestock farmers may also benefit from studies of hoatzin digestion. 鈥淢any tropical countries, including Venezuela, cannot use their own forage 鈥 rich in nutrients but toxic 鈥 and must rely on expensive imports of soya beans to feed cows, pigs, sheep and chickens,鈥 says Dominguez-Bello. 鈥淚f we could identify the degraders, we could inoculate the animal or treat the forage, so the toxins could be broken down before passing through the animal鈥檚 digestive system.鈥
One immediate recipient for the hoatzin 鈥渟uper鈥 degraders might be the Pin~ero cattle, some of which dine regrettably on a toxic legume during the rainy season, resulting in paralysis and death. Transferring a toxin degrader from the stinky cow bird to a Pin~ero steer isn鈥檛 a tall order. Recent research advances have made digestive toxin degraders a valuable commodity (see: 鈥淎 new trend: digestive toxin degraders).
By sunrise the next morning, we find ourselves floating down another muddy river, collecting older chicks along with specimens of their leaf diet. The vegetation of the llanos, flush during the rainy season, teems with powerful chemical defences. Many of these species contain harmful alkaloids, hormones and toxic amino acids that often poison domestic ruminants and other animals. Yet here is a bird that has evolved an ecosystem within itself, a bacterial symbiont to not only counter, but to use these chemical factories to its own benefit. As with the most complex ecosystems, the stinky cow bird, its bacterial symbiont and the environment are inexorably linked, says Dominguez- Bello. 鈥淭he hoatzin must eat to nourish and feed the bacteria, which enables the bird, which flies poorly, to exploit and detoxify nearby food sources and produce needed nutrients.鈥
Toxic advantage
Coincidentally, perhaps, this toxic palate offers additional advantages to the bird. The evidence 鈥 a pile of leafy branches in the bottom of our boat. Lecythidaceae or monkey cap, as it鈥檚 more commonly known, says Rodri麓guez, contains powerful antifungal and antiparasitic compounds. Many parasitic worms are the scourge of birds, typically robbing the host of important nutrients. But autopsies show that the hoatzin鈥檚 intestine and crop are completely free of parasites and fungi.
Returning to New York City, I have plenty of time to think about this quirky evolutionary mix of bird and cow. The hoatzin is thought to have evolved independently of ruminant mammals, yet it has a cow-like fermentation system. How can that be? As it turns out, the green goop holds some of the answers to this mystery. Studies by two different groups of researchers, only recently published, now suggest that the fermentation systems of the hoatzin and ruminant mammals 鈥渃onverged鈥 somewhere on the evolutionary ladder.
In the Journal of Comparative Physiology B, Dominguez-Bello and her IVIC colleagues report that the hoatzin鈥檚 appearance in Argentina at least 25 million years ago coincided with the expansion of grasses and ruminant mammals with primitive foregut fermentation systems. They further report that although the bird鈥檚 crop contains avian bacteria, there are striking similarities between the bacterial broths and fermentation chambers of the hoatzin and that of ruminant mammals. The hoatzin has similar types of bacteria and protozoa, which help ruminants digest food and which are not found in the crop of other birds. These dietary characteristics, which helped early herbivores (hindgut fermenters) overcome the chemical defence system of plants around 50 million years ago, required an enlarged gut that became a fermentation chamber, the IVIC scientists explain. For this purpose, herbivore mammals adapted a foregut; the hoatzin, an enlarged crop. This evolutionary exchange, however, shifted the high energy requirements needed for flying to the hoatzin鈥檚 detoxification tank.
Even more intriguing is a paper to be published in this month鈥檚 issue of Molecular Biology and Evolution, which reports that the hoatzin and ruminant mammals share a functional version of the common enzyme lysozyme. 鈥淧rimitive ruminant mammals recruited lysozyme 鈥 believed to be an ancient antibacterial agent that is found in most animals, eggshells, human tears and saliva 鈥 for digestive purposes,鈥 says Janet Kornegay who wrote the report when she was a postgraduate student at the stomach lysozyme laboratory of the University of California at Berkeley.
Tricky ancestry
Later, at least 25 million years ago, Kornegay explains, the hoatzin managed the same evolutionary trick by carrying within its lysozyme some of the same evolutionary codes necessary to convert an enzyme to a digestive function. This finding is all the more remarkable, she adds, because the hoatzin鈥檚 calcium binding lysozyme has been genetically separated from the conventional form found in mammals some 300 million years ago 鈥 the results of a gene duplication that predates the divergence of birds and mammals. Little is known, however, about the calcium-binding lysozyme (for example, a non- digestive variety is found in pigeon egg white), or why the hoatzin is the only known bird to carry the stomach version. But whether the avian-lysozyme link will be followed up is debatable; the University of California recently closed its lysozyme laboratory following the death of its principal investigator, Allan Wilson.
鈥淭his study is a real jewel, as there are very few examples of different genetic backgrounds producing functionally similar enzymes,鈥 explains Alejandro Grajal, senior author of the original Science article that identified the hoatzin鈥檚 foregut fermentation, and director of Latin American programmes for the New York Zoological Society鈥檚 Wildlife Conservation Society.
It is now about three years since my visit to Venezuela, and the IVIC researchers are still untangling the maze of hoatzin dietary toxins and degraders. I鈥檓 sitting in Grajal鈥檚 office, located within the Bronx Zoo Wildlife Conservation Park in New York City. Grajal oversees the only hoatzin group outside of the wilds of South America. I鈥檓 curious to find out how the stinky cow bird has adapted to city life since its arrival in late 1989.
Sensitive subjects
Grajal escorts me to the aquatic bird house. The exhibit features a bamboo curtain with slats for the peering eyes of the public. Behind it, hoatzin dine on a salad of chemically rich young greens as a rainy mist falls (it is, after all, the rainy season in Venezuela). Nearby, the zoo staff have built several twig nests in anticipation of next May, the beginning of the mating season.
For the most part, the public bypasses the hoatzin. That suits the birds just fine 鈥 they are very sensitive, as it turns out, to changes in personnel, food, temperature and lodging. The birds even peck at one another, Grajal suspects, because of territorial disputes.
鈥淥ther zoos have their pandas, but nothing compares to keeping hoatzin,鈥 says Grajal. It took Grajal and chief zoo nutritionist, Ellen Dierenfeld, 11 months to slowly shift the balance of the bird鈥檚 bacteria population to accommodate the chemistry of young dandelion and mustard greens, kale, and romaine lettuce.
鈥淏ut does the hoatzin still smell?鈥 I ask. 鈥淥h yes,鈥 answers Dierenfeld, explaining that 鈥測ou can change the diet of a cow and it will still smell like a cow.鈥 Ruminants will still produce the same volatile fatty acids as smelly fermentation by-products. The same holds true for hoatzin 鈥 it鈥檚 still all 鈥渂arnyard鈥. Understanding the relationship between the bird and its bacterial symbiont is crucial to the hoatzin鈥檚 quality of life in captivity. And it took about 60 years, points out Grajal, for zoos to figure this out 鈥 previous feeding attempts included banana and meat balls.
Before I left, I read the descriptive plaque adjacent to the exhibit. Nowhere does it mention the hoatzin鈥檚 stinky disposition. Grajal explains that the hoatzin has so many other interesting characteristics, that to mention its smell 鈥渨ould diminish the bird鈥. Politically correct, perhaps, but it鈥檚 ironic that hoatzin perfume 鈥 the very trait that the zoo seeks to minimise 鈥 has already yielded valuable evolutionary insights and may turn out to herald other important scientific discoveries.
A new trend: digestive toxin degraders
DIGESTIVE toxin degraders are the latest buzz word in ruminant research circles, with applications in all sorts of areas: ranching, poison control, medicine and environmental clean-up operations. Prior to the 1970s, however, rumen bacteria were seen as a 鈥渂lack box鈥, a biological oddity.
That view changed with the revelation that rumen fermentation systems are great detoxification chambers, able to break down a dazzling array of complex compounds, including some that poison domestic animals. Then in the last decade, research showed that 鈥渞uminant microbial populations could be manipulated to enhance the rate of toxin degradation鈥, says rumen microbiologist Milton Allison, who pioneered this research. He works at the National Animal Disease Center (NADC) in Ames, Iowa, and is professor emeritus at Iowa State University.
The classic example that all rumen researchers like to cite is that of leucaena, a tropical shrub imported to Australia many years ago. It contains a toxic amino acid that breaks down into deadly dihydroxypyridine (DHP). About a decade ago, a researcher discovered that Hawaiian goats (actually an Asian species) could safely munch on leucaena; in Australian goats, this had fatal results. It transpired that the Hawaiian goat carried a protective bacterial degrader for DHP (a newly identified species called Synergistes jonesii) that protected the host animal. Later, the degrader was cultured and injected into the guts of Australian goats and sheep, which can now forage safely on leucaena. This has turned out to be an inexpensive inoculation process, as the degrader is passed naturally from animal to animal through food, water, air and faeces. Very good news for developing nations, but not for companies that can鈥檛 bank on patent rights. 鈥淎fter that discovery, financial interest dropped,鈥 says Mark Rasmussen, a research microbiologist at NADC, 鈥渂ut that may change now that rumen bacteria can be genetically engineered鈥.
Last April, Australian scientists at the University of New England鈥檚 Institute of Biotechnology announced that they had designed a rumen bacteria that detoxifies deadly fluoracetate, found in native foraging plant such as gidgee and heartleaf. In the study, test animals were inoculated and now safely forage on these plants, which cover vast areas of Queensland and cost ranchers millions of dollars. Before inoculation can be routinely implemented, a government oversight committee must be assured that the engineered rumen bug won鈥檛 disturb the fragile ecosystem. Researchers will have to prove by tracking their genetically altered bacterial degrader that it cannot exist outside the rumen where it might transfer its resistance to the micro- organisms carried by insects, which could then attack the forage.
As researchers such as Allison have gradually unravelled the intricate relationship between a ruminant, its symbiont and the environment, this information has had an immediate and positive financial impact on the cattle industry, which ultimately would like to wean livestock off grain and onto natural forage. Grain is costly, and taxes the environment. For example, American ranchers first introduce cattle to forage that contains low levels of oxalate, thus boosting their bacterial population of protective oxalate degraders. Only then are the ruminants exposed to forage with higher oxalate levels. In a similar vein, other researchers have found that sheep in the Appalachian region of the eastern US carry the specific degrader for a somewhat toxic forage legume, the flatpea. Alter their diet, however, and the sheep become susceptible to flatpea intoxication and death.
Research on rumen oxalate degraders, says Allison, has also led to a rethinking of a human problem 鈥 kidney stones. 鈥淭here鈥檚 some evidence that humans are colonised with oxalate degraders, which may limit absorption of dietary oxalate [found in greens].鈥 If this is true, he adds, oxalate could be a factor in the development of kidney stones. German studies, for example, found that people who repeatedly suffered from kidney stones did not carry the oxalate degrader; those that did were free of attacks. But the research isn鈥檛 conclusive, Allison points out.
In the area of environmental clean-up, Dutch scientists are researching the effectiveness of digestive bacteria in detoxifying tea by-products such as tannin. Manufacturers in India routinely dump the toxin in rivers, causing environmental havoc. Venezuelan rumen microbiologist Maria-Gloria Dominguez- Bello believes the hoatzin鈥檚 tannin degraders could be used for this purpose.
Lack of research funds, however, plagues the field. The Queensland ranchers had to rustle up most of the funds for research on the gidgee degrader. And the US Department of Agriculture鈥檚 Poisonous Plants Research Laboratory, says research leader Lynn James, lacks adequate staff to pursue the potential of rumen degraders.