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)