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, Anna Rouvière talks with us about her new paper Rouvière et al. 2022: ‘The Effects of Local Enhancement on Mean Food Uptake Rate.’ We chat about how you spot locally enhancing behavior in vultures and other creatures, when local enhancement might be a beneficial strategy vs when it might not, how understanding local enhancement behavior can impact species conservation, and more. You can read Anna’s full paper here: https://www.journals.uchicago.edu/doi/10.1086/717207.

Still foraging for answers? Email Anna at anna.rouviere@outlook.com.

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Credits

Featured Guest: Anna Rouvière, formerly St. Andrews University, Scotland

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

Original Music: Daniel Nondorf, University of Virginia

Transcript:

Welcome to Naturalist Selections, an interview series featuring student and postdoc-authored work in The American Naturalist, produced by the American Society of Naturalists Graduate Council. Today we hear from undergraduate student first-author Anna Rouviere about her new paper ‘The Effects of Local Enhancement on Mean Food Uptake Rate.’ Anna conducted her undergraduate research with Graeme Ruxton at the University of St. Andrews in Scotland. She studied local enhancement, a behavioral strategy where foraging individuals cue on groups of other foragers to locate distant food patches. But is this strategy any good? Graeme’s previous theory work from the 90s suggested that animals using local enhancement actually consumed less food than they would if they had searched the environment on their own. Anna’s revised model confirms Graeme’s findings and clarifies a few cases when we might expect local enhancement to still be beneficial for foragers. I spoke to Anna to enhance my understanding.

Sarah:

So the first thing I want to ask you is if you can describe for us what local enhancement is, and how would you determine whether the species that you work on does local enhancing behavior.

Anna:

Okay. So local enhancement is a foraging strategy that’s used in the search for food. And it’s when a searching individual sees a group of animals in the distance and it assumes that there’s going to be food there, even though it’s too far away to see the food at that point. So it joins the group hoping to find food. And in that way, it can locate food more quickly since big groups are often easier to spot from a distance than just an unoccupied food patch. But it is actually really difficult to spot in nature. It’s really difficult to spot because it involves decision making, first of all, which is a difficult thing to study because you’re never in the head of the animal that you’re studying. So you don’t know why they make the choices they make. And it’s also a behavior that occurs over very long distances. So there have been many empirical studies that have said that a certain taxon uses local enhancement. And the way that they showed that it’s local enhancement is that they showed that individuals of that taxon purposefully join a feeding group. So, for example, a bird lands out of feeding group more often than would be expected just by chance, if that makes sense. But the thing is, there are many reasons to join a feeding group other than wanting to find food more quickly. I mean, you could join a group for safety because there’s safety in numbers. You could join a group because it facilitates your access to food, like cattle egrets following cattle around because they dig up insects for them. You could also join a group to find a mate. So then how can you tell if it’s actually local enhancement? And it’s really difficult, but I do think that’s kind of where studies like ours come in and are useful because instead of empirically trying to figure out which animals use local enhancement, we can try to theoretically predict which animals would benefit from it, and then that would give us an indication on which animals probably do use it.

Sarah

Is there one animal system where you think there is really convincing evidence of local enhancement behavior? I know in your paper you talk a lot about vultures.

Anna

Yes. Vultures are kind of the poster child for local enhancement. I feel like because, as obligate scavengers, they have a food source that’s very rare, and it’s very scarcely distributed in the environment. And as the paper we wrote kind of outlines, a rare food source is one of the reasons why you would want to use local enhancement. And yeah. So there’s been tons of studies on them, and it’s been shown that they do kind of join carcasses that are already occupied maybe more often than they would join other carcasses. The reason why I find that kind of more convincing than other studies like that is that they’ve also looked at the detection distances of vultures. So there was this kind of old paper where they were flying next to vultures in a glider and trying to figure out at which point the vulture sees this whole plume of vultures circling over a carcass. And it was often from tens of kilometers away. And you wouldn’t expect a vulture to be able to see just a single carcass on the ground from that distance. Right.

Sarah

Huh. Well, that makes me wonder if part of the reason why the vultures circle over their food before they land is to maybe facilitate local enhancing? Do you think that’s possible?

Anna

Maybe. I don’t know if that would be the kind of behavior that you would want to facilitate for others?

Sarah

Yeah.

Anna

I don’t know.

Sarah

I don’t know how you would test that, but it’s such a conspicuous display that they do. If I was a Vulture, I would certainly follow that.

Anna

Yeah. But yeah, there could really be reasons to believe that it has something to do with local enhancement and making that food more visible. We’d have to find a way to test that. Could be exciting!

Sarah

So getting a little bit into the theory of your paper and why you wanted to undertake this study, the paper that you wrote for American Naturalist revisits a previous paper in American Naturalist from 1995 that your advisor Graham Roxton wrote. You talk a little bit in the paper about why that older paper was so controversial when it first came out. So why was it controversial and why did you want to go back to it and dig into it again?

Anna

Yeah. So that paper, when it came out, it was quite the bombshell in the whole local enhancement foraging behavior research area because it basically said that local enhancement decreases feeding efficiency. And that was controversial because when you think about local enhancement as behavior and what it does, it actually reduces an individual’s search time, time spent searching for food. So you’d think if I spend less time searching for food, then surely I’m going to be able to eat more in a given time unit over a certain amount of time.

Sarah

Yeah.

Anna

But what that study said was that it was actually the opposite. That reduction in search time led to less efficient feeding, and that’s quite counter intuitive. And it didn’t really explain why that would be so it caused a lot of puzzlement in that field. So 25 years later, we kind of wanted to dig back into it for several reasons. First of all, because it was such a controversial and surprising finding. And also that study used a model of local enhancement. And when we looked back into that model, we found two main reasons why we wanted to dig deeper into it. And the first one was that it made a very restrictive assumption in its simulation of local enhancement. And that is that it assumed that once a searching forager has spotted a group, it will lock its trajectory in and head towards that group no matter what. So when we reviewed that, we thought, well, maybe that’s why the model says that local enhancement is detrimental. And the second reason why we wanted to revisit that model is that in the original study, the parameter range that was explored wasn’t very wide. And what I mean by that is that they didn’t simulate local enhancement in situations where the food patches would be very rich or in situations where there would be very few food patches or lots of other situations like that. So we wanted to really dig deeper with our investigation and try to uncover the effects of local enhancement on the uptake rate of food in as many situations as we possibly could to get that kind of overall view.

Sarah

Yeah, I think that’s so clever, because it also helps you identify particular places in nature where you might look for local enhancement, like you said, and places where you’re probably not going to see it.

Anna

Yeah exactly.

Sarah

I would say in the 1995 paper, I think the foragers had a little bit of tunnel vision. They were very singularly focused. And pulling the blinders off is helpful.

Anna

Exactly. See the thing is, how correct was that? And how correct is what we did as well. In our simulation, we said, well, you know, when a forager sees a distant group, it’ll start traveling towards it. But if that group disperses in the meantime, then it’ll resume random searching. And if it sees something else in the meantime, it can change its trajectory. But if we’re looking at a bird or a bird species or something like that, maybe when they’re in a very directed journey, they’re not really sweeping the environment looking for other things. So maybe there is some aspect of tunnel vision, but we chose to kind of go on the other end of the spectrum. Because if we went on the complete opposite end of the spectrum and there was still this kind of detrimental side to local enhancement, then we would know that it definitely wasn’t because of that kind of tunnel vision assumption.

Sarah

Mm hmm. And you ran all these simulations and your results really hold with what your advisor found in 1995. Were you guys surprised by that?

Anna

Yes, we honestly, we were genuinely surprised. We really thought that the assumption was at least mostly responsible for local enhancement coming out as detrimental in terms of uptake rate. So when we saw that that was still happening, we really started scratching our heads and trying to figure out why it might actually decrease feeding efficiency like that. And we came up with a hypothesis which I don’t know, maybe I can try to explain?

Sarah

Yes, please.

Anna

Okay. So imagine that you can see an environment from above, right. And you can see several patches of food that are dispersed in the environment. And there’s a bunch of animals roaming around looking for food. Now, if these animals are not using local enhancement, then you’d expect that after a while of random searching, they would all be kind of equally distributed at all the food patches. Now, imagine that the foragers are more easily attracted to an occupied patch than an unoccupied one, which is what local enhancement is. What you’re going to see probably is kind of large groups of animals concentrated on a few patches while other patches are left untouched. So you can imagine that the exploited patches are going to get depleted at some point, and especially if they’re very crowded, and then the animals are going to disperse in search of more food. But now they’re all clumped together. So as soon as one of them finds another patch nearby, they’re probably all going to swarm towards it because they’re still using local enhancement. So once again, each forager isn’t going to get very much food. And this continues. All the while, you might be seeing some perfectly good food patches on the other side of the environment that you’re looking at. Sure. But they’re unoccupied because the group is clumping together. So that’s what kind of what we came up with to explain why in many cases, not all cases, but many cases, local enhancement might actually decrease the feeding rate of an animal.

Sarah

Your discussion of that in the paper and your explanation right now kind of blew my mind. Because I’d never thought of that before. And it sounds like you guys hadn’t really thought of it either before you recovered this result, which is that when you reduce search time during foraging, you’re also reducing search area.

Anna

Yeah, so at first glance, it appears counter intuitive. But when you start thinking about what actually happens, it does kind of make sense.

Sarah

It definitely does. Yeah. And I think one of the coolest results that you found in exploring all the wider range of parameters that you built into the new version of the model was the idea that local enhancement could be beneficial for individuals as long as there are very few of those individuals in the population. I think that really makes sense given what we’ve just been talking about, how there might be these two strategies, and there’s kind of this negative frequency dependent selection maybe on locally enhancing behavior because of how it reduces your ability to find food. Do you know of any examples in nature where we see both of those strategies going on?

Anna

Yeah. So that’s a good question. Like I said, local enhancement is really hard to spot. So it’s also hard to know if that coexistence is actually happening in nature. But you know it might be possible that within a species, the decision to use local enhancement or not can, for example, depend on the personality of an individual. And I’m basing this on a paper I read when I was doing research for my study, and they looked at barnacle geese in captivity, and they found that the geese with the highest scores in terms of boldness tended to queue on others a lot less when foraging. Right. So maybe there’s this kind of individual variation going on when we’re looking at a species when we’re looking interest specifically. But that being said, it’s also really important to keep in mind that as a local enhancer, the group that you cue on doesn’t have to be made up of members of your own species.

Sarah

Sure. Yeah.

Anna

Right. So if you consider the, quote, unquote population as being a community of species, some of which use local enhancement and some of which don’t, then there you might have a coexistence, too. So, for example, say you have two species, two different species. One of them is terrestrial, walking, and the other is a bird species. They might eat the same thing, so they might target the same kind of sources of food, but one of them is going to use local enhancement and another might not. So the bird might be able to spot very distant occupied patches of food and use local enhancement, whereas the terrestrial animal, like the walking animal on the ground, might not be able to use it. So maybe that’s another way that that coexistence exists in nature.

Sarah

Oh, yeah, I think that’s a great idea. I definitely have seen examples of that where one species is really adept at finding the food and then there’s another species kind of trailing them. So if you could design a dream experiment based on your model and maybe one of the predictions that came out of it, what would you want to test and what animal would you want to use? Or animals if you’re thinking about a whole community.

Anna

Mm hmm. So one thing that I found is that species that have a food source that’s very rare and sparsely distributed in the environment benefit most from what would benefit from local enhancement. And I guess it could be really interesting to go back through the literature again and find an example of a species that has been reported to use local enhancement based on its group joining behavior, but that is not expected to use local enhancement based on our results and then looking on that group joining behavior more specifically and trying to figure out if it really is local enhancement or if it’s more likely something else that’s driving the group joining behavior.You could equip individuals of that species with GPS trackers and maybe if they’re birds, like down facing cameras so you can see what they’re flying over. And ideally, we could even do all of that again with another species this time that is expected to benefit from local enhancements and compare the two results. So, yeah, maybe we could get those two kinds of species on opposite ends of our predictive spectrum. But again, the reason that we model local enhancement is because it’s so difficult to identify in the field. So I don’t know if there actually is a good way to test these predictions in nature, but I’d be excited to find out.

Sarah

Yeah. I mean, I think you’re definitely on the right track. Especially looking for cases where you don’t expect individuals to benefit from doing local enhancement compared to cases where you do.

Anna

Yeah.

Sarah

And I think it’s our role as theoreticians and as empiricists to try and break our understanding of something by looking for cases where it seems the least likely. And that’s where you really test whether your predictions are correct or supported.

Anna

Mm hmm. That would be really interesting to try out if I have some GPS trackers and microscopic cameras on hand.

Sarah

You know, the technology is getting pretty good.

Anna

It really is. Yeah. New exciting opportunities.

Sarah

Cool. Do you think that’s something that you would want to continue to work on into your PhD?

Anna

I do want to go into maybe more conservation side of research, something that would have conservation applications.

Sarah

Yeah.

Anna

But local enhancement is actually sometimes used for conservation purposes because it’s density dependent behavior. So for vultures, for example, they’re in decline. So what’s going to happen to their foraging efficiency if they can’t use local enhancement as much as they could before? Because there aren’t any vultures to queue on, then are they going to actually be able to find food? So there are some conservation applications.

Sarah

Cool. Yeah. We’ll see where it takes you! Well, I think it was a really fantastic paper to read. I think it was so well organized and so written. And I loved the way that you stepped us through each of the questions that you were asking. And yeah, it was just a really clever paper and fun to read. Congratulations.

Anna

Thank you so much. Thank you. It’s really nice to hear.

Thank you so much, Anna, for our thoughtful and fun conversation. We’re all super excited to see what you’re going to do in your graduate work! Thank you to the editors and reviewers for their contributions to the paper. Thank you to Daniel Nondorf for composing our lovely intro and outro music. And thank you for listening! Now that we’ve attracted your attention, let’s all locally enhance on Anna’s paper and then ask her even more questions! Discussion doesn’t have to end with the discussion section. I’m grad council rep Sarah McPeek, here to keep the conversation going.