Trophic ecology of invasive Argentine ants in their native and introduced ranges Chadwick V. Tillberg*†, David A. Holway‡, Edward G. LeBrun‡§, and Andrew V. Suarez*¶ *Departments of Entomology and Animal Biology, University of Illinois at Urbana–Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801; and ‡Division of Biological Sciences, MC 0116, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0116 Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved November 7, 2007 (received for review July 24, 2007) Although the ecological effects of invasions often become obvious In this study we examine the direct effects of Argentine ant soon after introduced species become established, more gradual (Linepithema humile) invasions on native ant diversity and then effects may take years to manifest and can thus require long-term quantify how dietary flexibility in this widespread invader affects data for quantification. We analyzed an 8-year record of stable spatiotemporal variation in its trophic position. Invasive ants isotope data on Argentine ants (Linepithema humile) from south- provide an ideal system to test how trophic flexibility contributes ern California to infer how the trophic position of this widespread to invasion success. With many species introductions, it can be invasive species changes over time as native ant species are difficult to separate the effects of the invader from covarying displaced. We couple this longitudinal analysis with a biregional factors, such as habitat disturbance, that might also negatively comparison of stable isotope data (␦15N) on ants from Argentina affect natives (2, 6). Because Argentine ants aggressively displace (native range) and California (introduced range) to quantify (i) how above-ground foraging native ants (7), changes in the diet of L. the trophic position of L. humile differs between native and humile that occur during and just after invasion can be linked to introduced populations, and (ii) how relative trophic position as native ant displacement. Second, invasive ants, such as L. humile, estimated by ␦15N values of Argentine ants compare with those of are highly omnivorous and frequently form nonspecialized as- other ants at the same site. Both long-term and biregional com- sociations with honeydew-producing Hemiptera (7–10). Greater parisons indicate that the Argentine ant’s relative trophic position use of honeydew and other plant-based resources in introduced is reduced at sites with a longer history of occupation. Over the populations might result in a decrease in trophic position course of 8 years, the relative trophic position of L. humile re- (relative to that of native populations), such that invasive ants mained high at the leading edge of an invasion front but declined, would persist at higher densities than if they were acting as on average, behind the front as native ants disappeared. Relative carnivores (7, 11, 12). Similar arguments have been proposed to to native populations, where L. humile is among the most carniv- explain the great abundance of ants in tropical rainforest can- orous of ants, Argentine ants from California occupied lower opies (13). Although the exploitation of honeydew and other plant-based resources might subsidize invasive ants at high trophic positions. These results support the hypothesis that Ar- densities, few data are available to evaluate this hypothesis. gentine ants shift their diet after establishment as a result of An important obstacle in this area of research concerns the resource depletion and increasing reliance on plant-based re- quantification of ant diets. Incomplete dietary information sources, especially honeydew-producing Hemiptera. Our results greatly hinders an understanding of the community-wide effects demonstrate the value of long-term and biregional data in uncov- of ant invasions. Invasive ants forage extensively on liquids (11, ering ecological effects of invasions. 14, 15), so observational data on diets are of limited use, because the exact composition of consumed or stored liquids remains ͉ ͉ biological invasions stable isotopes food webs unknown (e.g., the relative proportions of nectar, honeydew, and hemolymph). For these reasons, we use stable isotope analysis, iological invasions threaten biodiversity and drain economic an approach of demonstrated value in quantifying trophic rela- Bresources. Despite the importance of species introductions, tionships in ants (13, 16, 17). the short-term and small-scale nature of most invasive species We combine longitudinal and biregional comparisons (i)to research is a recognized limitation of this field (1). Additionally, track changes in nitrogen isotopic ratios of Argentine ants over confounding environmental factors can obscure links between time (i.e., as they actively displace native ants), and (ii)to the spread of invasive species and decline of natives (2). Spa- compare the trophic position of L. humile between its native and tiotemporal fluctuations in the population sizes of introduced introduced ranges. To measure changes in Argentine ant trophic species (3) that result from changes in resource use or availability position and native ant diversity during the course of an invasion, (4) can greatly alter the extent to which invaders disrupt eco- we sampled an active invasion front over an 8-year period. We systems. Because a better understanding of such variation will predict that the trophic level of resources assimilated by L. inform both ecological theory and management strategies, there humile will drop if the process of invasion either (i) depletes is an urgent need for long-term studies as well as for research that resources from high trophic levels (e.g., the consumption of investigates ecological interactions in the native ranges of intro- duced species. Author contributions: C.V.T., D.A.H., and A.V.S. designed research; C.V.T., D.A.H., E.G.L., One underappreciated source of variation regarding intro- and A.V.S. performed research; C.V.T., D.A.H., E.G.L., and A.V.S. analyzed data; and C.V.T., duced species concerns dietary flexibility and shifts in trophic D.A.H., E.G.L., and A.V.S. wrote the paper. position between native and introduced populations. This form The authors declare no conflict of interest. of ecological plasticity may enhance invasion success in a number This article is a PNAS Direct Submission. of ways. Species capable of extracting required nutrients from †Present address: Department of Biology, Linfield College, 900 SE Baker Street, McMin- multiple trophic levels might establish in a broader range of nville, OR 97128. environments compared with more specialized consumers. Fur- §Present address: University of Texas, Brackenridge Field Laboratory, 2907 Lake Austin thermore, theory predicts diminishing biomass at higher trophic Boulevard, Austin, TX 78703. levels, suggesting that species feeding at lower trophic levels ¶To whom correspondence should be addressed. E-mail: [email protected]. might attain greater abundance (5). © 2007 by The National Academy of Sciences of the USA 20856–20861 ͉ PNAS ͉ December 26, 2007 ͉ vol. 104 ͉ no. 52 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0706903105 10 100 Table 1. Native ant species detected in Rice Canyon, San Diego 1996 1997 County, California 8 80 Before invasion After invasion 6 60 Genus and species (1996) (2003) 4 40 Dorymyrmex bicolor X 2 20 Dorymyrmex insanus X 0 0 Tapinoma sessile X 1998 2000 Forelius mccooki X 8 80 Brachymyrmex depilis X 6 60 Paratrechina cf. terricola X Camponotus fragilis X 4 40 Camponotus yogi X 2 20 Prenolepis imparis X Stenamma diecki X 0 0 Pheidole hyatti X 2002 2001 120 8 Pheidole vistana X 100 Pheidole clementensis X 6 80 Crematogaster mormonum X 60 4 Crematogaster californica X 40 Solenopsis xyloni X 2 20 Solenopsis molesta XX 0 0 Temnothorax andrei XX number of native ant species (closed circles) 123456789 2003 Messor andrei X 8 80 Cyphomyrmex wheeleri X 6 60 number of Argentine ant workers per trap (open squares) Neivamyrmex californicus X 4 40 Neivamyrmex nigrescens X Pseudomyrmex apache X 2 20 0 0 123456789 Rice Canyon as a whole, the number of native ant species dropped Fig. 1. Displacement of native ants by Argentine ants over an 8-year period from 23 before 1996 to just 2 by 2003 (Table 1). in Rice Canyon, San Diego County, California. Sampling stations (1–9) are As L. humile spread through Rice Canyon and displaced shown on the x axis. Open squares, number of Argentine ant workers captured resident ants (Fig. 1), its average ␦15N value decreased over the per pitfall trap at each sampling station; closed circles, number of native ant ECOLOGY species captured in pitfall traps at each sampling station. The photograph 8-year period of investigation (Fig. 2A). For seven of the nine 15 (Bottom Right) shows an aerial view of Rice Canyon (coastal sage scrub fixed sampling stations, the ␦ N value for the first year that L. surrounded by residential development) and the approximate location of the humile was recorded at a station (i.e., at the leading edge of the center of each sampling station. Image provided by Google Earth. invasion front) exceeded that of the mean ␦15N value for that station in all subsequent years (i.e., after the displacement of native ants) (paired t test: t8 ϭ 3.07, P ϭ 0.0154) (Fig. 2B). native ants and other arthropod predators), or (ii) leads to increased exploitation of plant-based resources. Alternatively, a Biregional Comparisons of Trophic Ecology. At our six study sites in ␦15 downward shift in trophic position would not be expected if Argentina and California, N values for ants as a whole resources exploited by Argentine ants remained stable through encompassed a broad range of values (Fig. 3), suggesting that time, or if plant-based resources, such as honeydew, were ants at each site occupy several trophic levels.