The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest

  1. David Muru
  2. Nicolas Borowiec
  3. Marcel Thaon
  4. Nicolas Ris
  5. Madalina I. Viciriuc
  6. Sylvie Warot
  7. Elodie Vercken

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Abstract

The rise of the Asian chestnut gall wasp Dryocosmus kuriphilus in France has benefited the native community of parasitoids originally associated with oak gall wasps by becoming an additional trophic subsidy and therefore perturbing population dynamics of local parasitoids. However, the successful biological control of this pest has then led to significant decreases in its population densities. Here we investigate how the invasion of the Asian chestnut gall wasp Dryocosmus kuriphilus in France and its subsequent control by the exotic parasitoid Torymus sinensis has impacted the local community of native parasitoids.

We explored 5 years of native community dynamics within 26 locations during the rise and fall of the invasive pest. In an attempt to understand how mechanisms such as local extinction or competition come into play, we analyzed how the patterns of co-occurrence between the different native parasitoid species changed through time.

Our results demonstrate that native parasitoid communities experienced increased competition as the D. kuriphilus levels of infestation decreased. During the last year of the survey, two alternative patterns were observed depending on the sampled location: either native parasitoid communities were represented by an extremely limited number of species occurring at low densities, in some cases no native parasitoid species at all, or they were dominated by one main parasitoid: Mesopolobus sericeus . These two patterns seemed to correlate with the habitat type, M. sericeus being more abundant in semi-natural habitats compared to agricultural lands, the former known to be natural reservoirs for native parasitoids. These results highlight how the “boom-and-bust” dynamics of an invasive pest followed by successful biological control can deeply alter the structure of native communities of natural enemies.

This article has been peer-reviewed and recommended by Peer Community in Zoology https://doi.org/10.24072/pci.zool.100004

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  1. Peer Community In Zoology

    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.

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  2. Version published to 10.1101/2019.12.20.884908 on bioRxiv