Might the health of an ecosystem be affected by the ability of the various species inhabiting it to communicate with each other? That’s the question that marine biologist Mike Gil has been exploring in coral reef systems.
Gil, a post-doctoral research fellow at the University of California, Davis, has analyzed the behavior of non-schooling reef fish in the rich feeding grounds off the remote island of Mo’orea in French Polynesia. These fish perform a vital ecosystem service by consuming algae that can outcompete coral for space and even directly kill coral. Gil and his colleagues found that fish enter risky feeding grounds abundant in algae when they see others doing the same, exhibiting a sort of copycat behavior. But when fewer fish are present — due to overfishing, for example — they are more risk averse and eat less, which can allow algae to grow unchecked.
Biologist Mike Gil scuba diving in French Polynesia.
In an interview with Yale Environment 360, Gil talks about studying these complex social interactions and the role they should play in reef management plans, particularly at a time when corals across the globe are being assaulted on multiple fronts, from pollution to ocean warming to overfishing. These interactions “very much change how we think these systems will respond to changes like fishing,” Gil says. “When you remove those fish, you’re not just removing the mouth that eats the algae, you’re also removing the social influence that fish had on remaining fish.”
Yale Environment 360: To understand the implications of your research we first have to understand the service that reef fish provide coral.
Mike Gil: Many of the fish species that people have come to love in coral reefs, species like parrotfish and surgeonfish, they actually perform an ecologically critical service in that they consume algae that grow on the bottom of the reef. [These algae] are actually competing directly with corals for space. They can shade corals, they can abrade coral tissue with hard, sharp parts, and more recent research shows that these algae can synthesize what we call secondary metabolites, which are essentially chemical weapons that these algae can use to kill coral tissue on contact. So by consuming these algae and preventing them from becoming too abundant on the reef, these herbivorous fish can be vital to the functioning of the greater reef ecosystem.
e360: You and your colleagues came up with a way to observe fish behavior on a reef in French Polynesia without being part of the action. How challenging that was?
Gil: These herbivorous fish are typically large-bodied, highly mobile fish that are very difficult to study in the field. So I came up with this idea … to create sort of a jungle-gym-like structure that would allow us to watch large areas all at once with a bunch of cameras. We actually affectionately refer to this as the “fear frame.” We’re looking at how fish are responding to these dangerous but nonetheless resource-rich habitat patches. Not a lot of places to hide from things like sharks, but lots of algae grow there.
“A given fish is more likely to enter these dangerous feeding grounds if it witnesses other fish doing that first.”
e360: What did your analysis of those videos tell you about how these fish, which belong to a number of different species, were communicating with one another?
Gil: We had over 4,000 decisions by fish to either enter these foraging grounds or exit them into the adjacent reef structures that provide them shelter from predators like sharks and spear fishermen. … What’s particularly cool is that when you have this amount of data, you can extract insights that you otherwise wouldn’t be able to. And so if you or I were to watch a given trial, we would see fish kind of coming and going. They’re not schooling.
e360: When you say they’re not schooling, you mean they’re not hardwired to move as one body.
Gil: That’s correct. None of the fish species that we capture with this study are doing that sort of hardwired schooling behavior. They’re coming and going, seemingly incidentally. What we first noticed, in analyzing our footage, was what we call temporal correlation. Individual decisions to enter or exit this foraging ground are clumped in bursts. They’re actually coming and going in groups, despite not being schooling fish.
And so that grouping of entry and exit events, that could be driven by two non-mutually-exclusive drivers. One would be, these fish — again, different species, not schooling — are actually paying close attention to one another and they’re following one another into these feeding grounds and out of these feeding grounds. That’s one possible explanation. An additional explanation would be that these fish are actually responding independently to some external, shared stimulus. They share predators like sharks, so maybe something in the environment is actually causing them to have this sort of clumped behavior in time, choosing to enter and exit these feeding grounds.
WATCH: Cameras track reef fish social interactions in French Polynesia.
And so we wanted to try to separate those two different mechanisms. And this is where we conducted an experimental manipulation. We wanted to impose a very strong, highly controlled external stimulus into this system. To do this, I tested out my acting abilities and dressed up as a spear fisherman. That’s the experimental perturbation that we imposed. And we saw this community-wide mass exodus from these feeding grounds when the spear fishermen entered, just like you would expect these fish to do. This area’s pretty heavily spearfished, so they’re relatively familiar with seeing these kinds of large things with a pointy stick. You’re seeing this community-wide response, [which] showed us that our experimental treatment worked.
What we then want to do is say, okay beyond that effect, are these fish affecting one another… even when they’re different species and even when they’re not schooling? And our analyses of our mountain of data we were able to extract from our videos indicates that the answer is yes. Fish are influenced by the presence and actions of other fish such that a given fish is more likely to enter these dangerous feeding grounds if it witnesses other fish doing that first. And it’s more likely to exit these feeding grounds if it witnesses other fish doing that first. And an additional cool part, which was unexpected, was that the sensitivity of an individual fish to watching other fish leave this dangerous feeding ground declined when there were more fish around. So any given fish leaving was less influential on a fish if it was surrounded by more fish.
Now, we don’t know why they’re doing this. But all signs point to a perception of greater safety when they’re in a greater number. This is sort of an intuitive thing that humans can relate to this. Going through a haunted house alone is much more terrifying than going through a haunted house with five of your friends around you, right?
e360: So if these individual fish are less likely to leave if there’s a certain minimum density of fish, that means that each individual fish gets to eat more that day.
Gil: That is the ultimate finding of this work. Their feeding rate does not significantly change across fish densities. When there are more fish around them and they stay longer, they are eating more algae, which means they are doing their job of preventing the over-accumulation of algae better. They’re doing that job better and they’re able to do that job better because of a higher density of surrounding fish that, again, share the same predators. We don’t know why they’re doing this, but it does seem that this likely has a lot to do with other fish being around, indicating safety to do one’s job of filling your belly. But for the greater coral reef, it also means algae get controlled better than they otherwise would.
“These fish are potentially able to function ecologically at the community level in a much stronger way when there are more of them around.”
e360: Can anything be said about the minimum density required for these fish to be able to pick up these eat-or-flee cues? How many guests do fish require before they consider it a dinner party worth staying for?
Gil: I don’t think we have the power to answer that yet. That’s something we want to poke and prod much more with additional field studies and importantly with additional mathematical models that simulate across time these phenomena that we observed in this relatively short-term experiment. What does it mean for the kinds of time scales that we care about when we think about sustainability and conservation in these ecosystems? That’s an open question, but one that we’re very keenly aware of and interested in probing more.
So this is stage one, and it shows this phenomenon that we’ve not been able to show before. And honestly, if you would talk to people that have spent a lot of time in coral reefs or particularly field biologists that work in coral reefs, they wouldn’t be surprised by this conclusion. We’re simply stating what is probably fairly obvious to people who have watched this ecosystem. We’re stating this with a level of rigor that no one has been able to state it with. These fish pay attention to one another. These fish are potentially able to function ecologically at the community level in a much stronger way when there are more of them around because of this reinforcing phenomenon that we’re seeing.
e360: You’ve actually been able to tease out the percentage of algae eaten by these fish because of their copycat behavior. How did you discern that, and what is that figure?
Gil: We put a statistical model to the data and that model shows us the strength of different drivers of fish behavior. What we see is that the social information component [of the model] actually accounts for a very large percentage of the variation in these fish decisions to enter and exit these feeding grounds. When we zero out that social information effect, we see around 70 percent decline in community fish consumption.
Gil and colleagues assemble the "fear frame," a structure rigged with cameras to allow them to remotely study fish behavior. Courtesy of Mike Gil
e360: That’s a tremendous amount.
Gil: In fairness, this is just one study in one ecosystem and the exact value of that contribution is likely highly variable across different environmental contexts in different systems that have very different histories. But nonetheless, this does suggest that even if it’s not a dominant factor in driving fish behavior, it is likely a strong factor and one that demands further investigation if we hope to properly model these systems so we can predict how they’re going to respond over time to environmental change. This can very much change how we think these systems will respond to changes like fishing, for example, which we traditionally think of as just removing fish. But what our study suggests, which up to this point has not been formally considered in any models or management plans, is that when you remove those fish, you’re not just removing the mouth that eats the algae, you’re also removing the social influence that fish had on remaining fish. And those remaining fish, according to our data, are likely to eat less when they have fewer fish around them, perhaps because they were overfished. And if they eat less, they’re performing this ecological function less effectively. And potentially making these ecosystems more vulnerable to takeover by algae than we previously thought.
e360: Coral reefs are under multiple threats: pollution, warming oceans, ocean acidification. Where do you see the threat of declining fish populations fitting into that?
Gil: These ecosystems are generally pretty resilient. The big challenge is that we are manipulating land on the coast and that’s causing a lot more pollution in the form of, for example, fertilizer and waste entering these ecosystems. That’s happening in tandem with other local and regional stressors like overfishing. And that’s happening in tandem with other stressors at the global level, like warming oceans and plastic pollution.
These things all happening together is really what is the biggest threat to these systems. It’s variable how important fishing is. Some coral reef ecosystems are really well-managed, and there’s a lot of local compliance among fishermen because they realize that if they want a sustainable fishing industry they need to not overfish the system. But in many coral ecosystems, overfishing is a very big problem. And it’s even more problematic when we’re talking about things like subsistence fishing, because how are you going to tell someone, hey you can’t feed your family because if you as a village do that too much, you threaten the integrity of this ecosystem. That’s a real big challenge to deal with.
“A little bit of nutrient pollution can really tip the scale in favor of algae. And our sole saviors to prevent that algae takeover are herbivores.”
e360: Australia has just announced a multi-million dollar protection plan for the Great Barrier Reef, which underwent catastrophic bleaching events in the last two years. Given your findings, do you think that every reef recovery plan should take into account fish numbers?
Gil: I think the short answer is yes. I think it’s undeniable how important these fish are ecologically speaking by controlling populations of algae. We know how detrimental an overabundance of algae can be to coral reef ecosystems. There’s not really an argument in the scientific community about that. So I think any management plan that hopes to sustain the ecological function of coral reefs has to take into account fishing and how many fish are in the system and try to foster a partnership among stakeholders that allows fish populations to not collapse.
And even if you had a system that doesn’t presently have nutrient pollution and you remove the fish from the system, it may seem like it’s going to be okay in the short term, but all it takes is additional stressors to the system to allow algae to get its foothold and potentially overcome coral and come to dominate the system. So, a little bit of nutrient pollution can really tip the scale in favor of algae. And our sole saviors, I would argue, to prevent that algae takeover are herbivores. So I think it’s essential that we re-prioritize the prevention of overfishing in these ecosystems. But that of course is not an easy solution in some places.
e360: You also say that, based on your findings, as reef fish populations decline because of habitat degradation and overfishing, they may be susceptible to sudden collapses. Why is that?
Gil: There is a feedback loop in this system whereby if you remove fish, you’re removing the social influence on remaining fish. And so if remaining fish cannot perform as well, then those fish may not survive as well. They can’t fill their bellies as effectively. So you can have a situation where removing fish also reduces the ability of remaining fish to survive and reproduce. And if that’s true, then you can have this slippery slope phenomenon where the decline in the fish population could be much more rapid than you would have otherwise thought it to be.
