NATURALIST SELECTIONS IS AN INTERVIEW SERIES PRODUCED BY THE AMERICAN SOCIETY OF NATURALISTS GRADUATE COUNCIL. WE SHOWCASE GRADUATE STUDENT AND POSTDOC AUTHORED WORK IN THE AMERICAN NATURALIST, A PREMIER PEER-REVIEWED JOURNAL FOR ECOLOGY, EVOLUTION, AND ANIMAL BEHAVIOR RESEARCH. CATCH UP ON EXCITING NEW PAPERS YOU MAY HAVE MISSED FROM THE JOURNAL, AND MEET SOME TRULY BRILLIANT EARLY CAREER NATURALISTS!

In this episode, Claire Teitelbaum chats with us about her new paper Teitelbaum et al. 2022: ‘Habitat specialization by urban wildlife reduces pathogen spread in urbanizing landscapes.’ We talk about how to dissect complex patterns in ecological models, and how different kinds of pathogens may spread in urban landscapes, and how Claire’s work can inform conversation efforts in urban spaces. Is habitat specialization always a good strategy to reduce pathogen spread? You can read Claire’s full paper here: https://www.journals.uchicago.edu/doi/10.1086/717655.

Infected with curiosity about urban disease ecology? Email Claire at claire.teitelbaum@gmail.com!

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Credits

Featured Guest: Dr. Claire Teitelbaum, Quantitative Ecologist at the USGS Eastern Ecological Science Center

Host, Editor, Producer: Sarah McPeek, University of Virginia, US

Original Music: Daniel Nondorf, University of Virginia, US

Transcript:

You’re listening to Naturalist Selections, an interview series featuring graduate student and postdoc-authored work in The American Naturalist, produced by the American Society of Naturalists Graduate Council. I’m Sarah McPeek and today I’m talking with postdoc first-author Claire Teitelbaum about her new paper, ‘Habitat specialization by urban wildlife reduces pathogen spread in urbanizing landscapes.’ Claire completed this work during her PhD at the University of Georgia, US, where she was co-advised by Richard Hall and Sonia Altizer. Her graduate work focused on understanding how animal movement among urban and rural landscapes affects the transmission of pathogens. The models in this paper build off Claire’s research on white ibises, which transmit salmonella and other bacterial pathogens as they move between urban and rural habitat patches. In the paper, Claire uses a spatial model of animal movements among resource patches to explore how pathogen prevalence in a host population varies across space and time in landscapes with different proportions of urban vs. rural habitat patches. Her findings suggest that animals that specialize on one habitat type, either rural or urban, experience reduced pathogen transmission by limiting contact among urban-specialized and rural-specialized subsets of the host population. I’m excited to transmit to you all of Claire’s insight about the complex world of ecological population modeling.

Sarah

I thought it was really interesting that there seemed to be a lot of conceptual overlap between spatially or temporarily patchy environments and what you described as urban environments. So would you consider an urban environment to be a type of patchy environment, or do you think that there’s something particularly unique about urban spaces that distinguishes them from other types of patchy habitats?

Claire

Yes and yes. So I think that is like an astute observation. And it’s definitely true of this model, especially because the model is designed to be general. And I think we make a few points in the paper about how you could think about it in terms of other sorts of patchy environments that do or don’t vary temporarily. But at the same time, obviously, intuitively, urban environments are distinct from other sort of patchy environments in different ways. So I think one of those is a question of spatial scale, maybe that some people might consider an urban environment actually to be very homogeneous because maybe from one side of a city to another, you don’t get a lot of variation at small scales, but at the big city wide scale, it’s all sort of the same. Whereas that might not be true for an area of the same size right next door. With everything in ecology, there’s this question of scale. But for me, I think one of the most interesting things about urban environments is like the degree of human influence and human control for an environment that when you looked at diversity of habitat types across space, a natural versus an urban one, that what is composing those habitat types is really different in an urban environment. And I also, I say urban and natural because it’s convenient, and I think we kind of know what that means, but it’s convenient and somewhat arbitrary and definitely constructed distinction. So I don’t want to imply that people aren’t part of nature and people don’t affect nature outside of urban areas. But I think if I say urban, you more or less know what I mean? And that’s helpful.

Sarah

Yeah, I guess one thing that struck me from your description of these urban environments and the way that you envision that in your model was the consistency of the resources across time, which was something that I hadn’t really thought about. But it’s true that plants are only flowering for a certain time, but if you have a Hummingbird feeder, you can feed your hummingbirds basically all year round. So that’s a consistent resource patch across time as well as space.

Claire

Right, yeah. And that maybe is the distinction or an important distinction is like maybe urban environments vary a lot across small spatial scales, but not as much across time. And that is sort of the point that we’re making in the paper.

Sarah

Yeah. But I also know that concentrated resources can also come with cost, one of them being disease. So is that what really motivated you to think about this in your paper?

Claire

Yeah. This paper, for me, it’s exciting because it was like sort of in my dissertation. It’s sort of like this third or fourth third of a series of things, and it was putting them all together. So that is exciting. One of the papers was a somewhat simpler version of the model. I don’t know if it was simpler, but it just looked at movement and didn’t have a pathogen component. And we also looked at movement behavior in the Ibis system. So looking at how Ibis move between natural and urban sites in Florida, and this paper was trying to, like, take those that model and those observations and put them together to understand the pathogen component

Sarah

Did you know that you wanted to look at pathogens when you first started your PhD in this project? Or did that come out of observations of the movement of the Ibises in these urban versus natural landscapes?

Claire

Yeah. One of the biggest goals of the Ibis project is to sort of link urbanization and pathogen transmission. Specifically, the project is focused on Salmonella, you know, just understanding how urbanization affects health. Salmonella is interesting because it can also affect people. But I personally, yes, definitely knew I wanted to do the pathogen part. I had studied different aspects of animal movement behavior before and always had this sort of line in the introduction or the discussion of a paper saying, like, animal movements are important because they affect things like seed dispersal and pathogen transmission. And so I wanted to be able to actually put those things together and see how they’re actually related instead of just saying, well, in theory, this is important.

Sarah

So it sounds like you started with the simpler model of just movement, and then you kind of built off of that to add more parameters and look at more complexity.

Claire

Yeah. That also required sort of simplifying the movement model, though. Oh, yeah.

Sarah

How’s that?

Claire

In the original the first paper, let’s say we looked at how animals might make decisions about when to depart a patch. So if you’re in a really temporarily variable environment and you don’t have information about the places where you’re going because they’re far away, you can’t sense that far. And it’s not predictable. So unlike, like, a seasonal migration where, you know, okay, well, it’s Greening up in the Northern Hemisphere. Now if you’re in an environment that’s less temporarily predictable than that, you don’t know what’s going on elsewhere. So if you’re just basing your decision to move on local cues, what is the sort of optimal decision making rule that you can use? So we looked at one where animals might be deciding to move based on conspecific density or resource availability or just randomly, which is sort of how the classical random walk models work. And we found that the sort of most optimal movement rule tended to be a combination of resource availability and density. So that’s the one movement role that we took over into this pathogen transmission model so that component of different species might move different ways sort of got taken out so that we could add more on top of it.

Sarah

That makes a lot of sense. Yeah. Simplify one aspect so you can complicate another. I was really interested in the idea of frequency dependence because I know in your model you set up that you could be a specialist or a generalist, and the proportion of specialists versus habitat generalists was related to the proportion of habitat that was considered urban versus natural or rural. I’ve also read a lot of theory that suggests that specialization is kind of a frequency dependent behavior in terms of how it is expressed with selection, because if you are a specialist but everyone is in the same habitat patch that you are, then there might be a cost of that because fewer resources for an individual. So specialization might be favored as a rare strategy. How do you think that could relate to the results that you find here?

Claire

Yeah, that is definitely true. And those sort of starting conditions that we chose where it’s almost sort of like an equilibrium type assumption that if we started with more urban specialists, let’s say those habitats would end up with higher densities because they would move in no matter where they started, they would move and they would be more likely to stay than to leave. So we then would probably experience relatively high mortality rates at the urban sites. And we didn’t include birth in this model. We just ran it for a non breeding season. If you did have that component, I think that at some point you should end up with it balancing out, given the right construction of the model, that the ratios should end up the way we started them. And the thing that complicates that a little is in the modelwe had a component of the model, a parameter of how much resources are available at urban sites. So if urban sites have really high resource availability, they can support more individuals. And then in that case, you might expect there to be able to be more urban specialists than would be expected based on the number of patches, just because each patch can hold more.

Sarah

Yeah, that makes sense. I was also really interested in your result that the pathogen prevalence ended up being highest at intermediate urbanization, and that when everything was fully urban and when everything was fully rural we actually saw lower pathogen transmission than when there was this patchy habitat. Were you surprised by that at all?

Claire

Yeah, definitely. This is the story of doing mechanistic models. I feel like is it surprising? And then it makes a lot of sense once you figure out because we put all the mechanisms in the model. So it was all there in the first place. We just didn’t know exactly how everything would balance out. But that I think the most interesting thing about that finding to me is that all environments pretty much fall somewhere in the middle. There’s no environment that we would say is 100% stable, like these urban environments. So that’s sort of the realm in which we’re actually observing things. And within there we still had this sort of hump shaped relationship even in that middle section. But the ends of it, which we’re comparing it to, are sort of like the toys, the null hypotheses in a way. They don’t really exist.

Sarah

Yeah. Do you think that that hump shape of that relationship would hold for a lot of different animal taxa in these kind of patchy habitats, or do you think there’s aspects of those animals, maybe behaviors or life history that might shift that relationship?

Claire

Yeah, I think it’s going to depend on a lot of things. The first thing that isn’t about the host taxon, but I think the pathogen transmission patterns could make a big difference. So if we had a density dependent transmission mode here, if it was frequency dependent, where it doesn’t depend on the density at the patch, that could make a pretty big difference there because high densities at urban patches was one of the main mechanisms that was driving that hump.

Sarah

What would be the next thing that you would add to this model or maybe subtract to get it?

Claire

Interesting question. I think this is like a slightly technical one. Not technical, but I am interested in different types of pathogens and different types of transmission and how that could affect the patterns. You see, a lot of the pathogens that I’ve studied have an environmental stage, so they persist in the environment and they then get taken up through feeding, especially. And that really could complicate things especially. You could derive even a greater benefit from leaving somewhere and having it be empty for a while and sort of get cleaned out.

Sarah

That just made me think about I wonder if the environmental stage of the pathogen could itself be affected by resource variability or consistency independent of the host. I guess it really depends on what kind of pathogen you’re looking at.

Claire

Yeah. You can imagine definitely maybe not directly related to host resources necessarily, but the environment really does determine the persistence of the environmental stage of almost any pathogen. Right. That like microbe is going to persist for longer at colder temperatures almost universally and things like that. So like salinity and PH of the water that it’s in. Inevitably, when I’m thinking about the Ibis system that’s different between the natural wetlands and like a little pond in an urban Park, I don’t know exactly what I don’t take water samples, but there’s no way the PH in those two places is the same, and there’s definitely no way the salinity is the same. So you could also have that component differ. And you can sort of the fun thing about modeling is it’s for me often about asking, well, how much of this do I need to do before the result gets different? Because we know almost inevitably I can make the results come out differently if I inflate this parameter to some enormous unrealistic value. But does the value have to be unrealistic for me to get there? At what point do those things change? That’s when I’m just like, I feel like I’m turning the dials and seeing what happens.

Sarah

Taking the perspective of, say, a restoration ecologist who wants to conserve habitat within cities to provide resources for wildlife, but is also concerned about disease risks over density, all of those kinds of things. What kinds of factors should they keep in mind when they’re designing these habitats?

Claire

Yeah, it’s a really interesting question and one that I don’t really feel qualified to answer because there’s so much that goes into that. Right. But I think one of the main things is just, like, clearly defining what the goals of the restoration even are, and that’s sort of just like that’s, like almost a tenet of project management or something. But if you don’t, you might not care about infections if they’re not, if they don’t have an effect on the population size, if you just care about population size, then you can discount the sort of pathogen component and just think about what might maximize the effectiveness of this patch that I’m building for population size. And that would probably be things we often think about, like connectivity to other patches. If you are concerned about pathogens, making sure that the thing that you’re building is not going to be a source of them. So that’s like cleaning your bird feeders, for example, or I don’t know a lot about I think we think about pollinators a lot. I don’t know a lot about diseases and bees, but it’s definitely a thing. And, from my perspective, something that’s interesting, but I don’t know if it’s extremely actionable is thinking about the movement behavior of the species that you are trying to protect in some way and thinking about whether you want to encourage them to move or you want to discourage them from moving. As we sort of show here, that resource availability can be really important for encouraging or discouraging movement. If you, for example, had your little habitat path in a place that was, like, surrounded by busy roads, and you really didn’t want whatever was coming in there to get squashed, you might want to encourage them to come and stay for a while, and then you would maybe focus on consistent resource availability, even though that’s maybe not as natural as having a lot of native plants that senesce or only flower for, like, a small amount of time.

Sarah

Yeah, definitely. I guess that also comes down a lot to whether the animal you’re working to conserve is a specialist or a generalist. That’s a hard word, either in types of resources that it uses or even in sites like site fidelity could be really important there, right?

Claire

Yeah.

Sarah

I thought it was a really cool paper. It gave me a lot to think about. I hadn’t really thought a lot about disease as being a key component of urban environments and how they might affect wildlife. So that was really interesting to think about. And I just thought the process of building the models and the way that you walked us through it was really intuitive, and it was a really good lesson for me as someone who also does a bit of modeling in how you build this complexity from the ground up and then tease it apart mechanistically. So Congratulations. Very cool.

Claire

Thank you. Yeah, it was fun to work on. It was really nice to put all of the components together, have, like, resources, drive movement, which drives pathogen transmission, and have all of those links in one place was really something I’ve been wanting to do. So I’m glad that it came across that way.

Sarah

Yeah, absolutely it did. And I think there’s still a lot of cool things to do.

Claire

Yeah, definitely so many things to do.