Ecological communities are composed of many species, forming complex networks of interactions. Current environmental changes are altering the structure and species composition of ecological networks, which could modify interactions, either directly or indirectly. To predict changes in the functioning of communities, we need to understand whether species interactions are primarily driven by network structure (i.e. topology) or the specific identities of species (i.e. nodes). Yet, this partitioning of effects is challenging and thus rarely explored. Here we disentangled the influence of network structure and the identities of species on the outcome of consumer-resource interactions using a host-parasitoid system. We used four common community modules in host-parasitoid communities to represent network structure (i.e. host-parasitoid, exploitative competition, alternative host and a combination of exploitative competition and alternative host). We assembled nine different species combinations per community module in a laboratory experiment using a pool of three Drosophila hosts and three larval parasitoid species (Leptopilina sp., Ganaspis sp. and Asobara sp.). We compared host suppression and parasitoid performance across community modules and species assemblages to identify general effects linked to network structure and specific effects due to species community composition. We found that multiple parasitoid species enhanced host suppression due to sampling effect, weaker interspecific than intraspecific competition between parasitoids, and synergism. However, the effects of network structure on parasitoid performance were species specific and dependent on the identity of co-occurring species. Consequently, multiple parasitoid species generally strengthen top-down control, but the performance of the parasitoids depends on the identity of either the co-occurring parasitoid species, the alternative host species or both. Our results highlight the importance of preserving parasitoid diversity for ecosystem functioning and show that other effects depend on species community composition, and may therefore be altered by ongoing environmental changes.

Biology Centre of the Czech Academy of Sciences Institute of Entomology České Budějovice Czech Republic

Department of Life and Earth Sciences Georgia State University Perimeter College Clarkston Georgia

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Zobrazit více v PubMed

Alexander, J. M., Diez, J. M., & Levine, J. M. (2015). Novel competitors shape species' responses to climate change. Nature, 525(7570), 515-518. https://doi.org/10.1038/nature14952

Bascompte, J., & Melián, C. J. (2005). Simple trophic modules for complex food webs. Ecology, 86(11), 2868-2873. https://doi.org/10.1890/05-0101

Bográn, C. E., Heinz, K. M., & Ciomperlik, M. A. (2002). Interspecific competition among insect parasitoids: Field experiments with whiteflies as hosts in cotton. Ecology, 83(3), 653-668. https://doi.org/10.1890/0012-9658(2002)083[0653:ICAIPF]2.0.CO;2

Boulétreau, M., & Wajnberg, E. (1986). Comparative responses of two sympatric parasitoid cynipids to the genetic and epigenetic variations of the larvae of their host, Drosophila melanogaster. Entomologia Experimentalis et Applicata, 41(2), 107-114. https://doi.org/10.1111/j.1570-7458.1986.tb00516.x

Burnham, K. P., & Anderson, D. R. (2002). Model Selection and Multimodel Inference. In Model Selection and Multimodel Inference. Springer. https://doi.org/10.1007/B97636

Carton, Y., & Kitano, H. (1981). Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup. Biological Journal of the Linnean Society, 16(3), 227-241. https://doi.org/10.1111/j.1095-8312.1981.tb01849.x

Carton, Y., Poirié, M., & Nappi, A. J. (2008). Insect immune resistance to parasitoids. Insect Science, 15(1), 67-87. https://doi.org/10.1111/j.1744-7917.2008.00188.x

Cusumano, A., Peri, E., & Colazza, S. (2016). Interspecific competition/facilitation among insect parasitoids. In Current Opinion in Insect Science (Vol. 14, pp. 12-16). Elsevier Inc.. https://doi.org/10.1016/j.cois.2015.11.006

Finke, D. L., & Snyder, W. E. (2008). Niche partitioning increases resource exploitation by diverse communities. Science, 321(5895), 1488-1490. https://doi.org/10.1126/science.1160854

Fleury, F., Ris, N., Allemand, R., Fouillet, P., Carton, Y., & Boulétreau, M. (2004). Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. In P. Capy, P. Gibert, & I. Boussy (Eds.), Drosophila melanogaster, Drosophila simulans: So Similar, So Different (pp. 181-194). Springer.

Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W., & Holt, R. D. (2010). A framework for community interactions under climate change. Trends in Ecology & Evolution, 25(6), 325-331. https://doi.org/10.1016/j.tree.2010.03.002

Gurr, G. M., S. D. Wratten, & W. E. Snyder (Eds.) (2012). Biodiversity and insect pests: Key issues for sustainable management. John Wiley & Sons.

Godfray, H. C. J. (2004). Parasitoids. Current Biology, 14(12), R456. https://doi.org/10.1016/j.cub.2004.06.004

Greenop, A., Woodcock, B. A., Wilby, A., Cook, S. M., & Pywell, R. F. (2018). Functional diversity positively affects prey suppression by invertebrate predators: a meta-analysis. Ecology, 99(8), 1771-1782. https://doi.org/10.1002/ecy.2378

Hartig, F., & Hartig, M. F. (2019). Package ‘DHARMa’. R Development Core Team.

Harvey, J. A., Poelman, E. H., & Tanaka, T. (2013). Intrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology, 58(1), 333-351. https://doi.org/10.1146/annurev-ento-120811-153622

Holt, R. D. (1997). Community modules. In A. C. Gange & V. K. Brown (Eds.), Multitrophic interactions in terrestrial ecosystems. Blackwell Science.

Jeffs, C. T., Terry, J. C. D., Higgie, M., Jandová, A., Konvičková, H., Brown, J. J., Lue, C. H., Schiffer, M., O'Brien, E. K., Bridle, J., Hrček, J., & Lewis, O. T. (2021). Molecular analyses reveal consistent food web structure with elevation in rainforest Drosophila - parasitoid communities. Ecography, 44(3), 403-413. https://doi.org/10.1111/ecog.05390

Jones, T. S., Godfray, H. C. J., & van Veen, F. J. F. (2009). Resource competition and shared natural enemies in experimental insect communities. Oecologia, 159(3), 627-635. https://doi.org/10.1007/s00442-008-1247-z

Kaartinen, R., & Roslin, T. (2013). Apparent competition leaves no detectable imprint on patterns of community composition: observations from a natural experiment. Ecological Entomology, 38(5), 522-530. https://doi.org/10.1111/een.12048

Kawatsu, K., Ushio, M., van Veen, F. J. F., & Kondoh, M. (2021). Are networks of trophic interactions sufficient for understanding the dynamics of multi-trophic communities? Analysis of a tri-trophic insect food-web time-series. Ecology Letters, 24(3), 543-552. https://doi.org/10.1111/ELE.13672

Kéfi, S., Berlow, E. L., Wieters, E. A., Navarrete, S. A., Petchey, O. L., Wood, S. A., Boit, A., Joppa, L. N., Lafferty, K. D., Williams, R. J., Martinez, N. D., Menge, B. A., Blanchette, C. A., Iles, A. C., & Brose, U. (2012). More than a meal… integrating non-feeding interactions into food webs. Ecology Letters, 15(4), 291-300. https://doi.org/10.1111/j.1461-0248.2011.01732.x

Lenth, R. V. (2018). Emmeans: Estimated marginal means, aka least-squares means. R Package Version.

Letourneau, D. K., Jedlicka, J. A., Bothwell, S. G., & Moreno, C. R. (2009). Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics, 40(1), 573-592. https://doi.org/10.1146/annurev.ecolsys.110308.120320

Lüdecke, D., Makowski, D., & Waggoner, P. (2019). Performance: Assessment of regression models performance. R Development Core Team.

Lue, C.-H., Buffington, M. L., Scheffer, S., Lewis, M., Elliott, T. A., Lindsey, A. R. I., Driskell, A., Jandova, A., Kimura, M. T., Carton, Y., Kula, R. R., Schlenke, T. A., Mateos, M., Govind, S., Varaldi, J., Guerrier, E., Giorgini, M., Wang, X., Hoelmer, K., … Hrcek, J. (2021). DROP: Molecular voucher database for identification of Drosophila parasitoids. Molecular Ecology Resources, 21, 2437-2454. https://doi.org/10.1111/1755-0998.13435

McPeek, M. A. (2019). Mechanisms influencing the coexistence of multiple consumers and multiple resources: resource and apparent competition. Ecological Monographs, 89(1), e01328. https://doi.org/10.1002/ecm.1328

Milo, R., Shen-Orr, S., Itzkovitz, S., Kashtan, N., Chklovskii, D., & Alon, U. (2002). Network motifs: simple building blocks of complex networks. Science, 298(5594), 824-827. https://doi.org/10.1126/science.298.5594.824

Morris, R. J., Müller, C. B., & Godfray, H. C. J. (2001). Field experiments testing for apparent competition between primary parasitoids mediated by secondary parasitoids. Journal of Animal Ecology, 70(2), 301-309. https://doi.org/10.1111/j.1365-2656.2001.00495.x

Myers, J. H., Higgins, C., & Kovacs, E. (1989). How many insect species are necessary for the biological control of insects? Environmental Entomology, 18(4), 541-547. https://doi.org/10.1093/ee/18.4.541

Nouhaud, P., Mallard, F., Poupardin, R., Barghi, N., & Schlötterer, C. (2018). High-throughput fecundity measurements in Drosophila. Scientific Reports, 8(1), 4469. https://doi.org/10.1038/s41598-018-22777-w

Ode, P. J., Vyas, D. K., & Harvey, J. A. (2022). Extrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology, 67, 305-328. https://doi.org/10.1146/ANNUREV-ENTO-071421-073524

Parmesan, C., & Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421(6918), 37-42. https://doi.org/10.1038/nature01286

Paterson, R. A., Dick, J. T. A., Pritchard, D. W., Ennis, M., Hatcher, M. J., & Dunn, A. M. (2015). Predicting invasive species impacts: A community module functional response approach reveals context dependencies. Journal of Animal Ecology, 84(2), 453-463. https://doi.org/10.1111/1365-2656.12292

Pedersen, B. S., & Mills, N. J. (2004). Single vs. multiple introduction in biological control: The roles of parasitoid efficiency, antagonism and niche overlap. Journal of Applied Ecology, 41(5), 973-984. https://doi.org/10.1111/j.0021-8901.2004.00953.x

Poelman, E. H., Gols, R., Gumovsky, A. V., Cortesero, A. M., Dicke, M., & Harvey, J. A. (2014). Food plant and herbivore host species affect the outcome of intrinsic competition among parasitoid larvae. Ecological Entomology, 39(6), 693-702. https://doi.org/10.1111/een.12150

R Core Team. (2021). R: The R project for statistical computing. https://www.r-project.org/

Rip, J. M. K., McCann, K. S., Lynn, D. H., & Fawcett, S. (2010). An experimental test of a fundamental food web motif. Proceedings of the Royal Society B: Biological Sciences, 277(1688), 1743-1749. https://doi.org/10.1098/rspb.2009.2191

Schmitz, O. J. (2007). Predator diversity and trophic interactions. Ecology, 88(10), 2415-2426. https://doi.org/10.1890/06-0937.1

Sentis, A., Gémard, C., Jaugeon, B., & Boukal, D. S. (2017). Predator diversity and environmental change modify the strengths of trophic and nontrophic interactions. Global Change Biology, 23(7), 2629-2640. https://doi.org/10.1111/gcb.13560

Siddon, C. E., & Witman, J. D. (2004). Behavioral indirect interactions: Multiple predator effects and prey switching in the rocky subtidal. Ecology, 85(11), 2938-2945. https://doi.org/10.1890/03-0519

Sih, A., Englund, G., & Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in Ecology & Evolution, 13(9), 350-355. https://doi.org/10.1016/S0169-5347(98)01437-2

Snyder, G. B., Finke, D. L., & Snyder, W. E. (2008). Predator biodiversity strengthens aphid suppression across single- and multiple-species prey communities. Biological Control, 44(1), 52-60. https://doi.org/10.1016/J.BIOCONTROL.2007.09.006

Snyder, W. E., Snyder, G. B., Finke, D. L., & Straub, C. S. (2006). Predator biodiversity strengthens herbivore suppression. Ecology Letters, 9(7), 789-796. https://doi.org/10.1111/j.1461-0248.2006.00922.x

Thierry, M. (2021). Data from: Multiple parasitoid species enhance top-down control, but parasitoid performance is context-dependent. Zenodo. https://doi.org/10.5281/zenodo.6122978

Thierry, M., Hrček, J., & Lewis, O. T. (2019). Mechanisms structuring host-parasitoid networks in a global warming context: A review. Ecological Entomology, 44(5), 581-592. https://doi.org/10.1111/een.12750

Thierry, M., Pardikes, N. A., Rosenbaum, B., Ximénez-Embún, M. G., & Hrček, J. (2021). Warming decreases host survival with multiple parasitoids, but parasitoid performance also decreases. BioRxiv, 2021(8), 24.457463. https://doi.org/10.1101/2021.08.24.457463

Tylianakis, J. M., Tscharntke, T., & Lewis, O. T. (2007). Habitat modification alters the structure of tropical host-parasitoid food webs. Nature, 445(7124), 202-205. https://doi.org/10.1038/nature05429

van Veen, F. J. F., van Holland, P. D., & Godfray, H. C. J. (2005). Stable coexistence in insect communities due to density- and trait-mediated indirect effects. Ecology, 86(12), 3182-3189. https://doi.org/10.1890/04-1590

Wajnberg, E., Scott, J. K., & Quimby, P. C. (2001). Evaluating Indirect Ecological Effects of Biological Control. CABI. https://books.google.fr/books?hl=fr&lr=&id=Nrtmz5jO3D0C&oi=fnd&pg=PR11&dq=Evaluating+Indirect+Ecological+Effects+of+Biological+Control&ots=C6_eRGHMi0&sig=c3Q8tSRCnLMOI2REDWrkI2JnOM8#v=onepage&q=Evaluating:IndirectEcologicalEffectsofBiologicalControl

Werner, E. E., & Peacor, S. D. (2003). A review of trait-mediated indirect interactions in ecological communities. Ecology, 84(5), 1083-1100. https://doi.org/10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2

Wong, M. K. L., Guénard, B., & Lewis, O. T. (2019). Trait-based ecology of terrestrial arthropods. Biological Reviews, 94(3), 999-1022. https://doi.org/10.1111/brv.12488

Woodcock, B. A., & Heard, M. S. (2011). Disentangling the effects of predator hunting mode and habitat domain on the top-down control of insect herbivores. Journal of Animal Ecology, 80(2), 495-503. https://doi.org/10.1111/j.1365-2656.2010.01790.x

Xu, H. Y., Yang, N. W., Duan, M., & Wan, F. H. (2016). Functional response, host stage preference and interference of two whitefly parasitoids. Insect Science, 23(1), 134-144. https://doi.org/10.1111/1744-7917.12186

The presence of multiple parasitoids decreases host survival under warming, but parasitoid performance also decreases