Multiple parasitoid species enhance top-down control, but parasitoid performance is context-dependent

This blog post is provided by Melanie Thierry, Nick Pardikes, Miguel González Ximénez de Embún, Grégoire Proudhom, Jan Hrcek and tells the #StoryBehindThePaper for the paper “Multiple parasitoid species enhance top-down control, but parasitoid performance is context-dependent“, which was recently published in the Journal of Animal Ecology. They explore how different combinations of hosts and parasitoid species interact in miniature worlds, also known as microcosms, showing how these interesting species act as predators in the system.

You have probably heard about the Alien movies, those horrific science fiction films featuring monsters using humans as nurseries. But did you know that these Alien parasites were inspired by organisms that really live in our world? They are fascinating insects called parasitoids, and they use other arthropods as a living host for their offspring to feed on (Fig. 1). Once fully developed, the offspring will emerge from their host and kill them in the process. They thus are a particular type of predator and play an important role in controlling the populations of organisms in agricultural and natural ecosystems (i.e., top-down control).

Fig 1. Ganaspis sp. (Hymenoptera, Figitidae) developing inside the pupal of its host Drosophila. (Photo credit: Chia-Hua Lue)

            In our research published in the Journal of Animal Ecology, we studied the ecological consequences of current climate change on these parasitoids. With ongoing environmental changes, species’ ranges and phenologies are shifting, but not all species respond equally, which disrupts historical patterns of interactions and co-occurrences. To study the effects of such changes on complex ecological networks, we can disassemble them into community modules (i.e., a small number of species interacting in a specified pattern, Fig. 2).

Fig 2. Schematic representation of the experimental treatments with the potential direct and indirect interactions in each community module. Orange and pink nodes and larvae represent different Drosophila host species, and green and blue nodes and wasps represent different parasitoid species. We assembled four different community modules in a fully factorial design, which is illustrated schematically beneath their corresponding experimental box: a) host-parasitoid pair (one host and one parasitoid species), b) exploitative competition module (one host and two parasitoid species), c) alternative host module (two host and one parasitoid species) and, d) both exploitative competition and alternative host module (two host and two parasitoid species). In the community module schema, solid lines represent trophic interactions, and dashed lines represent non-trophic interactions (in b) either exploitative competition, interference, or facilitation between parasitoids, c) indirect interactions between hosts and d) potential for all the above). Direct interaction between host species was not allowed. See Thierry et al., (2019) for a detailed description of each interaction type. Drawing credit: Tereza Holicová

In our study, we created small worlds in the laboratory (i.e., microcosms, Fig. 3a) with a wild-caught tropical Australian Drosophila host-parasitoid system to observe the outcome of host-parasitoid interactions depending on their community context (Fig. 3b). We used four common community modules in host-parasitoid communities to represent four different network structure scenarios: host-parasitoid pair in isolation (Fig. 2a), exploitative competition between parasitoid species for a shared host (Fig. 2b), alternative host for a parasitoid (Fig. 2c), and a combination of exploitative competition and alternative host (Fig. 2d).

Fig 3. Experimental set up. (a) The microcosms: boxes contained two vials with 25 two-days-old Drosophila larvae. Four three-to-five days old parasitoids (1:1 sex ratio) were placed in each box for 24 hours. The experiment counts a total of 216 boxes. (b) The rearing of the vials to see the outcome (fly, parasitoid, or nothing). (Photo credit: Mélanie Thierry)

            We assembled nine different species combinations per community module using a pool of three Drosophila hosts (D. birchii, D. simulans, D. pallidifrons) and three larval parasitoid species (Leptopilina sp., Ganaspis sp., and Asobara sp.). To understand which aspects of species interactions are primarily driven by network structure and which are driven by species identities, and thus better understand the impact of climate change on the functioning of communities, we compared host suppression and parasitoid performance across community modules and species assemblages.

            We found that multiple parasitoid species generally enhanced top-down control (i.e., host suppression), and this finding was due to a combination of several mechanisms. The presence of the most efficient parasitoid species (Ganaspis sp.) was driving some of the positive effects of parasitoid diversity on host suppression. This is called the sampling effect, which means that communities with higher parasitoid diversity have higher probabilities to have a superior one among them, thus a higher top-down control. We also observed weaker interspecific competition between parasitoid species than intraspecific competition, which we suggest was due to some degree of resource partitioning. This mechanism can be more important than diversity per se to explain an increase in top-down control with multiple predator species in some cases. Lastly, we observed some synergistic effects between parasitoids, coming from the fact that hosts were more likely to die when multi-parasitized (i.e., more than one parasitoid egg laid in a single host) (Thierry et al., 2021). Our results support previous studies and demonstrates the enhancement of top-down control with multiple parasitoid species across several species assemblages (reviewed in Letourneau et al., 2009) and highlights the importance of preserving predator diversity for proper ecosystem functioning. However, the effects of network structure on parasitoid performance were species-specific and dependent on the identity of co-occurring species, making future predictions difficult.

These species-specific effects on parasitoid performance have important implications for biological control programs that rarely consider the impact of co-occurring species (alternative prey species and/or other predators) on biological control agent efficiency in suppressing pests. It remains to be determined if the identity of co-occurring species is as essential in prey-predator systems or if this is a unique feature of real-world aliens.

About the authors

Mélanie Thierry was a PhD student at the University of South Bohemia in Czech Republic during this work. She has now moved to the Theoretical and Experimental Ecology Station (SETE) in Ariège National Center for Scientific Research (CNRS) as a postdoctoral research associate.

Nick Pardikes was a postdoctoral research associate at the Czech Academy of Sciences. He is now lecturing at the Utah State University.

Miguel González Ximénez de Embún is a postdoctoral research associate at the Czech Academy of Sciences.

Grégoire Proudhom is a PhD student at the University of South Bohemia in Czech Republic.

Jan Hrcek is a group leader at Czech Academy of Sciences (http://lab.hrcek.net).

Read the paper

Thierry, M., Pardikes, N. A., Ximénez-Embún, M. G., Proudhom, G., & Hrček, J. (2021). Multiple parasitoid species enhance top-down control, but parasitoid performance is context dependent. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.13782

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