NS – Valerio Sbragaglia – fishing-induced evolutionary changes in shoaling may increase fish vulnerability to other predators

*Featured image photo credit: Valerio Sbragaglia

In this episode, Valerio (Postdoctoral fellow, Institut de Ciencias del Mar, Barcelona Spain) takes us on a deep dive of his paper: Sbragaglia, Klamser, et al. 2022: ‘Evolutionary Impact of Size-Selective Harvesting on Shoaling Behavior: Individual-Level Mechanisms and Possible Consequences for Natural and Fishing Mortality.’ We discuss how size-selective fishing practices can have unintended behavioral and ecological consequences for fisheries populations, and how interdisciplinary collaborations – in this case between behavioral ecology and biophysics – can enhance our understanding of complex feedbacks at individual and group levels. Listen to our chat and then read Valerio’s full paper here!

Fishing for more answers? Email Valerio at valeriosbra@gmail.com.

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!

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Credits

Featured Guest: Valerio Sbragaglia, Institut de Ciències del Mar, Barcelona, Spain

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

Original Music: Daniel Nondorf, University of Virginia, US

Transcript:

You’re listening to Naturalist Selections, a science podcast featuring graduate student and postdoc-authored work in The American Naturalist, produced by the American Society of Naturalists Graduate Council. I’m grad council rep Sarah McPeek and today I’m talking with postdoc first-author Dr. Valerio Sbragaglia! Valerio is currently a postdoctoral researcher at the Institut de Ciències del Mar in Barcelona, Spain. His recent paper is called: “Evolutionary Impact of Size-Selective Harvesting on Shoaling Behavior: Individual-Level Mechanisms and Possible Consequences for Natural and Fishing Mortality.” In this paper, Valerio and his colleagues ask how size selective fishing practices may impact the evolution of shoaling behavior in fisheries populations. They used Dr. Robert Arlinghaus’ lab’s established long-term experimental evolution study on zebrafish, originally established in 2006 by Dr. Robert Arlinghaus in the IFISHMAN group at the Leibniz-Institute of Freshwater Ecology and Inland Fisheries, in Germany. The project was started with funding from the Leibniz-Community Pact of Innovation and Research and was largely the output of hard work by a PhD student Silva Uusi-Heikkilä, who today works in Finland. The lines have been maintained through internal funding by the Leibniz-Institute over the years, and various postdoc projects have been associated with the zebrafish model, including Valerio’s work during his time in the lab. In Valerio’s experiments with the zebrafish, the researchers removed either the largest 75% of fish or the smallest 75% of fish each generation for eight total generations of selection in replicate lines of fish. Several generations after selection stopped, Valerio and colleagues found that fish in the large-harvested lines exhibited increased vigilance while small-harvested lines exhibited decreased vigilance. To dig deeper into the consequences of these behavioral changes, Valerio partnered with two physicists, Pascal Klamser, who shares co-first authorship on the paper, and Pawel Romanczuk. They use fluid movement biophysics to model how these evolved changes in individual vigilance behavior could affect group shoaling behavior and vulnerability to both human fishing gear and non-human predators. Their findings indicate that large-harvested lines may decrease their group shoaling behavior, which may increase their susceptibility to natural predators even while it makes them less vulnerable to mass-fishing practices. These findings contribute to a long list of ways human fishing practices can affect the evolution of fished populations and can have cascading consequences for entire food webs. So without further ado, let’s dive in with Valerio.

Sarah

I’m curious what you think about fishing as a source of predation. Is there some way that it’s fundamentally distinct from, say, predation by another fish species? Is there something unique about that?

Valerio

Yes, I think in a conceptual way, fishing can be compared to a predator because we are acting on mortality of prey or target species, whatever. But I think there is some distinctions that make fishing quite interesting from an evolutionary perspective. So first of all, we have many fishing gears around the world, passive and active fishing gears. A passive fishing gear could be a trapper net, a net that you leave at the sea bottom and wait, then the fish moving around just get trapped into the net. That’s a passive capture. And then there are other gears, such as active fishing gears such as a trolling net, is an active fishing gear because it pushes the fishes and then tries to capture them. Another very interesting active fishing gear is something that I work with in my previous papers is spearfishing, which is a unique kind of fishing predation, let’s say, because humans are underwater with a visual contact with the prey and a spear gun or a pole spear. So they can really select the prey according to a double behavioral interaction, the spear fisher and the fish.

Sarah

Yes.

Valerio

And this can occur on a commercial and recreational basis. So it’s a very complex selection environment if you want, because there are many gears used for different purposes. What accommodates all of them is that if in a natural context, usually larger fish have lower mortality rates than smaller fish in a fishing context, either for commercial or recreational purposes, fishers are selectively search for larger fish. They have more commercial value usually. And then for recreational purposes, a big fish is a trophy fish. So that’s, I think, is the main difference between fishing mortality and natural mortality. It’s size selection. And this is what we simulated in our experiment.

Sarah

Yeah. Are you a fisherman yourself?

Valerio

Yes, I am a recreational spear fisherman.

Sarah

Oh, wow. Cool.

Valerio

When I have time, I would say.

Sarah

Do you think that because of the work you do, you’re more conscious about what size of fish you go after when you’re spearfishing?

Valerio

Yeah. We are working a lot with stakeholders and recreational fishers in order to communicate this important message. That’s quite an interesting topic at the moment because many recreational fishers, in particular spear fishers, have the belief that harvesting larger fish is the most sustainable way to practice recreational spear fishing. They say, okay, these big guys have already spawned. So we just select them and we leave the small ones. We allow the small ones to reproduce, to breed. But then the scientific community is showing that that’s not always the case. We are engaged with NGOs and other stakeholders to communicate this message to the community. It’s very hard because it’s a very deep belief which is governing their behavior.

Sarah

Yeah. I guess there would be the assumption that the larger fish would be the older ones. They’ve already reproduced. They’re kind of on their way out anyway. But we know that it’s the larger, older fish who contribute disproportionately to the reproduction in the population. So you’re really removing the fittest members of the group.

Valerio

Yes. And also, if you look at the regulation of fishing, there are minimum size limits, but not larger size limits, in particular in my context here in the Southern Europe and the Mediterranean Sea. So they are right. They never got the message that you need to save the big ones. I mean, it’s a very interesting topic to dig in.

Sarah

Absolutely. When you select on size, you’re selecting on all of these other traits that you aren’t intending to carry along with you. And in this paper, you specifically looked at social behavior. I’m really curious what gave you the idea to dig into that particular aspect of behavior specifically? Because I wouldn’t have naively suspected that there would be a link.

Valerio

Yeah, you are right. Size is a very simple but complex trade. So it adds so many complexities into that. And so the experiment was inspired by a paper published in Science in 2002 by Conover and Munch which selected on Menidia menidia. It’s a small marine fish.

Sarah

Yeah.

Valerio

Similar experiment, large and small selection.And we got this idea basically not from classic theory or a specific hypothesis but by common sense. After doing several behavioral trials, we were getting results that were not in accordance with respect to the main hypothesis of the study. I was quite depressed at the moment because, OK, nothing makes sense. What’s wrong here? And then just by observing the holding tanks in which selection occurred, if you think just using your common sense, this is a social context. So even if the main hypothesis was that there was a coevolution of body size, life history traits and behavior, there were many hypotheses suggesting that, for example, fast and slow life history were correlated to sociality and social behavior. In reality, what we discovered is that the body size in the selection environment in the lab in our holding tanks was governed by a correlated selection response, which means larger individuals grow faster but also they have more access to the food probably. And this can be driven by the behavior.

Sarah

Yeah.

Valerio

What our experiment is suggesting is that when we were feeding the fish ad libitum with dry food at the surface, so the individuals that were able to spend more time at the surface of the tank feeding, so they have more access to the food resources, were probably able to reach a far larger size. This was directly linked to boldness because the surface of the water is a risky environment for zebrafish, which suffers a lot of predation by birds.

Sarah

Okay.

Valerio

And consequently by looking at classic predictions in collective behavior, you can link boldness with risk perception with social behavior in this particular case, shoaling behavior and shoal cohesion, to be more precise. So the paper represents the outcome of many years of testing and in particular a specific prediction that at the beginning, at the individual level were not really give a specific insight of what was going on in the experimenter.

Sarah

Yeah, and I think the modeling approach you took here was really clever, really complicated for sure, lots of physics involved. A lot of the behavior emerged from the interactions of these individuals, which I thought mimics the social context better than just giving all the individuals their own fixed traits and then putting them together. So what do you think you gain by specifically letting the behavior emerge from having these individuals interact with each other?

Valerio

So first of all, I’m not a physicists, my brother is a physicist.

Sarah

Oh cool.

Valerio

And a good one. And the idea of the model came out in a coffee break. So I was participating to interdisciplinary network project, these kind of workshops which was putting together Princeton University in US and Umbold University Zuberlin. So basically we’re interchanging ideas and groups of people between these two groups in Berlin and Princeton. I was a Postdoc at that time in Berlin and I was involved in this interdisciplinary workshop. At the beginning I was like lost I would say, because a lot of mathematics in particular by physics and a lot of language that I didn’t know about. So the first barrier was understanding the language, which is a common problem when you are putting together interdisciplinary working group.

Sarah

Oh sure.

Valerio

But then in a coffee break I had a chat with Pawel and Pascal Klamser. Indeed the paper I published is a first co ownership with Pascal, who is the researcher that developed the model and tested all the simulations. And he was working at that time about risk perception in collective moment. And we started to chat about my experiments and this model and we really saw that there was an overlapping interest and then we started to combine our ideas it was a long journey. I think it took about four years from the first idea publishing the paper, which is common when you speak to these people because at the beginning you just wasting a lot of time because you do not understand the others. And then I think at the end the final product is a very elegant and new way to look at the problem.

Sarah

Yeah.

Valerio

And regarding your second question, I think the idea that as Pascal and Pawel proposed of using speed and as an emergent property of the model is that the model has been used to indirectly measure vigilance, which is the key parameter of our experiment which is assumed to be linked to boldness. So using this model, we were able to fit the model with experimental data about the tracking and then use an error function, run the model, run the simulation and check the agreement between the model output and experimental data using the error function. As you can see in our paper, in that case we were able to find a good agreement between the model and experimental data. And so that was a strong suggestion that the model was representing in a good way our experimental data.

Sarah

Right. So it’s all about making the experimental data and the data from the model interact and fit well together.

Valerio

Exactly. It’s a two-way interaction.  The experimental data fitting the model and the model is giving back a result to confirm the experimental findings to answer to our main research questions.

Sarah

Right. What a cool collaboration.

Valerio

So this was not planned in this way at the beginning but was a step by step co-production of this interdisciplinary paper. Indeed, if you look at the definition of interdisciplinary, is that kind of collaboration that give us specific insights that would not be possible if you approach that from the different disciplines in a separate way.

Sarah

Right. The emergent properties of scientists working together.

Valerio

Exactly. So for me it was a very inspiring moment in my career, not only for the product by itself but for the process.

Sarah

Yeah. For sure. Yeah. I think the results that you saw in terms of social cohesion were kind of exactly the opposite of what I would have predicted because I would predict that if you’re selecting out the larger fish, you’re left with a smaller fish and I would have expected those smaller fish to school together more and be more cohesive. And you saw the exact opposite. So it’s not this life history driven, fast life history, boldness, all of that. So how do you go about interpreting why you saw this opposite pattern between your large and your small lines?

Valerio

The key issue for understanding that is that what we have found in previous experiments is that the most clear selection response of the lines was in terms of boldness. So this risk that they take on the surface of the tank while feeding. So assuming this boldness is linked to vigilance and adding this model representing the selection lines in terms of shoal cohesion, I think that was the key to have this kind of information. Selecting larger fish, we are selecting those fish that have a specific behavior that allow them to grow to access more food than the others. Probably they also have differences in life history in terms of growth rate. But the correlated selection response of boldness is probably stronger. And the important thing to consider in this experimental system is that we selected on size for five generations, but then the experimental outcome that we have seen in the paper is eight generations after selection has stopped.

Sarah

Right, yeah.

Valerio

So it’s a sort of fixed behavioral changes. It’s sort of steady evolutionary state. We are assuming that.

Sarah

Yeah. And it’s a long lasting effect, too. They haven’t experienced the pressure in eight generations and they’re still fundamentally different. Wow. That is striking. So if you were going to take the results of this experiment and try and look for the same patterns in a natural system, what would you look for? What would you look for in the fisheries? What would you look for in the predators to say that, yes, size selective fishing is increasing mortality to predators.

Valerio

So we have some anecdotal evidence from spear fishing. We are investigating to that. But I think the most interesting aspect of the moment, speaking about a real fisheries scenario is what is occurring here in Cataluña and many other places. So I’m living in Barcelona and here in the Catalan Coast, there is a strong small pelagic fisheries, sardines and anchovies are very big fisheries in the past form of cultural and economic perspective. So what is going on at the moment is the size of the anchovies and sardines is going down. Fishers are saying, okay, that’s a problem. And in particular, our catches are going down as well, together with the average size of the fish. And the problem is tunas, the yellow fin tunas. So what is going on? In the last ten years, tuna’s population has been managed in a very strict way for the first time in history. So there is a strict quota for commercial and recreational fishers. So as a result of this management, tuna’s population is recovering and you can really see signs of tuna is more you can see more tunas than before if you practice sea sports or whatever, they are jumping out of the water. So the population seems to respond to this management. And what some small pelagic fishers are saying is that the tuna are eating out all the anchovies and sardines. So we have started to plan some research project together with them. And as you can see, small projects are usually fished using burst seiners.

Sarah

Yes.

Valerio

And these boats have a very powerful echosounders through which they can locate and even understand the species that is down there and the size of the fish. So they are very powerful instruments.

Sarah

Yeah.

Valerio

So we have started collaborating with them and they gave us some screenshots of the anchovies, changing the conformation of the fish shoals in the presence of tunas. So I have a question for you. If you are a small pelagic fish and there is a natural predator around, what’s your response in terms of shoaling behavior?

Sarah

I think I would want to increase shoaling behavior because the fish can’t catch all of us.

Valerio

Yes. So you are trying to seek cover into the group for the several hypotheses that have been published in the history of studying this behavior, confounding effects toward the predator. So you want to form a big shoal, synchronized shore to confound and escape the predator. Okay. So what is going on at the moment is that the small pelagic fish in the presence of a tuna that you can see both of them on the echo sounder, they are splitting in small groups.

Sarah

Oh, no.

Valerio

Which is totally, I would say a maladaptive behavior towards the arrival of a natural predator. So probably what is happening there is that after several decades of our fishing, probably the small pelagic have been selected for specific behavior that are good to evade the fishing pressure. So splitting small groups so you cannot catch all of us. But then with the recovery of a natural predator, this behavior that we are actually seeing, it is probably not the best one to decrease natural mortality, but it’s a good one for decreasing fishing mortality, which is actually what we are suggesting with our experimental system on zebrafish. So at the moment, this is what we are trying to investigate. So to link this model system with simulations to a real world scenario, which is quite complex but not impossible.

Sarah

Wow, that’s fascinating. I guess I didn’t know that size selective practices were also harming the tiny fish species as well. We think of it affecting the cod fisheries or the collapse of tuna populations. But even when we’re looking at fish that are relatively much smaller, we’re still seeing this size selective change. Oof.

Valerio

Yeah. Imagine that anchovies when you buy anchovies, the price is determined from the size of the individual fish.

Sarah

Yeah.

Valerio

And then with the echosounder, you can clearly, with some experience and the fishers have them, you can clearly estimate the size of the fish.

Sarah

And target those larger groups.

Valerio

And target those or even when you close the net, you can still open it if they are too small. At the same time, what you can also do is selecting for not individual size, but probably collective phenotypes, the shoal size, which is more reasonable. If you form bigger shoals, you are more vulnerable to fishing. So this is probably also another selection that is occurring at the moment, but we don’t know.

Sarah

So we’ve talked a lot about how fishing can increase mortality to different kinds of natural predators in these fishing systems. Are there other consequences of reducing social grouping in these large-selected lines that you could think about? Do we have any evidence that there are other cascading effects other than interacting with predators?

Valerio

Feeding is, I think, the most common one that comes through my mind, but social interaction in general. For example, dominance hierarchies, leadership within the groups could be another big one. So finding fishing grounds move to the right place at the right time using the leaders of the group. This could be I think there is an emerging evidence of these kind of mechanisms in collective behavior, but we don’t know what could happen in terms of fishing pressure on this kind of collective traits. And what we are starting to investigate is a sort of cascading effect, but not within the same species, but in a food web context, which I think is the ultimate question to answer because fishing is harvesting different prey and predators, and these prey and predators are organized in a food web with other components and other also social and economic activities that are built around the ecosystem. So what is the effect of these changes into a global and integrate view of the ecosystem? I think that’s the question we should try to answer. And at the moment we are using this foodweb modeling and trying to simulate that.

Sarah

Very cool. So thinking about the things that the smaller fish species themselves are feeding on, how they’re affecting larger species and all of the connections. Oh, wow.

Valerio

Yeah. And there biomass balanced food web modeling, which are mechanistic. So there are some parameters that can really help you simulate this behavioral interaction. In particular with predator and prey. You have a functional response of prey consumption, and prey behavior is one of these parameters that allow you to have a specific functional response that is close to reality. When you look at the final outcome of our paper in terms of natural mortality, what you are modulating there is a functional response between a predator and predator.

Sarah

Sure. Yeah. Lots to look at.

Valerio

Yeah. In particular, something that I would like to highlight is that all of this is not per se negative because by means we are harvesting fish. Fishing is an important cultural and economic activity. What most of the studies are suggesting, including ours, is that fishing can adapt to fishing pressure and reduce fishing mortality. I think this is positive from a fishing perspective because fish is still there. Catch ability is going down. Yes. But the resource is still there.

Sarah

Right. And it’s more about making sure that our fishing practices aren’t upsetting other pressures on the fish. I think in some ways it is important not to try and separate it out entirely from other sources of mortality on the fish because we don’t want to make it seem like we are doing something entirely apart from nature. We want to have the perspective that we are integrated with the environment and it’s our job to maintain that. I don’t want to say balance, but maybe that flow of energy through the ecosystem, maybe we have to think more like tuna and less like fishermen.

Valerio

Exactly. It depends on the perspective that you used to look at the problem.