The highly lethal form of avian influenza circulating the globe since 2021 has killed tens of millions of birds, forced poultry farmers in the United States to slaughter entire flocks and prompted a brief but alarming spike in the price of eggs.

Most recently, it has infected dairy cows in several states and at least one person in Texas who had close contact with the animals, officials said this week.

The outbreak, it turns out, is proving to be especially costly for American taxpayers.

Last year, the Department of Agriculture paid poultry producers more than half a billion dollars for the turkeys, chickens and egg-laying hens they were forced to kill after the flu strain, H5N1, was detected on their farms.

Officials say the compensation program is aimed at encouraging farms to report outbreaks quickly. That’s because the government pays for birds killed through culling, not those that die from the disease. Early reporting, the agency says, helps to limit the virus’s spread to nearby farms.

The cullings are often done by turning up the heat in barns that house thousands of birds, a method that causes heat stroke and that many veterinarians and animal welfare organizations say results in unnecessary suffering.

Among the biggest recipients of the agency’s bird flu indemnification funds from 2022 to this year were Jennie-O Turkey Store, which received more than $88 million, and Tyson Foods, which was paid nearly $30 million. Despite their losses, the two companies reported billions of dollars in profits last year.

Overall, a vast majority of the government payments went to the country’s largest food companies — not entirely surprising given corporate America’s dominance of meat and egg production.

Since February 2022, more than 82 million farmed birds have been culled, according to the agency’s website. For context, the American poultry industry produces more than nine billion chickens and turkeys each year.

The tally of compensation was obtained by Our Honor, an animal welfare advocacy group, which filed a Freedom of Information Act request with the U.S.D.A. The advocacy organization Farm Forward collaborated on further analysis of the data.

The breakdown of compensation has not been publicly released, but agency officials confirmed the accuracy of the figures.

To critics of large-scale commercial farming, the payments highlight a deeply flawed system of corporate subsidies, which last year included more than $30 billion in taxpayer money directed to the agriculture sector, much of it for crop insurance, commodity price support and disaster aid.

But they say the payments related to bird flu are troubling for another reason: By compensating commercial farmers for their losses with no strings attached, the federal government is encouraging poultry growers to continue the very practices that heighten the risk of contagion, increasing the need for future cullings and compensation.

“These payments are crazy-making and dangerous,” said Andrew deCoriolis, Farm Forward’s executive director. “Not only are we wasting taxpayer money on profitable companies for a problem they created, but we’re not giving them any incentive to make changes.”

Ashley Peterson, senior vice president of scientific and regulatory affairs at the National Chicken Council, a trade association, disputed the suggestion that the government payouts reinforced problematic farming practices.

“Indemnification is in place to help the farmer control and eradicate the virus — regardless of how the affected birds are raised,” she said in an email. The criticisms, she added, were the work of “vegan extremist groups who are latching on to an issue to try and advance their agenda.”

The U.S.D.A. defended the program saying, “Early reporting allows us to more quickly stop the spread of the virus to nearby farms,” according to a statement.

Although modern farming practices have made animal protein much more affordable, leading to an almost doubling of meat consumption over the past century, the industry’s reliance on so-called concentrated animal-feeding operations comes with downsides. The giant sheds that produce nearly 99 percent of the nation’s eggs and meat spin off enormous quantities of animal waste that can degrade the environment, according to researchers.

And infectious pathogens spread more readily inside the crowded structures.

“If you wanted to create the ideal environment for fostering the mutation of pathogens, industrial farms would pretty much be the perfect setup,” said Gwendolen Reyes-Illg, a scientist at the Animal Welfare Institute who focuses on meat production.

The modern chicken, genetically homogenous and engineered for fast growth, compounds those risks. Selective breeding has greatly reduced the time it takes to raise a barrel-breasted, table-ready broiler, but the birds are more susceptible to infection and death, according to researchers. That may help explain why more than 90 percent of chickens infected with H5N1 die within 48 hours.

Frank Reese, a fourth-generation turkey farmer in Kansas, said that the modern, broad-breasted white turkey is ready for slaughter in half the time of heritage breeds. But fast growth comes at a cost: The birds are prone to heart problems, high blood pressure and arthritic joints, among other health issues, he said.

“They have weaker immune systems, because bless that fat little turkey’s heart, they are morbidly obese,” said Mr. Reese, 75, who pasture-raises rare heritage breeds. “It’s the equivalent of an 11-year-old child who weighs 400 pounds.”

Highly pathogenic avian influenza has been circulating since 1996, but the virus had evolved to become even more lethal by the time it showed up in North America in late 2021. It led to the culling of nearly 60 million farmed birds in the United States, and felled countless wild ones and a great many mammals, from skunks to sea lions. Last week, federal authorities for the first time identified the virus in dairy cows in Kansas, Texas, Michigan, New Mexico and Idaho. The pathogen has also been implicated in a small number of human infections and deaths, mostly among those who work with live poultry, and officials say the risks to people remains low.

The virus is extremely contagious among birds and spreads through nasal secretions, saliva and feces, making it tough to contain. Migrating waterfowl are the single greatest source of infection — even if many wild ducks show no signs of illness. The virus can find its way into barns via dust particles or on the sole of a farmer’s boot.

While infections in North America have ebbed and flowed over the past three years, the overall number has declined from 2022, according to the U.S. Animal and Plant Health Inspection Service.

On Tuesday, the nation’s largest egg producer, Cal-Maine Foods, announced that it had halted production at its Texas facility and culled more than 1.6 million birds after detecting avian influenza.

Federal officials have been debating whether to vaccinate commercial flocks, but the initiative has divided the industry, in part because it could prompt trade restrictions harmful to the nation’s $6 billion poultry export sector.

Many scientists, fearing that the next pandemic could emerge from a human-adapted version of bird flu, have been urging the White House to embrace a vaccination campaign.

The agency’s livestock indemnity program, part of a farm bill passed by Congress in 2018, pays farmers 75 percent of the value of animals lost to disease or natural disaster. Since 2022, the program has distributed more than $1 billion to affected farmers.

Critics say the program also promotes animal cruelty by allowing farmers to euthanize their flocks by shutting down a barn’s ventilation system and pumping in hot air, a method that can take hours. Chickens and turkeys that survive are often dispatched by a twist of the neck.

Crystal Heath, a veterinarian and co-founder of Our Honor, said the American Veterinary Medical Association, in partnership with the agriculture department, recommended that ventilation shutdown be used only under “constrained circumstances.” She added that a vast majority of farms relied on it because the process was inexpensive and easy to carry out.

“All you need are duct tape, tarps and a few rented heaters,” Dr. Heath said. “But ventilation shutdown plus is especially awful because it can take three to five hours for the birds to die.”

Thousands of veterinarian have signed a petition urging the association to reclassify ventilation shutdown as “not recommended” and say that other methods that use carbon dioxide or nitrogen are far more humane, even if they are more costly. Since the start of the outbreak through December 2023, ventilation shutdown was used to cull 66 million chickens and turkeys, or about 80 percent of all those killed, according to analysis of federal data by the Animal Welfare Institute, which obtained the data through a Freedom of Information Act request.

Last summer, the institute filed a petition asking the agriculture department to require farms to devise depopulation plans that are more humane as a condition for receiving compensation. The agency has yet to respond to the petition.

Tyson and Jennie-O, the top recipients of federal compensation, have both used ventilation shutdown, according to an analysis of federal data. Tyson declined to comment for this article, and Hormel, which owns the Jennie-O brand, did not respond to requests for comment.

Some animal welfare advocates, pointing to recent outbreaks that were allowed to run their course, question whether killing every bird on an affected farm is even the right approach. When H5N1 hit Harvest Home Animal Sanctuary in California in February 2023, killing three birds, the farm’s operators steeled themselves for a state-mandated culling. Instead, California agriculture officials, citing a recently created exemption for farms that do not produce food, said they would spare the birds as long as strict quarantine measures were put in place for 120 days.

Over the next few weeks, the virus claimed 26 of the farm’s 160 chickens, ducks and turkeys, but the others survived, even those that had appeared visibly ill, according to Christine Morrissey, the sanctuary’s executive director.

She said the experience suggested that mass cullings might be unnecessary. “There needs to be more research and effort put into finding other ways of responding to this virus,” Ms. Morrissey said, “because depopulation is horrifying and it’s not solving the problem at hand.”

With the northward migration in full swing, poultry farmers like Caleb Barron are holding their breath. Mr. Barron, an organic farmer in California, said there was only so much he could do to protect the livestock at Fogline Farm given that the birds spent most of their lives outdoors.

So far, the birds remain unscathed. Perhaps it’s because Mr. Barron raises a hardier breed of chicken, or maybe it’s because his birds have a relatively good life, which includes high-quality feed and low stress.

“Or maybe,” he said, “ it’s just luck.”