Is the hummingbird-mistletoe-marsupial mutualism a keystone interaction?
Complexity of both pollination and seed dispersal networks were different between intact forest sites with and without the keystone interaction. The diversity of motifs and the frequency of largest motifs suggest that networks are more complex in the presence of the hummingbird-mistletoe-marsupial interaction, with a wider range of direct and indirect interactions (Milo et al. 2002; Simmonset al. 2018). The high diversity of interaction types found may increase persistence and stability of communities due to the influence of direct and indirect interactions on the structure and organization of communities (Wootton 1994; Mougi & Kondoh 2012; Aschehoug & Callaway 2015). In addition to affect persistence and stability of communities, the diversity of interactions may influence ecological processes on a larger time scale. Ecological interactions play an essential role on driving the selection of traits, mainly in multiple partner mutualism such as pollination and seed dispersal interactions (Strauss & Irwin 2004; Guimarães Jr et al. 2011). Under normal disturbance conditions, the high number of direct and indirect pathways in sites with the hummingbird-mistletoe-marsupial interaction may allow to reshape continuously and slowly the direction of trait selection, promoting the emergence of species traits (Guimarães Jr et al.2011; Guimarães Jr et al. 2017). However, this high number of pathways also may slow down the response of species when rapid environmental changes occur, increasing its vulnerability to strong disturbances (Guimarães Jr et al. 2017).
The higher number of plant and pollinator species at generalist positions suggests greater network stability in intact forest sites with the keystone interaction than in sites without it. Several studies have demonstrated that the loss of generalist species produces stronger cascade effects and faster network collapse than the loss of specialized ones (Memmot et al. 2004; Kaiser-Bunbury et al. 2010). However, the impact of generalist species loss may be attenuated by functional redundancy among species when they perform similar roles in the community (Lawton & Brown 1993). The great number of pollinator and plant species that occupied positions with a high number of direct interactions indicates low network susceptibility to generalist species extinction by partial functional redundancy among them. Thus, the hummingbird-mistletoe-marsupial mutualism can be considered as a keystone interaction that provides a strong robustness to species extinction on pollination networks by promoting the presence of multiple generalist species that support specialized ones (Okuyama & Holland 2008; Thébault & Fontaine 2010).
When the keystone interaction is present, the mistletoe and hummingbird are key members of the community by occupying high number of positions and exerting great direct and indirect interactions. The increase in their ecological importance may be induced by the spatial distribution of the mistletoe and the co-evolutionary history of both species. Since mistletoe population has a contagious distribution (García et al.2009), the high mistletoe abundance in may increase its probability of interacting directly and indirectly with other species (Vázquez et al. 2009). Moreover, the mistletoe-hummingbird interaction become specialist in winter because mistletoe flowers are the only nectar resource available for the hummingbird, promoting its permanence in patches with high mistletoe abundance (Smith-Ramírez 1993). In contrast with the mistletoe and hummingbird, the presence of the keystone interaction did not affect the dispersal role of the marsupial. Its ample diet of insects, bird eggs, insects and fleshy fruits (Fontúrbelet al. 2012) may allow the marsupial to sustain a stable population without consuming large amount of mistletoe fruits in sites with low mistletoe density. Indeed, the presence of the marsupial and mistletoe in these sites may be a potential source of the mistletoe contagious distribution and become sites with high density of the keystone interaction in the future due to the full dependence of the mistletoe on the marsupial for its seed dispersal (García et al.2009; Amico et al. 2011)