New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion

Abstract

The indirect effects of biological invasions on native communities are poorly understood. Disruption of native ant communities following invasion by the Argentine ant (Linepithema humile) is widely reported to lead indirectly to the near complete collapse of seed dispersal services. In coastal scrub in southeastern Australia, we examined seed dispersal and handling of two native and two invasive alien plant species at Argentine ant-invaded or -uninvaded sites. The Argentine ant virtually eliminates the native keystone disperser Rhytidoponera victoriae, but seed dispersal did not collapse following invasion. Indeed, Argentine ants directly accounted for 92% of all ant-seed interactions and sustained overall seed dispersal rates. Nevertheless, dispersal quantity and quality among seed species differed between Argentine ant-invaded and -uninvaded sites. Argentine ants removed significantly fewer native Acacia retinodes seeds, but significantly more small seeds of invasive Polygala myrtifolia than did native ants at uninvaded sites. They also handled significantly more large seeds of A. sophorae, but rarely moved them >5 cm, instead recruiting en masse, consuming elaiosomes piecemeal and burying seeds in situ. In contrast, Argentine ants transported and interred P. myrtifolia seeds in their shallow nests. Experiments with artificial diaspores that varied in diaspore and elaiosome masses, but kept seed morphology and elaiosome quality constant, showed that removal by L. humile depended on the interaction of seed size and percentage elaiosome reward. Small diaspores were frequently taken, independent of high or low elaiosome reward, but large artificial diaspores with high reward instead elicited mass recruitment by Argentine ants and were rarely moved. Thus, Argentine ants appear to favour some diaspore types and reject others based largely on diaspore size and percentage reward. Such variability in response indirectly reduces native seed dispersal and can directly facilitate the spread of an invasive alien shrub.

Quantitative analysis of the effects of the exotic Argentine ant on seed-dispersal mutualisms

“…However, the ultimate impact of Argentine ants on seed dispersal in a community may be mediated by seed size. For example, Rowles & O'Dowd (2009) showed that Argentine ants removed large as well as small diaspores but this was influenced by elaiosome mass. Additionally, when they do remove seeds, dispersal distances by invasive ants are often shorter than those of native species (Bond & Slingsby 1984;Horvitz & Schemske 1986;Ness 2004;Rowles & O'Dowd 2009).…”

“…Additionally, when they do remove seeds, dispersal distances by invasive ants are often shorter than those of native species (Bond & Slingsby 1984;Horvitz & Schemske 1986;Ness 2004;Rowles & O'Dowd 2009). Finally, not only do invasive ants disrupt seed-dispersal mutualisms between native species but they also successfully disperse seeds of exotic plants (Rowles & O'Dowd 2009).…”

“…As a result, invasive ants frequently fail to disperse large elaisome-bearing seeds while readily dispersing small native and exotic seeds (Ness 2004;Witt et al 2004;Rowles & O'Dowd 2009). However, the ultimate impact of Argentine ants on seed dispersal in a community may be mediated by seed size.…”

Invasive ants disrupt frugivory by endemic island birds

“…Invasive ants are well known to disrupt seed removal by native ants (Rowles & O'Dowd 2009 by native forest birds. This effect on frugivory emerges just 1 -2 years after supercolony formation.…”

Seed Dispersal Distances by Ants Increase in Response to Anthropogenic Disturbances in Australian Roadside Environments

“…There are numerous ant species that remove and transport seeds, however most dispersal events are performed by a few key removers (e.g., Andersen, 1988;Gove et al, 2007;Zelikova and Breed, 2008). Ants generally disperse seeds only short distances to their nests where they remove the elaiosome to feed to their larvae (Culver and Beattie, 1978;Hughes and Westoby, 1992;Rowles and O'Dowd, 2009;Gómez and Espadaler, 2013). However, infrequent long distance dispersal events can also occur by ants (Andersen, 1988).…”