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  • Post date: 1 year 7 months ago
    Citation for this post: BibTeX | RIS

    In 1998, and published in Nature reporting results of experiments that showed that scrub jays had “episodic-like” memory. This was the first behavioural evidence for this kind of memory from a non-human animal. Eighteen years after the paper was published, I spoke to Nicola Clayton about the making of this study and what we have learnt since about episodic memory in animals.

     (Interview conducted via Skype on 14th July 2016)


    Hari Sridhar: What was the specific motivation behind doing this study?

    Nicky Clayton: It came out of an interest in .


    HS: And where did that interest come from?

    NC: Well, I have always been a bird watcher and have observed and wondered about this behaviour numerous times.


    HS: How did the collaboration between you and Anthony Dickinson start?

    NC: Tony and I first met at a conference in 1996. In fact, at that conference, when I first suggested to him that jays might have memory he was completely dismissive. He said: “I can’t think of a single reason why they would need it”. And I said “Well, what about the fact that they hide perishable food? Wouldn’t it be important for them to be able to remember when or how long ago their cached their food, in order to know when they needed to recover their caches of food?” He didn’t know anything about the caching of perishable foods and so he said: “Oh gosh, I hadn’t thought about that”. So then we went away and spent much of the rest of the conference talking and discussing. I told him what I knew about the behaviour of the birds in the wild, from my observations of them, and it was at that point that he said: “Oh well, I just made an assumption, I didn’t know about this”. And I said “Well, this is something that we could test empirically”. And he said: “Absolutely, yes”. So then we got into a collaboration designing experiments to test whether or not the birds could remember the “what, where and when” of past caching episodes.

    Around the same time, was on sabbatical at the University of California, Davis, where I was based. I talked to Endel a lot about what, from a human psychological point of view, he would find convincing as the evidence potentially for episodic memory in animals. Obviously we called it “episodic-like” because we have no way of knowing whether or not they have the associated phenomenology that would accompany the conscious experience of episodically recording the past in humans. But in the absence of agreed behavioural markers in animals there is no way of knowing. Endel agreed that episodic-like memory was a fair term to use since we were just talking about the behavioural criteria. He also said that if the birds were to do this it would be a serious challenge for the work of cognitive neuroscientists. While he was not sure that he would go as far as saying that that showed that animals had episodic-like memory, it would certainly cause him to tighten up his definition of what episodic memory in humans is.

    So we did the experiment and to our amazement we were able to show that jays do remember the “what, where and when” of specific past caching episodes. We, obviously, controlled for relative familiarity, which is an important factor to be controlled for in the human research. Receiver operating characteristics suggest that familiarity and recall are distinct and separate processes, both psychologically and in terms of areas of the brain. So we controlled for that and showed that, yes, they did appear to be remember specific “what, where and when” of caching episodes.

    Then, having talked to Endel about it, we thought that the work was of sufficient salience to be submitted to Nature. We did that, they just sent it out to review and then, a couple of months later, I heard that the paper had been accepted, almost with no revisions actually. I think the reviewers were , who won a Nobel Prize recently for his work on place cells, and Endel Tulving. So that is sort of the brief history of this paper.


    HS: In the last line of the paper you say “This is the first conclusive behavioural evidence of episodic-like memory in animals” Since then has it been discovered in other animals?

    NC: It has been shown in other animals, but that was the first demonstration. Some of the other studies haven’t really controlled for things properly. I mean we didn’t do everything in that paper but, obviously, in subsequent papers , and that . So it’s not just that they remember after a short delay and forget after a long delay. We have been able to show that they actually remember the different types of food items in the integrated episodes. But since then, yes, it’s and .


    HS: Did you do all the work related to the experiments – training of birds, care of birds, etc. – yourself?

    NC: Well, I had a team of people. So for the first experiment I did pretty much all of it myself, because I was an assistant professor setting up my lab. But then, obviously, as my lab grew I had PhD students and postdocs to help. Kara Shirley Yu was the first research assistant I had, and she was a co-author on a number of the initial papers. She helped me collect the data, but was not involved in helping design the experiments, analysing the data and writing it up. Most of that I did on my own or in conjunction with Tony. Whilst I was in Davis and he was in Cambridge, we used to talk on the phone once a week, and then I was invited to apply for a position in Cambridge, which I got. Obviously, since then life’s been a lot easier because Tony and I have been in the same place.



    HS: How long did the writing take?

    NC: I am a fairly quick writer, so I don’t think it took more than a month or so to write it up.


    HS: During the writing, did you communicate with Anthony Dickinson mostly on the phone?

    NC: Yes, Tony and I spoke mostly on the phone during that period, because I was in California and he was in Cambridge.


    HS: Did he visit California anytime during when the experiments were being conducted?

    NC: Oh yes, he came to visit and spent about three weeks, I think, in California.


    HS: Did this paper have a big impact on your career and your future research?

    NC: Yes, definitely. I am now and I would say that the Nature paper was one of the big influences. To be elected, the key question is what contribution you have made to science, but also, specifically, they want to know if you have changed the field. Is the field different as a result of the work that you have done? I think the work presented in this paper was one of three key pieces of evidence in favour of my case.  The second was the work on the social side of caching, particularly the research I conducted with my husband , showing that it is only experienced thieves who re-hide the caches when others have watched them cache. That was also . Thirdly, there was on the jay’s ability to plan for the future, which is a necessary follow-on from the episodic-like memory. In addition to the empirical findings, another seminal piece of work really was suggesting that jays and other members of the crow family are as clever as the great apes. So when it comes to intelligence you can think of them as - that was a term Nathan coined. So I would say that these were probably the key papers. And the power comes from converging evidence. If you have just got a one-off study, well, that’s interesting, but that’s all it is. It is only when you have a body of evidence all leading in the same direction that things become really convincing.


    HS: This paper has been cited over 900 times. At the time when it was published did you anticipate that it would have such a big impact?

    NC: No, I had no idea.


    HS: Do you know what it mostly gets cited for?

    NC: There’s probably two main strands, I think. One is memory research in general - mental time travel, episodic memory, future planning etc. And the other is within comparative cognition. For example, our work showing that these birds are as clever as the great apes. I think it’s been cited quite a bit in comparative cognition and even in developmental cognition as well.


     HS: The material you used in these experiments – peanuts, worms, lego blocks, ice trays – do you continue to use these in your experiments today?

    NC: Oh yes, I still use ice cube trays full of sand and corn kibble and a few Lego Duplo bricks.


    HS: I read somewhere that when you moved from California to Cambridge you took the jays with you? Do you still use some of these birds for your experiments?

    NC: Yes, I made that conditional on my job offer. I said that I would be delighted to accept the position but only if I could bring my jays with me. So I requested 25 avian lectureships! And I’ve still got five of those jays left. The oldest one is 21 now. But I also use Eurasian jays these days, which are easier to get hold of in the UK, and delightful to work with. It's a real honour to be able to work with corvids. They are so intelligent.


    HS: Do you know what has happened to the experimental infrastructure you used when you were in UC Davis?

    NC: Well, it was used by other people the last time I visited Davis, but I don’t know what’s going on now as I haven’t been back in years. I have so many fond memories.


    HS: If you were to repeat this experiment today, would you do anything differently?

    NC: I don’t think I would, actually. I think, as a starting point, once you have made the initial discovery, there are, obviously, other things to control for. But I think I would still do that initial experiment in pretty much the same way, because it was guided by the bird’s natural behaviour. That’s where the inspiration came from.


    HS: Were the main findings of this experimental study substantiated by evidence from field studies later on?

    Not of this experimental study specifically, because field studies aren’t amenable to comparing birds with and without experience of degraded worms, but the studies on the social cognition of Corvids have been replicated in both field and lab studies, and other laboratory studies have found evidence of this specific experimental study on memory (namely episodic-like memory) in other Corvids and also other species of birds and mammals.


    HS: Were the findings controversial when they were published? Did they attract a lot of attention?

    NC: It attracted a lot of attention and I was very lucky to have people like Endel Tulving supporting me. A lot of people in human memory research probably wouldn’t have looked at my research on birds. It wasn’t be a species of bird that most people in this field hadn’t even heard of at that time. But Endel Tulving told everyone about it. So it immediately got the attention of other influential people in the human memory work, who have become good friends and colleagues since.  People like , and others.

    I know at that time I was worried that people would develop a rat model and the jay work would just be forgotten. The rat brain would be so much more amenable to doing neuroscience studies, because we know so much more about the rat brain. Also, the rat brain is, obviously, a better model if you are interested in mammalian brains. I was also not willing to do invasive work with my scrub jays. With rats you can just order them and specify the number of males and females and there they are. With my scrub jays, I have to find the nests and hand-raise the chicks and all that sort of thing, so they are too valuable a resource for me to do invasive work. So given all this, I was worried that people would just turn to rats and the jays would get ignored, but that wasn’t the case. I was very lucky I think.


    HS: Have you ever read the paper after it was published?

    NC: Yes, but only in terms of refreshing my mind about what we said at the time.


    HS: What would you say to a student about to read this paper today? What should he or she take away from it?

    NC: The same as what it was then really. I think it still remains the same. When Endel Tulving coined the term episodic memory he talked about spatio-temporal relations. I would then point out how his definition has changed over time to include integrated memories of multiple features, . I would point out the issue of distinguishing between recall and familiarity, which was really developed by the time of . And then I would point them to the idea that, since then, people have made this link between episodic memory and future planning in the form of mental time travel. The influential work of Dan Schacter and others show that these memories are primarily for the future - . But I don’t think I would have wanted to make that initial paper more complex by having future planning in it. Nature papers are very short, so you need quite a simple design. And I think the trick to Nature papers, from what I have seen, is, really, to have a couple of really solid experiments that provide the firm footing in other journals. Then if you do a really exciting experiment and it works, then you can publish a short paper in Nature with this body of other evidence in other journals to substantiate your claim. I think a lot of people have done that. That’s the technique that, for example, used in all his rat spatial memory water maze work. I would say it’s also the technique that John O’Keefe used with his seminal work on place cells.


    HS: Among the papers you have published, is this one of your favourites?

    NC: Yes, it’s one of my favourites because it the first of my papers to reveal the remarkable cognitive abilities of these wonderful birds.




  • Post date: 1 year 7 months ago
    Citation for this post: BibTeX | RIS

    In 1994, Andreas Kruess and published in Science reporting the results of their experiments looking at how habitat fragmentation affects diversity and natural pest control in agricultural fields. Twenty-two years later, I spoke to Teja Tscharntke about the making of this study and what we have learnt about habitat fragmentation effects in agricultural ecosystems since.

     Questions sent by email on 16th July 2016; responses sent by email on 8th August 2016

     Hari Sridhar: You say "we tested the hypothesis that extinctions in small and isolated habitat should not affect all species equally. Natural enemies of phytophagous insects are expected to become extinct first, thereby increasing the risk of pest outbreaks." I would like to ask you what your motivation was for doing this study. Did it come mainly from the debates about island biogeography happening around that time, or from a more applied interest in the management of agricultural landscapes, or was it a combination of both?

    Teja Tscharntke: The main idea was to identify how habitat fragmentation in agricultural mosaic landscapes affects species richness and associated trophic interactions such as biological control. The concept of island biogeography was definitely influential, but as I just started my position as professor in Agroecology (in 1993), I was keen to give my research a more applied focus.


    HS:  Why did you pick red clover (Trifolium pratense) for your study and Vicia sepium for the supplementary study?

    TT: In the field, communities and food webs are utterly complex, so I was interested in mini-ecosystems with few species that allow for tritrophic interaction research. Flower heads of Trifolium and pods of Vicia have proven to support a number of interacting herbivore and parasitoid species on a small and well-defined resource. We are still keen to analyze such handy small ecosystems (e.g., grass stems, Brassicaceae plants, bundles of nesting resources for bees, wasps and their parasitoids) as they potentially yield insights that one cannot derive from more complex systems.


    HS: How did this collaboration between you and Andreas Kruess for this paper come about? What roles did each of you play in this study?

    TT: Andreas Kruess was my doctoral student and this Science paper was the first part of his thesis, so we had frequent, direct exchanges about the study. In fact, his name is Andreas Krüß, but he decided to adapt his last name (with an umlaut and ß) to Anglo-American writing. At the time of this field experiment (1992) we were both still at the Zoological Institute at Karlsruhe University. We designed the study, he performed the experiments and we jointly performed analyses and writing.


    HS: The paper presents a lot of natural history information about the plant and its insects. Was all this already known or was it information collected during the course of this study?

    TT: The specifics of the relations between the plant, herbivore and parasitoid species were found in the natural-history literature in Germany. The quantitative data were collected during the study.


    HS: You say that “each patch was created in March 1992". How long after this were the experimental clover habitats surveyed for their insect fauna?

    TT: The island patches were created in the early spring and the colonization and field surveys done in summer of the same year.


    HS: You say "The red clover (variety Odenwalder Rotklee) had been sown in an experimental field in April 1990". Who did this and what was it done for?

    TT: Red clover is a perennial species, so you need at least two years of growing to get fully blooming plants. This is why we took plants that we had already sown two years ago for our experimental patches.


    HS: Can you give us a timeline of this study - from idea, to design, to experimental work, to analysis and writing up?

    TT: The idea and detailed design were developed in 1991, experimental work was carried out in 1992, analyses and writing were mainly done in 1993.


    HS: Specifically, can you tell us how long the writing took and when it happened? How did you share and edit manuscript drafts (I am guessing this was before MS Word introduced "track changes")?

    TT: Andreas and I met regularly in person, so this was not a problem. Indeed, at that time we had no emails (but only ordinary snail-post letters or fax) and no sophisticated word processor software.


    HS: Did this paper have a smooth ride through peer-review? Was Science the first place you submitted it to? How much did the paper change from the first submitted version?

    TT: In fact, the editor and later the reviewers were very positive about our manuscript. Science was the first journal we submitted it to. The text was dramatically altered by the Science staff to make it read smoother. However, results, tables, figures, conclusions etc. remained similar.
    HS:  What did you use to draw the figures presented in the paper?

    TT: We used menu-driven Statgraphics software.


    HS: Did the paper attract attention when it was published?

    TT: This paper immediately attracted a lot of attention by colleagues and in the public. In 1994, this was (and still is) a topical story confirming expectations of agriculture disrupting food webs and destroying associated services such as biological control. My impression is that this paper stimulated a lot of applied research, since applied ecology in 1994 was not as popular as it is today (it was in the shadow of the more highly valued basic science). Many colleagues invited me for seminars and keynotes based on this topic.


    HS:  At the time this was published, did you anticipate that it would be cited so much? Would you know what this paper has been mostly cited for?

    TT: In 1994, emails, search machines etc. were not available (at least not for me), so I realized only much later that the paper has been cited so often. Even more importantly, at that time, the number of citations was not checked by everybody and not the hype it is today. Our paper was usually cited as providing evidence that the dynamics in agricultural landscapes impede biological control, disrupt food chains and release herbivores from their natural enemies.


    HS:  What impact has this paper had on your research and your career? Did it open up new lines of investigation? Did you continue to work with Andreas Kruess after this paper?

    TT: Indeed, this was our first truly applied paper published in a major journal. In the following years, we published many papers showing similar effects of habitat fragmentation and agricultural intensification on biodiversity and associated functioning such as biological control. In particular, we managed to publish on this topic, quantifying how simplification of landscape structure causes major losses of biocontrol and, subsequently, high crop damage in oilseed rape. For a number of years, Andreas Kruess was a postdoc. in my group and then moved to an influential position at the German Federal Agency for Nature Conservation.


    HS: In your paper you talk about the importance of "abundant and widely distributed species like S. dubius for biocontrol". Did this find resonance in biocontrol development after the study was published?

    TT: This interesting result, emphasizing the role of common, not rare, species for ecosystem services such as biocontrol, has been less referred to. Only recently has this topic become more important in the literature ().


    HS: Based on your results, you say that "food chains should be shorter in small islands than in larger habitats". Was this borne out by future research on food webs in fragmented landscapes?

    TT: Yes, truncation of food chains on habitat islands became a major issue afterwards and has been reviewed (for example, ; ).


    HS: Did your study have any impact on management of agricultural landscapes for habitat connectivity?

    TT: Enhancing habitat connectivity was already at that time a major topic. Later on, .


    HS:  If you were to redo this experiment today, would you change anything about it, given the developments in technology, theoretical understanding, analytical techniques etc. since 1994?

    TT: The experimental evidence and the conclusions drawn from it still hold today. Improvements would be to add more real-world complexity to the experiment. For example, studying potential successional changes over the years would be interesting and considering different landscape contexts should show how fragmentation effects depend on the surrounding landscape complexity. Further, integrating life history traits of the organisms involved may shed new light on the results. So far the Science paper tested only species rarity and population fluctuations, which were good predictors of species extinction in these experimental islands.


    HS:  What would you say to a student about to read this paper today? What should he or she take away from it? Would you add any caveats?

    TT: The patterns described are based on annual colonization and extinction, which is typical in agricultural landscapes dominated by annual cropland. However, we showed in a side experiment that also old and small meadow fragments are characterized by reduced parasitism rates of phytophagous insects. Hence, enhancing habitat connectivity, and counterbalancing extinction, is clearly a major task in landscape-wide conservation programs.


    HS:  Have you ever read the paper after it was published? When you read it now, what strikes you the most about it?

    TT: Indeed, I just read it again – and fortunately (and kind of surprisingly), I found the paper still ecologically worthwhile.


    HS:  A question about the acknowledgements: who were B.A. Hawkins, W.J. Boecklen and R. Brandl and how did you know them? How did you know S. Vidal and M. Capek, who helped you with some taxonomic work?

    TS: I got a lot of support from Bradford A Hawkins (UC Irvine), whom I first met at a conference and who stimulated us to submit the manuscript to Science and gave a lot of advice on how to proceed. At that time, most ecological papers authored by German scientists were still written in German and submissions to high-ranked Anglo-American journals almost absent.
    Bill Boecklen and Roland Brandl were so kind to add critical comments that further improved the paper. In western and eastern Europe, there is a long tradition in natural-history and taxonomic studies, so we knew experts in parasitoid identification. However, lack of taxonomic knowledge becomes more and more of a severe bottleneck in current ecological research.


    HS: Is this your favorite paper among all the papers you have published?

    TT: As this important paper appeared so early in my career and shaped my scientific future, it is still one of my favorite papers, besides the above-mentioned , and later on, a few other nice papers, e.g. on pollination, tropical research and socioeconomic-ecological studies.



  • Post date: 1 year 8 months ago
    Citation for this post: BibTeX | RIS

    In 1999, and published a 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.


    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 (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 .


    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 . 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, , 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 . There is this term , 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, was the first journal that we submitted this to, and we were really excited about this new journal. The 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. 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 (, , ), 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 . 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. . 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 , by Von Holle and Simberloff, in Ecology.



  • Post date: 1 year 8 months ago
    Citation for this post: BibTeX | RIS

    In 1990, , James Fox, and published in Nature showing that, during courtship, male exploit a pre-existing neural bias in females towards lower-pitched calls. This experiment provided evidence in support of a third hypothesis for the evolution of female choice (in addition to runaway sexual selection and natural selection): ‘sensory exploitation’. Twenty-six years after the paper was published, I interviewed Michael Ryan about the making of this paper and what we have learnt since then about the sensory exploitation hypothesis.


    Hari Sridhar: Before this study, you had already done a lot of work on Tungara frogs and sexual selection. You had even written about it. Can you tell us what the specific motivation was to do the work presented in this paper, on the neural basis for female preference?

    Michael Ryan: Well, when I started to work with frogs for a Master’s thesis, before I went to Cornell to do my PhD, the dogma was - most of which was true – that frog calls evolved to indicate the species - the species identity of the caller. And that females were under strong selection to mate with males of the same species. That’s certainly true. And then when I went to Cornell and started working with - I was not working with calls then; I was studying territoriality – I was struck by how variable their calls were. I mean a bull frog call sounds like a bull frog call, but I could clearly tell males apart. I would hear a male and know that he was on a neighbouring territory the night before. That he’d moved over. That’s how I became interested with the frog call, as it had to do with mate selection within a species. The thought then would have been that the variation is just noise; that it’s not very meaningful. Then I came across , read Darwin and then got very excited about studying the calls as a sexually-selected character. But when I went to Cornell, I was down the hall from this faculty member, . Capranica had done ground-breaking work on how frogs extract biologically meaningful information from the call. He was a very serious neurobiologist who had received his PhD at MIT, then was at Bell labs for a number of years, before he went to Cornell. Capranica and a whole series of students had shown how the frog’s brain was organised to cause the female to find calls of its own species the most attractive. I thought that if this brain is wired to detect calls, and if there is a lot of variation in calls, then some calls must sound more attractive than other calls. Then the same year I was hired in the zoology department in Texas, just by chance, they hired a post-doc from Capranica’s lab – Walt Wilczynski - in the psychology department. We knew each other from before, though we weren’t close friends. But we both felt that looking at this question – variation in the neural basis of sexually-selected calls - would be very much worth doing. But before that, in my Tungara frog book, I actually sketched out a little model for how neural biases in the Tungara frog might cause females to prefer lower frequency calls. What I suggested then was wrong, but that’s when I started thinking that the variation in the auditory system could explain variation in female preferences for male calls.


    HS: Did you test your model in this paper?

    MR: We didn’t test that model specifically.  I tested that model behaviourally and showed that it was wrong. I had worked with Walt Wilczynski on another frog - - looking at variation among populations. That’s where Walt and I started this neuro-ethological approach. I am just going to quickly glance at my publications to see if we started publishing on cricket frogs before Tungara frogs. I am sorry, this will just take a few seconds. We were doing this research at the same time. Ah, here it is. In 1988 we had a paper in Science: “”. That study did not demonstrate that the brain was generating sexual selection within populations, but instead it was influencing how calls and preferences evolve amongst different populations. Then with the Tungara frog we asked that question at a different level. Instead of variation among populations we were asking about variation within a population. But the neural work on the Tungara frogs came after Walt and I started working on the brain and behaviour of the cricket frog. We had already been interested in the Tungara frog, so that was a very natural progression.


    HS: Going back one step, can you tell us how you first got interested in the Tungara frog?

    MR: I searched the literature for some species to work on for my PhD thesis. I wanted to look at how variation in calls influenced mate preference within the species, and I decided to work on in Panama. But they were very high up in the canopy and I was having a difficult time recording the males and a difficult time watching the matings. And when I was trying to record these males, all these Tungara frogs would be calling at my feet. They were very common and I would always be kicking the frogs to shut them out so I could hear the red eyed tree frogs calling. That’s when I thought that since these Tungara frogs are always calling, maybe I should study them instead. That’s how I started to study them.


    HS: You spoke about Walt Wilczynski’s role in this paper. Can you tell me about the roles of the other two authors – James Fox and Stanley Rand?

    MR: Stanley Rand is the most important person in this story. Stan had studied the Tungara frog in the 1960s, although he had not published anything on them. He was very well-known for his work on reptiles in Panama, but he had also done a lot of work on frog calls in Brazil. So when I went to Panama, to the Smithsonian institution, he was my mentor. However, during my PhD, I worked fairly independently of Stan. Because I was on Barro Colorado island, I would only see him for a short time, maybe once a week, when I went into the city. But after I received my PhD, he and I started this very serious and very long-term collaboration, working not only in Panama but all over south America. Stan had done the initial work in the Tungara frogs, describing the call variation. But like I said earlier, he had not worked on these frogs for 10 or 15 years before I started to. Stan then became a very very close collaborator and a very dear friend for many years. So the importance of Stan in all of this cannot be overemphasized. And Walt, who I also wrote with a few years ago, he and I are also very close friends. As were Walt and Stan. So the three of us collaborated a lot and were also personally close, besides being professionally close.

    Jim Fox was a graduate student of Walt’s lab. He was doing auditory neurophysiology for his PhD thesis and was also doing some computer modelling. Walt had recorded the tuning curves for the auditory system of the Tungara frog. So when I went to Walt and said that we needed to do the simulations that we did in this paper, Walt said Jim would be a very good person to do that part of the work.


    HS: Did you bring the frogs back to Texas for the lab work?

    MY: Yes we did. We brought them back from Panama. In that paper we have just the Tungara frog, but I think we in which we had nine different species of Physalaemus. Maybe there were eight, I forget, but it included all of the closest relatives of the Tungara frog and some outlier species. For those, Stan and I went all over South America - Ecuador, Peru, Venezuela and maybe Colombia - and brought those frogs back to the lab where Walt did the neurophysiology studies.


    HS: In the Acknowledgements, you thank the governments of Panama and Ecuador. Did you samples the other species you use in this study - coloradorum - in Ecuador?

    MR: Yes. I spent, probably, 4-5 months in Ecuador, working with Physalaemus coloradorum, as well as two other species of Physalaemus. There’s one in the Amazon - Physalaemus petersi - which we have done a lot of work with, and then another Physalaemus species from the Pacific coast - Physalaemus pustulatus. Then we added to that Physalaemus enesefae from Venezuela and then Physalaemus - I have forgotten what we called it, kaikai I think – it’s still an undescribed species. Then we had another species - Physalaemus roraima - that was from Brazil. We did many long and arduous field trips to record those animals in the field and bring them back to Texas in good shape and, of course, alive.


    HS: Why did you pick P. coloradorum for the comparison in this paper? Is it the closest relative?

    MR: No, it’s not the closest relative. The closest relative is something called Physalaemus petersi, which we did study, but I didn’t want to compare with petersi because there had been reports that some populations had complex calls and other populations did not have complex calls. So we didn’t know then if the complex call evolved independently in Tungara and petersi or if it was the common ancestor of those two. Those two are sister species. So then we decided to go kind of over to the next little group. And that’s where we started the work with coloradorum.


    HS: You say you recorded calls from 54 males. Did you make all the recordings yourself?

    MR: Yes, all of the acoustic work I did myself. Included in that is a transect that Stan and I did one time. We drove from Texas, through all of Central America, to Panama, and recorded Tungara calls from maybe 25 to 30 populations. And I did all the recording and all the acoustic analysis.


    HS: Was the equipment you used for recording then very different from what you use now?

    MR: Oh yes. It has changed a lot. In the very beginning I was using a tape recorder - big heavy reel-to-reel tape recorder - and occasionally another make called . From that we moved to high quality cassette recorders and then onto digital recorders.


    HS: Did you come up with the terms “whine” and chuck” to describe the Tungara frog’s calls?

    MR: No, ‘whine’ and ‘chuck’ are terms that Stan had already come up with. Again, the work wasn’t published. What’s interesting is that when I went to Panama these were not called Tungara frogs. They were called mud-puddle frogs. And then I asked a Panamanian if there is a Panamanian name for the frogs. He said ‘Tungara’. The word is onomatopoetic. Tungara sounds like a whine and two chucks – . Later, after I started to use that name, I found a field guide to the frogs of Nicaragua where the author independently was also calling this frog Tungara.


    HS: Did you do most of the writing for this paper?

    MR: Yes. In all of the frog work I did with Stan, in all of those papers - I don’t know if there are 50 or 80 or 100 - I did all the writing. I would say up until maybe 4 years ago, I did all the writing of papers myself. In the last 10 years, we have had a lot of grad. students working on the Tungara frogs and now they do a lot of the writing.


    HS: In the abstract, you say your results allow you “to reject two popular hypothesis for the evolution of this female preference (runaway sexual selection and natural selection) in favour of a third: sexual selection for sensory exploitation.” Were your results one of the first evidences in support of this mechanism?

    MR: Well yes, because the term sensory exploitation had never been used before. There are actually two papers – this one and - where I laid out this idea of sensory exploitation. Now, like most ideas, it wasn’t like brand new. It was very much related to ’s idea of , to some of ’s ideas about - I am blanking on the term she used – . Then, when I sent some of this work to , he wrote back and said this was exactly . So Endler came up with sensory biases about the same time I came up with this idea of sensory exploitation.


    HS: You say “In all studies to date in which female mate preferences based on call frequency are expressed, tuning of the peripheral auditory system predicts the preference by indicating frequencies that would most strongly stimulate the auditory system. There are no reported examples of any mechanisms overriding this peripheral bias”. Since then, have there been such examples?

    MR: I don’t think so. There was where they reviewed a lot of the data and showed that the dominant frequency of the male calls and the tuning of the female’s auditory system were fairly well correlated for a number of species. I think the R2 might have been 0.8 or 0.85. Now, I probably wouldn’t state that exactly the same way now, because there are frogs in which the females are much more attentive to temporal variation, for example, the pulse rate. I would have to check; I don’t know if people have played pulse rate against preferred dominant frequency and seen what happens.


    HS: You say that “As the chuck falls below optimal frequency, neural stimulation decreases only slightly, but there is a greater decrement in stimulation when the frequency of the chuck is increased above the optimal chuck”. Do you get the same asymmetry in preference when you play a range of frequencies around the optimum to the female?

    MR:  Do we get the same asymmetry..hmmm... The short answer is I don’t know. We have done the experiment, but I am not sure we have published the data in that context. We have a big paper in Animal Behaviour - - on preferences of spectral features, and I don’t know if the asymmetry pops up in those preferences or not.


    HS: Can you give us a sense of how long the whole project took. Of course, the fieldwork on the frogs had been going on for a long time, but can you tell us when all the lab work and writing was done for this specific paper? Would you remember how long it took from idea to execution and publication?

    MR: Yes, I have a pretty good idea, because I had stopped working with Tungara frogs for a couple of years and then I came to Texas for my faculty position. So I think it was about 1986 that Stan and I started to work together, and it was for this idea. We weren’t using the word sensory exploitation at the start. The term only came in 1990 when we used it in the titles of three papers – this one, the Oxford series and . So all that work started in 1986, and it probably took Walt a good year to do the recordings. I would say about four years from the beginning, with the idea already taking form in 1986.


    HS: How long did just the writing take?

    MR: I write very quickly. I’m guessing it took a couple of months. Just using this paper as an example - Stan and Walt and I would constantly talk about what was going to be in the paper. So by the time I started writing - and this is how I write always - the outline was already there. It was merely a matter of putting it on paper. I know other people write very differently. They think as they write, but I usually do most of the thinking before.

    But just to put one thing in context. I am not sure exactly when we started to use the internet, but in ‘86 when Stan and I started this work, we didn’t have any internet. Stan was in Panama, so we would have to mail manuscripts back and forth. That really slowed things down.


    HS: Would Stan, Walt and you meet often?

    MR: Walt is not here now, but he was in the psychology department here in Austin then. He was also my closest friend here, so we would see each other a lot. And Stan would come to Austin twice a year for visits. And, of course, I was in Panama every summer, and Walt would come to Panama occasionally. So we would meet a lot and constantly bounce ideas off one another.


    HS: Did all four authors ever meet as a group?

    MR: Oh yes. I forget exactly the time of the year, but I remember Stan was up for a visit and he met Jim Fox and Jim showed him the results of the simulation. Once Fox was done analysing those data, then the paper was fairly well outlined, and Stan met up with all three of us.


    HS: Do you remember how the figures in the paper were drawn?

    MR: Those were drawn with a ruler, a and Indian ink. And they might have been labelled with press type. It’s possible that an artist might have helped with some of this, but if so, she must have done it the same way, you know, by hand.


    HS: In the Acknowledgements you thank a few people for comments on the manuscript. Can you tell us how you knew these people?

    MR: is an evolutionary biologist who works on virus evolution. He’s down the hall from me. is pretty famous for his theoretical models of sexual selection. Kirkpatrick and I were post-docs. together at Berkeley. There, we started talking about sexual selection, and he taught me a lot about evolutionary genetics and runaway sexual selection. He was also in my department. was a good friend and an entomologist, who was very interested in phylogenetics and the comparative method. So she was a lot of help reading this paper. And was a graduate student of mine at the time.


    HS: Did this paper have an easy ride through peer-review?

    MR: It did. I was in England after submitting it to Nature and somebody - I’d rather not say who - came up to me and told me he or she had reviewed it and really liked it. So yes, we didn’t have to argue or anything about it.


    HS: It was submitted in the end of May and accepted by the end of October. So it took just five months.

    MR: I guess I was impatient in those days, but it did seem long then! But a lot of people disliked that paper when it came out.


    HS: Why was that?

    MR: Well, it was different and it was new. I first talked about this paper at a behavioural ecology congress in Uppsala in 1990. I was asked to give a plenary talk - this is before I had published anything on this. So I gave the talk and gave a talk later. That talk of Maynard Smith became famous in the field because in it he acknowledged that he had made a mistake criticizing ’s . Zahavi and I are close friends, so I was sitting next to Zahavi when Maynard Smith was giving that talk. But then, at the end of his talk, after acknowledging his mistake, he said – ‘And then Mike Ryan gave this talk and..’ and he pauses and I’m getting very nervous and he says - ‘And.. ah, I’m just not sure what to think about that’ Now I knew Maynard Smith, because he had come to Panama for a long time and we had become close friends. So I talked to him later on and he said he was very intrigued by my idea. He told me about work by on neural networks and said that I should contact him because he had the same ideas that I did. Then there was this group at Cornell, which is where I got my PhD thesis, who were very upset by this paper. These included , , and I know told me that no one at Cornell saw any validity in the idea. But Sherman especially was very very critical in print, and we went back and forth for a while. I think the problem was that people like Sherman - who I like a lot and have immense respect for - came out of those wars. He was a graduate student of and I think he was kind of an extreme adaptationist who viewed this sensory exploitation idea as anti-adaptation. But it’s not really anti-adaptation; it only has a very modular view of adaptation. I’m just finishing to write a book now called “The Nature and Neuroscience of Sexual Beauty”, in which the basic idea is this: the brain determines what is sexually appealing to it. These sexual preferences in the brain, e.g. the way we perceive beauty, some of that certainly evolves for adaptive mate choice, but the brain does many different things and sex is only one of them. I think Paul didn’t like that idea at all. He also didn’t think that historical contingency played much of a role and that the strength of natural selection would overpower any phylogenetic inertia. So I think Paul saw people like myself who were pushing this idea as falling more into the camp of, let’s say, than of .


    HS: Did the paper attract attention in the popular press when it was published?

    MR: It did, but not all that much. You know papers in Nature and Science always get some attention, but I don’t think it got attention in the press for the right reasons. , when I was 50 - which would have been in 2003 - and that’s when, for the first time, I got the feeling that at least some people in the media were understanding what people like myself and John Endler and Mary Jane West-Eberhard were talking about. For most people in the media, I think our message was too subtle.


    HS: Its now 27 years since this paper was published. Given all the work you have done since then, do you think the main findings of this paper still hold true?

    MR: Yes, it does. One of my colleagues here - , maybe in 2013. We reviewed over a couple of 100 studies that were, you know, supportive of these basic ideas of sensory bias and sensory exploitation and sensory traps - they all kind of blend into one another. But there’s a couple of hundred studies that we saw as support for these ideas, I should say.


    HS: If you were to repeat this experiment today would you change anything, given the advances in technology, theory and analytical techniques?

    MR: Well, probably. I mean, now, most of the brain work is done using (IEG). There is no doubt these genes have told us a lot about organisation in the central Nervous System, but these gene expression studies would not give us the information we got from putting an electrode in a cell and testing its characteristics. We are now interested in multimodal communication - how visual signals combine with acoustics. So, as we speak, we are doing IEG studies, but I also have a grad. student working in a medical school with one of my old postdocs because we feel that for some of these questions we are asking we still need to use electrodes and characterise cells. The gene expression studies can’t do that. So I think if we redid that study today, we would add gene expression studies to the neurobiology, but I don’t think we would have replaced it.

    And in terms of the phonotaxis experiments - we do them in big fancy walk-in chambers, and videotape all the responses, so they can be double-checked. For the female to go from the middle of the arena up to the speaker - we scored it as a choice when she is actually 10 cm in front of the speaker - if we were to scale that response to human body size, it would be the equivalent of travelling 80 metres. So this was a very robust response even then.

    We have adapted to new technologies to do the analysis of the calls, the recording of the calls and the way we do the experiments, but the basic experiment is the same - we ask the females to go to the calls and tell us which one she likes better.

    Can I just tell you another small incident about not everyone liking this paper?


    HS: Sure, go ahead.

    MR: I went to a workshop at Davis once, which had a lot of people working on communication. , who wrote a forward for my Tungara frog book and was a great hero of mine, had organised this. They had discussion groups you could join, and I was surprised to find one discussion group on sensory exploitation. I went there, and in that group of people was . I had met him a few times before, said hello, but we weren’t friends. In that discussion group, Hamilton said - I don’t really see anything - I forget his word; enlightening or important or worthwhile, something like that – in this idea. Then a couple of other people in the group said: ‘Ya, I agree with Bill’. ‘I agree with Bill’. Well, in those days, who would not agree with Bill Hamilton! I mean he was a genius.


    HS: Which year was this?

    MR: It was early 90s. But I have to make one thing clear: he wasn’t saying it at all in an aggressive way or a mean way. He was just stating what he thought. I met Hamilton another time and we talked about other things and he gave me some very good suggestions about some fish studies I was doing. But for someone like me who, you know, had recently published this idea, to have one of the greatest minds in evolutionary biology tell you that he didn’t think there was anything there - that was a bit deflating.


    HS: How much of an influence did this particular piece of work have on the future course of your research? Did it open up new lines of research?

    MR: Oh yes. I had , and I’m pretty sure that that was the first experimental demonstration of sexual selection by female mate choice. It was a year before .  But what this idea said to us is, you know, if sensory exploitation is right, we should be able to synthesise any kinds of calls that we want. This is one of the beauties of working with acoustic displays. So we decided we’ll just see how we can exploit the female’s sensory system. Can we add things to a whine that are not chucks but are as attractive as chucks? After Stan passed away a few years ago, brought together a whole lot of this research and showed all these different kinds of sounds that would have made males much more attractive if they possessed them. Our paper came out a little bit after , where he did pretty much the same thing with fish. He presented females with models of male fish with all these constructed variation in visual display. So yes, for us it opened up a very different approach, through which we have been exploring the female’s - now, I wouldn’t say auditory system - whole perceptual system. Because we are including the brain now. The work we have been doing since 2010 has been asking very similar questions, but at the level of cognition. So we had on Weber’s law and how that influences preference. I think since 2010 - if a paper we have submitted now gets accepted and it is very likely it will – we would have had five papers in Science, all of them based on exploring these biases, not just in the sensory system, but in the whole perceptual and cognitive systems of the females.


    HS: I know that Stan Rand passed away a few years ago. Do you continue to work with the other two authors of this paper?

    MR: Not with Jim Fox. I am not quite sure what became of Jim. But I do continue to work with Walt. Like I said, we even published a small Animal Behaviour text book together a few years ago. He left University of Texas maybe 8 years ago but he still has his house here. Just last week we had dinner together and we were talking about new things we might start to work on. He still serves on th committees of my students who have neurobiology components in their work. I am not a real neurobiologist. Walt is now at Georgia State University. He went there to become the director of .


    HS: Have you gone back to these field sites after this study? Do you continue to work there?

    MR: Yes, I continue to work in Panama, although I don’t work on the island anymore. We work on the mainland right across from the island. So yes, we’ve been working there for many years. Just to give you an example - the most basic female preference we have studied is this preference for “whine-chuck over “whine” I think we have about 20 years of data on the strength of the preference for “whine-chuck” over just “whine”.  We almost always have sample sizes over 100 so we have very good measures of the strength of that preference. Because of my accident, this is the first summer in many years that I have not been in Panama. Since we have stopped for a year, maybe I will start putting all that work together. We have lots of long-term data of this kind.


    HS: If you don’t mind my asking, why have you stopped working on the island?

    MR: Well for few reasons. We work in this small town called Gamboa. When we started working there, there weren’t many scientists, but since then the Smithsonian Tropical Research Institute . The very first lab building they built had our frog lab in there. And I still have it - the Smithsonian lets me keep it after Stan passed away. And there are many more Tungara frogs there than on the island. Also, as the phonotaxis experiments started to become more sophisticated, we needed to be closer to electronic shops and computer shops. From Gamboa it is easier to get to Panama City.


    HS:  Have you ever read the paper after it was published?

    MR: I generally don’t go back and reread my papers. I look at them, of course, when I reference them, to make sure I’m remembering correctly what is in the paper. But I did read that paper and the one in Oxford Surveys a few years ago and I was pleasantly surprised that I liked them so much.


    HS: Do you think the way you write has changed since this paper?

    MR: Not too much. The last two years I have been working on a popular book that I already mentioned, and that’s having a little bit of an influence on my writing now – I try to make things a little bit broader maybe. But, in general, I don’t think it has changed too much.


    HS: Do you know what this paper mostly gets cited for?

    MR: I certainly did, when , a couple of years ago. It’s usually cited by studies that are also finding evidence for sensory exploitation, but it’s also been cited by studies that are more broadly looking at the neurobiological basis of behaviour.


    HS: What would you say to a student who is about to read this paper today? What should he or she take away from this paper?

    MR: What they should take away from the paper is this: in sexual selection by mate choice, if you want to understand what the chooser - of course, in this case its females choosing males, but it can be the opposite - is doing, it is, of course, important to understand the fitness consequences. But to understand the true details of it, we really need to understand how the brain is processing these signals. And every stimulus processed by the brain is processed in a biased way, because all sensory filters, whether they are ears or noses or eyes or touch sensors, have tuning curves that are biased. They don’t perceive all stimuli equally.  For example, we don’t see ultra-violet or infra-red. And within the range of colours that we do see, we are more biased to the ones to which our cones are tuned. So if we want to understand biases in behaviour, we just have to look at biases in the stimuli that trigger those behaviours. This is similar to something my friend Mark Kirkpatrick once told me, when people started to study ‘good genes’ in sexual selection. He said: ‘If people want to understand ‘good genes’, at some point they are actually going to have to study genes’. And I feel the same way. If we want to understand biases in behaviour, we need to understand the neural biases that lead to the behavioural biases.


    HS: Is this one of your favourite papers, among those you have written?

    MR: It is certainly among them.  You know, I very much like . Even though, in that paper, I do suggest there could be a ‘good genes’ explanation to those preferences, but now, it’s not that I don’t believe that’s true, but we certainly don’t have any evidence that its true. But this paper is also certainly among my favourites.



  • Post date: 1 year 8 months ago
    Citation for this post: BibTeX | RIS

    In 1983, published a paper in on the impact of salamander predation on larval anuran assemblages in experimental ponds. This paper formed one of the three chapters in Peter Morin's PhD dissertation. Thirty-three years after its publication, I spoke to Peter Morin about the making of this paper and what we have learnt about this topic since then. 

    Questions sent by email no 26th July 2016; responses received by email on 1st August 2016


    Hari Sridhar: This paper formed a part of your PhD dissertation under . Please tell us what the motivation was for this specific piece of work, in relation to the rest of your PhD dissertation. Also, which came first: an interest in amphibians or an interest in understanding community structure?

    Peter Morin: I had a long-standing interest in herpetology, going back to when I was a young boy of about 5 or 6 years of age. Early on, the fascination was with snakes and lizards, but amphibians were also interesting. My interest in natural history was encouraged by my father, and in college I learned that it would be possible to study herps. for a living, especially if I pursued a career as a college professor. At the time, the interesting work on herps. was being done in the areas of population and community ecology, so that steered me toward doing graduate work in community ecology. I applied to several graduate programs, got into all but one of them, and decided to study at Duke with Henry Wilbur, who was a rising star in the field. Henry mostly worked with amphibians then, so that led me to work on amphibians too. Along the way, I came to appreciate some of the major issues and questions in community ecology.

    The work in the Ecological Monographs paper was one of the three chapters in my dissertation. All three chapters were based mostly on results from a single community-level experiment conducted in 1980. The chapters focused on the responses of different taxonomic groups, frogs, salamanders, and zooplankton, to the same experimental manipulations of top predators - two species of salamanders.


    HS: You say your experiments "were inspired by the natural history of temporary ponds in the Sandhills Game Management Area". Can you tell us a little more about your connection to this area and how it influenced you?

    PM: Henry Wilbur’s research at the time was focused on amphibians in the , so much of my early field experience in graduate school involved visiting ponds with Henry and his other students, sampling the ponds to see what lived there, and learning about what was common and rare. One thing was obvious: newts were abundant and nearly ubiquitous. They were the top predator, or one of the top predators, in most ponds. That made them a logical thing to study. There was also a high diversity of frogs breeding in the ponds, which made the question of what allowed so many ecologically similar species able to coexist an interesting one.


    HS: Who came up with the idea of using cattle-watering tanks for the experimental setup?

    PM: Henry Wilbur had already had a grant funded to use cattle-watering tanks as replicated ponds in the Sandhills. The idea was to place tanks in natural areas, controlling for size, historical effects, and the surrounding habitat, to create comparable communities that could be sampled in comparable ways. Even then, most of the tank communities tended to be rather unique, probably depending on the history of colonization, so it seemed like exerting more experimental control over starting conditions would be useful. I asked Henry to buy me some tanks that I could use for controlled experiments on the impacts of predators on frog tadpole assemblages. The rest is history.

    We weren’t the first people to use analogous containers as experimental units. had done this with small pools in the early 1970’s, and had done things on a larger scale in artificial ponds, first at Cornell and then later at Michigan State.


    HS: Would you know what has happened to this experimental setup after your time at Duke? Are these tanks still being used?

    PM: The ‘tank farm’ grew in size while I was at Duke, and afterwards, until Henry Wilbur moved to the University of Virginia. I don’t know what became of the original tanks. They were a bother to maintain, with most requiring a new coat of epoxy paint every year with much attendant scraping off of old paint. Most people using similar things for their experiments, including me, have switched over to plastic tanks which are easier to maintain.


    HS:  If you don't mind my asking: how come your PhD supervisor H.M. Wilbur was not an author on this paper?

    PM: Henry had an enlightened and generous philosophy about authorship. This probably came from his own experience at the University of Michigan. Basically, if he wasn’t involved in the set-up, data collection, analysis, and writing, he didn’t see the point in being a coauthor. I have applied the same rationale to my own students, though you don’t see that happening very much anymore. It wasn’t unusual in 1983 to see mostly single-authored papers in Ecological Monographs or Ecology. Now it’s rare.


    HS: Can you give us a sense of what a typical day was like for you when you were doing these experiments?

    PM: Once the tanks were set up, animals collected and introduced, and things were running, the daily routine was to visit the tanks, collect all metamorphosing amphibians from each tank, return those to the lab, where they were identified to species, weighed, and measured. That happened from sometime in April through the end of summer. There were weekly zooplankton samples taken from each tank. Once a week I went out at night to try and capture the salamanders so that I could monitor their growth and survival. Each was uniquely identifiable by its color pattern. Depending on what was metamorphosing and when, this could keep you rather busy. And then, the metamorphs were released periodically back in the Sandhills.


    HS:  You acknowledge a number of people for help in "collecting frogs or maintaining the experiments". Were all of these people also students in Duke University?

    PM: Mostly, but my wife, Marsha Morin, who is not a biologist by training, was also a big help in collecting the frogs that went into that experiment. She probably caught more frogs than anyone else!


    HS:  How long did the writing of this paper take? Did you have a particular writing routine - where you wrote, when you wrote - at that time?

    PM: It’s hard to recall the exact time frame, because this was just one chapter in my dissertation, and I was basically working on all three at the same time, along with a couple of other projects. Most of the writing happened in my office at Duke. I was one of the first students in my department to write my dissertation using a personal computer/word processor, a . Computers and word processing have changed since then, mostly for the better.

    HS: How were the figures for this paper made? Were they drawn by hand?

    PM: Some of the graphics were roughed out on a graphics terminal, but a lot of the artwork was done by hand, by me, either using press type or other ancient technologies, like a pen and India ink. That is probably why one of the species names is spelled incorrectly. Things have gotten much better since then, except for my spelling.


    HS: Did this paper have a smooth ride through peer-review? Was Ecological Monographs the first place you submitted this paper? How different was the final published version from the first submitted draft?

    PM: Relatively. Ecological Monographs was the first place that it was submitted to. . The major difference between the submission and the final paper was inclusion of an appendix spelling out the details and rationale behind the multivariate analysis of the results.


    HS: You thank for "many helpful editorial suggestions". Was Dr. Gill the handling editor of your paper at Ecological Monographs?

    PM: Doug was the handling editor. He is an excellent ecologist, and he was an authority on newts. His comments and those of the reviewers made it a much better paper.


    HS: You say "Computing funds were provided by the Department of Zoology, Duke University". Can you tell us a little more about what "Computing funds" were?

    PM: Where to begin? When I began graduate school, personal computers did not yet exist, or if they did, they were mostly used by hobbyists. Real computing power, which is now dwarfed by the laptop computer on which I am writing this, resided in massive room-filling machines that were time-shared by universities like Duke, UNC Chapel Hill, and NC State. The costs of running and maintaining those facilities were shared, and subvented to some extent, by charging users for the computer time used. I think this was mostly ‘funny money’, but major users were expected to pay for their computer use with grant funds. I was a minor user. One communicated with the computers using decks of IBM punch cards, read through a card reader, and results were returned sometime later by a device called a line printer. It is now all delightfully archaic. About the time I finished my degree, it became possible to communicate directly with the time-shared machines using new things called video terminals. I thought I’d died and gone to heaven…

    The changes in computing power that I’ve seen since 1976 when I started graduate school, and the ease of use of computing technology for statistical analysis, graphics, modeling, and things we never dreamed we’d be using computers for are unfathomable for today’s typical undergraduate student.


    HS:  What impact did this paper have on your career? In what way did it influence the future course of your research?

    PM: I guess that receiving the probably didn’t hurt my career. The impact of any single paper is hard for me to judge. These days, more students recognize me for my than for any of my papers. I continued to work on amphibians for quite a few years afterwards, as did some of my students, but then turned to other systems to address different questions. However, right now, one of my students is working on amphibians again, with a focus on the microbial ecology of amphibian disease resistance.


    HS:  What was the reaction to this paper at the time it was published?

    PM: I remember getting a large number of reprint request cards in the mail. You don’t see those any more, either. Oh yes, in the days before pdfs, we sent out things called reprints to people who requested them.


    HS: It's now 33 years since this paper was published. Would you say that the main conclusions of this paper still hold true?

    PM: Pretty much. One take home point was that predators have a big effect of community structure, favoring species that may not be the best competitors, but that are able to coexist with predators via various strategies and adaptations. Predators remain common, and the spring peeper remains one of the most common frogs in eastern North America, I think because it deals well with predators despite being a pretty poor competitor.

    When I was planning my dissertation work, ideas promoted by and were still taking hold, such that the role of predators in driving community patterns were still somewhat controversial. That is all much clearer now.

    We didn’t know much about other natural enemies back then, specifically the ones that are now having huge impacts on some amphibian populations – pathogens like . That could change everything.


    HS: If you were to redo this experiment today, would you do anything differently, given the advances in technology, ecological theory and analytical tools?

    PM: It would have been nice to have a predictive mathematical model of the community dynamics to compare with the empirical results. People have also become hypercritical about the use of artificial communities, so it would be nice to able to do the experiment, or part of it, in natural ponds. That, however, isn’t so easy.


    HS: You say "early-breeding species may have a lingering impact on resource availability, subsequently influencing the growth of species exploiting a pond later in the same year (Seale 1980). Such priority effects are an interesting topic for future research". Did you research "priority effects" further, after this paper? In general, did "priority effects" become an important area of research in the period after this paper was published?

    PM: We have studied priority effects in a variety of systems including amphibians, odonates, and microbes. I followed up on that, as did many, many others.

    HS: You say "the potential importance of newts as keystone predators is unambiguous". Was this statement borne out by subsequent research?

    PM: It appears to work in other artificial pond experiments, and it also shows up in surveys of natural ponds done by and his colleagues. Some people don’t see much evidence for it, especially in systems where amphibian densities are low and rarely get to the level where competition is important. The question there is whether low densities are set by predators, in which case there is no inconsistency, or whether low densities are set by supply-side dynamics, which raises other issues about what controls inputs in metacommunities.


    HS: Were your experimentally-derived patterns subsequently shown to be consistent with patterns in natural pond communities?

    PM: Somewhat, but I would like to see a much larger data set address the patterns in nature. Unfortunately, it’s not the kind of confirmatory study that any funding agency is likely to support. And it would be nice to see what happens before an amphibian plague wipes out the natural populations.

    HS: At the time this was published, did you anticipate that it would be cited so much? Do you know what this paper has been mostly cited for?

    PM: I hoped that it would be cited, and it’s nice to see that it has had some staying power over the years. According to Google Scholar, it is not my most highly cited publication, but it’s in the top 10.


    HS: What would you say to a student about to read this paper today? What should he or she take away from it? Would you add any caveats?

    PM: I guess I would say ‘Sorry that it is so long.’ I hope they would get a good idea of what a publishable chapter in a dissertation might look like.”


    HS: Have you ever read the paper after it was published? When you read it now, what strikes you the most about it?

    PM: Oh yes, I have read it. It’s still very long!

    HS: Is this your favourite paper among all the papers you have published? If yes, why? If no, and if you do have another favourite, which is it and why?

    PM: Although this is one of my early papers, I still like it. However, I’m basically against the idea of picking favorites. It’s a bit like having kids (which I don’t have), or graduate students (which I do). They are all special, in different ways.




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