Interaction exposure effects of multiple disturbances: plant population resilience to ungulate grazing is reduced by creation of canopy gaps

Abstract

The impact of multiple disturbances on populations could be synergistic or antagonistic via disturbance interaction and are considered to be provoked by alternation of the impact of an ecosystem disturbance due to the effect of a preceding disturbance. The impact of a focal disturbance can also change when a preceding disturbance alters the proportion of individuals in a population exposed to these disturbances (i.e., interaction exposure effects), although this effect has not been addressed to date. Herein, we propose and test interaction exposure effects by elucidating disturbance interactions between canopy gap formation and ungulate grazing. Based on a vegetation and seed bank survey conducted on an island in Hokkaido, northern Japan, we examined whether canopy openness changes the impact of ungulate grazing on the occurrence probability of palatable plant species through the facilitation of germination. Species occurrence in the seed bank significantly decreased with increasing canopy openness under the presence of grazing; however, it slightly increased under the absence of grazing, suggesting that gap creation, which facilitates germination, exposes the seed bank to ungulate grazing. Because disturbances of various types often modify the habitat structure, these proposed disturbance interactions are expected to operate within various ecosystems and taxa. An understanding of the impacts of disturbances on ecosystems is indispensable for comprehending the persistence of populations 1-3. Climate change and increasing pressures from human development have increased disturbance frequency; therefore, it is more likely that ecosystems will be exposed to multiple co-occurring disturbances 4,5 that could severely impact these environments 6-8. Therefore, the interacting effects of multiple disturbances on populations should be understood to help predict the fate of ecosystems 4,9. The population impact of multiple disturbances may be larger or smaller than the sum of the impacts of respective individual disturbances 4,10-14. These cumulative or antagonistic impacts have been attributed to two types of interaction effects: interaction chain effects (linked disturbances in the context of Buma et al. 5) and interaction modification effects 4,9. Within the interaction chain effects, the total impact of disturbances on a population is altered by the indirect effects of a supportive disturbance to the strength and/or extent of main disturbances 15-17 (Fig. 1a), e.g., a typical example of an interaction chain effect would be enhanced severity of a forest fire within a severely blown-down forest 16. Within interaction modification effects, indirect effect(s) of supportive disturbance(s) on main disturbances modifies the per capita impact of the main disturbance 18,19 (Fig. 1b). An example of interaction modification effects is that of savanna fires reducing the resistance of tree trunks to hurricanes, as rapid tree growth following fires results in low wood density 18. Although both interaction chain and modification effec...

Future dominance by quaking aspen expected following short‐interval, compounded disturbance interaction

“…Preferential browsing of aspen stems will likely slow the rate of canopy recovery rather than alter the species composition of the future forest canopy in our study area. Overall, the mechanisms by which prior disturbances have affected recovery following subsequent disturbances appear to be consistent with Shinoda and Akasaka’s (2020) concept of interaction exposure effects of multiple disturbances.…”

“…Thus, ungulate browsing may slow the rate of canopy recovery, but the future forest canopy is likely to be dominated by aspen in sites where aspen was present prior to fire. The stand‐replacing fires increased the relative abundance of juvenile trees and the overall proportions of trees susceptible to ungulate browsing (i.e., exposure disturbance interaction, Shinoda and Akasaka 2020), which in turn affects the rate and trajectory of forest recovery.…”

Four priority areas to advance invasion science in the face of rapid environmental change

“…rates of contemporary biodiversity change (Essl et al 2015c). Given the management implications of this phenomenon, ecological responses to compounded and cumulative stressors are becoming an increasing focus of theory, experiments, and time series analyses (Foster et al 2016;Candolin et al 2018;Kleinman et al 2019;Shinoda and Akasaka 2020).…”

Deer grazing changes seed traits and functions of grazing‐intolerant plants

“…Seeds in seed banks play a vital role in determining species richness and the stability of aboveground vegetation (Dawson et al, 2017; DiTommaso, Morris, Parker, Cone, & Agrawal, 2014; Oesterheld & Sala, 1990). Thus, the seeds in soil seed banks are prime conservation targets for plants, in order to avoid them being lost due to disturbances (Pakeman & Eastwood, 2013; Shinoda & Akasaka, 2019, 2020). Although it is recognized that seed quality is closely related to the formation and persistence of seed banks (Adebisi et al, 2013; Pakeman & Eastwood, 2013), the impact of ungulate grazing and other disturbances on seed quality has previously not been well studied.…”

“…Ungulate grazing is a type of disturbance that can have a major impact on plant population dynamics (Côté, Rooney, Tremblay, Dussault, & Waller, 2004; Sasaki, Furukawa, Iwasaki, Seto, & Mori, 2015). Grazing by ungulates can severely and continuously affect plant populations, in some cases restricting plants' reproduction and survival (Côté et al, 2004; Shinoda & Akasaka, 2020; Takatsuki, 2009; Wright et al, 2012). Such grazing can affect the persistence of plant populations both directly and indirectly: it directly decreases persistence when the impact of grazing exceeds the degree of resilience of the population (i.e., grazing affects on population beyond the capacity of the population to recover using seed banks), and it indirectly decreases persistence by decreasing the source of resilience (i.e., grazing reduces seeds in a seed bank) (Enright, Fontaine, Lamont, Miller, & Westcott, 2014; Ingrisch & Bahn, 2018; Ohashi et al, 2014; Scheffer, Carpenter, Foley, Folke, & Walker, 2001; Shinoda & Akasaka, 2019).…”