Interactions between seed-dispersing ant species affect plant community composition in field mesocosms.

In generalized mutualisms, species vary in the quality of services they provide to their partners directly via traits that affect partner fitness and indirectly via traits that influence interactions among mutualist species that play similar functional roles. Myrmecochory, or seed dispersal by ants, is a generalized mutualism with ant species varying in the quality of dispersal services they provide to their plant partners. Variation in ant species identity can directly impact seed dispersal patterns and plant community composition; however, we know less about how interactions among seed-dispersing ant species indirectly influence plant partners. The invasive ant Myrmica rubra, is a high-quality seed-disperser in its native range that interacts with myrmecochores (ant-dispersed plants) and the high-quality seed disperser Aphaenogaster sp. in its invaded range. We use this system to examine how interactions between two functionally similar mutualist ant species influence the recruitment and community composition of ant-dispersed plants. We performed a field mesocosm experiment and a laboratory behavioural experiment to compare discovery and dominance behaviours between ant species, and seed dispersal and seedling recruitment of four myrmecochore species among intraspecific interaction treatments of each ant species and an interspecific interaction treatment. We found that M. rubra was better at discovering and dispersing seeds, but Aphaenogaster sp. was dominantly aggressive over M. rubra. Interspecific interactions dampened seed dispersal relative to dispersal by the better disperser. Despite this dampening, we found no effect of interspecific interactions on seedling recruitment. However, community composition of seedlings in the interspecific interaction treatment was more similar to composition in the aggressively dominant ant (Aphaenogaster sp.) treatment than in the better discoverer ant M. rubra treatment. We show that interspecific interactions between mutualist species in the same functional guild affect the outcome of mutualistic interactions with partner species. Despite the native ant dispersing fewer seeds, its dominance over the subordinate (invasive) ant has the potential to allow for some level of biotic resistance against the effects of M. rubra on plant communities when these species coexist.

Invasive ants disperse seeds farther than native ants, affecting the spatial pattern of seedling recruitment and survival.

Mutualists can vary in the quantity and quality of service which they provide to their partners. Variation in seed disperser quality depends on seed-processing traits, dispersal distance, and deposition location, all of which ultimately affect plant fitness. Here, we compared these aspects of seed dispersal quality between a native and an invasive ant species, and examined how they affect competition and plant performance. Using experimental mesocosm communities, we examined how these two ant species affect the spatial pattern of recruitment and establishment for four myrmecochorous plant species, including one invasive species. We measured the locations of dispersed seedlings relative to ant nests, adult plants, and other dispersed seedlings, as well as measured the effects of location on plant performance. The invasive ant, Myrmica rubra, secondarily dispersed seeds farther from its nests, creating a less clumped pattern of seedling recruitment compared to the native ant, Aphaenogaster rudis. Plant species responded differently to dispersal. Invasive seedlings recruited farther from adult plants than native seedlings, and had higher survival the farther they were from conspecifics. In contrast, native plants had higher survival and grew taller when dispersed farther from invasive plants. We show that seed-dispersing ant partners differ in mutualist quality creating differences in dispersal distance and deposition location that affects a plant's competitive environment. Our results reveal the potential for long-term consequences on plant community structure with changing ant partner identity. We emphasize the need to examine dispersal quality in addition to quantity to uncover the importance of partner identity in structuring communities.

Asynchrony between ant seed dispersal activity and fruit dehiscence of myrmecochorous plants.

PREMISE OF THE STUDY: Phenological mismatch has received attention in plant-pollinator interactions, but less so in seed dispersal mutualisms. We investigated whether the seasonal availability of myrmecochorous seeds is well matched to the seasonal activity patterns of seed-dispersing ants. METHODS: We compared seasonal timing of seed removal by a keystone seed-dispersing ant, Aphaenogaster rudis, and fruit dehiscence of several species of plants whose seeds it disperses in a deciduous forest in southern Ontario, Canada. We examined the timing of elaiosome "robbing" by the nonnative slug Arion subfuscus and tested whether seed removal by ants declines in response to supplementation with additional elaiosome-bearing seeds (ant "satiation"). KEY RESULTS: Seed removal from experimental depots peaked early in the season for all plant species and correlated with temperature. In contrast, elaiosome robbing by slugs increased late in the season and thus may disproportionately affect plants with late-dehiscing fruits. Ant colonies removed seeds at similar rates regardless of seed supplementation, indicating that satiation likely does not impact seasonal patterns of seed dispersal in this system. Fruits of the five myrmecochorous plant species in our study dehisced at discrete intervals throughout the season, with minimal overlap among species. Peak dehiscence did not overlap with peak seed removal for any plant species. CONCLUSIONS: Fruit dehiscence of myrmecochorous plants and peak ant seed dispersal activity occur asynchronously. Whether future climate warming will shift ant and plant phenologies in ways that have consequences for seed dispersal remains an open question.

An invasive slug exploits an ant-seed dispersal mutualism.

Plant-animal mutualisms, such as seed dispersal, are often vulnerable to disruption by invasive species. Here, we show for the first time how a non-ant invasive species negatively affects seed dispersal by ants. We examined the effects of several animal species that co-occur in a temperate deciduous forest-including native and invasive seed-dispersing ants (Aphaenogaster rudis and Myrmica rubra, respectively), an invasive slug (Arion subfuscus), and native rodents-on a native myrmecochorous plant, Asarum canadense. We experimentally manipulated ant, slug, and rodent access to seed depots and measured seed removal. We also video-recorded depots to determine which other taxa interact with seeds. We found that A. rudis was the main disperser of seeds and that A. subfuscus consumed elaiosomes without dispersing seeds. Rodent visitation was rare, and rodent exclusion had no significant effect on seed or elaiosome removal. We then used data obtained from laboratory and field mesocosm experiments to determine how elaiosome robbing by A. subfuscus affects seed dispersal by A. rudis and M. rubra. We found that elaiosome robbing by slugs reduced seed dispersal by ants, especially in mesocosms with A. rudis, which picks up seeds more slowly than M. rubra. Taken together, our results show that elaiosome robbing by an invasive slug reduces seed dispersal by ants, suggesting that invasive slugs can have profound negative effects on seed dispersal mutualisms.

Mutualism between co-introduced species facilitates invasion and alters plant community structure.

Generalized mutualisms are often predicted to be resilient to changes in partner identity. Variation in mutualism-related traits between native and invasive species however, can exacerbate the spread of invasive species ('invasional meltdown') if invasive partners strongly interact. Here we show how invasion by a seed-dispersing ant (Myrmica rubra) promotes recruitment of a co-introduced invasive over native ant-dispersed (myrmecochorous) plants. We created experimental communities of invasive (M. rubra) or native ants (Aphaenogaster rudis) and invasive and native plants and measured seed dispersal and plant recruitment. In our mesocosms, and in laboratory and field trials, M. rubra acted as a superior seed disperser relative to the native ant. By contrast, previous studies have found that invasive ants are often poor seed dispersers compared with native ants. Despite belonging to the same behavioural guild, seed-dispersing ants were not functionally redundant. Instead, native and invasive ants had strongly divergent effects on plant communities: the invasive plant dominated in the presence of the invasive ant and the native plants dominated in the presence of the native ant. Community changes were not due to preferences for coevolved partners: variation in functional traits of linked partners drove differences. Here, we show that strongly interacting introduced mutualists can be major drivers of ecological change.