Introduction
A central attribute of ecological communities is that only few species
and interactions may be essential to maintain community structure and
ecosystem processes, even though many species might coexist and interact
(Ellison et al. 2005; Valiente-Banuet et al. 2015). The
loss of essential species and the disruption of essential interactions
may have cascading effects in the community and increasing species
extinction rates (Gilbert 1980; Koh et al. 2004; Dunn et
al. 2009; Rodriguez-Cabal et al. 2013). Thus, studying the loss
of native species and gains of non-native invasive species is crucial to
understanding the structure and functionality of communities in a
changing world.
In particular, mutualistic interactions such as pollination and seed
dispersal are essential in supporting terrestrial ecosystems because
most of the plant reproduction success relies on these interactions
(Bond 1994; Ashman et al. 2004). Ecological networks provide a
systematic way of representing, characterizing and comparing the
complexity of ecological communities, in which species are represented
by nodes and interactions by links between nodes (Pimm 1982; van Veenet al. 2008). In the last two decades, the study of mutualistic
networks has been critical to understand the structure and functionality
of communities (Bascompte et al. 2003; Bascompte & Jordano 2007;
Rohr et al. 2014). However, although several studies have focused
on the impacts of human-caused environmental change on mutualistic
interactions (Traveset & Richardson 2006; Rodriguez-Cabal et al.2007; Tylianakis et al. 2008; Traveset & Richardson 2014), few
studies have focused on how such change triggers the disassembly of
mutualistic webs (Fortuna et al. 2013; Rader et al. 2014).
Moreover, the indirect effects on interaction webs are not well
understood because indirect effects are complex to study and because
perturbations can be attenuated by functional redundancy (Lawton &
Brown 1993; Terborgh & Feeley 2010).
The temperate forest of Patagonia is known for its highly endemic flora
and high proportion of plant species requiring animal mutualists for
pollination and seed dispersal (Aizen & Ezcurra 1998). Almost 60% of
plant species require at least one animal species for pollination
(Riveros 1991) and nearly 50% of plants produce fleshy fruits
suggesting animal seed dispersal (Armesto et al. 1987). In the
northern portion of this temperate forest occurs a unique mutualistic
interaction involving a hummingbird (Sephanoides sephaniodes ), a
marsupial (Dromiciops gliroides ), a mistletoe (Tristerix
corymbosus ), and its main host (Aristotelia chilensis ), a common
understory shrub. The nectar produced by the mistletoe is the primary
food resource for the hummingbird during winter (Smith-RamÃrez 1993;
Aizen et al. 2002). In spring and summer the hummingbird
pollinates almost 20% of the endemic woody genera in this region (Aizen
& Ezcurra 1998; Aizen 2003). The marsupial provides an efficient seed
dispersal service by dispersing at least 16 fleshy-fruited species,
including large fruits (>11 mm) not dispersed by the native
birds (Amico et al. 2009), and is the only seed disperser of the
mistletoe (Amico et al. 2011), which thus depends fully on the
marsupial for its persistence. Previous studies found that herbivory onA. chilensis by non-native ungulates leads to the disassembly of
the hummingbird-mistletoe-marsupial interaction (Rodriguez-Cabalet al. 2013). Owing to the high degree of asymmetry of
plant-animal mutualisms in the temperate forest of Patagonia, where most
of the plants depend only on a few mutualistic partners (Armestoet al. 1987; Riveros 1991; Aizen & Ezcurra 1998), the disruption
of this interaction could trigger a cascade of linked extinction events
throughout the community.
In this study, we evaluate whether the disruption of a
hummingbird-mistletoe-marsupial interaction by non-native ungulates can
have cascading effects on pollination and seed dispersal networks in the
temperate forest of Patagonia, Argentina. Specifically, we address the
following questions: (1) Is the hummingbird-mistletoe-marsupial
mutualism a keystone interaction? We expect that the complexity and
functional redundancy among generalist species of pollination and seed
dispersal networks will be greater in sites with this interaction than
in sites without the interaction. We also expect that the ecological
importance of the species involved in this proposed keystone interaction
will be greater in
sites with this interaction, occupying a high number of positions in the
networks. (2) Does the disruption of this proposed keystone interaction
produce cascading effects on the community? We expect that the
complexity and functional redundancy among generalist species of
pollination and seed dispersal networks will be lower in sites invaded
by non-native ungulates than in intact forest sites.