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Category: Lemurs Page 1 of 4

To get a fuller picture of a forest, sometimes research requires a team effort

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Film by Riccardo Morrelas, Zahava Production

For some people, the word “rainforest” conjures up vague notions of teeming jungles. But Camille DeSisto sees something more specific: a complex interdependent web.

For the past few years, the Duke graduate student has been part of a community-driven study exploring the relationships between people, plants and lemurs in a rainforest in northern Madagascar, where the health of one species depends on the health of others.

Many lemurs, for example, eat the fruits of forest trees and deposit their seeds far and wide in their droppings, thus helping the plants spread. People, in turn, depend on the plants for things like food, shelter and medicines.

But increasingly, deforestation and other disturbances are throwing these interactions out of whack.

DeSisto and her colleagues have been working in a 750,000-acre forest corridor in northeast Madagascar known as the COMATSA that connects two national parks.

The area supports over 200 tree species and nine species of lemurs, and is home to numerous communities of people.

A red-bellied lemur (Eulemur rubriventer) in a rainforest in northeast Madagascar. Photo by Martin Braun.

“People live together with nature in this landscape,” said DeSisto, who is working toward her Ph.D. in ecology at the Nicholas School of the Environment.

But logging, hunting and other stressors such as poverty and food insecurity have taken their toll.

Over the last quarter century, the area has lost 14% of its forests, mostly to make way for vanilla and rice.

This loss of wild habitats risks setting off a series of changes. Fewer trees also means fewer fruit-eating lemurs, which could create a feedback loop in which the trees that remain have fewer opportunities to replace themselves and sprout up elsewhere — a critical ability if trees are going to track climate change.

DeSisto and her colleagues are trying to better understand this web of connections as part of a larger effort to maximize forest resilience into an uncertain future.

To do this work, she relies on a network of a different sort.

The research requires dozens of students and researchers from universities in Madagascar and the U.S., not to mention local botanists and lemur experts, the local forest management association, and consultants and guides from nearby national parks, all working together across time zones, cultures and languages.

Forest field team members at camp (not everyone present). Photo credit: Jane Slentz-Kesler.

Together, they’ve found that scientific approaches such as fecal sampling or transect surveys can only identify so much of nature’s interconnected web.

Many lemurs are small, and only active at night or during certain times of year, which can make them hard to spot — especially for researchers who may only be on the ground for a limited time.

To fill the gaps, they’re also conducting interviews with local community members who have accumulated knowledge from a lifetime of living on the land, such as which lemurs like to munch on certain plants, what parts they prefer, and whether people rely on them for food or other uses.

By integrating different kinds of skills and expertise, the team has been able to map hidden connections between species that more traditional scientific methods miss.

For example, learning from the expertise of local community members helped them understand that forest patches that are regenerating after clear-cutting attract nocturnal lemurs that may — depending on which fruits they like to eat — promote the forest’s regrowth.

Camille DeSisto after a successful morning collecting lemur fecal samples.

Research collaborations aren’t unusual in science. But DeSisto says that building collaborations with colleagues more than 9,000 miles away from where she lives poses unique challenges.

Just getting to her field site involves four flights, several bumpy car rides, climbing steep trails and crossing slippery logs.

“Language barriers are definitely a challenge too,” DeSisto said.

She’s been studying Malagasy for seven years, but the language’s 18 dialects can make it hard to follow every joke her colleagues tell around the campfire.

To keep her language skills sharp she goes to weekly tutoring sessions when she’s back in the U.S., and she even helped start the first formal class on the language for Duke students.

“I like to think of it as language opportunities, not just language barriers,” DeSisto said.”

“Certain topics I can talk about with much more ease than others,” she added. “But I think making efforts to learn the language is really important.”

When they can’t have face-to-face meetings the team checks in remotely, using videoconferencing and instant messaging to agree on each step of the research pipeline, from coming up with goals and questions and collecting data to publishing their findings.

“That’s hard to navigate when we’re so far away,” DeSisto said. But, she adds, the teamwork and knowledge sharing make it worth it. “It’s the best part of research.”

This research was supported by Duke Bass Connections (“Biocultural Sustainability in Madagascar,” co-led by James Herrera), Duke Global, The Explorers Club, Primate Conservation, Inc., Phipps Conservatory and Botanical Gardens, and the Garden Club of America.

Rewilding the Gut

Processed foods and overuse of antibiotics can wreak havoc on the trillions of bacteria and other microbes that inhabit the gut. A new study of the gut microbiomes of lemurs looks at whether reconnecting with nature can help restore this internal ecosystem to a more natural state. Credit: Sally Bornbusch.

Modern life messes with the microbiome -– the trillions of bacteria and other microbes that live inside the body. Could reconnecting with nature bring this internal ecosystem back into balance?

A new study suggests it can, at least in lemurs. Led by Duke Ph.D. alumnus Sally Bornbusch and her graduate advisor Christine Drea, the research team collected fecal samples from more than 170 ring-tailed lemurs living in various conditions in Madagascar: some were living in the wild, some were kept as pets, and some were rescued from the pet and tourism industries and then relocated to a rescue center in southwestern Madagascar where they ate a more natural diet and had less exposure to people.

Collecting fecal samples in Madagascar

Then the researchers sequenced DNA from the fecal samples to identify their microbial makeup. They found that the longer lemurs lived at the rescue center, the more similar their gut microbes were to those of their wild counterparts. Former pet lemurs with more time at the rescue center also showed fewer signs of antibiotic resistance.

By “rewilding” the guts of captive animals, researchers say we may be able to better prime them for success, whether after rescue or before translocation or reintroduction into the wild.

This research was supported by grants from the National Science Foundation (1945776, 1749465), the Triangle Center for Evolutionary Medicine, Duke’s Kenan Institute for Ethics, the Margot Marsh Biodiversity Fund and Lemur Love.

CITATION: “Microbial Rewilding in the Gut Microbiomes of Captive Ring-Tailed Lemurs (Lemur catta) in Madagascar,” Sally L. Bornbusch, Tara A. Clarke, Sylvia Hobilalaina, Honore Soatata Reseva, Marni LaFleur & Christine M. Drea. Scientific Reports, Dec. 27, 2022. DOI: 10.1038/s41598-022-26861-0.

Robin Smith
By Robin Smith

When the gut’s internal ecosystem goes awry, could an ancient if gross-sounding treatment make it right?

Lemur researchers make a case for fecal transplants to reduce the side effects of antibiotics. Photo by David Haring, Duke Lemur Center.

Dr. Cathy Williams knew something wasn’t right. The veterinarian had felt off for weeks after her 2014 trip to Madagascar.

At first she just felt bloated and uncomfortable and wasn’t interested in eating much. But eventually she developed a fever and chills that sent her to the emergency room.

When tested, doctors found that what she had wasn’t just a stomach bug. She was suffering from an infection of Clostridium difficile, a germ that causes severe diarrhea and abdominal pain and can quickly become life-threatening if not treated promptly.

“It was horrible,” Williams said.

The condition is often triggered when antibiotics disrupt the normal balance of bacteria that inhabit the gut, allowing “bad” bacteria such as C. difficile to multiply unchecked and wreak havoc on the intestines.

To get her infection under control, Williams asked her doctors if they could try an approach she and other veterinarians had used for decades to treat lemurs with digestive problems at the Duke Lemur Center. The procedure, known as a fecal microbiota transplant, involves taking stool from a healthy donor and administering it to the patient to add back “good” microbes and reset the gut.

At the time it was considered too experimental for clinical use in human cases like Williams’. She was prescribed the standard treatment and was sent home from the hospital, though she wouldn’t feel well enough to go back to work for another month. But now new research in lemurs is confirming what Williams and others long suspected: that this ancient if gross-sounding treatment can help an off-kilter gut microbiome get back to normal.

In a recent study in the journal Animal Microbiome, a research team led by Duke professor Christine Drea, former PhD student Sally Bornbusch and colleagues looked at the gut microbiomes of 11 healthy ring-tailed lemurs over a four-month period after receiving a seven-day course of the broad-spectrum antibiotic amoxicillin.

The lemurs were split into two experimental groups. One was a wait-and-see group, with continued follow-up but no further treatment after the antibiotics. The other group was given a slurry of their own feces, collected prior to antibiotic treatment and then mixed with saline and fed back to the same animal after their course of antibiotics was over.

“It sounds crazy,” Williams said. But she has used a similar procedure since the 1990s to treat illnesses in Coquerel’s sifaka lemurs, whose infants are known to eat their mother’s poop during weaning — presumably to get the microbes they’ll need to transition to solid food.

A baby Coquerel’s sifaka tries some of her first solid foods. Photo by David Haring.

Drea, Bornbusch and team used genetic sequencing techniques to track changes in the lemurs’ gut microbiome before, during and after treatment.

As expected, even a single course of antibiotics caused the numbers of microbes in their guts to plunge compared with controls, briefly wiping out species diversity in both experimental groups before returning to baseline.

“Antibiotics had dramatic effects, even in healthy animals,” Drea said.

But in terms of which types of bacteria bounced back and when, the patterns of recovery in the two groups were different. Lemurs that received the “poop soup” treatment started to stabilize and return to their pre-antibiotic microbiome within about two weeks. In contrast, the bacterial composition in the wait-and-see group continued to fluctuate, and still hadn’t quite returned to normal even after four months of observation.

This kind of therapy isn’t new. Reports of using fecal transplants to treat people suffering from food poisoning or diarrhea date back as far as fourth century China. The evidence for its effectiveness in captive settings has Bornbusch advocating for freezing stool at Smithsonian’s National Zoo, where she is now a postdoctoral fellow.

“If we can bank feces from animals when they’re healthy, that can be a huge benefit down the road,” Bornbusch said. “It can help the animals get better, faster.”

And now if any of her lemur patients were to get sick with C. difficile like she did, Williams said, “I would absolutely go with a fecal microbiota transplant.”

“People are put off by it,” Drea said, “But the disgust for this approach might actually have been holding up a fairly cheap and useful cure.”

Ring-tailed lemurs at the Duke Lemur Center in North Carolina. Photo by David Haring, Duke Lemur Center

This research was supported by the National Science Foundation (BCS 1749465), the Duke Lemur Center Director’s Fund, and the Duke Microbiome Center.

CITATION: “Antibiotics and Fecal Transfaunation Differentially Affect Microbiota Recovery, Associations, and Antibiotic Resistance in Lemur Guts,” Sally L. Bornbusch, Rachel L. Harris, Nicholas M. Grebe, Kimberly Roche, Kristin Dimac-Stohl, Christine M. Drea. Animal Microbiome, Oct. 1, 2021. DOI: 10.1186/s42523-021-00126-z.

By Robin Ann Smith

Why Ruffed Lemurs (and Their Gut Microbes) Need to Eat Greens

We offered fruit-eating ruffed lemurs at the Duke Lemur Center fresh lettuce each afternoon for 10 days. They happily ate it and their gut microbiomes shifted, suggesting that leafy greens could be incorporated into the lemurs’ standard dietary regimen to boost foraging opportunity and fiber intake.

Red-ruffed lemurs and black-and-white ruffed lemurs are some of Madagascar’s most iconic wildlife. Sporting a long snout and a neck ruff to rival those of the Elizabethan court, these primates naturally live in the rainforests, where they mostly eat fruits and flowers, and make their living as seed dispersers and pollinators.

Ruffed lemurs really like romaine lettuce and their gut bugs do too! (Lydia Greene)

Ruffed lemurs also live in zoos worldwide, where they are given fruit-rich diets to match those foraged by their wild peers. But scientists are starting to realize that the fruit eaten by wild lemurs is quite different from the domesticated fruit provided at zoos. Wild fruits are seedy, pulpy, and thick-skinned, whereas orchard fruits are fleshy, plump, and sweet. From a nutritional standpoint, wild fruits contain more fiber, whereas orchard fruits contain more sugar. 

Our team wondered if a fiber boost might benefit Duke’s ruffed lemur colony. But would these fruit-loving lemurs eat their veggies?  

Cue the salad bar.

To test this idea, we offered ruffed lemurs at the Duke Lemur Center a lot of lettuce. Lettuce seemed like a pretty palatable way to stimulate foraging behavior, while boosting fiber intake.

With help from the research department, we offered 19 ruffed lemurs 150-200 grams of romaine lettuce each day, which is about double the weight of their standard diet. We repeated this regimen every day for 10 days, while recording the lemurs’ feeding behavior and collecting fecal samples for gut microbiome analysis. Because gut microbes are chiefly responsible for converting plant fiber into energy for the lemurs, measuring changes to the lemurs’ microbiomes offered a way to ‘see’ the impact of lettuce consumption.

It turns out that ruffed lemurs really like lettuce. They consistently ate lettuce every day and showed no decline in consumption across the study. Younger animals ate more lettuce than did geriatric lemurs, but all lemurs spent more time crunching on lettuce stalks than the leaves.

And their gut microbiomes responded. We noted two microbes that were more abundant on the lettuce diet: a known fiber digester from the Ruminococcaceae family, and a microbe known for its positive association with host health in other animals called Akkermansia.

Despite their classification as fruit eaters, ruffed lemurs readily eat lettuce. We think lettuce can be used to extend the lemurs’ foraging time while boosting dietary fiber. And it might just help replicate the lifestyles experienced by wild ruffed lemurs in their native Malagasy rainforests.     At the Duke Lemur Center, lettuce is now a routine item offered to ruffed lemurs (and other species too!). Next time you come out for a tour (once it’s safe to do so), you might get to see them crunching away on their new favorite snack!

( Read our paper here: https://onlinelibrary.wiley.com/doi/abs/10.1002/zoo.21555 )

Guest Post by Lydia Greene Ph.D., an NSF-sponsored postdoctoral fellow in biology working at the Duke Lemur Center.

For Lemurs, Water Holes Are a Matter of Taste

It’s 1 PM and you’re only halfway through a 6-hour hike, climbing in steep terrain under a 100° cloudless sky. Your water bottle is nearly empty, and you’ve heard the worst of this hike is yet to come.

And then, just as you are making peace with the fact that you may collapse from dehydration at any second, you approach a small river. The germaphobe side of your brain is shouting for you not to drink from that. The dehydrated animal in you, however, is seriously considering it.

What do you do?

That is the question that Dr. Caroline Amoroso and her collaborators from Duke’s department of evolutionary anthropology, set out to answer. With a slight difference: rather than unprepared hikers, they asked that question to red-fronted lemurs in Madagascar.

Although we often associate Madagascar with lush forests, some regions have a very marked dry season during which water becomes a limited resource. Water holes are few and far apart.

A red-fronted lemur in Kirindy Forest, Madagascar, tanks up at a watering hole. (Photo: Caroline Amoroso)

“On my first visit to Kirindy forest I was amazed at how these waterholes – which are essentially just puddles of standing water – serve as a source of life for so many animals,” says Amoroso.

However, with animals, comes poop. Throughout the season, these water holes quickly become contaminated with fecal matter from all the mammals, birds and reptiles that come have a drink. Amoroso says that fecal contamination was easily detectable even to human observers. “Approaching some waterholes I could tell that lemurs had been there recently because their droppings left such a smell!”

By experimentally manipulating water quality, following groups of radio-collared lemurs and observing lemur behavior at natural water holes, Amoroso and her team found that, all else being equal, lemurs prefer to drink clean water.

Indeed, when offered the choice between a bucket of clean water and a bucket of water containing lemur feces that had been disinfected by boiling, to kill all possible pathogens, lemurs virtually always drank from the clean water bucket. When the buckets were removed and lemurs had to go visit natural water holes, however, they prioritized water holes closer to their resting site, even if they were more contaminated than further ones. Proximity was more important than cleanliness, but if multiple water holes were at similar distances, then lemurs seem to choose the least-contaminated source.

“I was surprised to find evidence that the lemurs chose natural waterholes with lower levels of fecal contamination,” says Amoroso. “I thought that [in a natural setting] avoidance of fecal contamination would be relatively low on the lemurs’ list of priorities.”

After some watchful waiting for predators, and a discussion perhaps, a quartet of Kirindy lemurs visits a tiny watering hole. (Photo: Caroline Amoroso)

The authors highlight that many other factors can influence a lemur’s choice of water hole, such as exposure to potential predators or visits by competing groups. Indeed, Amoroso says that drinking water can be a very risky business for lemurs: “Lemurs would spend upwards of thirty minutes scanning the vegetation nervously and making sure there was no sign of predators before approaching the waterhole and drinking.”

Lemurs prefer clean water, unless it’s too much trouble. In that hike you were on? Lemurs would definitely drink from the river.

Guest Post by Marie Claire Chelini, a postdoctoral fellow in evolutionary anthropology.

Love at First Whiff

Many people turn to the Internet to find a Mr. or Ms. Right. But lemurs don’t have to cyberstalk potential love interests to find a good match — they just give them a sniff.

A study of lemur scents finds that an individual’s distinctive body odor reflects genetic differences in their immune system, and that other lemurs can detect these differences by smell.

Smell check: Fritz the ring-tailed lemur sniffs a tree for traces of other lemurs’ scents at the Duke Lemur Center.
Smell check: Fritz the ring-tailed lemur sniffs a tree for traces of other lemurs’ scents. Photo by David Haring, Duke Lemur Center.

From just one whiff, these primates are able to tell which prospective partners have immune genes different from their own. The ability to sniff out mates with different immune genes could make their offspring’s immune systems more diverse and able to fight more pathogens, said first author Kathleen Grogan, who did the research while working on her Ph.D. with professor Christine Drea at Duke University.

The results appeared online August 22 in the journal BMC Evolutionary Biology.

Lemurs advertise their presence by scent marking — rubbing stinky glands against trees to broadcast information about their sex, kin, and whether they are ready to mate.

Lemurs can tell whether a mate’s immune genes are a good genetic match by the scents they leave behind.
Lemurs can tell whether a mate’s immune genes are a good genetic match by the scents they leave behind. Photo by David Haring, Duke Lemur Center

For the study, Grogan, Drea and colleagues collected scent secretions from roughly 60 lemurs at the Duke Lemur Center, the Indianapolis Zoo, and the Cincinnati Zoo. The team used a technique called gas chromatography-mass spectrometry to tease out the hundreds of compounds that make up each animal’s signature scent.

They also analyzed the lemurs’ DNA, looking for differences within a cluster of genes called MHC that help trigger the body’s defenses against foreign invaders such as bacteria and viruses.

Their tests reveal that the chemical cocktail lemurs emit varies depending on which MHC types they carry.

To see if potential mates can smell the difference, the researchers presented lemurs with pairs of wooden rods smeared with the bodily secretions of two unfamiliar mates and observed their responses. Within seconds, the animals were drawn to the smells wafting from the rods, engaging in a frenzy of licking, sniffing, or rubbing their own scents on top.

In 300 trials, the team found that females paid more attention to the scents of males whose immune genes differed from their own.

MHC genes code for proteins that help the immune system recognize foreign invaders and distinguish “friend” from “foe.” Since different genetic versions respond to different sets of foreign substances, Grogan said, sniffing out genetically dissimilar mates produces offspring more capable of fighting a broad range of pathogens.

Just because females spent more time checking out the scents of dissimilar males doesn’t necessarily make them more likely to have kids together, Grogan said. Moving forward, she and her colleagues plan to use maternity and paternity DNA test results from wild lemurs living in Beza Mahafaly Reserve in Madagascar to see if lemur couples are more different in their MHC type than would be expected by chance.

Similar results have been found in humans, but this is the first time the ability to sniff out partners based on their immune genes has been shown in such distant primate kin, said Grogan, who is currently a postdoctoral fellow at Pennsylvania State University.

“Growing evidence suggests that primates rely on olfactory cues way more than we thought they did,” Grogan said. “It’s possible that all primates can do this.”

This research was supported by the National Science Foundation (BCS #0409367, IOS #0719003), the National Institutes of Health (F32 GM123634–01), and the Duke University Center for Science Education.

CITATION: “Genetic Variation at MHC class II Loci Influences Both Olfactory Signals and Scent Discrimination in Ring-Tailed Lemurs,” Kathleen E. Grogan, Rachel L. Harris, Marylène Boulet, and Christine M. Drea. BMC Evolutionary Biology, August 22, 2019. DOI: 10.1186/s12862-019-1486-0

Post by Robin A. Smith

Some Lemurs are Loners, Others Crave Connection

DURHAM, N.C. — If lemurs were on Facebook, Fern would have oodles of friends, liking and commenting on their posts. Captain Lee, on the other hand, would rarely send a friend request.

Best buddies Fern and Alena at the Duke Lemur Center in Durham, North Carolina. Photo by Ipek Kulahci.

Best buddies Fern and Alena at the Duke Lemur Center in Durham, North Carolina. Photo by Ipek Kulahci.

These are just two of the distinct personalities discovered in a recent study of group dynamics in ring-tailed lemurs, primate cousins that live in groups of up to two dozen on the island of Madagascar.

First author Ipek Kulahci spent several years studying ring-tailed lemurs housed at the Duke Lemur Center in North Carolina and the St. Catherines Island Lemur Program in Georgia. Along the way, she noticed a lot of variation in social behavior from one lemur the next. She observed socialite Fern, loner Captain Lee, best buddies Limerick and Herodotus and other lemur characters.

Some individuals seemed more outgoing than others. To try to quantify that, she followed four groups of ring-tailed lemurs over two consecutive years and recorded their behavior a minimum of four times a week for at least two months.

A social network of lemurs. Each circle represents an individual lemur, and lemurs who respond to each other’s calls are connected by arrows. Thicker arrows indicate lemurs who respond more frequently and have a stronger social bond.

A social network of lemurs. Each circle represents an individual lemur, and lemurs who respond to each other’s calls are connected by arrows. Thicker arrows indicate lemurs who respond more frequently and have a stronger social bond.

Using a method called social network analysis, she was able to measure how many connections each lemur had, with whom, and how strong those connections were. She was also able to figure out which lemurs were most influential in each group — either because they connected others, or because they had well-connected friends.

Kulahci and colleagues found that lemurs behaved consistently no matter what their age, sex or social situation. Some lemurs like Fern tended to seek connection; reinforcing social bonds by frequently picking through their friends’ fur and responding to other lemurs’ calls and scent marks.

Their interactions weren’t always amicable — the more socially active lemurs were also more likely to chase others or pick fights with individuals with whom they weren’t on friendly terms. “But they have a drive to interact with others, rather than be a loner,” said Kulahci, now a postdoctoral researcher at University College Cork in Ireland.

The researchers also found that lemurs, like us, don’t bond with just anyone. Whether they were extroverted or shy, all lemurs had an inner circle of groupmates they tended to groom, call back, or otherwise keep in touch with more than others.

Ipek Kulahci, postdoctoral researcher at University College Cork in Ireland.

Ipek Kulahci, postdoctoral researcher at University College Cork in Ireland.

“They essentially have buddies,” Kulahci said.

“This is important because social connectedness influences health, immunity, survival,” Kulahci said. “This is true for animals as well as humans.”

The results appeared online Dec. 9, 2017, in the journal Animal Behaviour.

Other authors on this study include Asif Ghazanfar and Daniel Rubenstein of Princeton University. This study was funded by grants from the Animal Behavior Society, American Society of Mammalogists, American Society of Primatologists and Princeton University.

CITATION:  “Consistent Individual Variation Across Interaction Networks Indicates Social Personalities in Lemurs,” Ipek Kulahci, Asif Ghazanfar and Daniel Rubenstein. Animal Behaviour, Dec. 9, 2017.  https://doi.org/10.1016/j.anbehav.2017.11.012

by Robin Smith

by Robin Smith

Captive Lemurs Get a Genetic Health Checkup

DURHAM, N.C. — Careful matchmaking can restore genetic diversity for endangered lemurs in captivity, researchers report.

Ring-tailed lemurs born at the Duke Lemur Center have seen a recent infusion of new genetic material at key genes involved in the immune response, finds a new study.

Thanks to a long-term collaborative breeding program that transfers animals between institutions to preserve genetic diversity, genetic variation at one region was restored to levels seen in the wild.

The findings, published in the journal Ecology and Evolution, are important for the ability of future generations to fight disease.

Baby lemur twins Nemesis and Narcissa were the product of a breeding program developed by the American Association of Zoos and Aquariums to preserve the future genetic health of North America’s captive ring-tailed lemurs. Their mother Sophia was among 62 ring-tailed lemurs recommended for breeding across 20 institutions nationwide in 2016. Photo by David Haring, Duke Lemur Center.

Baby lemur twins Nemesis and Narcissa were the product of a breeding program developed by the American Association of Zoos and Aquariums to preserve the future genetic health of North America’s captive ring-tailed lemurs. Their mother Sophia was among 62 ring-tailed lemurs recommended for breeding across 20 institutions nationwide in 2016. Photo by David Haring, Duke Lemur Center.

Distant primate cousins with long black-and-white striped tails, ring-tailed lemurs live on the African island of Madagascar and nowhere else except in zoos and other captive facilities.

Some studies suggest that as few as 2,500 ring-tailed lemurs live in the wild today. Habit loss, hunting and the illegal pet trade have reduced their numbers by at least 50 percent in recent decades.

An additional estimated 2,500 ring-tailed lemurs live in zoos around the world, where experts work to maintain their genetic health in captivity.

The researchers studied DNA sequence variation at a region of the major histocompatibility complex, or MHC, a part of the genome that helps the immune system identify disease-causing bacteria, viruses and parasites.

Because different MHC gene variants recognize different types of pathogens, greater MHC diversity means animals are able to fend off a wider array of invaders.

The researchers estimated the number of MHC variants in 121 captive individuals born at the Duke Lemur Center and the Indianapolis and Cincinnati Zoos between 1980 and 2010.

They also compared them with 180 wild individuals from southwestern Madadgascar at the Bezà Mahafaly Special Reserve, where the animals regularly interbreed with lemurs from nearby forests.

Not surprisingly, MHC diversity was lower in captivity than in the wild.

Today’s captive ringtails came from a small group of ancestors that carried only a small fraction of the total genetic variation found in the larger wild population. Since their establishment, gene flow between captive populations and wild lemurs has been restricted.

Overall, the researchers found 20 unique MHC variants in the captive population, fewer than half the number in their wild counterparts.

However, efforts to identify good genetic matches across dozens of institutions have helped to preserve and even improve upon the diversity that is left.

For infants born at the Duke Lemur Center, MHC gene diversity remained low but stable for three decades from 1980 to 2010, then increased significantly from 2010 to 2013, researchers found.

Genetic contributions from several transplants contributed to the comeback.

An arranged marriage between ring-tailed lemurs at the Duke Lemur Center in North Carolina produced healthy twins Griselda and Hedwig in 2016. The infants are among 40 to 60 ring-tailed lemur infants born in North American zoos and other facilities each year. Photo by David Haring, Duke Lemur Center.

An arranged marriage between ring-tailed lemurs at the Duke Lemur Center in North Carolina produced healthy twins Griselda and Hedwig in 2016. The infants are among 40 to 60 ring-tailed lemur infants born in North American zoos and other facilities each year. Photo by David Haring, Duke Lemur Center.

The American Association of Zoos and Aquariums (AZA) tries to maintain a genetically healthy population by moving animals between institutions as potential mates. A team of experts uses computer software to help pick the best pairs for breeding.

Between 1980 and 2013, more than 1,160 ring-tailed lemurs were transferred between 217 institutions in North America alone.

In 2009, a male named Randy was transferred from the Saint Louis Zoo to the Duke Lemur Center for pairing with Sprite, a resident female. Experts also brought a mother-daughter pair, Schroeder and Leisl from the Zoo at Chehaw in Georgia, as potential mates for a resident male named Aracus.

“They saw an immediate improvement in the diversity of the offspring that were born,” said lead author Kathleen Grogan, who conducted the study while working on a doctorate with co-author Christine Drea at Duke University.

Grogan and colleagues are now examining whether MHC gene diversity helps the animals live longer or produce more offspring, as has been shown for other species.

“Not only do these lemurs serve as an assurance against extinction of their Malagasy counterparts, but maintaining as many variations of genes is important for keeping the individual lemurs, as well as the population healthy for any future challenges it may face,” said AZA Species Survival Plan Coordinator Gina Ferrie, a population biologist at Disney’s Animal Kingdom.

Conserving genetic diversity in captive populations over multiple generations is challenging due to their small size and relative isolation, but careful breeding can stem the loss, said Grogan, now a postdoctoral fellow at Pennsylvania State University.

Other authors include Michelle Sauther of the University of Colorado-Boulder and Frank Cuozzo at LaJuma Research Centre in South Africa.

This research was supported by Duke University, the International Primatological Society, Primate Conservation Inc., the University of Colorado-Boulder, the University of North Dakota, the National Science Foundation (BCS 0922465, BCS-1232570, IOS-071900), the Margot Marsh Biodiversity Foundation, the St. Louis Zoo and the American Society of Primatologists.

CITATION:  “Genetic Wealth, Population Health: Major Histocompatibility Complex Variation in Captive and Wild Ring-Tailed Lemurs (Lemur Catta),” Kathleen Grogan, Michelle Sauther, Frank Cuozzo and Christine Drea. Ecology and Evolution, Date. DOI: 10.1002/ece3.3317

Aging Gracefully, and Cheaply, in a Small Space

The old joke is, “We’ve cured cancer several times — in mice!”

But the trouble with our favorite lab animal is that they aren’t nearly as close to humans as we had hoped.

Researchers who are working on human longevity obviously need a model organism — they can’t keep their funding going for 100 years to see how a person dies. And other primates aren’t ideal, either; they’re also pretty long-lived and expensive to house, besides.

microcebus mouse lemurs

Mouse lemurs at a lab outside Paris eagerly lap up their calories. Sometimes it’s great being in the control group. (CNRS photo)

So what if you had a primate that was relatively short-lived, say 13 years tops, and quite small, say 100 grams, a bit bigger than a mouse? Behold the Mouse Lemur, Microcebus, the smallest member of the primate family.

In a pair of presentations Friday during the Duke Lemur Center’s 50th Anniversary scientific symposium, gerontologists Fabien Pifferi of the French national lab CNRS, and Steven Austad, chair of biology at the University of Alabama-Birmingham (UAB), made their arguments for how well “le microcèbe” might work in studying aging in humans.

Pifferi works at one of two mouse lemur breeding colonies in France, which is housed in an elegant old chateau in Brunoy, a suburb southeast of Paris. There, a 450-member breeding colony of grey mouse lemurs produces about 100 pups a year, and the scientists have devised many clever, non-invasive ways to test their physical and mental abilities as they age.

“It seems like their normal aging is very similar to humans,” Pifferi said. But about 20 percent of the tiny lemurs follow a different trajectory, marked by the formation of brain plaques, atrophy of the brain and cognitive declines. It’s not exactly Alzheimer’s disease, he said, but it may be a useful scientific model of human aging.

Aging, UAB’s Austad began, is already the number one health challenge on the planet and will remain so for the foreseeable future. We need a good research model to understand not just how to achieve longevity, but how to live healthy longer, he said.

Filbert, a grey mouse lemur, was born at the Duke Lemur Center in June 2013, weighing less than two cubes of sugar. He should still be around in 2023 at least.

Filbert, a grey mouse lemur, was born at the Duke Lemur Center in June 2013, weighing less than two cubes of sugar.

Citing some early studies on using calorie restriction and rapamycin to increase longevity, Austad said mouse lemurs may be “a mid-way model between mice and humans.”

The CNRS colony at Brunoy tried to replicate a study on calorie restriction and longevity that had yielded mixed results in other animals. The mouse lemurs in the experimental condition thrived.

“I saw this colony last year,” Lemur Center Director Anne Yoder said. “The one remaining control animal was old and feeble and sort of pathetic. The four calorie-restricted animals were bouncing around, they were glossy.” Though suffering age-related blindness at that point, they were very much alive and frisky, Pifferi added.

“I think the mouse lemur is a great intermediate to do these sorts of studies,”  Austad said.

But, as you may imagine, some members of the lemur community who have dedicated their lives to preserving rare and critically endangered lemurs might struggle with the idea of  breeding up mouse lemurs to use as lab animals, even if the tests are non-invasive. Nobody asked hostile questions, but the discussion is sure to continue.

Karl Leif BatesPost by Karl Leif Bates

How to Get a Lemur to Notice You

Duke evolutionary anthropology professor Brian Hare studies what goes on in the minds of animals.

Duke evolutionary anthropology professor Brian Hare studies what goes on in the minds of animals.

Duke professor Brian Hare remembers his first flopped experiment. While an undergraduate at Emory in the late 1990s, he spent a week at the Duke Lemur Center waving bananas at lemurs. He was trying to see if they, like other primates, possess an important social skill. If a lemur spots a piece of food, or a predator, can other lemurs follow his gaze to spot it too?

First he needed the lemurs to notice him. If he could get one lemur to look at him, he could figure out if other lemurs then turn around and look too. In similar experiments with monkeys and chimps, oranges had done the trick.

“But I couldn’t get their attention,” Hare said. “It failed miserably.”

Hare was among more than 200 people from 25 states and multiple countries who converged in Durham this week for the 50th anniversary celebration of the Duke Lemur Center, Sept. 21-23, 2016.

Humans look to subtle movements in faces and eyes for clues to what others are thinking, Hare told a crowd assembled at a two-day research symposium held in conjunction with the event.

If someone quickly glances down at your name tag, for example, you can guess just from that eye movement that they can’t recall your name.

We develop this skill as infants. Most kids start to follow the gaze of others by the age of two. A lack of interest in gaze-following is considered an early sign of autism.

Arizona State University graduate student Joel Bray got hooked on lemurs while working as an undergraduate research assistant in the Hare lab.

Arizona State University graduate student Joel Bray got hooked on lemurs while working as an undergraduate research assistant in the Hare lab.

“Gaze-following suggests that kids are starting to think about the thoughts of others,” Hare said. “And using where others look to try to understand what they want or what they know.”

In 1998 Hare and researchers Michael Tomasello and Josep Call published a study showing that chimpanzees and multiple species of monkeys are able to look where others are looking. But at the time not much was known about cognition in lemurs.

“When you study dogs you just say, ‘sit, stay,’ and they’re happy to play along,” Hare said. Working at the Duke Lemur Center, eventually his students discovered the secret to making these tree-dwelling animals feel at home: “Lemurs like to be off the ground,” Hare said. “We figured out that if we just let them solve problems on tables, they’re happy to participate.”

Studies have since shown that multiple lemur species are able to follow the gaze of other lemurs. “Lemurs have gone from ignored to adored in cognitive research,” Hare said.

 

Ring-tailed lemurs are among several species of lemurs known to follow the gaze of other lemurs. The ability to look where others are looking is considered a key step towards understanding what others see, know, or might do. Photo by David Haring, Duke Lemur Center.

Ring-tailed lemurs are among several lemur species known to follow the gaze of other lemurs. The ability to look where others are looking is considered a key step towards understanding what others see, know, or might do. Photo by David Haring, Duke Lemur Center.

Robin SmithPost by Robin A. Smith

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