An empirical attack tolerance test alters the structure and species richness of plant-pollinator networks

Abstract

Ecological network theory hypothesizes a link between structure and stability, but this has mainly been investigated in-silico. In an experimental manipulation, we sequentially removed four generalist plants from real plant-pollinator networks and explored the effects on, and drivers of, species and interaction extinctions, network structure and interaction rewiring. Our results indicate that cumulative species and interaction extinctions increased faster with generalist plant loss than what was expected by co-extinction models, which predicted the survival or extinction of many species incorrectly. In addition, network nestedness decreased, modularity increased, and opportunistic random interactions and structural unpredictability emerged, which are all indicators of network instability and fragility.Conversely, interaction reorganization (rewiring) was high, asymmetries between network levels emerged as plants increased their centrality. From the experimental manipulations of real networks, our study shows how plant-pollinator network structure has low stability and changes towards a more fragile state when generalist plants are lost. IntroductionInteractions are organized in complex networks, and the way these structures react to disturbance is crucial for understanding network functioning, their ability to buffer negative impacts and also for their conservation 1-4 . This is usually verified with "attack tolerance tests" that assess the functionality of a system after knocking out its important components 5 . In ecology, such tests usually consist in removing all species in one trophic level and then in assessing how many species in another level lost all interactions 6,7 . So far, in pollination networks, this has been addressed mainly theoretically with numerical simulations that show a higher rate of pollinator extinction when highly linked plants are removed 7-10 . However, these theoretical predictions were not compared to empirical data from similar manipulations, which is urgently needed to assess their reliability 11 . Manipulative experiments of plant-pollinator networks can illuminate the factors maintaining network stability and the processes of network reorganization. For instance, previous experiments removing only one generalist plant 12,13 showed that networks are quite stable to this loss, and that other species occupy the role in the network of the removed species. Conversely, when multiple invasive plants are removed, network interaction diversity and generalisation are impacted 14 , indicating that losing multiple species can strongly affect real networks. Moreover, after disturbance, network stability could depend on the amount of interaction rewiring 18 , i.e. foragers' ability to use alternative resources after depletion or disappearance of those previously used 15-17 . Rewiring and the establishment of interactions between plants and pollinators may be regulated by several ecological drivers, such as species trait matching 19,20 , flower's rewards 21,22 or species abundances 23,24 . Sim...

The effects of experimental floral resource removal on plant-pollinator interactions

“…The changes we observed in pollinator visitation rates and species composition in response to the removal of Helianthella flowers gave rise to the altered structural properties of the plant-pollinator interaction networks. Other experiments that have removed generalist plant species have found conflicting results: Biella et al (2020) observed increased network specialization, whereas others have observed increased generalization (Goldstein and Zych 2016, Kaiser-Bunbury et al 2017). Here, we find that experimental floral removal gave rise to more specialized and less nested networks.…”

“…To date, relatively few studies have experimentally removed plant or pollinator species from intact pollination networks to investigate the consequences of their loss, but the available evidence suggests a variety of responses (plant removals: Biella et al 2020; Biella et al, 2019; Ferrero et al 2013; Goldstein and Zych 2016; Kaiser-Bunbury et al 2017; pollinator removals: Brosi and Briggs 2013; Brosi et al 2017). Complete removal of generalist floral resources from a landscape can bring about dramatic reductions in visitation rates and redistribution of visitors to the remaining plant community (Biella et al 2019).…”

“…Such shifts in pollinator foraging may functionally act as pollinator species loss from a localized interaction network. In concert, these changes may restructure interaction networks such that they become more specialized (e.g., Biella et al 2020) or more generalized (e.g., Goldstein and Zych 2016; Brosi et al 2017)—with possible consequences for their sensitivity to future perturbations.…”

Are plants in sown flower strips suitable for communities of wild bees? Pollination network approach in conservation biology

“…However, we argue that TCM has also still some interpretative advantages over SCM: the SCM assumes that each species depends on its partners proportionally to the observed frequencies of interactions between them, so it does not take into account the flexibility of species (in our case pollinators) to shift their interactions after the extinction of some of their previous partners (visited plants). Such flexibility has been experimentally documented for example by Biella et al (2019, 2020). On the other hand, TCM assumes the opposite extreme, i.e.…”

“…that a species survives until any single partner of the species remains present. Despite their conceptual differences, both coextinction models received comparable empirical support based on field experiments in grasslands in central Europe (Biella et al 2020). Moreover, the simulations can be used to quantify the functional importance of individual species in the network (Pocock et al 2012).…”