Invasive species modulate the structure and stability of a multilayer mutualistic network.

Species interactions are critical for maintaining community structure and dynamics, but the effects of invasive species on multitrophic networks remain poorly understood. We leveraged an ongoing invasion scenario in Patagonia, Argentina, to explore how non-native ungulates affect multitrophic networks. Ungulates disrupt a hummingbird-mistletoe-marsupial keystone interaction, which alters community composition. We sampled pollination and seed dispersal interactions in intact and invaded sites. We constructed pollination and seed dispersal networks for each site, which we connected via shared plants. We calculated pollination-seed dispersal connectivity, identified clusters of highly connected species, and quantified species' roles in connecting species clusters. To link structural variation to stability, we quantified network tolerance to single random species removal (disturbance propagation) and sequential species removal (robustness) using a stochastic coextinction model. Ungulates reduced the connectivity between pollination and seed dispersal and produced fewer clusters with a skewed size distribution. Moreover, species shifted their structural role, fragmenting the network by reducing the 'bridges' among species clusters. These structural changes altered the dynamics of cascading effects, increasing disturbance propagation and reducing network robustness. Our results highlight invasive species' role in altering community structure and subsequent stability in multitrophic communities.

The disruption of a keystone interaction erodes pollination and seed dispersal networks.

Understanding the impacts of global change on ecological communities is a major challenge in modern ecology. The gain or loss of particular species and the disruption of key interactions are both consequences and drivers of global change that can lead to the disassembly of ecological networks. We examined whether the disruption of a hummingbird-mistletoe-marsupial mutualism by the invasion of non-native species can have cascading effects on both pollination and seed dispersal networks in the temperate forest of Patagonia, Argentina. We focused on network motifs, subnetworks composed of a small number of species exhibiting particular patterns of interaction, to examine the structure and diversity of mutualistic networks. We found that the hummingbird-mistletoe-marsupial mutualism plays a critical role in the community by increasing the complexity of pollination and seed dispersal networks through supporting a high diversity of interactions. Moreover, we found that the disruption of this tripartite mutualism by non-native ungulates resulted in diverse indirect effects that led to less complex pollination and seed dispersal networks. Our results demonstrate that the gains and losses of particular species and the alteration of key interactions can lead to cascading effects in the community through the disassembly of mutualistic networks.

A keystone mutualism promotes resistance to invasion.

It is not uncommon for one or a few species, and their interactions, to have disproportionate effects on other species in ecological communities. Such keystone interactions might affect how communities respond to the invasion of non-native species by preventing or inhibiting the establishment, spread or impact of non-native species. We explore whether a keystone mutualism among a hummingbird-mistletoe-marsupial promotes ecological resistance to an invasive pollinator, the bumblebee Bombus terrestris, by comparing data collected at sites prior to bumblebee invasion to data collected 11 years after the invasion in sites with and without the keystone mutualism. We built pollination networks and focused on network motifs, regarded as building blocks of networks, to identify the central pollinators and estimate the change in their interactions after invasion of B. terrestris. We also estimated the interaction rewiring across the season in post-invasion networks and tested it as a possible mechanism explaining how the keystone mutualism increased ecological resistance to invasion. We found two times more species in post-invasion sites with the keystone mutualism than in post-invasion sites without the keystone mutualism. Moreover, we found that invasive bumblebee reduced the strength and interaction niche of the five central pollinator species while increasing its own strength and interaction niche, suggesting a replacement of interactions. Also, we found that the keystone mutualism promoted resistance to B. terrestris invasion by reducing its negative impacts on central species. In the presence of the keystone mutualism, central species had three times more direct interactions than in sites without this keystone mutualism. The higher interaction rewiring, after invasion of B. terrestris, in sites with the keystone mutualism indicates greater chances of central pollinators to form new interactions and reduces their competence for resources with the non-native bumblebee. Our results demonstrate that a keystone mutualism can enhance community resistance against the impacts of a non-native invasive pollinator by increasing species diversity and promoting interaction rewiring in the community. This study suggests that the conservation of mutualisms, especially those considered keystone, could be essential for long-term preservation of natural communities under current and future impacts of global change.

Es común que una o unas pocas especies y sus interacciones tengan efectos desproporcionado sobre otras especies en las comunidades. Estas especies y sus interacciones claves podrían afectar el modo en que las comunidades responden a la invasión de especies no nativas al prevenir o disminuir su establecimiento, su propagación o el impacto de las mismas. En este estudio evaluamos si un mutualismo clave entre un colibrí, un muérdago y un marsupial promueve la resistencia de la comunidad frente a un polinizador invasor, el abejorro Bombus terrestris, mediante la comparación de datos colectados en sitios previos a la invasión del abejorro y datos colectados 11 años después de su invasión, en sitios con y sin el mutualismo clave. Construimos redes ecológicas planta-polinizador y nos centramos en los modos de interacción ("interaction motifs"), los cuales son usados como bloques en la construcción de las redes, para identificar los polinizadores centrales y estimar el cambio en sus interacciones después de la invasión de B. terrestris. Además, en las redes posteriores a la invasión estimamos la reconexión de interacciones a lo largo de la temporada y la evaluamos como un posible mecanismo mediante la cual el mutualismo clave aumentó la resistencia a la invasión. En sitios posteriores a la invasión con el mutualismo clave encontramos dos veces más especies que en sitios posteriores a la invasión ausentes de éste. Además, en los sitios ausentes del mutualismo clave, encontramos que el abejorro invasor redujo la fuerza y el nicho de interacción de los cinco polinizadores centrales mientras incrementó su propia fuerza y nicho de interacciones, sugiriendo un reemplazo de interacciones. Asimismo, encontramos que el mutualismo clave promovió la resistencia de la comunidad a la invasión de B. terrestris al reducir sus impactos negativos sobre las especies centrales. En presencia del mutualismo clave, las especies centrales presentaron tres veces más interacciones directas que en sitios ausentes de esta interacción. La gran reconexión de interacciones encontrada en sitios posteriores a la invasión con el mutualismo clave indica mayores probabilidades de que los polinizadores centrales formen nuevas interacciones y reduzcan la competencia por recursos con el abejorro no nativo. Nuestros resultados demuestran que un mutualismo clave puede mejorar la resistencia de la comunidad frente a los impactos de especies invasoras al incrementar la diversidad de especies y promover la reconexión de interacciones en la comunidad. Este estudio sugiere que la conservación de las interacciones mutualistas, principalmente aquellas consideradas claves, podría ser esencial para preservar las comunidades naturales frente a los impactos del cambio global.