In a paper published in Science in 1999, Jay Stachowicz, Robert Whitlach and Richard Osman showed, using experimental communities of sessile marine invertebrates that invasion success was lower in more species rich communities. The like reason for this pattern was that space, which was the limiting resource in the system, was more fully and efficiently used if more species were present in a community. Seventeen years after the paper was published, I spoke to Jay Stachowicz about his motivation to do this study, memories of experimental work, and what we have learnt since about the relationship between species richness and invasion success.
Citation: Stachowicz, J. J., Whitlatch, R. B., & Osman, R. W. (1999). Species diversity and invasion resistance in a marine ecosystem. Science, 286(5444), 1577-1579.
Date of interview: 1 December 2016 (via Skype)
Hari Sridhar: Your PhD research on an interaction between crabs, corals and seaweed. The work presented in this paper came soon after your PhD. Could you trace for us your motivation to do this work in relation to what you did in your PhD?
Jay Stachowicz: It is. You are right. It was a very serendipitous sort of thing. This is the first piece of work out of my postdoc. I had been following, through the early and mid 1990s, the work out of Dave Tilman‘s lab on diversity, stability and diversity-ecosystem function,and I just thought this was really exciting work. When I arrived at my postdoc at the University of Connecticut, my postdoc advisor had been working on invasions, on these marine invertebrate communities that grow on piers and docks and whatnot. And they had a wonderful wealth of natural history information about all of these species, and they knew how to culture them and grow them in the field. They had just developed this movable tile apparatus, which was the technique that we ended up using to manipulate diversity in these experiments. It just all sort of clicked. They had this idea that they wanted to do something like this, and I showed up and had thought about all this diversity-function stuff that I’d read in the literature, and it just sort of all came together in this really nice, very lucky way. Everything just happened to be in the right place at the right time. I had spent a lot of time in my PhD thinking about mutualisms and facilitation among organisms. My first thought was, I wonder if increasing diversity will actually facilitate invasion, because of increasing numbers of positive interactions among species. I really wasn’t sure what direction it would go. I thought that was one direction. The other could be the classical theory of increasing diversity leading to more competition and suppressing invasions. I really didn’t know what the outcome was going to be, when I started the study.It was exciting for me. I felt like no matter how it turned out, it was going to be interesting.
HS: How did you get interested in invasion biology?
JS: Honestly, prior to this work I had no interest in invasions at all, other than it was a really relevant ecosystem function to measure in this system. This system is heavily invaded. People know a fair bit about some of the more recent arrivals.People are concerned about them because they overgrow aquaculture operations and those sorts of things. I don’t have any intrinsic interest in invasive species, per se. It was just the right thing to measure as a response variable in the system.
HS: Was this the first experimental study to use a known invasive species to look at the impact of diversity on invasion?
JS: There were a bunch of people doing these experiments around the same time. Jonathan Levine’s work that was published in Science in 2000 was going on at virtually the same time as mine, if not earlier. I think a lot of people had this idea around the same time, because there had been this long history in invasion biology of doing correlations between native richness and exotic or invasive richness.There hadn’t been a whole lot of experiments. At the same time, you had Dave Tilman, the European group led by Hector et al. and others doing these species diversity manipulations, and it was just the obvious thing to do., I think lots of people were seeing this at the same time and saying, aha, we need to experimentally test this with invasions. If you look at the literature on species diversity-invasion manipulations, sometime between when my paper came out and a couple of years later, there’s this huge spike in the number of people publishing these things.
HS: Stepping back a bit,how did you get interested in marine biology? As early as 1991, you were working in a fisheries department as a research assistant. Was this an interest that was there for a long time before you started doing research?
JS: You know, to be honest with you, I always liked the ocean, and I always liked marine systems. But I never thought that you could get paid to do it. It seemed like a dream job that no one would ever be able to actually get. And then, when I got to college, I took a lot of ecology classes,and those were really inspiring to me. Lots of hands on stuff, doing little field experiments for small assignments. I really got interested in doing ecological studies. But, at that stage, during my undergraduate, it was all terrestrial ecology. I did a set of independent projects, and then decided if I was going to go to grad school and do ecology, I really wanted it to be in something that I was super passionate about. And I was more passionate about ocean stuff than terrestrial stuff. I’d been studying plant-herbivore interactions in terrestrial systems. I had a professor in college who said, well, if you’re interested in plant-herbivore interactions, and you want to do marine stuff, you should really look at this guy named Mark Hay in University of North Carolina. I looked at his research, and felt, this is exactly what I want to do. I was instantly attracted to working with Mark. And it sort of went on from there.
HS: How did this group of authors come together, and what did each of you bring to the study?
JS: Bob Whitlatch was my postdoctoral advisor. It was sort of a funny postdoc. As I understand it, Bob was department chair. In exchange for being department chair, and all the time that took away from his research, he got to have a postdoc. And that was me. He and Rick Osman, who’s the third author on the paper, are longtime collaborators. They have been studying the early life histories of these marine organisms and the reasons behind some of their early invasion success, for almost a decade before I got there. So, they had this incredible wealth of natural history information. And they had developed all of these really neat techniques for how to spawn these guys in the lab, and how to get larvae to settle so that you could do the manipulations. In many ways, they did all the hard work of figuring out how you would actually do this experiment. I just showed up at the right time with the right question, and we all got together and said this would be the right thing to do. So it was definitely a collaborative effort between the three of us, with me bringing some ideas and being the one who is in charge of conducting much of the work, and them being the ones that had the great background and helpful interpretation and the ideas for how to actually do the work, in the first place. It was really just a perfect collaboration as a postdoc as far as I’m concerned. It is exactly how a postdoc should work. But, you know, and obviously, I’m a little biased.
HS: In response to an earlier question, you said that these were also the people who developed these tile experiments.
JS: Yes. They had never done an experiment with these tiles before, but when I got there, they showed me the setup that they had. And it was just, like, oh, my God, that’s so perfect. But this was the first experiment that they did with those tiles.
HS: Did you start this postdoc knowing that this is the experiment you wanted to do, or did you develop these ideas developed after you went there?
JS: No, I actually did not go there wanting to do this experiment. I had no idea that this is what I would do for my postdoc. I had done a bunch of chemical ecology as a graduate student. One of these invasive species that Bob and Rick were studying didn’t seem to get eaten very much by any of the native predators, and they were wondering whether there were any chemical defenses that this invasive were producing. And so, that’s one of the things that I went there thinking I would do. But when I got there and saw this other thing that they had going on, that I could be involved in, I thought that’s just way more interesting. I jumped right on it. I did a few experiments on the chemistry thing, and there probably was some chemical stuff there, but I never followed up on it, because this other stuff on diversity just took off so fast, and seemed so much more interesting to me than the other stuff.
HS: Was the invasive species you used in your experiment the same as the one whose chemical ecology Bob and Rick were interested in?
JS: Yeah, it is in fact the same invasive species – Botrylloides violaceus.
HS: In the paper it is B. diegensis
JS: It’s probably violaceus. I think we misidentified it in the Science paper originally. B. violaceus is also an introduced species, but it’s just from a different place.
HS: Why did you pick this species?
JS: At the time, it was one of the most dominant invaders in the area. And it was one that seemed to escape predation by some of the natives, at an earlier stage than some of the natives did. I think that those were the reasons why we focused on that. It also happens to be bright orange, and it’s really easy to identify, and it doesn’t look like anything else in the area. It’s certainly visually arresting. It’s pretty obvious when it’s there. There’s no way to mistake it.
HS: How did you choose your eastern Long Island Sound near Groton, Connecticut as your field site? Was it because Bob and Rick were already working there?
JS: Yes, it was. It’s the site of the University of Connecticut Marine Lab. They had been working there for decades before I got there. At least, a decade.
HS: Give us a sense of what the fieldwork involved – how difficult was it and what was your daily routine like?
JS: The first stage, and probably the most challenging stage, was to grow individuals of all of these species on these little tiles that we could move around. The biggest challenge was getting them all to be ready to use at the right size at the same time. They grow at different rates, and they settle at different times of year, and so we had to bring them into the lab, and expose them to a certain regime of light and dark cycles. That induces them to spawn and release larvae or release gametes. And then with some further light-dark changes, you can get them to settle on these artificial substrates. The first tough part was getting them to settle on these artificial substrates. Then you put them out in the field for a few weeks to let them get large enough that you know that they’re going to survive and that they’ll cover the whole tile. Then you bring them into the lab and assemble them into these different communities, just like a puzzle; people call them like Scrabble tiles. Once you do that, to be honest with you, then it’s just monitoring the experiment. Basically, every week we would take a photo of these things, and look for the invaders and make sure to see if the invaders were still there, how big they were, and make notes of it. In some cases, when all the invaders had died, we stopped the experiment. It’s a very seasonal environment, and when you get to October-November, most of the organisms start to die back die back a little bit and certainly don’t grow very much after that. That’s another cue we used to stop the experiment.
HS: How far was this site from the university? Did you have to stay at a field station?
JS: This site was, literally, about 100 meters. The marine station is right on the ocean, and the field site where we did this was right in front of the marine lab. It was very convenient. It was the sort of experiment that required intensive monitoring.It would have been very difficult to do if it were at some sort of remote field site, unless you went and camped there, right. But for a lot of the assembly and a lot of the figuring out some of the spawning we needed microscope access and those sorts of things. So, it would have been challenging to do at a remote field location.
HS: Were you staying at the marine station when you were doing this research?
JS: I lived not too far. I lived probably 10-15 minutes from the marine station by car. My advisor was based at the marine station, and so that’s where I was based.
HS: Do you still have the tiles you used in this experiment?
JS: I do have some of them still, yeah. They are a little challenging to make.It requires some very precise milling of the plastic. A couple of students here developed an idea that I think is even easier than what we did. They basically just have flat plastic tiles that have Velcro on the bottom of them. And so, they can just attach them and make them really easily. That seems to work pretty well. It’s not quite as rigid, but it seems to work very well. You can make 1000s of tiles very quickly, whereas these were more challenging, and then you had to do some sanding of the tiles afterwards to make sure they fit.It just it just took a little bit longer.
HS: Do you use similar setup for experiments even today?
JS: Yes, I do.
HS: Can we go over the names of people you acknowledge, to get an idea of who these people were and how they helped?
JS: Absolutely.
HS: M Berger
JS: Mike Berger helped develop some of the spawning protocols for how to get the larvae out of the adults and get them to settle at the right time onto these tiles. He was an undergraduate in Professor Whitlatch’s lab. Maybe a year after I was there, he left and went to the University of Oregon, where he did his PhD in Richard Emlet’s lab, I think.
HS: H Lisitano
JS: I’m pretty sure that Heather was an undergraduate summer researcher who worked with us, but I can’t remember more than that.
HS: You thank H Lisitano, E Rogers, and S Smith for assistance in conducting the experiments.
JS: Yeah. The other folks there would have helped with maintaining the organisms and spawning them. Once you have these little tiny larvae that might be, you know, 200 microns in diameter, settled on the tiles, you garden them to remove anything else to ensure that you get just one individual growing on that plate. That was a lot of work, to do the constant gardening and maintenance on these things. They also helped me take photos of these things, bring them back and forth from the lab to the field so we could take good photos. At the time, digital Photography was brand new.We had one of the first digital SLR cameras, but it was in the lab. We didn’t take it out in the field. It was up on this tripod so that you could get a really precise photo of these things. It is really easy to do all that now, but, at the time, it was a little more challenging. Erica Rogers was a Master’s student with Professor Whitlatch at the time. She did a lot of really interesting work that that actually inspired me to do other research that I was interested in, on mutualisms between snails and native seaweeds. She was looking at these snails that live on marine plants in the area, and they eat a lot of the invertebrates, like some of these invasive species that can settle and grow on these plants. Her work was very inspirational for me to do a different line of research that I was interested in, and that was continuing on the mutualism work. I ended up blending that with diversity, because it turns out there are multiple species of snails, and they each do different things on the seaweed – consume different invertebrates – and so, the diversity of snails benefits the plants more than just any one snail would. It ended up kind of coming together,but her work was pretty influential for me, in that regard.
HS: Were all these people students at the time?
JS: Yeah, they were all students. Erica would have been a Master’s student, and the others would have been undergraduates.
HS: You thank A Lohrer and P Renaud for comments on earlier drafts on the manuscript.
JS: Andrew Lohrer was a finishing PhD student in Professor Whitlatch’s lab, at the time and he and I were at very much the same career stage and helped each other out a lot. Paul Renaud was a postdoc, or maybe a research faculty member, in the Department, who had just arrived. I had never met him before. But his Master’s advisor was my PhD advisor, and so we had a natural connection. He was just a good colleague that I passed the manuscript to, to ask for comments.
HS: You say you used image analysis to look at the availability of primary space. Tell us a little more about that. Did you have a particular software to do this?
JS: It’s a program that’s still around today. It’s called ImageJ. We had these digital photographs, and we would basically just circle the area on the photograph of which we want to figure out the. Then you circle a standardized area of known size to compare. It was the first time I had used that technology.
HS: How long, roughly, did it take you to write the paper, and when and where you did most of the writing?
JS: I can visualize exactly where it was when I did most of the writing. It was in my office at the marine lab. I could practically see the field site from my office, though it was probably covered by snow and ice while I was writing. I ran the experiments in the summer into early fall of 1998. I did most of the analysis in early 1999 and then presented the work at a conference in March of 1999 and wrote the paper after that—from the journal I can see that it was submitted in June of 1999, so it went pretty fast. The paper was published in November.
HS: Were all the authors involved in the writing? Did the three of you have regular discussions while you were writing?
JS: Every time we got results we talked about it. But my recollection is that I drafted the manuscript, based on discussions we’d already had, and then passed it to them for comments. And then, they commented on the manuscript. But I don’t remember all the details of how that worked. They commented on the manuscript, suggested changes – maybe you should try this, what about this, this doesn’t make sense, whatever. And then, I made the changes and submitted it.
HS: Was Science the first place you submitted this to?
JS: Yeah, it was.
HS: Did it have a relatively smooth ride through peer review?
JS: Um, it did, sort of, shockingly enough. Boy, I struggle to remember the details of this. This would have been in 1999. I do remember that I got an express mail, like a Federal Express envelope, from Science that had the reviews in it. And I remember when I saw that there was a Federal Express envelope from Science in my mailbox, I was like, oh, that’s gotta be good news. They wouldn’t send me a Federal Express letter just to tell me they’ve rejected my paper. I don’t remember the details of the reviews, but I remember them being supportive and having some constructive ideas that definitely improved the paper. There was no major change to the analysis that I’m remembering from the peer reviews.
HS: Do you remember how it was received when it was published and whether it attracted a lot of attention?
JS: I do. It did. It was my first time publishing something like that. And having media outlets, call you and say, well, we saw this paper in Science; what does it mean? It was very interesting to me to now be doing interviews with the press, which I had never done before. A paper in Science always attracts that sort of thing. And invasive species was, and is still, a hot topic. And so people wanted to know what this meant. I would certainly say I was a little bit unprepared for that, but I enjoyed it. I can very distinctly remember it, because the paper came out within a few days of the birth of my son. I didn’t have a cell phone or anything like that. I remember going to the payphone and trying to call a reporter back or something like that, while my wife is in the hospital. She still grumbles about that (justifiably!). It was exciting for me, having my son on the way, and then having my research being publicized, and being in local newspapers and even regional newspapers and national magazines. It was very different than anything that I had experienced before.
HS: Would you say this paper had a big impact on your career?
JS: Yeah, I think it did. It definitely impacted the direction of my research, because, after this paper, I really took off on doing a bunch of diversity-ecosystem function related research. But it didn’t really affect me getting a job at all, because I got the job offer before I had published this paper. I didn’t even present any of these results in my job talk. But it certainly helped me once I got the job, figuring out what I wanted to do next, and what the interesting line of research was. All of a sudden, there were lots of opportunities. There were working groups that people wanted me to be a part of, there were collaborations that materialized because of this area that I was in that people were really hot on. I guess if I hadn’t published that paper, my career would definitely have a very different direction.
HS: Would you say the main conclusions from this paper still hold true, more or less?
JS: Yeah, I think they do. This was something that people hadn’t really tested or considered before. Our paper showed, yeah, this could actually happen.The theory made sense, but lots of theory makes sense and isn’t borne out by empirical results. You know, here was some theory that made sense, empirical results confirmed that it could happen, and so then the question just becomes, well, how important is this relative to other drivers of invasion? I think that’s where we are right now. Diversity sits as one of several things that can impact invasion success. Just like people don’t say, predation is the only thing that affects community structure, diversity is not the only thing that affects invasion success. There are lots of things. There’s propagule pressure, there’s diseases, there’s abiotic conditions; all sorts of things. To me, the basic results still holds, in the sense that I still see this happening in lots of communities, but it’s one of a number of things that might contribute to invasion success.
HS: Subsequent to this study, in the last 17 years, has this been demonstrated in other systems, with other invasive species?
JS: Yes, it has. I think the most exciting studies are ones that show where it does and where it does not happen. In other words, just showing that it does happen someplace else is great. But I’m, in many ways, more interested in the ones that show that it does not happen, and wondering why is that. You know, what are the other things that are important? And even better are studies that perform these sorts of things in multiple locations, or under multiple types of conditions, and find that, well, in this area, it looks like it’s sort of confirmed,while in this area it looks like it’s not confirmed. Those sorts of multifactorial studies are very challenging to conduct, especially with diversity, because there are a lot of treatments involved. But I think those can be pretty powerful.
HS: If you were to sort of redo these experiments today, would you change anything about them?
JS: I would do them, just as we were talking, across a broader range of conditions, for a longer period of time. Because one of the things that we’ve subsequently found out is that one of the major ways in which the species in this community and in many temperate communities are differentiated is that they have different phenologies; they have different seasonal niches. In some ways, our experiments started to get at that, but it would have been interesting to conduct those over multiple years that differ in how warm or cold they are, and which species were more or less important. Expanding the temporal or spatial scale of these kinds of experiments is something that would have been useful. I would never have tried that first, especially as a postdoc, but if I wanted to go back and follow up, that’s the sort of thing that I would be interested in.
HS: Have you already done some work along these lines?
JS: We’ve done it in some observational ways, for example, using seasonal patterns of larval settlement to quantify the seasonal niche and the use those seasonal niches to model what might be expected in communities with complementary vs overlapping seasonal niches. We’ve also looked for correlations between the abundance and diversity of native and exotic species, and at various spatial scales, and under different environmental conditions. The experiments to manipulate diversity and environmental conditions at many sites would have been a lot of work, and we didn’t end up doing those. And it didn’t feel to me like we would have gotten as much out of that. To be honest, I’ve been doing less work on introduced species recently. Not that I don’t think it’s still interesting,it’s just there’s a lot of stuff to do. Things go through phases where you’re more or less interested in them,and right now, it’s one that I’m a little less involved with.
HS: Have similar experiments been done with other marine invasive species?
JS: Yes. We tried it with two others in our experiments in a subsequent paper in the same system, and found basically the same results. Others have done them with marine algae (White & Shurin 2007, Arenas at al. 2006), other marine invertebrates (Dunstan and Johnston 2004), and, as we were discussing, sometimes they find the same result that we did and sometimes they don’t. And, usually, when they don’t, there’s a good explanation for why they don’t. There’s some other factor that is of greater importance, which they can demonstrate is what’s really driving invasion success and swamping out the effects of diversity.
HS: This paper has been cited over 600 times. Do you have a sense of what it mostly gets cited for?
JS: I think it is one of the, if not the, first experimental manipulation of how species diversity affects invasion. I think it gets cited a lot for that. That’s probably the biggest thing. For example, something like, “Diversity affects invasion in marine systems (Stachowicz et al. 1999)”. That’s probably pretty common. Although, I haven’t looked carefully to see who has cited it. Often, as a paper gets older, it gets cited for more and more things that it doesn’t say. So, I don’t know, it might get cited for just something general about marine invasions or something like that. But it’s humbling that it’s been cited that many times. I would never have thought that that paper that I did as a postdoc would be been cited that many times.
HS: Do you continue to work in Long Island Sound?
JS: Nope, I don’t. I live on the opposite Coast of the US now; I live on the Pacific coast. Many of the same species are here, and, certainly the same types of communities are here, so there really isn’t any need for me to go back there to work. It was just a convenient place to work because that’s where I was living at the time.
HS: And when was the last time you visited that site?
JS: Oh, probably 2000- 2001. It was a while ago.
HS: Do you know if that site has changed in any way since the time of this study?
JS: That’s a good question. I don’t know.My postdoc advisor has retired. He’s no longer an active researcher in this area. We published a study in 2002 that compared changes in the community in warmer versus colder years, showing that, in warmer years, invasive species were more dominant than in colder years. Given that the temperature has risen in the waters in that area, my guess is that there’s probably a greater dominance of invasive species than there was when we were working there. I know there’s at least one additional invasive species that’s shown up that wasn’t there earlier. You know, if you didn’t know what you were looking at, you’d pick it up and go, yeah, it’s still a bunch of marine invertebrates. But I’d probably look at it and go, wow, the species composition is different than when I was here 15-20 years ago doing this work. Although, I haven’t been back there, so I really don’t know.
HS: Today, do we also know more about the mechanisms by which greater species diversity increases the resistance to invasion? In this paper, you say that though you don’t know that for sure that the results support the hypothesis that reduced resource availability is responsible for the decreased success of invasions in communities with increased diversity. Do we know more about this, and is that still the best explanation: species rich communities are buffered from fluctuations in space availability?
JC: I think that’s absolutely true for this community. One of the pieces of evidence that I think we have to support that is that when we do some surveys of relationships between native and invasive diversity, we find that, where there’s free space, we lose that negative relationship between native and exotic diversity, and where all the space is covered, we more often find that negative relationship; not always, but more often. So I think, for this system, that’s a pretty fair conclusion to make.
HS: You say, “Differences in primary space availability appear to drive the relation between diversity and invisibility in this system, but this model should be applicable to any system in which the limiting resources (such as light or nutrients) are clearly identifiable.” Has that found support in subsequent work in other systems, including terrestrial ones?
JS: I think you find this anytime you have a resource limited system, and diversity draws that resource down to lower levels. It might not be space, per se, but it might be light or water or nutrients in some terrestrial plant community, for example. So, yeah, I think that would probably still hold true.
Tilman laid the argument out really well in his 1999 Ecology paper, and showed evidence that this probably underlies the general relationship between diversity and productivity or biomass. Some of his later students followed up on this with invasion (for example, Fargione and Tilman 2005)
HS: Have you ever read the paper after it was published?
JS: Yes, but it’s probably been a really long time. It’s almost embarrassing to read your own paper. You read things and you go, oh, my God, why did I say it that way? It’s like watching yourself on TV or listening to a recording of yourself? It’s very uncomfortable.
HS: In what context have you gone back and read it again?
JS: It probably would have been when I was in some discussion group, and they were going to read this paper and discuss it, and I was going to be there,and I wanted to make sure that I remembered everything. So that when somebody asked me a question I would be able to recall it. Or if I’m teaching something out of that paper in a class, I might look up one of the details, just to make sure I have it right.
HS: Would you count this as one of your favorite pieces of work?
JS: Yeah, I would. I’m not trying to toot my own horn here, but it’s such a nice combination of really interesting and timely basic question in science and a wealth of natural history information that had been accumulated about these species over 10 to 15 years, plus the applied dimension of invasive species. In many ways, it has all the things you’d like to see in a paper. And, I don’t think I really expected it to come out the way it did, just because it seemed too perfect for it to work that way. It was an exciting result and the research was actually fun to do because you could see the results so quickly. So yeah, it is it is one of my favorites.
HS: What would you say, to a student who’s about to read this paper today? What should he or she take away from this paper? Would you add any caveats they should keep in mind when reading this paper?
JS: That’s a good question. What would I tell them? I wouldn’t tell them that I wanted them to take anything away from it. I would instead want to know, what do they take away from it? I would encourage them to be like I am while reading any paper. Be critical and skeptical of what you’re reading. Does it make sense? Do you buy it? What do you take out of it? What are the things that you think are exciting about it? I’m always interested to hear what other people take, rather than color their opinion with what I think they should take out of it. That’s kind of a cop-out answer, but that’s kind of how I feel.
HS: would you would you also point them to other papers that they should read along with this?
JS: Sure, I would. I think the immediate follow-up was the 2002 Ecology paper out of my lab. And then, sort of expanding that would be a 2006 paper that me and my student Jarrett Byrnes published in Marine Ecology Progress Series. I’m gonna blank on specific papers, but there is some good work by Graeme Clark and Emma Johnston at the University of New South Wales in the early 2010s. especially a paper they published in Ecology Letters. There’s also one that came out recently that I like, in Proceedings B, by Marraffini and Geller. I think these papers would be good to read along with our 1999 paper.
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