Discussion
Here, we experimentally test the interactive effects of multiple disturbances on resident diversity, by exposing a bacterial community to different regimes of pulse mortality and invader disturbances. A challenge in understanding the effects of multiple disturbances is the potential for different interactive mechanisms to operate at different levels of disturbance (Foster et al. 2016). We found a significant interaction between the disturbance types, such that at low pulse disturbance frequencies invasion had a positive effect on total resident diversity, whereas at high pulse disturbance invasion had a negative effect. Consequently, our results demonstrate that, depending on the disturbance regime, multiple disturbances can act both antagonistically (have reduced combined effects on diversity) or synergistically (have greater combined effects on diversity).
It is commonly hypothesised that co-occurring disturbances have synergistic effects on diversity because communities that are disrupted by one disturbance may be less stable, and therefore less resilient to a second disturbance (Christensen et al. 2006; Crain et al.2008; Burton et al. 2020). However, evidence for such synergism between disturbances is mixed, with previous work frequently finding no or even antagonistic interactions between multiple disturbances (Darling & Côté 2008). Here we show a possible reason for such mixed empirical results: the direction of the interaction can depend on the regimes of the disturbances involved, and synergistic interactions may only be apparent in highly disturbed systems.
The dependence of the direction of the interactive effect on the disturbance regime strongly suggests that the negative effects of invasion on resident diversity might be missed at some disturbance frequencies. This may result in an invader erroneously being categorised as beneficial based on its positive effects at other disturbance frequencies. That the effect of the invader is highly contingent on the pulse disturbance regime may be particularly important for the passenger, driver and back seat driver hypothesis, which categorises an invader based on its effect on resident diversity (Didham et al.2005; MacDougall & Turkington 2005; Bauer 2012; Wilson & Pinno 2013; Fenesi et al. 2015). A ‘driver’ invader changes ecosystem properties and causes a decline in resident diversity independently from other factors of change going on in that environment (MacDougall & Turkington 2005; Wilson & Pinno 2013). In contrast, a ‘passenger’ invader takes advantage of available resources created by other causes of change, such as disturbance, but does not cause biodiversity or functionality loss themselves (MacDougall & Turkington 2005; Bauer 2012). Lastly, ‘back seat drivers’ act synergistically with other factors of change – they require ecosystem change to establish, like a passenger, but once established will themselves cause change, like a driver (Berman et al. 2013; Fenesi et al. 2015). In our experiment, the invaders acted as a back seat driver: they benefitted from higher disturbance frequency (as this lowered resident densities and offered more periods of reduced priority and dominance effects, and hence reduced invasion resistance), and subsequently affected the resident community. However, at low disturbance this may be missed, and the invader erroneously categorised as a passenger due to having no negative effect on the resident community. Similar phenomena may be observed with other pulse disturbance types. This shift in apparent invader effect at different levels of disturbance highlights the need to consider the characteristics of the disturbance regime when drawing inference, and raises concerns that invaders previously considered harmless (passengers) may shift to being detrimental for resident diversity (back seat drivers) as other disturbances increase.
Our finding of the pulse-invader interaction shifting from antagonistic at low levels of pulse disturbance to synergistic at high levels highlights the importance of looking at multiple disturbances over different regimes. A recurrent theme in understanding the effects of disturbances on diversity is that different disturbance aspects can interact in a complex way to shape communities, and that our interpretations of the disturbance-diversity relationships depend crucially on the extent and resolution of the observations. Even under a single disturbance type, a gradient of aspects of disturbances (e.g., frequency, severity) interact to produce various disturbance-diversity relationships. This may help to resolve previously reported conflicting patterns on disturbance-diversity relationships (Miller et al.2011; Hall et al. 2012). Similarly, previous analyses of the interactive effects of multiple disturbances (Darling & Côté 2008) have shown that the empirical patterns generated by interactions are mixed. Here, we use multiple disturbance regimes to show that, as in previous disturbance-diversity studies, a gradient of disturbance is crucial to fully understanding the effect of simultaneously co-occurring disturbances.
That the invader shifts to having severe negative consequences for diversity at high mortality pulse disturbance, and even qualitatively changes the pulse disturbance-diversity relationship, raises applied concerns as the number, frequency and intensity of disturbances is increasing with climate change (Essl et al. 2020). In our experiment, one mechanism underlying the synergistic effect of high disturbance in the invaded treatments is that the invader could have been interacting similarly with each member of the resident community (i.e. , reducing each resident species’ population equally). We observed, however, that this is not the case; the invader only negatively affects some species. This highlights that conservation efforts need to consider a species’ vulnerability to invasion under different disturbances and disturbance regimes, as well as that of the entire community. For example, if just pulse mortality is considered in our system, A. agilis would require greater resources to conserve than P. corrugata as it is more vulnerable under a changing disturbance regime. However, if we then additionally consider vulnerability to exclusion by an invader in a situation with high pulse mortality, P. corrugata would be regarded as more at risk thanA. agilis and therefore would receive more resources. One reason for this interaction being particularly present in P. corrugatais that it is closely related to our invader, P. aeruginosa , and so is more likely to compete for the same niche. We find that at low pulse frequencies, P. corrugata benefits from a priority effect and excludes P. aeruginosa . High frequencies, however, can reduce this priority effect and consequently, P. aeruginosa (a better competitor) can outcompete P. corrugata . This suggests that the finding that invaders that are more related to residents have less of an impact (Ricciardi & Atkinson 2004; Cox & Lima 2006; Saul & Jeschke 2015) may be in part due to priority effects, and may therefore not hold when disturbance regimes change. These findings further suggest that increasing disturbance may cause previously latent invaders to start competitively driving diversity loss. Moreover, this in itself may act as a disturbance, creating a positive feedback loop that facilitates further invasion (Wonham et al. 2005).
The differences in vulnerability to invasions among the resident species and the resulting changes in diversity imply that community robustness against invasion may significantly change over different disturbance regimes. This could be because frequent disturbances open up resources and niches, and therefore reduce the competitive advantage of some resident species over the invader (i.e., eliminate any priority or dominance effects they have). It is also important to note that in a stably coexisting community, such as the one studied here, an invader may indirectly reduce a resident species’ fitness by outcompeting a different species on which the resident relies.
Importantly, our findings can be applied to other natural microbial communities. For example, frequent disturbances by antibiotics have been shown to not only facilitate the invasion of clinically relevant opportunistic pathogens, such as Clostridium difficile , into a host microbiome, but also to have catastrophic effects for the diversity of the resident community (Shah et al. 2021). The antibiotic and pathogen may then interact synergistically and feedback to one another to reduce microbiome diversity, and consequently may further increase the risk of dysbiosis and infection (Blaser 2016; Ribeiro et al.2020), including from pathobionts (Ribeiro et al. 2020). Our results suggest that this interaction may reduce diversity principally by eliminating specific species – this could have particularly severe consequences in the microbiome, where species can play specific roles in host health and defence (Lange et al. 2016).
In conclusion, we provide experimental evidence that the interactive effect of two disturbances on resident diversity is dependent on their regime. Specifically, we find higher frequencies of pulse disturbance to increase the success of an invader, and to lead to multiple extinctions and a collapse in diversity, whereas at low pulse disturbance the invader had a positive effect on resident diversity. These findings help to create a predictive framework to understand how multiple disturbances interact to affect diversity – a pressing issue under climate change. Moreover, they demonstrate the importance of recording or deliberately using different disturbance regimes when testing for the interactive effects of multiple disturbances on diversity. Furthermore, we show that invaders can aggravate the negative effect of high pulse frequency on diversity. This raises serious concerns for global biodiversity, as the global trend towards increasing disturbance frequency may amplify negative effects of invasion worldwide, and the increasing number of invasions may amplify the negative effect of frequent pulse disturbances worldwide.