In 1999, Daniel Simberloff and Betsy Von Holle published a review paper in Biological Invasions documenting the prevalence of positive interactions among nonindigenous species, and discussing the importance of such interactions in facilitating invasion. Seventeen years after the paper was published, I spoke to Betsy Von Holle about the making of this paper and what we have learnt about this topic since the paper was published.
Citation: Simberloff, D., & Von Holle, B. (1999). Positive interactions of nonindigenous species: invasional meltdown?. Biological invasions, 1(1), 21-32.
Date of interview: 15th July 2016
Hari Sridhar: What motivated this paper?
Betsy Von Holle: When I started my dissertation work with Dan Simberloff, he told me he had this really exciting new idea about synergisms between non-native species. As we all know, a synergism is where the joint impact of two entities is greater than the sum of the two individual impacts. So in the case of non-native species, the idea is that the impact of the two invasive species together is greater than each of those species individually. We found that idea so exciting. So then I researched the ecological literature and came up with these different categories, or types of non-native species interactions, that would have really big impacts if they occurred together. So, for example, non-native herbivores such as pigs disturbing the habitat and at the same time dispersing non-native species much more widely than they would have managed on their own. So we found all these very interesting examples that we were able to pull together in a paper. Have you heard of the National Centre for Ecological Analysis and Synthesis (NCEAS) in Santa Barbara? Basically we took these ideas and developed them during a set of NCEAS workshops about impacts of invasive species that was led by Ingrid Parker.
HS: What was the topic of your PhD dissertation?
BVH: My PhD work looked at what, of the various hypothesized determinants of invasion success of a non-native species, was the most important. When I was doing my dissertation work in the late 90s, the reigning paradigm was that biotic resistance to invasion was the main determinant of whether or not a species was going to be in the habitat. But I felt that more important than biotic resistance was this idea of environmental resistance, or abiotic forces, determining whether or not that species can even exist in that habitat. The other big issue was propagule pressure. Propagule pressure is something that I heard a lot about as an intern at the Smithsonian, with Greg Ruiz. Marine invasion biology researchers, like Greg Ruiz himself, had developed quite a bit of theory around propagule pressure, which wasn’t as developed in the broader invasion biology literature. So I tried to wrap all of these different hypotheses together in one single field experiment. And what I found, in a paper that I published with Dan Simberloff, was that propagule pressure was the leading determinant of whether or not you find that species in that habitat. This was a paper that became very highly cited in Ecology, and I think it was a major determinant in pushing the invasion biology field forward towards investigating the importance of propagule pressure for invasion into natural habitats.
HS: Who came up with the term ‘invasional meltdown’? Did you consider other alternatives?
BVH: That’s a really good question. No, I don’t think we considered other alternatives. I believe that term came out of Ingrid Parker’s NCEAS working group. There is this term ‘genetic meltdown’, which was widely known in the literature, and I believe, inspired by that, our term came out of a brainstorming session at the NCEAS working group.
HS: You use a database put together by Ingrid Parker. What was this database originally built for?
BVH: The database built by Ingrid Parker was originally used for understanding the impacts of different categories of invasive species. Dan and I actually built a separate database from this, where we looked at the impacts of two or more invasive species that were found together.
HS: How long did the entire process take – searching the database for data and writing the paper?
BVH: It was really fast, actually. I did most of the legwork in terms of looking through the literature for these examples. We would take those examples from the searching that I did to each of these NCEAS working groups, and we wrote most of the paper at these working groups. We also spent a lot of time in the UC Santa Barbara library, where Dan would tabulate the number of skateboards he saw in the library! Obviously, we had to spend time finishing the manuscript after the working group was over.
HS: If you don’t mind my asking, how was the order of authors decided? It is somewhat unusual for a student to be last author and supervisor to be first
BVH: That’s another good question. In ecology, the lead author is the person who receives most of the credit. And so it was always just assumed that Dan would have the lead on this, because he came up with the idea.
HS: Was Biological Invasions the first place you submitted this to? Did it have a smooth ride through peer review?
BVH: Yes, Biological Invasions was the first journal that we submitted this to, and we were really excited about this new journal. The paper by Ingrid Parker and colleagues as well as ours were some of the first articles to come out in the first issue of Biological Invasions. The process was very fast, I think because they were trying to get interest in that new journal.
HS: You thank a lot of people in the acknowledgements. Can you quickly tell me who they were and how they helped?
BVH: The first set of people we acknowledge (L. Stevens, F. Howarth, M. Hossaert,
D. McKey, R. Mack, A. Ricciardi and C. Thebaud) provided us with information. Once I had read their articles about synergisms between two or more species, I would call them or Dan would call them and ask a little bit more in terms of the details. And so that kind of information was really helpful for telling our story.
The second set of people in the Acknowledgements (P. Kareiva, I. Parker, L. Goldwasser, J. Byers, M. Wonham, K. Goodell, P. Moyle, M. Williamson and M. Lonsdale) were all members of the NCEAS working group. That was a really great time for me because as a new graduate student I was able to work with this large group of very experienced invasion biologists and it was a tremendous learning opportunity for me, and it was just a lot of fun
HS: Did the paper create a buzz when it was published?
BVH: I think so. Tony Ricciardi immediately looked to find examples in his system – the Great Lakes – in terms of supporting our idea of invasional meltdown. I certainly think people were really interested in it, and they tried to find examples in the literature. So I do think that it probably was something that caused a buzz in the community.
HS: This paper has been cited over a 1000 times. Do you know what it mostly gets cited for?
BVH: Another good question. I used to follow all of the citations of this paper at the beginning. But as you noted there are a lot of citations at this point. Some of them are theoretical, in terms of citing it as one route of interactions between non-native species. Another set of citations are from researchers who are supporting it through their examples in their systems. Right now, I can honestly say I don’t know what the majority are citing it for.
HS: One of the things you say in your paper is that most of the reports of interactions between non-native species are anecdotal, and there haven’t been many population-level studies. Has that changed?
BVH: Not as much as it should. In the exchange between Dan Simberloff and Jessica Gurevitch (original paper, comment, rejoinder), the primary point is that people aren’t documenting the feedbacks between both species. So a lot of people are going out into the field and they’re finding a positive influence from one species on the other, but they’re not actually documenting that feedback from the other species back on that species, which would be the invasional meltdown part. This is something that’s really hard to document and quantify. So more effort has to be put in, in terms of quantifying these types of interactions, and how they sometimes can add up to greater than the impacts of each species individually.
HS: Have new types of interactions been discovered between non-native species?
BVH: Yes. There definitely have been a lot more of these really good examples between non-native species that could be categorized as invasional meltdown. I provide a number of these examples in my review of invasional meltdown in the Encyclopedia of Biological Invasions by Simberloff and Rejmankek, 2011. The exchange between Gurevitch and Simberloff might have been premature. That set of papers was published seven years after our paper was published. I think it’s going to take a lot more time to unveil invasional meltdowns in the field. These are very complicated interactions, they are hard to document, they are hard to find and it’s going to take a lot more time than five or six years.
HS: In general, do you think positive interactions are getting more attention these days?
BVH: That’s a good question. I certainly think they’re getting more attention than when we first published that paper in 1999. However, the excitement following the publication of that paper has died down, and there are probably fewer groups of researchers going out and trying to uncover these types of invasional meltdowns in natural systems.
HS: Another thing you say might be interesting to study is using the order of invasions to understand interactions. Have there been studies along these lines?
BVH: That’s a really good question. That is a really hard thing to study. In my opinion, the best way to do that would be to do that in an experimental context. And, to my knowledge, I haven’t seen anybody do that yet.
HS: What kind of impact did this paper have on your career? Has it influenced the kind of research you have done since then?
BVH: Yes. I started to look for invasional meltdowns in the systems that I worked in. So far, I’ve only been able to see the positive effect of one species on another set of invasive species. So in my work in Cape Cod, I looked at Black Locust (Robinia pseudoacacia), which is a nitrogen fixing tree. Cape Cod, Massachusetts is a very invasion-resistance habitat. The soils are very poor – nutrient poor – and dry, and you see very few non-native species in these habitats. However, right underneath black Locust trees, you see a wealth of non-native species flourishing. And the soils seem very different under these trees. However, I haven’t been able to see any kind of positive feedback from these non-native understory plants on the non-native over-story species.
Hari Sridhar: Have you ever had the need to read this paper since it was published?
BVH: Yes, I still go back and read it from time to time. When I go back to read this paper, I’m usually looking for specific examples of invasion or meltdown. I don’t think my style of writing has changed that much over time.
HS: What would you say to somebody who is about to read this paper today – what should she or he take away from it? Any caveats to keep in mind?
BVH: When I have my students read this paper, I ask them to think about examples that would fit the description of invasion meltdown, and how they would test that.
HS: Among all the papers you have written, is this your favourite? If yes, why? If no, and if you do have another favourite, which one is it and why?
BVH: This was the first paper of mine that was ever published, and so it is special in that way. My favorite paper, of those that I have written, is the synthesis of my dissertation research Ecological resistance to biological invasion overwhelmed by propagule pressure, by Von Holle and Simberloff, in Ecology.