In a paper published in Nature in 2003, Mark Torchin, Kevin Lafferty, Andrew Dobson, Valerie McKenzie and Armand Kuris provided evidence to suggest that reduced parasite load in their introduced range might contribute to an exotic species’ invasive success. Using data from 26 exotic species from a variety of taxa, Torchin and colleagues found that parasite species richness and proportion of individuals infected were typically lower in introduced range compared to their native range. Thirteen years after the paper was published, I spoke to Mark Torchin about his motivation to do this work, how the authors came together and what we have learnt since about the relationship between parasite load and invasive success.
Citation: Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J., & Kuris, A. M. (2003). Introduced species and their missing parasites. Nature, 421(6923), 628-630.
Date of interview: 1 September 2016 (via Skype)
Hari Sridhar: This paper came soon after your PhD, when, I think, you were a postdoc at NCEAS. What was the motivation to do this work?
Mark Torchin: Actually, I was doing my thesis research on the topic. So, I was actually a graduate student at the time. And I was really interested in how parasites and the diseases they cause shape populations and communities of free-living species that we see in nature. I was always told, or I guess the conventional wisdom was that introduced species often escaped their natural enemies, things like parasites, and that gives them an advantage in their native range. So, it seemed reasonable to me to use these natural experiments, these introduced species, to figure out what happens with and without parasites. And when I was writing my thesis and trying to figure this out, I was pretty frustrated because I didn’t really find any quantitative data suggesting this. I was really, you know, stumbling, trying to put together the introductory chapter for my thesis. The data weren’t really there, and I was unsure as to how to go about approaching this. So, the NCEAS thing comes up. First up, NCEAS is the National Center for Ecological analysis and Synthesis. Are you familiar with this?
HS: Yes.
MT: Okay. It’s this cool place where people come together from all around the world to work on ecological ideas and problems. I was at UC Santa Barbara, right down the road from NCEAS. And at the time, there’s a working group on diseases and conservation. It was led by Andy Dobson. My advisor at the time, Armand Kuris, and another one of my mentors, Kevin Lafferty, were also involved in the group. I forget if they actually invited me to come to one of these meetings, or I just crashed it; I forget. But, in any case, it was this cool opportunity to work with some really interesting and dynamic people and put together, sort of, the data that would ultimately go on to become part of this paper.We’re really interested in this very basic question -Do introduced species escape their parasites -and to do that, we compared native and introduced populations of several different species. The trick was, first, we had to find the data. So, each person worked on a different taxonomic group and entered the data into a standard spreadsheet and then we started assessing the problem. So, I would say that the question, sort of, stemmed back to my thesis, really got assembled in this working group and then we ended up publishing it after the working group was done, and subsequently I became a postdoc at NCEAS as well.
HS: Stepping back a little bit, how did you get interested in marine biology, and specifically in parasites and invasives?
MT:I don’t know how far back you want to go.
HS: I want to know what your motivation was to do your PhD on this particular topic.
MT: Okay. My first underlying interest was, really, in the role of parasites in ecosystems. How parasites influence the ecology of free-living species, and how that then feeds back to influence the distribution and abundance of parasites and disease-causing organisms. With that, I also had an interest in introduced invasive species and I was interested in putting those two together, initially, really for the idea of using introduced species as, kind of, natural experiments to test hypotheses about parasites in natural systems. And then that sort of just evolved more into looking at the role of parasites in invasions.
HS: How did you choose to work on marine fish?
MT: I really kind of work across taxa, you know, depending on which group of organisms is best suited to answer that sort of question. I work on marine invertebrates, so things like snails, crabs, but also sea squids, bryozoans, as well as fishes. Some folks in my lab, students in my lab, work on a variety of different organisms ranging from cane toads to marine snails to freshwater snails; there’s even somebody working on algae in my lab. So, you know, the taxonomic breadth is pretty diverse.We really try to look at what groups are useful for answering the particular questions we’re interested in and our hypotheses we want to test.
HS: For your PhD, how did you choose to work on marine fish?
MT: Ah, okay. For my PhD, I worked on a marine crab, the European green crab, snails – an introduced and native snail species, here, on the west coast of the United States – and native and introduced fishes. That was, sort of, the empirical part of my PhD, working on crabs, snails and fishes. And then the more synthetic part involved, you know, putting together data from a variety of different species. I really enjoyed that approach. I’m a field biologist at heart, I really like going out in the field, looking at patterns, coming up with questions and testing those. But, you know, I also recognize the utility and the value of existing data that’s already out there and synthesizing that. There’s a wealth of existing data that can be used to address similar questions and, really combining those approaches, I found, has been a pretty effective approach to doing science.
Hari Sridhar: At the time you were deciding on your PhD topic, did you consider working on terrestrial species?
MT: I have always had a marine bent to what I do. I think marine systems are interesting and they’re often not as extensive explored as terrestrial systems. I grew up in California surfing, snorkeling and scuba diving, and so, I’ve been around the ocean all my life and that’s where I started asking questions early on.
HS: How did the five authors on this paper come together and what did each person sort of bring to this piece of work?
MT: Sure. This was part of a working group at NCEAS, as I mentioned, and each author contributed, in shaping the ideas as well as working on particular groups of organisms. We came up with an approach to gather the data to the spreadsheet, and then everybody went off and worked on their particular taxonomic groups, and brought those data back in to the community to then analyze. We had another graduate student, Val McKenzie, who worked on the herps. We had Andy Dobson, who was the leader of the working group, who did some of the mammals and was instrumental in, sort of, shaping the ideas as well. My advisor, Armand Kuris, and Kevin Lafferty, each worked on different organisms, but also helped shape the ideas and on the analysis. It was, really, a nice collaboration where we worked intensely during the NCEAS meetings, and then we went to our home institutions, worked independently, had the opportunity to come back to NCEAS and work on those ideas again, refine the ideas, do the analysis on the data. I think the structure of NCEAS really helped in doing that. The other cool thing that I need to mention is there was another group, within the same working group, that focused on the same sort of idea, same question, on plants and plant pathogens. So that’s Charles Mitchell and Sunny Power, who published a companion paper, which essentially addresses the same issue. So those were kind of side by side, you know, and came out of the same working group.
HS: You mention this in the paper,a complementary study of pathogens on introduced plant species.
MT: Yes.
HS: How often did you meet as a group at NCEAS?
MT: Ah, good question.I would say a couple times over the course of two to three years. Some of these working groups go longer, some are shorter, but typically you meet two to three times per year.
HS: Did you write the paper at NCEAS or back in the university?
MT: The writing, actually didn’t take that much time. It was, really, getting the data which took most of the time, followed by the analysis.The writing was probably the fastest part. And it was, I think, done mostly at our home institutions. I mean, certainly bits and pieces were composed within NCEAS. We were shaping the outline and the analyses, but, really, the main component was the data collection.
HS: How long did the writing take?
MT: My guess is about a month.
HS: Did you do most of the writing?
MT: It was a joint endeavor. You know, I came up with the first draft and then it metamorphosed from there.
HS: Did you share drafts over email or did you discuss them in-person?
MT: I think both. Email was certainly a main part of that. But, where face-to-face was possible, we would certainly do that, you know, either in the meeting or at UC Santa Barbara. I was able to talk to both Kevin and Armand at UC Santa Barbara. Certainly, face-to-face was an important component of this process and really, you know, was facilitated by the NCEAS structure. I think the NCEAS is a really great place. That’s why I ended up doing my postdoc there as well.
HS: Did the work in this paper go into your PhD?
MT: Yeah, it’s essentially the first chapter my thesis. It was published after I graduated. So, you know, it was revised after that. But. essentially, you know, I submitted it as the first chapter of my thesis.
HS: Did this paper have a relatively easy ride through peer review?
MT: Ooh, good question.It was relatively straightforward. I certainly had many papers that were more challenging to put through peer review. We certainly got a lot of really good comments from reviewers, but nothing hostile. The revisions really improved that paper. But it was it was a pretty straightforward review process.
HS: Do you know if it through one or two rounds of review?
MT: Good question. I can probably look back at my files and figure that out. I would imagine a couple rounds. But I’d have to confirm that.
HS: Was Nature the first place you submitted this to?
MT: Yeah, it was. I think that was the first place that we submitted it.
HS: What kind of attention did this paper get when it was published, in academia and in the popular press?
MT: Yeah, we got a fair amount of media attention right after publication. I recall, I think, I was on vacation in Hawaii around the time it came out, and was fielding calls while I was there. The really cool part, to me, has been to see how many interesting papers that have come, you know, addressing a similar issue since it was written. I think that’s, really, the main value.It has been most impressive or cool to me to see how much new data there are now, how many papers have built on information relating to parasites and invasions. It would certainly be a lot easier to write that paper now than it was when we did it. There are much more data now.
HS: If you were to redo this study today, would you do anything differently?
MT: Well, I think the main thing is there would be a broader, more extensive data set that we could examine. There are, now, different angles that you could approach to that question, which, at least, we didn’t find the appropriate data to do so. But I think now, just the diversity and the number of studies being done on parasites, diseases and invasions is really…I think the opportunities are much greater now than they were previously.
HS; Can you can you give us some examples of what else you can do now that you weren’t able to do then?
MT: Yeah. We had a really simple question, actually: are introduced populations less parasitized than their native counterpart populations, if you look at species pairs. One thing that we were not able to do is look at how that translates into the performance of introduced species. I think now data are accumulating to do that. And the question is much more complex. But there are much more data assessing some of those components, that it would be worth exploring that further, to see the extent to which that question could be addressed now.
HS: Have there been other such analysis by other groups looking at parasites in introduced and native populations, you know, using a more extensive data set?
MT: Yeah, I think there have been many more comparisons. Certainly, there have been various follow ups and some really good critiques as well. So, there have been some analyses with different species. April Blakeslee did a follow-up paper more recently, as did Maria Anouk Goedknegt. I can send you some of those with a little bit more digging.
HS: Do you know what the paper mostly gets cited for?
MT: Yeah. I mean, it’s typically cited for research on parasites and invasions,role of parasites and invasions, or looking at patterns of parasitism in introduced or invasive species.
HS: Would you say that the main conclusions from this piece of work still hold true, more or less?
MT: I would say, yeah. In general, the conclusions are pretty consistent. You know, there are certainly exceptions to the case. But, in general, my assessment of the literature that that has been coming out is that it’s been pretty consistent with what we found.
HS: What kind of an impact did this paper have your career and on the future course of your research?
MT: I would say it had a fairly big impact. it I don’t know if this paper did, but, sort of, the question and my interest in this question has shaped what I’m doing now. The paper was just part of that process, but I certainly continue to pursue areas of similar research. I’ve branched out now a little bit looking at how other biotic interactions, things like predators and competitors, influence invasions. But I’m still, fundamentally, interested in how parasites and infectious agents and the diseases they cause,shape ecosystems and free-living communities. And I often do that in the context of working with introduced species, I should say.
HS: What about in terms of your career?
MT: Yea. I think it certainly helped. And it continues to, sort of, be a cornerstone of the research that I do. My research has broadened out but my real interest still lies in that area.
HS: Can we go over the Acknowledgements, just to get a sense of how you knew these people and how they helped?
MT: Sure.
HS: S. Altizer.
MT: We had the benefit of everybody in the working group at NCEAS review the paper before submission. That certainly helped in the review process, I suspect. So, there are folks in the working group that helped shape the ideas, but also read the paper, provided suggestions. Sonia was one of those in the working group. The other group of people were folks that provided unpublished data for the analyses. So those are sort of the two categories, I would say.
HS: Is the first set of names all people on the working group – S.Gaines, P.Hudson, H.McCallum, A.W. Miller, C.Mitchell and A. Power?
MT: Yes. Gaines was not in the working group. He was on my PhD committee and really helped in the process of writing my thesis, and also in shaping, particularly, some of the analyses for the paper.
HS: What about A. Dove and G. Ruiz?
MT: They, I believe, provided some unpublished data.
HS: L. Mababa?
MT: Ah, Luz. Yeah, she was an undergrad working with me. She helped to, I think, organize and gather some of the data.
HS: Was she also at UC Santa Barbara?
MT: Yes.
HS: In the paper you hint at certain topics about which not much was known then and which you thought were important to research in the future. One speculation you make is about why introduced populations have fewer parasites.Today,do we know more about that?
MT: Yeah.Some of the reviews that I was mentioning address that a bit more in depth. There are certainly different mechanisms that are possible. Some of those are easier to test than others. I think we’ve advanced a bit on that, but certainly could advance more.
HS: In the supplementary material, you say that the data for amphibians, reptiles, birds and mammals were comprised exclusively of parasitic helminths. Now, do we have information on other kinds of parasites, as well, for these taxonomic groups?
MT: Good question. I know there are certainly good data sets for other parasites.Whether they have you know, the sort of companion data, or the complementary native-introduced data, I’m not quite sure.
HS: Do we know more about the relationship between invasion success and parasite load, i.e. whether invasives with fewer parasites tend to do better?
MT: Yeah, I think that’s where the complexity lies. I don’t think that’s been analyzed in a synthetic way.Interestingly, it’s probably pretty variable.
HS: Towards the end of the paper, you say,“More generally, invasions provide several opportunities to assess how parasites regulate host populations”. Has that happened?
MT: Yeah. I guess kind of relates to your previous question,how parasites influence the performance of introduced species and whether they able to regulate or control populations.That’s something I think that is certainly more nuanced and likely depends on the particular species, and the context in which it’s introduced. I think there have been some studies suggesting that that, it does, and some studies suggesting that, it doesn’t. Again, that’s where, I think, a lot of variability lies. And certainly, you know, parasites are one possible form of biotic resistance, which may be lacking in an introduced location. That, I think, is still ripe for research. We have more data on that now but that data hasn’t been fully synthesized. My take is, looking at the studies that have been done, there’s variability in that. Part of that is the nature of the question and how the question is asked. I think you know, the beauty about asking a simple question, like, are introduced populations less parasitized than native populations – it’s a fairly straightforward comparison, but, I think, when you get into the nuances of whether parasites control populations or the extent to which they affect population that’s a bit more of a nuanced and complex question to address; and much more interesting, frankly.
HS: In the last sentence of the paper, you say,“In addition, their absence from introduced pest species suggests that the full potential of biological control to mitigate invasive species has not been explored as yet.” To what extent has that happened, both in terms of more research and actual application?
MT: Parasites have been used pretty extensively in biological control, historically. I think the point there is layering that into a rigorous scientific approach to assessing, both, the safety and the efficacy of that is still something that can be developed. I think, traditionally biological control has been more of atrial and error approach, in many senses. Not always, I mean, there are some good examples of bio-control and there are some pretty bad examples of where biological control hasn’t had any of the success that it was intended to have, and it has had some pretty dire ecological and environmental consequences.I think the point of that statement was that applying a rigorous scientific approach to biological control would be a valuable step.
HS: Have you continued with this group of authors after this study?
MT: Yup. I’ve continued to work with everyone on that authorship list.
HS: Was this paper the first time you worked with these people?
MT: It was my first publication with Andy Dobson, I believe. It was not with Kevin and Armand. I believe it was the first with Val. I haven’t published much with Val Mackenzie; maybe a couple of other things. She was at UCSB with me. But I keep in contact with all of them. I would say I interact mostly with Armand Kuris, Kevin Lafferty and Andy Dobson.
HS: Have you ever read this paper after it was published?
MT: No, I put it as far away as possible! I’m just joking. Yeah, I read it occasionally.
HS: In what context? What makes you pick it up again?
MT: I think I pick it up to look at, both, the analyses we did and the groups that we worked with. I would say, mostly, I go into the data that we have on those, to see what other information can be extracted for the particular groups of organisms, if we are working on any of those, for example.
HS: Do you think the way you write has changed over the years?
MT: Hmm.I don’t know. That’s a good question.I probably have, but I haven’t really identified how that is. Nothing sort of jumps out at me, in particular.
HS: In the paper you mention a manuscript in preparation with J.Byers and T.Huspeni about a trematode species that infect a snail in Japan and has invaded the west coast of North America. Was that published later as a paper?
MT: Yeah, I can send that that to you. That was another sort of piece of my thesis. We’ve gone on to study that system pretty extensively. In fact, I was working with a postdoc from Japan, who’s now a very good colleague and collaborator of mine. His name is Osamu Miura. He came to work with me in Panama for three years to follow up on some of these questions. In fact, here in California now, I’m continuing work on that system. So, that has really expanded.
HS: Would you count this as one of your favorites among all the papers you’ve published?
MT: Ah, probably, although I like some of the empirical papers better, even though even though they’re probably not read as much. I think the empirical stuff is what I really enjoy and what gets me going and motivated. But I would put it up there as, probably, one of the favorites; not the favorite.
HS: What would you say to a student who is about to read this paper? What should he or shetake away from this paper written 13 years ago?
MT: I think they are in a much better situation to assess and critique the topic. I’ll probably tell them to look at a citation map and read some of the key papers that have dealt with the topic and have critiqued this paper and, essentially, try to develop their own kind of idea of the topic and the subject. And I think they are in a much better position to do so now than 13 years ago. That’s a long time ago.
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