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Journal ArticleDOI

Redispersal of seeds by a keystone ant augments the spread of common wildflowers

01 Apr 2012-Acta Oecologica-international Journal of Ecology (Elsevier Masson)-Vol. 40, pp 31-39

TL;DR: A novel seed-tracking technique is used to quantify secondary dispersal of seeds from the nest into the surrounding leaf litter by the keystone seed-dispersing ant, Aphaenogaster rudis, and suggests myrmecochory benefits plants in eastern North American forests by increasing the distance between the seed and parent plant and reducing competition among siblings.

AbstractMyrmecochory (dispersal of seeds by ants) is an evolutionarily and ecologically common mutualism. Most of the research on the costs and benefits of myrmecochory in North America assumes that ant-dispersed seeds are taken to, and left in, the ant nest. Here, we use a novel seed-tracking technique to quantify secondary dispersal of seeds from the nest into the surrounding leaf litter by the keystone seed-dispersing ant, Aphaenogaster rudis. We found that A. rudis redispersed >90% of the seeds it took into its nest an average distance of 51.5 cm. A mathematical model shows redispersal increases the rate of population spread of the myrmecochores Hexastylis arifolia and Asarum canadense by 22.5%, and increases the expected cumulative dispersal distance away from the parent plant by 24%. Our results suggest myrmecochory benefits plants in eastern North American forests by increasing the distance between the seed and parent plant and reducing competition among siblings.

Topics: Myrmecochory (64%), Elaiosome (63%), Biological dispersal (56%), Population (51%), Hexastylis (50%)

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Citations
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Journal ArticleDOI
TL;DR: It is shown that strongly interacting introduced mutualism-related traits between native and invasive species however, can exacerbate the spread of invasive species (‘invasional meltdown’) if invasive partners strongly interact.
Abstract: 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.

46 citations


Journal ArticleDOI
11 Mar 2014-PeerJ
TL;DR: The results suggest that while temperature may play a role in regulating seed removal by ants, ant plant seed-dispersal mutualisms may be more robust to climate change than currently assumed.
Abstract: Climate change affects communities both directly and indirectly via changes in interspecific interactions. One such interaction that may be altered under climate change is the ant-plant seed dispersal mutualism common in deciduous forests of eastern North America. As climatic warming alters the abundance and activity levels of ants, the potential exists for shifts in rates of ant-mediated seed dispersal. We used an experimental temperature manipulation at two sites in the eastern US (Harvard Forest in Massachusetts and Duke Forest in North Carolina) to examine the potential impacts of climatic warming on overall rates of seed dispersal (using Asarum canadense seeds) as well as species-specific rates of seed dispersal at the Duke Forest site. We also examined the relationship between ant critical thermal maxima (CTmax) and the mean seed removal temperature for each ant species. We found that seed removal rates did not change as a result of experimental warming at either study site, nor were there any changes in species-specific rates of seed dispersal. There was, however, a positive relationship between CTmax and mean seed removal temperature, whereby species with higher CTmax removed more seeds at hotter temperatures. The temperature at which seeds were removed was influenced by experimental warming as well as diurnal and day-to-day fluctuations in temperature. Taken together, our results suggest that while temperature may play a role in regulating seed removal by ants, ant plant seed-dispersal mutualisms may be more robust to climate change than currently assumed.

27 citations


Cites background from "Redispersal of seeds by a keystone ..."

  • ...rudis is a keystone mutualist in this and other systems, responsible for the majority of ant-mediated seed dispersal (Zelikova, Dunn & Sanders, 2008; Ness, Morin & Giladi, 2009; Canner et al., 2012)....

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  • ...…PrePrints | https://peerj.com/preprints/137v2/ | v2 received: 13 Dec 2013, published: 13 Dec 2013, doi: 10.7287/peerj.preprints.137v2 P re P ri n ts 11 and other systems, responsible for the majority of ant-mediated seed dispersal (Zelikova et al. 226 2008, Ness et al. 2009, Canner et al. 2012)....

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Journal ArticleDOI
TL;DR: Handling by ants may be a benefit of myrmecochory and favourable nest conditions may enhance emergence, and functional differences in ant species may result in different outcomes for plant partners.
Abstract: Myrmecochory, or ant-mediated seed dispersal, is an important ecological interaction in which ants benefit by gaining nutrition from lipid-rich elaiosomes attached to seeds and plants benefit from having their seeds dispersed away from parent plants. Most research on the benefits of myrmecochory focuses on primary dispersal, in which ants move seeds to nests, or secondary dispersal, in which ants deposit intact seeds in middens after consuming elaiosomes. Less is known about how ants handle seeds inside nests and if handling influences plant fitness. The seed handling behaviours of a native ‘keystone disperser’, Aphaenogaster rudis s.l., and an invasive seed-disperser, Myrmica rubra L., on an introduced herb, Chelidonium majus L., were compared. We conducted a greenhouse experiment to test if handling by ants, manual removal of elaiosomes, or no handling (controls) influenced seedling emergence. Colony-level differences in handling behaviours and plant responses were also examined. Aphaenogaster rudis retained seeds inside nests longer than M. rubra, but there was no difference in the amount of elaiosome removed by the two species. There was no difference in the proportion of seedlings that emerged among treatments, but seedlings emerged earlier when handled by A. rudis. Additionally, more seedlings emerged and seedlings emerged earlier the longer seeds were retained inside ant nests. This study suggests that handling by ants may be a benefit of myrmecochory. This is probably not due to elaiosome removal; rather favourable nest conditions may enhance emergence. Also, functional differences in ant species may result in different outcomes for plant partners.

22 citations


Cites background from "Redispersal of seeds by a keystone ..."

  • ...For example, Servigne and Detrain (2010) found that M. rubra removed the majority of seeds of C. majus from artificial nests within 6 h of picking up seeds, whereas Canner et al. (2012) found 6.8% of seeds remained in nests 7 days after seeds were fed to A. rudis colonies in the field....

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  • ...…Florida, 32611, U.S.A. E-mail: priorkm@gmail.com their nests (primary dispersal), remove and feed elaiosomes to larvae inside nests (handling), and then deposit intact seeds in middens inside or outside of nests (secondary dispersal) (Giladi, 2006; Servigne & Detrain, 2010; Canner et al., 2012)....

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  • ...Both of these species secondarily disperse seeds outside their nests in waste piles or middens (Servigne & Detrain, 2010; Canner et al., 2012)....

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Journal ArticleDOI
TL;DR: It is shown that myrmecochory can involve more than one dispersal phase and that fire indirectly influences myrmicochory by altering the abundances of seed-dispersing ants.
Abstract: Seed dispersal by ants (myrmecochory) can be influenced by changes to ant assemblages resulting from habitat disturbance as well as by differences in disperser behaviour. We investigated the effect of habitat disturbance by fire on the dispersal of seeds of a myrmecochorous shrub, Pultenaea daphnoides. We also investigated the consequence of the seed relocation behaviours of two common dispersers (Pheidole sp. A and Rhytidoponera metallica) for the redispersal of seeds. Pheidole sp. A colonies did not relocate seeds outside their nests. In contrast, R. metallica colonies relocated 43.6 % of seeds fed to them, of which 96.9 % had residual elaiosome that remained attached. On average, R. metallica relocated seeds 78.9 and 60.7 cm from the nest entrances in burned and unburned habitat, respectively. Seeds were removed faster in burned than in unburned habitat, and seeds previously relocated by R. metallica were removed at similar rates to seeds with intact elaiosomes, but faster than seeds with detached elaiosomes. Dispersal distances were not significantly different between burned (51.3 cm) and unburned (70.9 cm) habitat or between seeds with different elaiosome conditions. Differences between habitat types in the frequency of seed removal, the shape of the seed dispersal curve, and the relative contribution of R. metallica and Pheidole sp. A to seed dispersal were largely due to the effect of recent fire on the abundance of Pheidole sp. A. Across habitat types, the number of seeds removed from depots and during dispersal trials most strongly related to the combined abundances of R. metallica and Pheidole. Our findings show that myrmecochory can involve more than one dispersal phase and that fire indirectly influences myrmecochory by altering the abundances of seed-dispersing ants.

21 citations


Cites background from "Redispersal of seeds by a keystone ..."

  • ...Seed relocation by ants has received little attention, despite the important implications it can have for the distribution and fate of myrmecochorous seeds (Hughes and Westoby 1992a; Gorb and Gorb 2003; Canner et al. 2012)....

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  • ...…and Detrain 2010), while seeds taken out of nests can be placed on nest mounds (e.g. Davidson and Morton 1981), or relocated to sites some distance away from nest entrances (Berg 1975; Kjellsson 1985; Hughes and Westoby 1992a; Gorb and Gorb 2003; Lubertazzi et al. 2010; Canner et al. 2012)....

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  • ...For example, seed relocation removes seeds from the nest negating any benefits provided by the nest environment (Canner et al. 2012), and may re-expose seeds to risks associated with being on the soil surface (Gomez and Espadaler 1998b)....

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  • ...In addition, seeds discarded from nests often have their elaiosomes removed (Hughes and Westoby 1992a; Gorb and Gorb 2003; Canner et al. 2012), although some ant species discard seeds that still have residual elaiosome attached (Berg 1975; Lopez-Vila and Garcia-Fayos 2005; Servigne and Detrain…...

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  • ...However, seed relocation represents a secondary phase of dispersal (Gorb and Gorb 2003; Canner et al. 2012) and may also facilitate the subsequent redispersal of seeds to other ant nests (Hughes and Westoby 1992a)....

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Journal ArticleDOI
TL;DR: Investigating the extent to which dispersal services by ants are influenced by anthropogenic disturbances associated with roadwork activities in southern NSW, Australia shows that myrmecochory is an unevenly diffuse mutualism, where few ant species contributed to much of the dispersal of seeds.
Abstract: Ants provide a common dispersal vector for a variety of plants in many environments through a process known as myrmecochory. The efficacy of this dispersal mechanism can largely determine the ability of species to track changes in habitat availability caused by ongoing land-use and associated disturbances, and can be critical for population gene flow and persistence. Field studies were conducted in a typical fragmented agricultural landscape in southern NSW, Australia, to investigate the extent to which dispersal services by ants are influenced by anthropogenic disturbances associated with roadwork activities (i.e. soil disturbance as the result of grading of roads). Observational experiments were performed in road segments that were divided into disturbed and non-disturbed zones, where Acacia pycnantha seeds were offered at multiple bait stations and monitored. For combined species, the mean dispersal distance recorded in the disturbed zone (12.2m) was almost double that recorded in the non-disturbed zone (5.4m) for all roadside sites. Our findings show that myrmecochory is an unevenly diffuse mutualism, where few ant species contributed to much of the dispersal of seeds. Iridomyrmex purpureus was responsible for all seed dispersal distances > 17m, where a maximum of 120m in disturbed, versus 69m in non-disturbed zones, was recorded. Rhytidoponera metallica and Melophorus bruneus were important seed dispersers in non-disturbed and disturbed zones, respectively. In general, large bodied ants tended to move more seeds to longer distances in disturbed zones, as opposed to non-disturbed zones, where smaller bodied species carried out a greater percentage of short distance dispersals (< 1m). We also recorded secondary dispersal events from nests by I. purpureus, a phenomenon previously not quantified. Infrequent, long distance dispersal to suitable sites may be highly important for seedling recruitment in disturbed or modified habitats in otherwise highly fragmented rural environments.

15 citations


Cites background from "Redispersal of seeds by a keystone ..."

  • ...Ants may remove discarded seeds to nearby rubbish heaps (Berg, 1975) or be relocated further distances away from nest entrances (Hughes and Westoby, 1992; Lubertazzi et al., 2010; Canner et al., 2012)....

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  • ...On most occasions, the elaiosome of the discarded seed is removed (Hughes and Westoby, 1992; Canner et al., 2012), which assists with breaking seed dormancy and influence subsequent germination success of species (Pacini, 1990; Lobstein and Rockwood, 1993)....

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References
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Journal ArticleDOI
01 Jun 2000-Ecology
TL;DR: A discrete-time model for biological invasions is constructed that couples matrix population models (for population growth) with integrodifference equa- tions (for dispersal), and it is found that, when dispersal contains both long- and short-distance components, it is the long-distance component that governs the invasion speed-even when long- distance dispersal is rare.
Abstract: A fundamental characteristic of any biological invasion is the speed at which the geographic range of the population expands. This invasion speed is determined by both population growth and dispersal. We construct a discrete-time model for biological invasions that couples matrix population models (for population growth) with integrodifference equa- tions (for dispersal). This model captures the important facts that individuals differ both in their vital rates and in their dispersal abilities, and that these differences are often determined by age, size, or developmental stage. For an important class of these equations, we demonstrate how to calculate the population's asymptotic invasion speed. We also derive formulas for the sensitivity and elasticity of the invasion speed to changes in demographic and dispersal parameters. These results are directly comparable to the familiar sensitivity and elasticity of population growth rate. We present illustrative examples, using published data on two plants: teasel (Dipsacus sylvestris) and Calathea ovandensis. Sensitivity and elasticity of invasion speed is highly correlated with the sensitivity and elasticity of pop- ulation growth rate in both populations. We also find that, when dispersal contains both long- and short-distance components, it is the long-distance component that governs the invasion speed-even when long-distance dispersal is rare.

620 citations


"Redispersal of seeds by a keystone ..." refers background or methods in this paper

  • ...…B for the myrmecochore and the movement matrix K(x,y) for seed dispersal to find the population density for each stage at location x at time t þ 1: nðx; t þ 1Þ ¼ ZN N ½Kðx; yÞ+B nðy; tÞdy; (A.1) where stands for the Hadamard product (element by element multiplication) (Neubert and Caswell, 2000)....

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  • ...…distribution, then the population has a traveling wave front of a fixed shape that moves at a constant rate, c. Based on these assumptions, Neubert and Caswell (2000), (Appendix A) show that the upper bound on the invasion wave speed, c*, is c* ¼ min s>0 1 s lnrðsÞ ; (A.2) where r(s) is…...

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  • ...To compare population spread rate both with and without redispersal, we used a spatially explicit model of stagestructured population dynamics (Neubert and Caswell, 2000)....

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  • ...where stands for the Hadamard product (element by element multiplication) (Neubert and Caswell, 2000)....

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Journal ArticleDOI
Abstract: The distribution of many woodland herbs extends 1000-2000 km in a north- south direction, yet the majority of these species grow clonally, have little recruitment by seed, and possess no obvious mechanism for long-distance seed dispersal. Although aware that woodland herbs disperse poorly, ecologists have tacitly assumed that, given long periods of time, even small dispersal distances would allow woodland herbs to colonize the vast geographic region they now occupy. We examined this assumption for the understory herb Asarum canadense. To estimate long-term rates of spread by seed, we calibrated seed- dispersal diffusion models with life history data and with data on seed carries by ants. We supplemented our field observations and modeling results forA. canadensewith a literature survey on the dispersal capabilities of other plant species. Ants transported A. canadense seeds up to 35 m, the largest distance ants are known to move the seeds of any woodland herb. Empirically calibrated diffusion models indicated that over the last 16 000 yr A. canadense should only have traveled 10-11 km from its glacial refugia. In actuality, A. canadense moved hundreds of kilometers during this time. Models that examined the tail of A. canadense's seed-dispersal curve indicated that oc- casional dispersal events had to have a high frequency ($0.001 on a per seed basis) and a large magnitude (dispersal distance .1 km) for A. canadense to have traveled over 200 km in 16 000 yr. The literature survey showed that most woodland herbs and many other forest, desert, coastal, and open-habitat plant species have limited seed-dispersal capabil- ities, similar to those in A. canadense. We conclude that woodland herbs, as well as many other plants, disperse so slowly that there is no documented mechanism by which most of these species could have reached their present geographical range since the last glacial maximum. This suggests that occasional events leading to long-distance dispersal dominate the Holocene colonization of northern temperate forest by woodland herbs, and this, in turn, has implications for issues ranging from the importance of genetic analyses to the structure of metapopulation models.

351 citations


"Redispersal of seeds by a keystone ..." refers background in this paper

  • ...With our addition of redispersal to the model, the population spread rate that we estimate is still small and falls short of the post-glaciation migration rates necessary to account for current myrmecochore ranges in eastern North America (Cain et al., 1998; Vellend et al., 2003)....

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01 Jan 2004
TL;DR: It is concluded that white-tailed deer represent a significant and previously unappreciated vector of seed dispersal across the North American landscape, probably contributing an important long-distance component to the seed shadows of hundreds of plant species, and providing a mechanism to help explain rapid rates of plant migration.

272 citations


"Redispersal of seeds by a keystone ..." refers background in this paper

  • ...The discrepancy may occur due to the omission from our model of rare, long-distance dispersal events by other ant species or vertebrates that may account for dispersal at a continental scale (Myers et al., 2004; Vellend et al., 2003)....

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Journal ArticleDOI
TL;DR: There was no evidence of specialization of particular ant species on particular Viola species, and the advantage of ant dispersal is relocation to a 'safe site' for germination, thus reducing predation, increasing germination stimuli, and increasing the available supply of nutrients.
Abstract: SUMMARY (1) The interactions of ants and diplochorous Viola seeds were studied at four forest and forest-edge sites in Monongahela National Forest, West Virginia. Of the nine Viola species studied, seeds of six (V. blanda, V. papilionacea, V. pedata, V. pensylvanica, V. rostrata and V. triloba) were readily taken. (2) The most important seed transporters were Aphaenogaster spp., but Formica subsericea, Lasius alienus, Leptothorax spp., Myrmica punctiventris and Tapinoma sessile also took seeds. Unlike the situation in Europe, ants of the Formica rufa group displayed little interest in Viola seeds. There was no evidence of specialization of particular ant species on particular Viola species. (3) Cleistogamous seeds were taken much less frequently than chasmogamous seeds, even though cleistogamous seeds had larger elaiosomes. This difference is apparently due to diet shifts of the ants in summer. (4) Most seeds picked up by ants were carried to the nest. The distances seeds were moved averaged about 75 cm, which is less than the average ballistic dispersal distance. (5) The advantage of ant dispersal is relocation to a 'safe site' for germination, thus reducing predation, increasing germination stimuli, and increasing the available supply of nutrients.

266 citations


"Redispersal of seeds by a keystone ..." refers background in this paper

  • ...They are also the most frequently cited seed-dispersing species in eastern North America (Beattie and Culver, 1981; Culver and Beattie, 1978; Heithaus, 1981; Gaddy, 1986; Warren et al., 2010; Zelikova et al., 2008) and considered the keystone seed disperser of myrmecochores in eastern North America (Ness et al....

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  • ...” For example, dispersal into ant nests may provide a nutrient-rich environment that increases plant fitness and survivorship (Beattie and Culver, 1983; Culver and Beattie, 1978; Hanzawa et al., 1988; Giladi, 2006), an effect often cited as a primary benefit to plants in European temperate forests (Culver and Beattie, 1980; Gorb et al....

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  • ...All rights reserved. parent (e.g., Andersen, 1988), reduction in seed predation due to dispersal (e.g., Culver and Beattie, 1978; Heithaus, 1981) and movement of the seed to a favorable germination site (e.g., Beattie and Culver, 1983; Hanzawa et al., 1988)....

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  • ...Several studies show that simply the handling of the seeds by ants has a positive effect on germination rates (Culver and Beattie, 1978, 1980) and redispersal is beneficial in European systems (Gorb et al., 2000)....

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  • ...They are also the most frequently cited seed-dispersing species in eastern North America (Beattie and Culver, 1981; Culver and Beattie, 1978; Heithaus, 1981; Gaddy, 1986; Warren et al., 2010; Zelikova et al., 2008) and considered the keystone seed disperser of myrmecochores in eastern North America…...

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Journal ArticleDOI
Abstract: For many plant species in eastern North America, short observed seed dispersal distances (ranging up to a few tens of meters) fail to explain rapid rates of invasion and migration. This discrepancy points to a substantial gap in our knowledge of the mechanisms by which seeds are dispersed long distances. We investigated the potential for white-tailed deer (Odocoileus virginianus Zimm.), the dominant large herbivore in much of eastern North America, to disperse seeds via endozoochory. This is the first comprehensive study of seed dispersal by white-tailed deer, despite a vast body of research on other aspects of their ecology. More than 70 plant species germinated from deer feces collected over a 1-year period in central New York State, USA. Viable seeds included native and alien herbs, shrubs, and trees, including several invasive introduced species, from the full range of habitat types in the local flora. A mean of >30 seeds germinated per fecal pellet group, and seeds were dispersed during all months of the year. A wide variety of presumed dispersal modes were represented (endo- and exozoochory, wind, ballistic, ant, and unassisted). The majority were species with small-seeded fruits having no obvious adaptations for dispersal, underscoring the difficulty of inferring dispersal ability from diaspore morphology. Due to their broad diet, wide-ranging movements, and relatively long gut retention times, white-tailed deer have tremendous potential for effecting long-distance seed dispersal via ingestion and defecation. We conclude that white-tailed deer represent a significant and previously unappreciated vector of seed dispersal across the North American landscape, probably contributing an important long-distance component to the seed shadows of hundreds of plant species, and providing a mechanism to help explain rapid rates of plant migration.

264 citations