Revisiting Kruess and Tscharntke 1994

In 1994, Andreas Kruess and Teja Tscharntke published a paper 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.


Teja Tscharntke (© Teja Tscharntke)

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.


Kruess & Tscharntke 94 - habitat island

A clover habitat island at the edge of a cereal field (© Andreas Kreuss and Teja Tscharntke)

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 another Science paper 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 (also in our group).


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, RD Holt et al. (1999); Tscharntke T & Kruess A (1999)).


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, we expanded our landscape perspective from habitat fragmentation to considering the composition and configuration of complete landscape sectors.


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 second Science paper (1999), my 2005 review in Ecology Letters and later on, a few other nice papers, e.g. on pollination, tropical research and socioeconomic-ecological studies.


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