Lillian Tuttle: Coral-reef predators must learn that the cleaner goby is a friend, not food

Lillian Tuttle of NOAA’s Pacific Island Regional Office in Honolulu, Hawai‘i talks about the inspiration behind her new research Differential learning by native versus invasive predators to avoid distasteful cleaning mutualists” and the privilege we have to be able to observe the natural world.

About the paper

A bar jack (Caranx ruber) swims over a field of soft gorgonian corals near Eleuthera Island in The Bahamas. Photo credit: Lillian Tuttle.
A bar jack (Caranx ruber) swims over a field of soft gorgonian corals near Eleuthera Island in The Bahamas. Photo credit: Lillian Tuttle.

What’s your paper about?
My co-authors and I studied the behaviours of invasive lionfish and cleaning mutualists on coral reefs. Lionfish are voracious predators across the Caribbean – they eat prey fish up to half their own body length and hunt dozens of fish species – and so, there was concern amongst conservationists that lionfish might threaten a very important fish in the region, the cleaner goby. The cleaner goby is a small, ubiquitous, and conspicuous member of Atlantic coral-reef communities where their role is to remove the parasites, dead skin, and mucus from the skin of larger fish “clients.” Thus, if lionfish were to eat cleaners, there could be cascading negative effects on the health of many coral-reef inhabitants. Using a combination of observations and experiments conducted in both the field and lab, we set out to determine whether or not invasive lionfish and native Caribbean predators 1) consume the cleaner goby, 2) change their behaviour towards the cleaner to be more or less antagonistic/mutualistic over time, and 3) affect wild populations of the cleaner goby.

How did you come up with the idea for it?
My co-author, Robbie Lamb, was an undergraduate field assistant during the early stages of the lionfish invasion of The Bahamas. In 2007 he became interested in this question of how lionfish interacted with the cleaner goby, so he brought both species into the lab for feeding trials. When I started as a graduate student in 2010 in the same lab that Robbie had worked in, I independently became interested in the same question, so I set out to build upon Robbie’s work. What started as relatively straightforward feeding trials in a few aquaria became a much more complicated set of questions and experiments over the course of my doctoral dissertation, which I answered with the help of another undergraduate field assistant and co-author, Allison Stringer…

There were so many unexpected results! First, while invasive lionfish seemed eager to gobble up the cleaner goby, it appeared that native predators also ate the goby, even though we had expected them to solicit cleaning from the goby. Second, it appeared that the goby was protected by a skin mucus because predators, both native and non-native, hyperventilated after eating a cleaner, which is something we had never seen predators do after eating other small fishes. Could lionfish and other predators learn to avoid eating the cleaner? Could they learn to cooperate with the cleaner? Did the patterns and behaviours we saw in the lab help explain those we saw in the field, especially on reefs with co-occurring lionfish and cleaners?

What are the key messages of your article?

Coral-reef predators must learn that the cleaner goby is a friend, not food:

-- Three small cleaner goby (Elacatinus genie) co-inhabit a coral head with sponges and annelids (social feather duster and Christmas tree worms) in The Bahamas. Photo credit: Lillian Tuttle.
— Three small cleaner goby (Elacatinus genie) co-inhabit a coral head with sponges and annelids (social feather duster and Christmas tree worms) in The Bahamas. Photo credit: Lillian Tuttle.
  • Cooperative cleaning behaviour may not be entirely instinctive, even among native fishes that have co-evolved on Caribbean reefs – native predators initially eat the cleaner goby, mildly hyperventilate in response to the cleaner’s distasteful “spice,” but eventually become the most frequently cleaned fish on coral reefs.
  • Invasive lionfish are initially eager to eat a cleaner, but after experiencing the cleaner’s intense “spice,” quickly learn to stay away from the cleaner altogether. Lionfish rarely interact with the cleaner in the wild, either antagonistically or cooperatively.

Thanks to its protective and distasteful mucus coating, the cleaner goby is among the remarkably few fishes on Atlantic coral reefs to escape the jaws of invasive lionfish!

How is your paper new or different from other work in this area?
The presence of an invasive predator in the Caribbean, the lionfish, allowed us to investigate the behavioural mechanisms by which a cleaner fish interacts with naïve and experienced, native and non-native predator fishes. Our results challenge the commonly held belief that cleaning mutualisms are instinctively cooperative interactions between cleaner and client. We present behavioural and demographic evidence from the field and lab that coral-reef predators must overcome their urge to eat the cleaner before they learn to cooperate with the goby, in the case of native predators, or learn to avoid the goby altogether, in the case of the invasive predator. This appears to be true of cleaning interactions on coral reefs in the Caribbean region but has yet to be tested in other regions with different cleaner and client species.

Does this article raise any new research questions?
What kind of trade-offs exist between a predatory fish choosing to cooperate with the cleaner goby or “cheat” by eating it? Are these trade-offs context-dependent? For instance, is a fish’s propensity to learn to cooperate affected by its parasite load?

What is the nature of the compound in the cleaner goby’s mucus coating that is so distasteful to potential predators? Is this compound found in other species of the same genus, even among those that do not clean other fishes?

Who should read your paper (people that work in a particular field, policy makers, etc.)?
We would love for coral-reef managers in locations affected by the invasive lionfish to read the paper and recognize both the importance of cleaners in the ecosystems they protect and the relative resistance of this cleaner to an otherwise devastating invasion. Additionally, we hope that anyone interested in the ecology and evolution of cooperative behaviour will find our paper fascinating!
 

About the research

What is the broader impact of your paper
Our paper addresses the critical conservation threat that invasive species represent for all native species with which they interact in their new habitats. On Caribbean coral reefs in particular, there is an urgent need to understand the ecological effects of invasive lionfish, which are voracious predators with the potential to weaken the resilience of reefs that are already threatened by a litany of other stressors, including climate change and overfishing.

A close-up of an invasive lionfish (Pterois volitans) in The Bahamas. Photo credit: Robert Lamb.
A close-up of an invasive lionfish (Pterois volitans) in The Bahamas. Photo credit: Robert Lamb.

Did you have any problems setting up the experiment/gathering your data?
We present the results of a series of experiments that occurred over 6 different summers of intense fieldwork. During that time, the most persistent threat we faced was from tropical storms and hurricanes, which occasionally interrupted experiments and observations. Also, we participated in hundreds of scuba dives to observe fish in their natural habitat, to set-up experimental densities of lionfish on patch reefs, and to capture hundreds of fish needed in our lab experiments. This required an enormous amount of coordination with field station staff at the Perry Institute of Marine Science and the Cape Eleuthera Institute, both in The Bahamas, and at the Central Caribbean Marine Institute in the Cayman Islands. We thank them for their hard work and patience in facilitating our research!

Were you surprised by anything when working on it?
Yes! As noted above, there were many unexpected results. While we set out to focus on interactions between invasive lionfish and the cleaner goby, it became clear that the interactions between native predators and the cleaner were just as interesting. After all, we did not expect there to be such a pronounced response to the “spicy” mucus coating of the cleaner, and such a latency to learn to cooperate among some native predators. These results opened up areas of inquiry that we would not have investigated otherwise, namely the evolutionary mechanisms that allow for cleaning mutualisms to exist and persist.

What does your work contribute to the field?
As noted above, our results challenge the commonly held belief that cleaning mutualisms are instinctively cooperative interactions between cleaner and client. We present behavioural and demographic evidence from the field and lab that some coral-reef fishes must overcome their urge to eat the cleaner before they learn to cooperate with it, in the case of native predators, or learn to avoid the cleaner altogether, in the case of the invasive predator.

What are the big questions still to answer?

  • What are the ecological and evolutionary mechanisms that allow cooperation among species to persist and thrive?
  • How will the ever-increasing rate of species introductions and climate-induced range-shifts affect recipient biological communities?
  • What can be done to protect vital ecosystem services and functions in the face of species introductions and other environmental changes?

About The Author

Study co-authors conducting fieldwork in The Bahamas. Counterclockwise from left is Allison Stringer with a live lionfish (Pterois volitans), Robert Lamb conducting a transect survey, and Lillian Tuttle observing cleaning stations at a coral patch reef. Photo credits: Lillian Tuttle, Tim Pusack, and Severin Vaillancourt, respectively.
Study co-authors conducting fieldwork in The Bahamas. Counterclockwise from left is Allison Stringer with a live lionfish (Pterois volitans), Robert Lamb conducting a transect survey, and Lillian Tuttle observing cleaning stations at a coral patch reef. Photo credits: Lillian Tuttle, Tim Pusack, and Severin Vaillancourt, respectively.

How did you get involved in ecology?

I fell in love with being underwater and with watching animals at a young age. Even though I went to a small liberal arts college in land-locked Kentucky, my passion motivated me to seek out ecology research opportunities during multiple summer internships in coastal locations. The first was as part of an NSF REU program in Newport, Oregon (U.S. National Science Foundation, Research Experience for Undergraduates), and the second was with a professor from my college who happened to study coral-reef parasites in the Virgin Islands.

What are you currently working on?
I just started a new position as a Fish Biologist at NOAA’s Pacific Island Regional Office in Honolulu, Hawai‘i where I will use my expertise to protect “Essential Fish Habitat,” especially Pacific coral reefs, from local stressors that include invasive species, overfishing, and degraded water quality. Most recently, I was a postdoctoral researcher studying water quality standards on coral reefs. I used systematic review and meta-analysis to identify thresholds for sediment, chemical contaminants, and nutrients in these fragile ecosystems. My prior postdoctoral positions investigated the unique behaviours of larval fish and plankton in both coral-reef and freshwater habitats.

What project/article are you most proud of?
I am very proud of this article! It represents the culmination of many years of intense work in the field and lab. Also, the results never ceased to amaze and surprise me – our work challenges paradigms and brings to the surface many more questions than it answers. Hopefully it will serve as fodder for young coral-reef scientists interested in the intersection of basic ecology research with applied conservation practice.

What is the best thing about being an ecologist?
I love getting to spend my time watching and thinking about the natural world. As ecologists, we are privileged to gain access to incredible ecosystems that many people only get to see on television. In other words, we each get to be our own David Attenborough!

What is the worst thing about being an ecologist?
It is disheartening to work in ecosystems that are deteriorating before our eyes, especially when so little is done by governments and people to protect these places from further harm. Coral reefs, as we have known them, may not exist in a matter of decades. It is incredibly important to maintain hope in the face of these challenges so that future generations can continue to enjoy and benefit from these precious places.

What do you do in your spare time?
I love volunteering at ancient Hawaiian fishponds (loko i‘a) and taro patches (lo‘i), which are actively being restored by a new generation of native Hawaiian conservation practitioners. Their millennia of place-based ecological knowledge humbles and inspires me to continue doing work that contributes to humankind’s understanding of natural processes. More generally, I love spending time outdoors – especially surfing, diving, swimming, and hiking – and playing music with friends.

One piece of advice for someone in your field…

I live by a handful of quotes, all from my favourite writer, fellow Kentuckian, Wendell Berry:


“No matter how much one may love the world as a whole, one can live fully in it only by living responsibly in some small part of it.”

“It may be that when we no longer know which way to go that we have come to our real journey. The mind that is not baffled is not employed. The impeded stream is the one that sings.”

“The care of the Earth is our most ancient and most worthy, and after all our most pleasing responsibility. To cherish what remains of it and to foster its renewal is our only hope.”

…in other words: live well, persist, and keep the faith!

Read the article in full here.

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