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Invasive Ants Disperse Seeds Farther Than Native Ants, Affecting The Oecologia https://doi.org/10.1007/s00442-019-04553-3 PLANT-MICROBE-ANIMAL INTERACTIONS – ORIGINAL RESEARCH Invasive ants disperse seeds farther than native ants, afecting the spatial pattern of seedling recruitment and survival Shannon A. Meadley‑Dunphy1,2 · Kirsten M. Prior1,3 · Megan E. Frederickson1 Received: 22 January 2019 / Accepted: 5 November 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract 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 afect plant ft- ness. Here, we compared these aspects of seed dispersal quality between a native and an invasive ant species, and examined how they afect competition and plant performance. Using experimental mesocosm communities, we examined how these two ant species afect 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 efects 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 diferently to dispersal. Invasive seedlings recruited farther from adult plants than native seedlings, and had higher survival the farther they were from conspecifcs. In contrast, native plants had higher survival and grew taller when dispersed farther from invasive plants. We show that seed-dispersing ant partners difer in mutualist quality creating diferences in dispersal distance and deposition location that afects a plant’s competitive environ- ment. 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. Keywords Aphaenogaster rudis · Biological invasions · Myrmecochory · Myrmica rubra · Seed dispersal · Spatial patterns Introduction Many plants depend on animals to disperse their seeds. The efectiveness of an animal as a seed disperser depends on both the number of seeds it moves and on whether Communicated by Susan Whitehead. dispersed seeds survive, germinate, and grow into adults (Schupp 1993; Schupp et al. 2010). Where a seed ends up Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s0044 2-019-04553 -3) contains after dispersal establishes the abiotic and biotic environ- supplementary material, which is available to authorized users. ment, it will experience throughout its life. This includes local resource availability and microhabitat conditions; as * Shannon A. Meadley-Dunphy well as the strength of its interactions with other plants, ani- [email protected] mals (e.g., herbivores), and soil or other microbes (Kjells- 1 Department of Ecology and Evolutionary Biology, son 1991; Kalisz et al. 1999; Gorb and Gorb 2003; Tanaka University of Toronto, 25 Willcocks Street, Toronto, and Tokuda 2016). Thus, where an animal moves, a seed ON M5S 3B2, Canada afects plant performance for many years following the dis- 2 Present Address: Department of Biology, McGill University, persal event, and is a key component of an animal’s seed 1205 Dr Penfeld Ave, Montreal, QC H3A 1B1, Canada dispersal efectiveness. However, because it is difcult to 3 Present Address: Department of Biological Sciences, track seeds through space and monitor their fates through Binghamton University, State University of New York, time, most studies measure only the quantity and not the P. O. Box 6000, Binghamton, NY 13902, USA Vol.:(0123456789)1 3 Oecologia quality of seed dispersal (including our own, Meadley Dun- Aphaenogaster rudis s.l. This ant is considered a keystone phy et al. 2016). To fully understand the efectiveness of mutualist, because A. rudis disperses as many as 70% of the diferent seed dispersers, we need to measure their efects seeds it encounters and is also the most common woodland on the whole dispersal process, from how many seeds they ant (Ness et al. 2009). Plants gain multiple benefts from move, to where they deposit seeds, to the efect of deposition dispersal by ants including reduced parent–ofspring or seed- location on plant performance. Here, we investigate how ling competition (Kalisz et al. 1999; Boyd 2001), reduced two seed-dispersing species difer in their dispersal qual- seed predation (O’Dowd and Hay 1980; Heithaus 1981), and ity. In particular, we compare (1) how the ant species afect directed dispersal to favorable microhabitats (Gibson 1993). the spatial pattern of seedling recruitment and (2) the efect The outcome of myrmecochory is often sensitive to of deposition location on later stages of plant performance, changes in the local ant assemblage, because ant species including plant survival and growth (Fig. 1). difer in how they interact with seeds (Gorb and Gorb 1999; We focused on seed dispersal by ants (myrmecochory), Giladi 2006; Ness et al. 2009; Prior et al. 2015). Most myr- which, especially in eastern North America, is a widespread mecochory studies measure only the rate of seed removal or mutualistic interaction (Beattie and Culver 1981; Handel quantity of dispersal from depots by diferent ant species, et al. 1981). Generally, seed-dispersing ants pick up seeds because the small size of ants and the seeds which they carry with nutrient-rich food bodies (elaiosomes) attached, bring makes them difcult to track (Canner and Spence 2011). them to their nests (primary dispersal), remove and feed Diferences in seed removal rates between ant species are the elaiosomes to their larvae, and fnally deposit seeds in a often attributed to diferences in ant or seed size, because midden (secondary dispersal) (Gorb and Gorb 2003; Giladi small ants are unlikely to move large seeds (e.g., Christian 2006). Worldwide, the seeds of an estimated 11,000 plant 2001; Ness et al. 2004). However, the quality of seed dis- species have elaiosomes (i.e., are myrmecochores) (Lengyel persal also varies among ant species, including the length et al. 2009), and in the deciduous forests of northeastern of time which a seed remains within an ant nest (Prior et al. North America, as many as 30% of herbaceous plants have 2014), the distance seeds are dispersed (Ness et al. 2004; seeds with elaiosomes (Beattie and Culver 1981; Handel Leal et al. 2014a), and deposition location (Gorb et al. 2000), et al. 1981). In eastern North America, members of this all of which can afect plant ftness. In eastern North Ameri- diverse plant guild have their seeds dispersed primarily by can forests, myrmecochorous plants have historically been (a) Removal (b) Deposition (c) Germination (d) Survival (2012) (2012) (2013) (2014) Removes fewer seeds A. rudis strong Native ant Seeds close together Plant Plant Ant traits Competition Competition Removes more seeds strong M. rubra Invasive ant Seeds far apart Prior et al.2014, 2015 This study Prior et al.2015 This study Fig. 1 Conceptual illustration of the mechanisms afecting the seed suggest that A. rudis deposited seeds in a clumped pattern closer to dispersal process in our experimental mesocosms. For both ants and their nests, while M. rubra spread seeds out around mesocosms. Rep- plants, native and invasive species are represented by black and red resentative A. rudis and M. rubra mesocosms show seedling loca- cartoons, respectively. Colored boxes represent mechanistic flters tions. c More seedlings of the invasive plant, C. majus, germinated in determining diferent stages in the dispersal process—seed deposi- the M. rubra mesocosm than any other plant–ant combination (Prior tion, and seedling germination and establishment. Solid black arrows et al. 2015). The current study shows that that outcome was likely show a positive efect of the mechanistic flters, while dashed arrows a result of a combination of strong parent–ofspring competition in show a negative efect. Gray arrows indicate no signifcant efect. C. majus and M. rubra moving seeds farther away from the parent a Variation in ant traits such as colony size, foraging rate, and seed plants. d Here, we show that for seedlings of all species, survival handling time afected how many seeds each ant species initially was negatively afected by the distance to the nearest C. majus plant. removed. The invasive ant, M. rubra, removed more seeds overall Native plants also grew taller when they were dispersed farther from regardless of plant species (Prior et al. 2014, 2015). b Although we C. majus. Distance to the nearest native plant did not afect seedling did not directly measure seed deposition location, seedling locations survival (color fgure online) 1 3 Oecologia most likely to interact with A. rudis (Ness et al. 2009), but ant species that best meet their dispersal needs, and plant with the recent introduction of ant species around the globe species may also be afected diferently by changes in ant (McGlynn 1999; Suarez et al. 2010; Wetterer and Radchenko community composition. 2011), ant-dispersed plants are increasingly likely to also In this study, we investigated how four myrmecochorous interact with diferent ant species, including invasive ants. plant species with two different life-history strategies There are about 200 introduced ant species globally respond to dispersal by two ant species, A. rudis or M. rubra. (Holway et al. 2002), and several are known to change the These two species belong to the same behavioral seed-dis- outcome of myrmecochory in their introduced ranges (e.g., persing guild, but vary in traits related to seed dispersal. Ness and Bronstein 2004; Stuble et al. 2009; Rodriguez- Three common myrmecochores native to our study region, Cabal et al. 2011). The invasive ants that have been well Anemone acutiloba L.
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