Fear and grazing in Kelp forests: How sunflower stars indirectly affect sea urchins

By Ross Whippo

Ross Whippo is a Ph.D. candidate at the University of Oregon. He got his undergraduate degree from UW SAFS in 2011 and a Masters in Zoology from the University of British Columbia in 2013, studying sea urchin ecology and invertebrate metacommunities, respectively. From 2015-2018 he worked as the central technician for the Smithsonian’s MarineGEO program. Currently he finds himself back in the San Juans, his favorite place on Earth, conducting research into the role the sunflower seastar plays in kelp forest ecology. You can find him at rosswhippo.com.

I remember the first time I saw a ‘monster Pycno’, that is, a very very large sunflower star (Pycnopodia helianthoides). It was during my first stint at FHL as an undergraduate in the Marine Biology Quarter of 2009. The program included foundational marine biology coursework, a practical research experience, and the opportunity to be trained as a scientific diver. It was during one of our training dives that I witnessed a truly surprising interaction, the kind that you only see when you’ve accidentally left your camera on the boat: a truly enormous sunflower star wrapped entirely around a seal carcass. This was my first introduction to sunflower stars, and one that has stuck with me through the years.

Now as a Ph.D. candidate at the University of Oregon, I’ve been able to ‘dive into’ the mysterious world of the sunflower star in an attempt to fill critical gaps in our knowledge about them. Ever since sunflower star populations were reduced by over 90% due to seastar wasting disease in 2013-14 (Montecino-Latorre et al. 2016), this previously ubiquitous predator has all but disappeared. Many of the once-dense kelp forests that could be found up and down the west coast of North America have also declined (Rogers-Bennett & Catton 2019). This leaves us with the question: what role did sunflower stars play in the maintenance and health of these kelp forest systems?

My lab, led by Dr. Aaron Galloway (also a UW and FHL alum), is concerned with trophic ecology: how food webs are arranged, how they change through time, and what impact this change has on marine habitats. When I decided to explore the trophic ecology of sunflower stars, I was certain I would find a treasure trove of literature stretching back decades; after all, they were one of the most common subtidal consumers and had been long recognized as important community members since before I was even born. Surprisingly this was not the case, at least in the published literature. I was only able to find =N:E= 20 studies that explicitly dealt with sunflower star diet, food choice, or trophic ecology. It’s interesting to note that several of these papers included research done at FHL or by FHL researchers (Greer 1961, Duggins 1983). Nevertheless, I was gobsmacked: how could such a formerly-abundant critter have so very little actually written about it?

With my slim binder of primary sources assembled, I set out to add to our knowledge of how sunflower stars fit into our understanding of kelp forest and other subtidal habitats. As Dr. Galloway and colleagues from The Nature Conservancy researched the ‘direct’ interactions between sunflower stars and purple sea urchins (Strongylocentrotus purpuratus), I tackled the ‘indirect’ interactions that may play out between urchins and sunflower stars. By ‘direct’, I mean consumptive predator-prey interactions (‘how many urchins could a sunflower star eat, if a sunflower star could eat urchins?’) while indirect interactions refer to an urchin’s response – if any – to the mere presence of a sunflower star in the environment. Urchins are known to display defensive behaviors including increased cryptic (hiding) behavior and reduced feeding rates when exposed to predation and to predator cues like crushed urchins and lobsters (Bernstein et al. 1981, Spyksma et al. 2020), so it was a good bet that sunflower stars might have a similar effect on purple urchins. But how much of an effect? This is important to know for kelp forests, as kelp is prone to grazing pressure and can quite quickly shift from a lush forest full of actively feeding urchins to a denuded barren of metabolically depressed urchin ‘zombies’ (Spindel et al. 2021). Understanding the direct and indirect effects of predator-prey interactions and how the metabolic condition of the urchins mediates these interactions may give clues to the causal factors that drive these tipping points, as well as potential solutions.

So, I set out to answer the following questions: 1) Do sunflower stars indirectly alter urchin grazing rates? and 2) Does the metabolic condition of an urchin (well fed like in a healthy kelp forest, or starved like in an urchin barren) change any indirect interactions with sunflower stars?

To answer my first question, I set up a feeding trial for urchins that were either exposed or not exposed to a sunflower star chemical cue (in the form of water outflow from a tank containing stars), and fed the urchins as much bull kelp as they could eat. After all my experimental trials were run, I found that urchins that were exposed to a sunflower star’s cue consumed 60% less kelp than those that weren’t. But how much would that work out to per day? Well, exposed urchins ate ~1.5 g of kelp tissue per day, and unexposed urchins ate ~2.5 g per day. That may not sound like a lot of kelp, but multiply that by a dozen urchins per square meter (in some places), and the values add up fast. It’s also important to remember that it doesn’t take a lot of biomass consumption to remove a lot of kelp biomass. Simply chewing on the stipe of a bull kelp can be enough to dislodge the entire plant, and juvenile kelp may be especially susceptible to small rates of consumption.

Next, I tested if there was an effect of urchin starvation state on indirect interactions with sunflower stars. This is interesting because in many places along the west coast of North America, kelp forests have been replaced by urchin barrens: places where hordes of urchins have grazed away all the kelp. Urchins in these barrens can survive for long periods of time without food by transitioning to a different metabolic condition that allows them to persist. The starvation state of an organism can directly affect their willingness to risk being eaten in order to get food, and I wanted to see if this was the case with urchins exposed to sunflower stars. Similar to the first experiment, I placed urchins in a tank that was supplied water that either had a sunflower star cue, or did not. In addition, I starved half the urchins for seven weeks to mimic a metabolically ‘barren urchin’ condition. Finally, I added a bull kelp cue to half the trials to test the urchin’s willingness to ‘stop and eat’ if a sunflower star was nearby. I ran 49 trials for one hour each, recording their behavior every minute for the duration of the trial: forty-nine hours of data! I found that starved urchins indeed behaved differently than fed urchins in the presence of a sunflower star cue, spending 33% more time on average interacting with a food cue (as opposed to running for their lives) than fed urchins (Figure 2). In fact, I never observed a single ‘fed’ urchin eating the kelp cue in any trial, whereas I nearly always saw the starved urchins feeding. Bottom line: a starved urchin is gonna eat!

This was great insight into the indirect interactions between sunflower stars and urchins. But given that sunflower stars would need to be close to the urchins to elicit a response, I started to think about how the sunflower stars themselves might behave toward urchins. This led me to my current project, testing a direct interaction in which I asked: if given a choice between various prey, what would a sunflower star prefer to eat? This is a critical missing part of the picture, and one that has only ever been tested in a pair-wise fashion by other researchers (i.e. – only two prey items at a time). There are several studies that describe the ‘wild diet’ of sunflower stars in various regions (Mauzey et al. 1968, Duggins 1983), but choice experiments are lacking. I ran a series of ‘cafeteria experiments’ where I offered sunflower stars an endless supply of possible prey items, and quantified their choices over ten days. I found that sunflower stars (at least the ones I tested) quite enjoyed eating green and purple urchins as well as mussels. Red urchins of a smaller size were also consumed on a semi-regular basis, but cucumbers and chitons were not on the menu. The biggest takeaway was that individual sunflower stars vary greatly in their feeding preferences and in how much they eat.

So what does this all mean? Well first, it demonstrates that sunflower stars do indeed have indirect effects on urchin grazing and behavior. Second, it hints at how urchin-barren urchins might respond differently than urchins in kelp forests. Finally, it shows that sunflower stars’ dietary preferences are complex in terms of preferred prey and consumption rates. So what’s next? I’m excited to use microCT scans to explore how urchins exposed to sunflower star cues may be physiologically affected by longer-term exposure to predators. With help from members of Dr. Adam Summers’ lab I was able to scan a subset of the urchins from my behavior experiment, and will be visualizing gonad volume (a proxy for physiological fitness) as well as other anatomy including the test (shell) and gut arrangement.

All this to say, this work and the work of my collaborators is helping us understand sunflower stars’ role in the environment and will allow us to better predict what might happen if and when our ‘monster Pycnos’ return.