Biol Invasions https://doi.org/10.1007/s10530-018-1829-6 (0123456789().,-volV)(0123456789().,-volV) ORIGINAL PAPER Invasive ants take and squander native seeds: implications for native plant communities Adam J. M. Devenish . Crisanto Gomez . Jon R. Bridle . Rosemary J. Newton . Seirian Sumner Received: 5 March 2018 / Accepted: 30 August 2018 Ó The Author(s) 2018 Abstract Seed dispersal is a fundamental process in placement, in order to determine the stages of seed the lifecycle of all flowering plants. Many plant dispersal most vulnerable to disruption by invaders. species have evolved specialist associations with Using the Argentine ant (Linepithema humile)asa biotic vectors to facilitate dispersal. Such specialised model, we show that invaded sites exhibited a interactions mean that these associations are poten- significant decrease in seed dispersal services across tially highly sensitive to disruption, e.g. from invasive all three phases of the dispersal process, relative to species. However, despite this threat we still under- non-invaded sites. Seeds dispersed in invaded sites stand remarkably little about how such perturbations were: (a) less likely to be transported; (b) potentially affect the dynamics and efficiency of the seed- distributed over a smaller spatial area, and (c) less dispersal process. In this study we quantify the impacts likely to be placed at soil depths favourable for of an invasive ant across three key phases of the seed germination and establishment compared to those dispersal process: seed removal, distribution and dispersed in non-invaded sites. These results reveal that ant-mediated seed dispersal services are signifi- cantly reduced by an invasive species at multiple Electronic supplementary material The online version of stages in the dispersal process. Reductions in the this article (https://doi.org/10.1007/s10530-018-1829-6) con- efficacy of seed dispersal, combined with shifts in the tains supplementary material, which is available to authorized ecological and geographical patterns of dispersal, may users. lead to cascading impacts on plant species composi- A. J. M. Devenish (&) Á J. R. Bridle Á S. Sumner tion and community structure. This study shows how School of Biological Sciences, University of Bristol, an invasive ant can affect seed dispersal at several Bristol, UK stages in the dispersal process. e-mail: [email protected] A. J. M. Devenish Á R. J. Newton Keywords Ant-plant mutualism Á Argentine ant Á Conservation Science, Royal Botanic Gardens Kew, Linepithema humile Á Myrmecochory Á Pheidole Wakehurst Place, Ardingly, UK pallidula Á Seed dispersal Á Iberian Peninsula C. Gomez Department of Environmental Sciences, University of Girona, Girona, Spain S. Sumner CBER, Department of Genetics, Evolution and Environment, University College London, London, UK 123 A. J. M. Devenish et al. Introduction Beattie 1980; Oliveras et al. 2005a). A mismatch between ants and their plant partners at any point in the Seed dispersal is a vital process in the life cycle of all seed dispersal process will likely modify the nature of flowering plants (O’Dowd and Hay 1980; Howe and this mutualism, reducing both seed dispersal and the Smallwood 1982; Hanzawa et al. 1988). Because survival of myrmecochorous flora. For example, not plants are sessile, they rely on abiotic (e.g. wind and all ant species handle seeds in a way that will result in water) and biotic (e.g. insect, bird, and mammal) successful germination and seedling establishment vectors to disperse their seeds. Invasions by non- (Go´mez and Espadaler 1998a, b). The need for native species threaten the efficacy of biotic seed- successful processing of seeds to occur at all steps dispersers, with potentially serious knock-on effects to makes many ant-plant interactions far more spe- the natural plant community structure (Ricklefs and cialised than they might initially appear to be, and Renner 1994; Webb and Peart 2001; Christian 2001; therefore this process is much more vulnerable to Ozinga et al. 2009; Ruxton and Schaefer 2012). disruption than might be expected. Even small Despite this threat, we often lack comprehensive data changes to ant communities may alter the composition on how specific biological invasions alter important of plant communities (Andersen and Morrison 1998; ecosystem processes like seed dispersal. This is Christian 2001; Ruxton and Schaefer 2012; Warren because assessments are often based on studies that and Bradford 2014), which can result in shorter seed focus on only one aspect of the seed dispersal process dispersal distances, reduced transportation rates of (e.g. seed choice), without consideration of the entire seeds to ant nests, and reduced seedling germination process (e.g. whether seeds ultimately end up in and establishment (Bond and Slingsby 1984; Christian favourable germination sites). This latter example can 2001;Go´mez and Oliveras 2003; Rodriguez-Cabal be used as a proxy for understanding the ultimate et al. 2009). In addition, the effects will not necessarily impact on plant community composition. be distributed equally across the native flora, which Ants are one of the major seed dispersal agents for means there can be significant shifts in plant commu- angiosperms in Mediterranean climates (Lengyel et al. nity structure, together with shifts in functional and 2010). Ant-mediated seed dispersal (myrmecochory) taxonomic diversity (Bond and Slingsby 1984; Chris- is geographically widespread, and observed in at least tian 2001). 11 000 (4.5% of all) angiosperm plant species, across Invasions by non-native ant species can signifi- 77 (12% of all) families (Bronstein et al. 2006; cantly alter the ecological distribution and phyloge- Lengyel et al. 2010). Plant species that rely on this netic structure of native ant communities (Holway and mode of dispersal use an oily seed appendage (called Case 2000; Lessard et al. 2009). These invaded ant an elaiosome) to attract ants which then remove the communities show reduced genetic and ecological seed back to their nest (Beattie 1985). In doing so, ants diversity (Holway and Suarez 2006), resulting in a loss place the seed out of reach of danger from seed of both keystone ant species (Christian 2001) and predators and of destruction by fire and waterlogging ecosystem function (Andersen 1997). For example, (Bond and Stock 1989; Fenner and Thompson 2005; Lessard et al. (2009) showed that across several Cuautle et al. 2005). Ants in turn benefit from the studies, ant invaders act as a form of environmental nutritious elaiosome (Gammans et al. 2005), which filter, resulting in a loss of native species in a non- they feed to their larvae (Beattie 1985). random manner. This disassembly of the native ant Ant behavioural and biological traits influence the community structure often results in the loss of efficacy of myrmecochory and thus the seed-dispersal specialist ant groups, such as seed dispersers (Suarez process. These traits include: Seed removal: an ant et al. 1998; Christian 2001). must locate a seed and remove it from where it fell; Linepithema humile Mayr, the Argentine ant (Hy- Nest distribution: an ant must deliver the seed to its menoptera: Formicidae) is one of the most invasive ant nest in an area away from the parent plant; Seed species in the world (Holway et al. 2002). Human placement: an ant must remove the elaiosome on activities have caused its rapid global spread since the arrival at the nest, and discard the intact seed in a 1800s, such that established populations have been suitable place for germination and establishment (e.g. found across six continents, in at least 55 countries, on refuse piles in or around the ant nest) (Culver and and on several oceanic islands (Tsutsui et al. 2001; 123 Invasive ants take and squander native seeds Wetterer et al. 2009; Suarez et al. 2001). In regions process. Specifically, across four sites in Spain, we with a Mediterranean climate and/or mild winters, the compared the seed-handling behaviour of both L. first recorded introductions were in 1858 (Holway humile and a dominant native seed-dispersing ant, 1998; Wetterer et al. 2009). Linepithema humile Pheidole pallidula. We test the hypotheses that invades both disturbed and undisturbed habitats, compared to seeds in non-invaded sites, seeds in sites resulting in changes to the native ant community invaded by L. humile are: (1) less likely to be removed structure (Bond and Slingsby 1984; Holway 1998; (seed removal: hypothesis 1); (2) distributed over a Christian 2001; Holway et al. 2002). smaller area (nest distribution: hypothesis 2); and (3) Observations of invasive L. humile populations in placed at depths less favourable for germination and native ecosystems have shown that they can alter the establishment (seed placement: hypothesis 3). Identi- patterns of myrmecochory. For example, a quantita- fying how L. humile ants differ from sympatric native tive analysis on the effects of L. humile on native ant seed-dispersers, with regard to how they handle seeds community structure by Rodriguez-Cabal et al. at different phases of the seed dispersal process, will (2009) found an average 92% reduction in the help achieve more accurate predictions as to the number of native ant seed dispersers within invaded detrimental impact of ant invasions on this important regions. This loss in native seed dispersers has been ecosystem service. This research may then help inform demonstrated to have a detrimental impact on seed any future efforts aimed at mitigating the conse- dispersal processes, with a reduction in both the quences of invasion by ants. distance seeds are transported and their likelihood of reaching ant nests (Go´mez and Oliveras 2003; Go´mez et al. 2003). While this effect has been Materials and methods detected in a wide variety of habitats (Christian 2001; Go´mez and Oliveras 2003; Rowles and O’Dowd Study area and ant communities 2009), the degree of effect can vary tremendously between studies, either because of differences in The Argentine ant was first recorded in the Iberian habitat types or sampling method used.