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(CNN)In rural Brazil, an outbreak of yellow fever that began in December is considered the largest in 14 years.
With fears of the deadly viral hemorrhagic disease spreading to urban areas, another worry is plaguing scientists and primatologists: the murder of monkeys.
Residents began shooting and beating monkeys to death after the deaths of 11 yellow fever patients in the small town of Ladainha, reported the news site Globo.com. One farmer in a rural village in the state of Minas said she believes that people are killing the monkeys, because she heard gunshots and then noticed fewer primates in the area.
The Brazilian Institute of Environment and Renewable Natural Resources also said it has received reports of villagers killing monkeys due to fears of yellow fever, according to Globo.com.
Roberto Alves, manager of the Vectorially Transmitted Illnesses Technical Vigilance Unit at Brazil's Health Ministry, is tracking the outbreak and explained that the death of a primate is an event of mandatory notification to health services. Notifications sometimes come from environmental protection workers or from the community itself, concerned that the monkey has passed on the virus to its members.
"Since we only discover the circumstances of death after the fact, we sometimes discover that some primates didn't have natural deaths but violent ones," Alves said. "This information does not represent the total, but it's a sample of what happens in some regions."
"What's happening is, people are killing howler monkeys because they're afraid that they're going to catch or their kids are going to catch disease from these monkeys," said Paul Alan Garber, professor emeritus in the Department of Anthropology at the University of Illinois and executive editor of the American Journal of Primatology.
Howler monkeys do not transmit yellow fever virus; it is transmitted through mosquitoes. In fact, the monkeys are highly sensitive to the disease, the most vulnerable of all the primates in Brazil.
"In areas where there is yellow fever, howler monkeys are dying from yellow fever at an alarming rate," Garber said.
'Protect our Guardian Angels'
The Brazilian Institute of Environment and Renewable Natural Resources is urging people to report any abuses of monkeys. "Striking or killing monkeys is an environmental crime," noted the government agency, which receives complaints about mistreatment of wild animals, on its website. "Photos and videos make it easier to investigate crime and identify those responsible."
The Health Ministry is working on information campaigns aimed at ending the violence, as are primatologists in Brazil, which is home to more species of non-human primates than any other country.
"I re-launched the Campaign 'Protect our Guardian Angels' in January with colleagues from my state," Jlio Csar Bicca-Marques, a primatologist and professor at Pontifical Catholic University of Rio Grande do Sul, wrote in an email. He launched the original campaign in April 2009 during another yellow feveroutbreak.
Yellow fever is endemic in tropical areas of 47 countries in Africa and Central and South America, according to the World Health Organization.
The main purpose of his latest campaign is to inform residents that the monkeys should be protected because they are major allies in the fight against yellow fever, Bicca-Marques explained.
The monkeys act as sentinels, he said. Their deaths are the first warning that yellow fever is circulating in a region.
"Without the monkeys in our forests, we'll be blind to detect the arrival of the YF virus before we start detecting human cases and casualties, increasing the risk of re-urbanization of the disease in Brazil," Bicca-Marques wrote.
Alves said he believes that "a lack of understanding of the disease transmission mechanism" is the motive when people do violence to primates.
"Since the monkeys fall ill from the disease and they fall ill near people, they end up thinking that the monkeys transmit the disease," Alves said. "But both in the transmission of the disease to monkeys and the transmission to people, the mosquito is always present."
The latest outbreak of yellow fever in the southeastern Brazilian states of Minas Gerais, So Paulo, Esprito Santo and Rio de Janeiro has caused the death of thousands of monkeys, Bicca-Marques said. The Brazilian Ministry of Health (PDF) is investigating 1,367 deaths as of April 27, having confirmed an additional 474.
Yellow fever has also claimed 240 human lives in Brazil as of April 27, with an additional 39 deaths under investigation.
Human worries
Dr. Anthony Fauci, director of the US National Institute of Allergy and Infectious Diseases, said yellow fever has not yet gotten to "the explosive urban phase."
However, he is concerned that "there is a large number of individuals that have been infected in the states that are abutting the big cities," he said. "There was a person a couple of days ago who got infected with yellow fever and wound up dying -- but he was only about 25 miles from the city of Rio de Janeiro."
Yellow fever can be spread through the Aedes aegypti mosquito, which also transmits the Zika virus, but the current outbreak has been spread through Haemagogus and Sabethes mosquitoes.
"Someone who is probably a rural worker in the woods, in the forest, in the jungle gets bit by a mosquito who is infected with yellow fever but likely got it from a monkey," Fauci said, a method called sylvatic spread. "So it goes from animal to human, but it doesn't get into the population of Aedes aegypti, which are very frequent in the big cities like Rio de Janeiro."
Fauci also noted a major effort to get the yellow fever vaccine to as many people in Rio de Janeiro as possible. The yellow fever vaccine is among the most highly effective vaccines ever made, he said, offering close to 99% protection against the disease.
Still, if yellow fever gets into the population of Aedes aegypti mosquitoes -- "and that's a big if" -- "you'll get the possibility of getting travel-related cases just as we saw travel-related cases of Zika in Florida and Texas."
"In an era of frequent international travel, any marked increase in domestic cases in Brazil raises the possibility of travel-related cases," Fauci and colleague Dr. Catharine Paules wrote in a recent essay in the New England Journal of Medicine.
"We're not there yet," Fauci said. Still, the number of infections among humans is high -- estimates from the Brazilian Ministry of Health indicate 715 confirmed cases of yellow fever and 827 cases under investigation as of April 27-- and, with the virus' 20 to 30% mortality rate, deaths are rising.
The death toll naturally leads to fear, which, combined with a lack of information, can lead to monkey murders.
Ecosystem stability
Garber does not believe we are close to the loss of howler monkeys as a species, but we are coming close to the loss of local populations of these monkeys, which can live in very fragmented or degraded forests or even in cattle pastures with trees.
"They are often living near human habitation," he said, noting that humans have encroached on howler monkey areas. "These monkeys play important roles in the health of ecosystems. They may pollinate trees; they disperse seeds."
One of the biggest dangers of losing an important component of an ecosystem is that it makes emerging diseases more likely, as they are usually held in check by the dynamic effects of a community.
"The monkeys are not increasing the prevalence of disease," Garber said. "In general, if you lose an important element of an ecosystem, the ecosystem becomes less stable, and then you're more likely to have additional or other kinds of epidemic diseases."
And so the effort to protect these monkeys focuses on educating people that the animals are not carriers of yellow fever and that vaccination is necessary.
As Bicca-Marques explains, "New World monkeys" avoid traveling via the forest floor, preferring trees. It is impossible, then, that they can move through the highly fragmented landscape of southeast and south Brazil fast enough to be efficient carriers of yellow fever.
"This is the reason why New World monkeys are major victims of the disease and play an important role as sentinels of the circulation of the yellow fever virus that somebody else is transporting," he said. He added that yellow fever virus can be transmitted "vertically" from the female mosquito to her daughters for generations. This means a female mosquito may be born carrying the yellow fever virus and "the reason why mosquitoes are considered vector-reservoirs in Brazil."
"People should be vaccinated," Bicca-Marques emphasized.
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