Raise and fall of an invasive pest and consequences for native parasitoid communities

Stefaniya Kamenova

A recommendation of:
David Muru, Nicolas Borowiec, Marcel Thaon, Nicolas Ris, Madalina Ionela Viciriuc, Sylvie Warot, Elodie Vercken. The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest. (2020), bioRxiv, 2019.12.20.884908, ver. 6 peer-reviewed and recommended by Peer Community in Zoology. 10.1101/2019.12.20.884908
Submitted: 31 December 2019, Recommended: 21 July 2020
Cite this recommendation as:
Stefaniya Kamenova (2020) Raise and fall of an invasive pest and consequences for native parasitoid communities. Peer Community in Entomology, 100004. 10.24072/pci.zool.100004

Host-parasitoid interactions have been the focus of extensive ecological research for decades. One the of the major reasons is the importance host-parasitoid interactions play for the biological control of crop pests. Parasitoids are the main natural regulators for a large number of economically important pest insects, and in many cases they could be the only viable crop protection strategy. Parasitoids are also integral part of complex food webs whose structure and diversity display large spatio-temporal variations [1-3]. With the increasing globalization of human activities, the generalized spread and establishment of invasive species is a major cause of disruption in local community and food web spatio-temporal dynamics. In particular, the deliberate introduction of non-native parasitoids as part of biological control programs, aiming the suppression of established, and also highly invasive crop pests, is a common practice with potentially significant, yet poorly understood effects on local food web dynamics (e.g. [4]).
In their study, Muru et al. [5] took advantage of an existing biological control program focusing on the Asian chestnut gall wasp Dryocosmus kuriphilus, an invasive (and highly damaging) pest of chestnut trees. The species is currently a successful invader in many geographic regions, including southern France, where local parasitoid communities failed to provide an adequate control since its widespread establishment in 2010 [6]. In response, the non-native parasitoid species Torymus sinensis, which is highly-specific to the Asian chestnut gall wasp, was massively released in commercial chestnut orchards across several regions in France and the island of Corsica. The pest population outbreak was successfully contained, and thanks to the vast amount of host-parasitoid interaction data collected as part of the program, the authors were able to explore the effects of the large fluctuations in Asian chestnut gall wasp natural abundances on native parasitoid communities, immediately before, and up to five years following the introduction of its natural enemy T. sinensis.
Using co-occurrence and clustering analyses, Muru et al. [5] demonstrate that the invasion and the consecutive (efficient) control of the Asian chestnut gall wasp by the parasitoid T. sinensis have a significant impact on the structure of local parasitoid food webs. In particular, following decline in the Asian chestnut gall wasp’s populations, native parasitoids markedly switched to alternative hosts, most likely due to their respectively higher relative abundances. This pattern seemed to be driven by the degree of generalism in native parasitoid species. Indeed, when its abundances were still relatively high, the Asian chestnut gall wasp was primarily attacked by species capable of exploiting a broad range of hosts, while at low population densities only specialist parasitoids such as Mesolobus sericeus were able to persist and compete with the non-native T. sinensis.
The current study is important for two major reasons. First, it underscores the value of long-term species interaction data in order to understand the dynamic nature of food webs, namely their structural flexibility in response to changes in the environment or, as in this case, large fluctuation in abundances of a major pest species. In this context, biological control programs could be a great source of data for exploring long-term, large-scale dynamics of species interactions, and their use in ecological studies deserves to be further emphasized. Second, the study adds to the increasing empirical evidence that mobile generalist foragers can display adaptive, frequency-dependent switching behaviour ([1], [7]), which has been suggested to act as a key stabilizing mechanism in food webs by buffering fluctuating population dynamics at larger spatial scales ([8- 10]).
However, the timing of such buffering seems important, especially in systems such as commercial chestnut orchards. Despite their capacity to adaptively switch their foraging behaviour, the response of the native parasitoid communities to the new, unfamiliar resource was not fast enough in order to contain the primary outbreak under an appropriate damage threshold, thus requiring the introduction of the more specialized parasitoid T. sinensis. Nevertheless, based on current ecological theory, results presented by Muru et al. [5] suggest that the response of native parasitoid community to fluctuating host dynamics – i.e. shifts in parasitoid foraging behaviour based on their traits – could be predictable. This is encouraging considering the growing impact of biological invasions and insect pest outbreaks, but also the need to implement efficient, yet sustainable strategies for crop protection. Future studies would show at what extent observations by Muru et al. [5] are generalizable over longer time periods or other model systems. Noticeably, better understanding about population dynamics and interactions with the broader community of hosts available across habitats should allow to fine-tune predictions about parasitoids’ response to fluctuating resources.


[1] Eveleigh ES, McCann KS, McCarthy PC, Pollock SJ, Lucarotti CJ, Morin B, McDougall GA, Strongman DB, Huber JT, Umbanhowar J, Faria LDB (2007). Fluctuations in density of an outbreak species drive diversity cascades in food webs. Proc. Natl. Acad. Sci. USA 104, 16976-16981. doi: 10.1073/pnas.0704301104
[2] Tylianakis JM, Tscharntke T, Lewis OT (2007). Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445, 202-205. doi: 10.1038/nature05429
[3] Murakami M, Hirao T, Kasei A (2008). Effects of habitat configuration on host–parasitoid food web structure. Ecol. Res. 23, 1039-1049. doi: 10.1007/s11284-008-0478-0
[4] Geslin B, Gauzens B, Baude M, Dajoz I, Fontaine C, Henry M, Ropars L, Rollin O, Thébault E, Vereecken NJ (2016). Massively introduced managed species and their consequences for plant–pollinator interactions. Adv. Ecol. Res. 57, 147-199. doi: 10.1016/bs.aecr.2016.10.007
[5] Muru D, Borowiec N, Thaon M, Ris N, Viciriuc M I, Warot S, Vercken E (2020) The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest. bioRxiv, 2019.12.20.884908, ver. 6 peer-reviewed and recommended by PCI Zoology. doi: 10.1101/2019.12.20.884908
[6] Borowiec N, Thaon M, Brancaccio L, Warot S, Vercken E, Fauvergue X, Ris N, Malausa J-C (2014). Classical biological control against the chestnut gall wasp 'Dryocosmus kuriphilus' (Hymenoptera, Cynipidae) in France. Plant Prot. Q. 29, 7-10.
[7] Bartley TJ, McCann KS, Bieg C, Cazelles K, Granados M, Guzzo MM, MacDougall AS, Tunney TD, McMeans BC (2019). Food web rewiring in a changing world. Nat. Ecol. Evol. 3, 345–354. doi: 10.1038/s41559-018-0772-3
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[10] Valdovinos FS, Ramos-Jiliberto R, garay-Narváez L, Urbani P, Dunne JA (2010). Consequences of adaptive behaviour for the structure and dynamics of food webs. Ecol. Lett. 13, 1546-1559. doi: 10.1111/j.1461-0248.2010.01535.x

Revision round #3


The authors have done fantastic work on integrating comments and changes into the manuscript, which reads now really well. Based on that I am ready to recommend its publication in PCI Entomology. Nevertheless, still quite some typos or omissions remain throughout the text - you can find my comments in the attached document. I propose that while I am working on my recommendation text, the authors use the time to integrate these last changes required. Additionally, I will ask them to make sure that:

1) Data is made available to readers after recommendation, either in the text or through an open data repository such as Zenodo (free), Dryad (to pay) or some other institutional repository. Data must be reusable, thus metadata or accompanying text must carefully describe the data;

2) Details on quantitative analyses (e.g., data treatment and statistical scripts in R, bioinformatic pipeline scripts, etc.) and details concerning simulations (scripts, codes) are made available to readers in the text, as appendices, or through an open data repository, such as Zenodo, Dryad or some other institutional repository. The scripts or codes must be carefully described so that they can be reused;

Also, please make sure to state that:

3) You have no financial conflict of interest relating to the article. The article must contain a "Conflict of interest disclosure" paragraph before the reference section containing this sentence: "The authors of this article declare that they have no financial conflict of interest with the content of this article.";

4) This disclosure has to be completed by a sentence indicating that some of the authors are PCI recommenders: “XY is one of the PCI Entomol recommenders.”

Author's reply:

Dear Stephanyia Kamenova,

We took into account all your final remarks (see our answers to your remarks in the attach document).

One of your remarks had us include a new small paragraph into the results section to address molecular results.

We figured that this small paragraph needs therefore to be reviewed before we can submit the final version of the article. That is why, and to speed up the process for this round of review, there will be no new version of the article uploaded in BiorXive. However, I will copy/paste said paragraphe here so that you can still review it. I will also attach the file with our answers to your remarks as usual.

The new Paragraph within the result section:

"Molecular-assisted species identification

The identification of individuals was realized in routine using morphological characters. The molecular characterization was however necessary for taxa in which a species’ complex is known (for instance, in the Eupelmus genus – see Al Khatib et al. 2014 and 2016) or for which few information is available. As shown in the Figure S2, the COI sequenced (between 550 and 612pb) were informative enough to distinguish closely related species, as in the Sycophyla and Torymus genera. For some taxa (Aulogymnus arsames, Eurytoma setigera, Megastigmus dorsalis, Torymus affinis), the within molecular diversity may suggest the presence of sister species and/or a marked intraspecific variability."

Revision round #2


Dear all, My apology for the delayed reply. I took the time to go through your revised manuscript, which has been indeed improved in many ways. However, I feel that it still deserves additional work in terms of writing and organisation. I don't think it needs to go through a second round of reviews but I attach a list of issues that still seem to me important to be addressed. I hope that you will be able to take them into consideration. As I am not entirely an expert in this topic, I am very much open to argumentation but as you can see it is not the work and approaches in overall that are questioned but rather the quality of the information presented. Please find attached my comments here below and good luck with the revision.

Very much looking forward to see the final version of the paper!

Revision round #1


Dear authors, After a first round of reviews, both the reviewers and I, agree that your paper has a great potential for addressing important scientific questions using a highly valuable dataset of host-parasitoid dynamics. Nevertheless, the manuscript will require a substantial amount of revision before it is accepted for publication. On top of some more specific remarks, the general criticisms revolve around the clarity of writings (especially regarding the Material & Methods and Results sections) and data analyses and interpretation. Additional effort will be required to better frame the scope of the study as well as the more specific questions/expectations.
We all provided numerous comments that we hope will help you throughout the revision. Please find all reviewers comments here below, and my own comments within the manuscript in attachment.
Good luck and looking forward to see your re-submission!

Author's reply:

Thank you for the great review of our article you provided. We have done our best to take into account everything the reviewers noticed. We have improved the paper all the way through and hope the reviewers will be satisfied with it.

In a nutshell: We added the recommended literature to the introduction and reworked the transitions for a easier reading and, we hope, increased clarity. We added a substantial amount of explications within the method sections and added a section talking about our sampling effort. We added new analyses without M. sericeus to see if its impact was covering an impact on some other species. We reworked most of our illustration. Now the heat map is a lot more explicit and PCA figures were merged into a single one. The discussion has had the most rework: literature has been added, text was restructured to be more comprehensive.

Of course the changes we made are not limited to what is above. Commentaries were numerous and we tried to take them all into account.

We hope the revision will reach expectations of the reviewers.