Our thirst for pineapple may be causing mutations in Costa Rica’s sloths

For more than a decade, animal rescue centers in Central America have reported receiving a strangely high number of baby sloths with genetic mutations. Dr. Rebecca Cliffe was working on her Ph.D. near San Clemente at the Sloth Sanctuary of Costa Rica when she first began noticing sloths with misshapen limbs, missing appendages and albinism.

“They were often missing fingers and toes, sometimes the entire lower arm would be missing, sometimes the entire limb. The ears and the jaws were very prone to being deformed,” Cliffe said in an interview with Salon. Besides sloths with genetic mutations that have been taken into rescue centers, many others have been spotted in the wild. “Here in the South Caribbean, we regularly see sloths with missing arms, missing fingers and toes, still living in the wild, some of them as adults thriving,” Cliffe said.

Although some missing appendages are lost to predators or other injuries, genetic mutations are apparent from birth. In the time since her first observations in 2010, Dr. Cliffe hasn’t been the only researcher in the area to notice this phenomenon. Andrés Bräutigam is one of the veterinarians for the Toucan Rescue Ranch, another animal sanctuary in Costa Rica. 

“Most of the alterations I have seen are more related to internal organs. I've seen specifically congenital conditions associated with problems and development of lungs, problems and developments of hearts,” Bräutigam said, also mentioning problems associated with cognition and temperature regulation. “Mutations like the ones I have personally seen are often underdiagnosed because they require heavy medical exploration.”

Some deformities can make it impossible for sloths to live more than a few days after birth. “Even if it was a missing finger, then they would often not survive,” Cliffe added, explaining during later necropsies of the animals, researchers “would find there were a lot of internal abnormalities as well, so they were being born very unhealthy.”

Sloths are a national symbol of Costa Rica, a country home to an estimated 5 percent of all species in the world. Costa Rica has a higher density or biomass of sloths than any other mammal.

Besides its status as a hub of biodiversity, Costa Rica also produces more pineapple than anywhere else. Almost 50 percent of the pineapples in the world are exported from Costa Rica, including over 80 percent of pineapple consumed in the U.S.

Want more health and science stories in your inbox? Subscribe to Salon's weekly newsletter Lab Notes.

A few centuries ago, pineapples could rack up as much as today’s equivalent of $8,000, and were available to rent as centerpieces for fancy dinner parties in Colonial America. While pineapples were initially only available for purchase by extremely wealthy colonizers, international trade during the 1800s made the fruit affordable for working class folks. In 1857, English writer Charles Lamb described the taste of pineapple as, “almost too transcendent” and “a pleasure bordering on pain, from the fierceness and intensity of her relish.” As  one of the fruits with the highest amount of natural sugar, pineapple was a hit, and today is only growing in global popularity.

Although sloths in Costa Rica naturally have 2 toes or 3 toes depending on the species, a sloth named Quatro by the Sloth Conservation Foundation was born with 4 digits on each paw. (Dr. Rebecca Cliffe/The Sloth Conservation Foundation)

Hawaii was the main source of U.S. pineapple for the first half of the 20th century, but by the post-World War II era production had mainly moved to newly-occupied territories like Thailand and the Philippines, where cheap labor further dropped production costs. Prices remained relatively the same for consumers, but an increased savings in production made the pineapple industry more profitable than ever.

Pineapple became a central ingredient in many popular mid-century foods, including pineapple upside-down cake, pineapple ham and, controversially, pineapple pizza. Costa Rica’s pineapple industry has grown to dominate the market in recent decades. However, nonprofit organizations campaigning for fair trade, such as Banana Link, have collected a range of labor and environmental allegations against Costa Rican farms associated with companies like Dole, Chiquita and Del Monte.

Salon spoke with union organizer Didier Leitón Valverde about common practices on tropical fruit farms. Valverde has worked on banana plantations in Costa Rica for over 20 years, and still suffers from health conditions he believes were caused by pesticides sprayed on crops. Today he is the general secretary for the Sindicato de Trabajadores de Plantaciones Agrícolas (SITRAP), and represents agricultural workers throughout the country. Holly Woodward-Davey from Banana Link provided interpretation during the interview.

According to Valverde, workers on pineapple or banana plantations may conduct shifts up to 16 hours a day, earning roughly $23 for each 8 hour period. It is estimated 50 percent of agricultural workers in Costa Rica are paid even lower wages, many of them being undocumented immigrants from neighboring Nicaragua. Companies are legally required to pay workers an extra 50 percent beyond an 8-hour shift, but according to Valverde, such overtime isn’t usually paid out.

“A lawsuit for unpaid salaries can take up to 2 years to go through the courts,” Valverde said. Violations like these are among many ongoing allegations against Costa Rican pineapple farms, including a lack of reported workplace accidents.

“The fewer accidents you report, the lower your insurance premium,” Valverde said, explaining one of the reasons large fruit plantations may hide the impacts their farms have on workers or wildlife. “There's a financial incentive for them not to report their accidents.”

Although Dr. Cliffe has not been able to prove what might be causing mutations in sloths, she suspects they are the result of unregulated farming practices. Encar García is founder of the nearby Jaguar Rescue Center in Limón, and has seen the ecological impact of farming firsthand.

“In this province, there is less capacity to control what is happening,” García explained, listing “deforestation, illegal hunting and pesticides” among violations. García added that she thinks Costa Rica depends on people from the Caribbean to protect nature.

“I think what has been preserving nature is because of the Afro-Caribbeans,” García said. “The culture is to live in peace and love. They never cut the huge cacao trees and that's why we still have primary forests here.”

Cutting trees for farming operations is one way unregulated construction can fragment sloth habitats. The smaller sloth habitats become, the more the animals are crowded together into a single area.

“You can have upwards of six to seven sloths in one tree. If you go one kilometer down the road to an area where you’ve got more well-connected forest — that’s old growth. You don't see that,” Cliffe said. “When people talk about habitat fragmentation and loss, they're generally talking about it on a very big scale. What we're seeing is that habitats for sloths can be fragmented and sloths can be isolated by just a couple of roads.”

Besides habitat fragmentation caused by roads, farms and other construction, electrocution by power lines is another major threat to sloths. Every factor that further isolates the species reduces their ability to mate outside their own gene pool, causing inbreeding that could be the source of the mutations.

“They will disperse and form conjoining territories next to their mothers, and so if the animal is not able to disperse further, that can easily cause issues with inbreeding,” Bräutigam said.

Sam Trull is another sloth biologist working on the Pacific side of Costa Rica, where she hasn’t seen any of the genetic mutations found in the south Caribbean. She believes this may be a sign the mutations have a separate cause, noting that while habitats are being destroyed throughout Costa Rica, there are no fruit farms in her region.

“We don't have the banana plantations, but we do have the habitat fragmentation,” Trull explained. “The sloths have a lot of issues, but we don't see weird genetic malformations on the outside.”

The sloth mutations observed by Dr. Cliffe have been restricted to the Limón province of Costa Rica where she conducts her research. A lack of genetic mutations in sloths on the western side of Costa Rica could be an indicator the abnormalities are local to Limón.

A coastal province where the majority of pineapple plantations in the country are located, Limón is known for its Rastafarian culture, wildlife sanctuaries and late fall carnival celebrations. Home to many people originally from Jamaica, Bermuda, Trinidad and Tobego and other West Indies communities, local dishes include jerk chicken, oxtail and rice and beans made with coconut and cacao. Pineapple is present within cuisine, but as a relatively recent local industry that didn’t go into large-scale production until the late 1980s, it isn’t often used as an ingredient in traditional foods.

“It's because of the demand of the big hotels: everybody wants pineapple,” García said. As a common ingredient on pizzas, in cocktails and smoothies, pineapple is the fifth most popular fruit consumed in the U.S. While sloths in captivity are sometimes fed pineapple, as a high-sugar food that doesn’t grow in forest canopies, the fruit falls outside of their natural diet of fresh leaves.

To maintain the country’s leading number of pineapple exports, Costa Rica uses more pesticides per capita than anywhere else in the world, even China. A 2019 report by the Costa Rican Department of Agriculture shows 19.5% of produce sold by Costa Rica exceeded the maximum number of pesticides allowed by their own national regulations. Although in 2022 the United Nations alerted Costa Rica about the country’s high pesticide use, studying the impact on wildlife has been left up to researchers like Dr. Cliffe, who regularly see cropdusters spraying areas outside targeted pineapple and banana plantations.

“They don’t turn off the jets as they're crossing over, so they’re coming right over and they’ll spray the chemicals all over the forest, the people, everything that’s there,” Cliffe said. “The use of it is astronomical and it has to be impacting the sloths.”

Previous studies have shown how pesticides damage sloths' abilities to create enzymes necessary for digestion, leaving toxic residues embedded in their microbiomes and saliva. Separately in Costa Rica, pesticides have been linked to an increasing number of howler monkeys with yellow patches in their fur. Connections like these have led Dr. Cliffe to question whether there may be a similar cause for some of the other mutations she has observed.

Bromacil, a pesticide known to cause birth defects that was banned in Costa Rica in 2017, may be among several agrochemicals tropical fruit farms have continued to use illegally. The University of Costa Rica has found evidence of Bromacil and other banned pesticides in waterways near San José. However, Andrés Bräutigam has reservations about attributing mutations in sloths he has observed in that area to any single cause. 

“That is at a university in the middle of San José in a forest reserve that passes the most contaminated river in the country. Is it inbreeding? Is it contamination? Is it water runoff? I wouldn’t be able to tell you,” Bräutigam said.

The possibility that some farms may be using illegal pesticides makes it difficult to identify specific chemicals as causes of mutations. Pesticides being sprayed are often unknown even to workers, according to SITRAP secretary Valverde, who said workers “can't know the quality or the brand of the chemicals being applied.” Finding a specific pesticide that may cause a specific mutation in sloths would be expensive and time consuming.

“We’d have to sequence the genome of the deformed sloths, look at where the mutations are, and then link that with known mutations caused by the pesticides that are sprayed on the farms,” Dr. Cliffe explained.

Research like this could help prove some farms in Costa Rica are using banned pesticides. However, as a veterinarian working in an area fragmented by urban expansion, Bräutigam believes inbreeding is the simplest explanation for the mutations.

“Some of the animals I have received with very apparent mutations come from areas of the country where we know they are inbreeding,” Bräutigam said, who thinks habitat destruction may be causing similar mutations in sloths not only in the Limón province, but all around the world, adding, “I don't think it's localized. I think it's a global phenomenon.”

Bräutigam also explained sloths are more likely to inherit mutations than other animals. “The biology of sloths is really prone to create mutations and to sustain those mutations until birth,” Bräutigam said. “Because they have such a slow metabolism, they are very susceptible to the accumulation of mutations that are not weeded out of the system.”

This can cause a wider variety of genetic traits within the same species. For example, sloths can have a varying number of vertebrae in their necks depending on the individual.

Dr. Cliffe’s initial observations led her and other researchers to test 300 hair samples in order to identify 4 distinct genetic varieties of sloths in Costa Rica, but the specific cause of the abnormalities has yet to be determined. However, this research has been useful for maximizing genetic diversity when reintroducing sloths to the wild, which helps reduce inbreeding.

Sloths can live for up to 40 years. In less than one generation, the species has seen a complete change in habitat. Now the species itself is changing, and all currently available evidence indicates the fragmentation of tropical forests and heavy use of pesticides as potential causes. The impact of unregulated farming in Costa Rica on the future evolution and survival of the species continues to be studied by a small, dedicated range of wildlife biologists at animal rescue centers.

CORRECTION: The union was previously identified as SITREP, not SITRAP. The story has been updated.