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Sally Bornbusch, Ph.D., is an NSF postdoctoral fellow in biology conducting microbial ecology research in animal care and conservation at the Smithsonian National Zoo & Conservation Biology Institute. She discusses how fecal microbiota transplants (FMTs) are being used to mitigate health concerns in wild animals in captivity, shares key findings about the milk microbiome from the Smithsonian milk repository, the largest collection of exotic animal milks in the world, and explains the science behind eating poo (Coprophagia).

Ashley's Biggest Takeaways:

• Animals under human care have very different microbial landscapes than those in the wild.
• Some of the factors that contribute to these differences include, diet, and the nutritional content of the food that is available in captivity, as well as exposure to humans and other animals.
• Nutritionists do their best to replicate the healthiest diet that an animal can have (i.e., as close to a wild diet as possible) in captivity. However, there are constraints to the types of foods that are available.
• Understandably, these differences in diet can impact the gut microbiome of animals under human care.
• Scientists are seeing health implications associated with such changes in diet, including dental disease, obesity and diabetes.
• Researchers at the National Zoo are tracking animal microbiomes, in relation to some sort of shift in diet or treatment, with the goal of improving the animals’ health and care.
• Many animals naturally practice coprophagia (consumption of feces) for nutritional and/or microbiological reasons.
• Lactation is extremely variable across mammal species. The shortest lactation for mammal is 5 days in a hooded seal, and the longest is 6-8 years in an orangutan.
• All mammals are born obligate lactivores. Milk was long thought to be a sterile substance, but scientists now know that there are microbial communities in milk, which are important for the early development of the microbiome of neonates.

Featured Quotes

Just like when humans are in environments that they may not have evolved or adapted to—that can cause health problems—we see similar patterns in animal species. And in a lot of cases, when we have animals that are under human care for conservation purposes, they are not necessarily evolved for those specific conditions, and we do sometimes see health concerns that arise from that kind of evolutionary mismatch, i.e., a mismatch between your evolved environment and your current environment.

This is particularly relevant for microbiomes for which humans and animals have evolved with their invisible, microscopic partners for millions of years. And the kinds of environments [in which] we have animals under human care have a very different microbial landscape. The microbes that animals are interacting with are different. The food that the animal is getting that is impacting its own internal, gastrointestinal microbiome, is going to be slightly different. They have other animals that they're interacting with. There are potentially humans in that environment. So, those factors can all contribute to shifts in microbial health patterns.

One of the things my research is focused on is mitigating these health concerns using microbial ecology and microbiome science.

Poop Science: FMTs and Coprophagy

I joke that I am a professional ‘turd nerd,’ because one of the best ways to study animal microbiomes, at least their gastrointestinal microbiome, is through feces. So, I spend a lot of time collecting fecal samples, and it's also really important for us, especially working with endangered animals that we do something non-invasive. We do not have the capacity to have animals in a lab that we could necessarily manipulate in a very tractable manner. We're working with animals where we are very hands off, both for their safety and for ours, and we are limited in what samples we can collect in a lot of cases. So, feces is really important, both for what we do with microbiomes, but also for genomics, hormone monitoring, behavioral monitoring, all of that.

We call this “poop science.” What we try to do, when we design a study to track an animal's microbiome in relation to some sort of diet shift or some sort of treatment, is set up an experimental design where we really try to make it as rigorous as possible. So, collecting control samples, collecting samples prior to any sort of manipulation, and then tracking longitudinally. And that requires a lot of poop.

I've got a long list, but right now, we're kind of focused on a couple key species. The first, we were working with our elephant herd. We also just got our 2 giant pandas, so we're doing a lot of research on their gut microbiomes. We're working with our sloths, our black footed ferrets, cheetahs and a number of other species. One of the benefits of working somewhere like the National Zoo is that you really do get a comparative approach to this. You really get to ask these questions in a very wide variety of animal systems, which has its pitfalls as well, because we don't have that many animals of each species. So, our sample sizes are somewhat small, but it is a really interesting way to examine how these microbial dynamics are different across these different species that are all under human care.

One of my main focuses here is, can we use microbiome science to improve health? So, if there are animals that have some sort of health concern, can we track the microbiome? Can we use the microbiome as a diagnostic tool? And then can we use things like microbial therapies to improve animal care in those situations?

But, you know, we’ve learned so much about human microbiomes, and we know how complicated they are. There's still so much we don't know. And imagine doing that for 27 different species. We're really just starting this research. There's so much left we still need to learn. But the reason we're kind of jumping into some of these things really quickly is because there are pressing concerns that animals have, and we want to be able to kind of learn on the go as we figure these things out and figure out a way to harness microbiome science.

Fecal microbiota transplants are a really fascinating kind of novel area of human medicine and human research, and the premise is that feces what a lot of people consider a whopping dose of probiotics plus prebiotics. There's some nutrition in there. There are also microbial metabolites in there. So, it's this kind of big package of all of the good things in a microbiome, and oftentimes feces has the bad things as well, which is why, for fecal transplants, the donor feces is heavily screened. So, normally, feces is collected from a healthy human donor. It is screened for pathogens, parasites, genes of concern. If it passes that screening, it then becomes potential donor material to use as a transplant in somebody who may have a gastrointestinal infection or some sort of microbial imbalance or dysbiosis, and this is all done under physician care.

In animals, we have some limitations. This does look slightly different. For example, I can't explain to a cheetah why it should eat feces, or why we are giving it a fecal transplant. We have a lot of options, though, for the preparation and administration [of FMTs]. One of the easiest ways is what we call poop pills. We have donor animals that are healthy, their feces is screened for pathogens of concern in that specific species, and once they're deemed safe, we can encapsulate the feces turn it into a little poop pill. And then, for example, for cheetahs, we feed it as a pill pocket.

In more critical clinical cases, we can provide FMTs to animals under anesthesia, obviously with veterinary care. But in a lot of cases where my research is involved, we haven't reached that clinical stage yet. We're trying to kind of preemptively prevent serious clinical issues, and we're trying to do this in a non-invasive manner.

And you know, it's interesting, because humans have this very strong, evolved disgust to feces, which makes sense. It can pass on diseases and parasites. We don't want to be touching it or handling it or anything. Animals don't always have that. So, even if I can't explain to a cheetah why we're giving it feces, there are some animals that will just eat it naturally, and that's called coprophagy.

Professionally and personally, I believe that coprophagy is understudied. I think it is actually a behavior that is surprisingly common in the natural world. But again, because we, as humans, have this very visceral reaction to feces, and the idea of eating feces is so disgusting, and we have that's an evolved defense for us, we have kind of always written it off as this aberrant behavior that we see in animals.

You know, it's, ‘Oh, they must be sick or there's something wrong. This is unnatural.’ But we actually see it is very common.

We actually just published a review paper, myself and a couple colleagues, on coprophagy as a nutritional strategy. We found reported anecdotes and studies showing it in over 150 species, and that's likely very underreported. There are many reasons why animals might eat feces, and we kind of go into this in the paper, but it includes things like nutritional support. For example, rabbits (lagomorphs), they have to eat feces or else they get sick and die, and they have a very specific type of feces that they eat. It's not their normal feces. So, they actually have a physiological mechanism to separate different types of their digesta and then excrete it at certain times for them to actually ingest.

Then from a microbial standpoint, we know that animals eat feces in order to gain microbes, and one of the most common examples of that is when mammals wean from being lactivores. We know from lots of research that the microbes required to digest those 2 different diets—a milk-based diet versus a plant-based diet, for example—are very, very different. So, how does a baby mammal get the microbes it needs to digest a plant-based diet? One of the one of the answers is they eat mom's feces, so they pick up microbes from their parents by eating feces in order to kind of colonize those adult microbes that they need to digest their adult diet.

Milk Microbiome

Just like in humans, the early life microbial communities of mammalian neonates, or very young babies, is formed a lot by that vertical transmission from the mother. We know about this in humans, that vaginal birth is a huge seeding event for these babies, and it's the same for most mammals, and that is an initial colonization that can be really important and very, very valuable for setting up the kind of trajectory of microbial growth and development in these animals.

But we also know that all mammals are born obligate lactivores, so they only drink milk for the first however long of their life, and lactation varies drastically across mammal species. We now know that there are microbial communities in milk. We call them the milk microbiome, that are transmitted from maternal sources to the offspring. And that is a process that happens throughout lactation. And that process changes over time, and we think that this is another kind of more gradual feeding event that starts setting up the young animals’ microbiomes and really training the immune system of the animal on what to tolerate. So, what's a good microbe, what's a bad microbe?

But interestingly, the shortest lactation for mammal is five days. That's it. It's in a hooded seal. And then the longest is six to eight years, and that is in orangutans. So, lactation is extremely variable across mammal species, and milk is not just nutrients and microbes, but there are so many other biological components to milk and so again, like feces, it is this very complex, very important and very fascinating biological substance that's really important for early life development.

Here at the Smithsonian National Zoo, we have a resource that is somewhat strange but very cool. We have the Smithsonian milk repository, which is the largest collection of exotic animal milks in the world. I think we're at over 15,000 samples from, I would say, 1000s of mammal species. It's very impressive, and that has given us a lot of insight into lactation across different mammal species. And it's a really interesting we've only recently started studying the milk microbiome, mostly because we actually thought that for the longest time, milk was sterile.

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