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Journal ArticleDOI

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

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.
Abstract: Myrmecochory (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.

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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.

58 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.

31 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.

28 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.

24 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.

17 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
TL;DR: It is shown that distance dispersal is likely to be a benefit of myrmecochory throughout Australia, independent of any targeting of seeds to ant nests, and influenced strongly by nest density and dispersion, population size and territoriality of seed-dispersing ants.
Abstract: Nutrient-enrichment and predator avoidance are generally considered the major benefits of myrmecochory, but this is apparently not so in Australia where some of the greatest known concentrations of myrmecochorus plants occur. Here I demonstrate that distance dispersal is a potential benefit of myrmecochory in the Australian environment. Although mean dispersal distance at a site in southeastern Australia was only 2.1 m, the dispersal curve was characterised by a narrow peak and long tail. A dispersal curve of this shape has been shown by Green (1983) to be optimal when safe sites for seedling establishment are rare, as is typically the case for Australian myrmecochores in the absence of fire. Both mean disperal distance and shape of the dispersal curve are influenced strongly by nest density and dispersion, population size, and territoriality of seed-dispersing ants. I argue that distance dispersal is likely to be a benefit of myrmecochory throughout Australia, independent of any targeting of seeds to ant nests.

132 citations


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

  • ...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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  • ...The distance dispersal hypothesis proposes that seed dispersal reduces competition between parents and offspring, as well as among siblings (Andersen, 1988; Giladi, 2006)....

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Journal ArticleDOI
01 Dec 2009-Oikos
TL;DR: The meta-analysis demonstrated that A. rudis is the primary seed dispersal vector for most of this rich temperate ant-dispersed flora, and the low levels of plant partner diversity for myrmecochores demonstrated here rivals that of tropical ant-plants (myrmecophytes) and well exceeds that typically observed in temperate plant-frugivore and plant-pollinator mutualisms and myRMecochory in other biomes.
Abstract: Ant-dispersed herbs (myrmecochores) can account for more than one-third of the stems in the temperate deciduous forests of eastern North America. Because many ant species have been observed collecting the seeds, this interaction is often described as a generalized mutualism. Here, we combine fieldwork and meta-analyses to test this assumption. Our meta-analysis demonstrated that Aphaenogaster ants (predominantly A. rudis) collect approximately 74±26% (mean± SD) of the myrmecochorous seeds in eastern North American forests where any encounters with Aphaenogaster were reported, and approximately 61 ±37% of the seeds in all the eastern forests where any seed collection has been monitored. This remarkable monopolization of seeds is due to at least two factors: 1) Aphaenogaster are significantly more likely to collect the ant-adapted seeds they discover than are ten other ant genera found in these forests and 2) the densities of Aphaenogaster and myrmecochorous plants are positively correlated at three nested spatial scales (within 20 x 20 m patches, among patches within a forest, and among 41 forests in the eastern United States). Although other ants can collect seeds, our analyses demonstrate that A. rudis is the primary seed dispersal vector for most of this rich temperate ant-dispersed flora. The low levels of plant partner diversity for myrmecochores demonstrated here rivals that of tropical ant-plants (myrmecophytes) and well exceeds that typically observed in temperate plant-frugivore and plant-pollinator mutualisms and myrmecochory in other biomes.

126 citations


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

  • ...The density of A. rudis nests in eastern North American forests is estimated to be greater than 1 colony per meter2 in suitable habitat (see references in Ness et al., 2009)....

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  • ...A. rudis is a keystone mutualist (Ness et al., 2009; Zelikova et al., 2008) on which many understory herb species exclusively or nearly exclusively depend for seed dispersal....

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  • ...We assume that a fraction p1 of seeds undergo primary dispersal by ants and fix p1 at 74%, which is the average removal rate for A. rudis when A. rudis is present (Ness et al., 2009)....

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  • ...We simulated dispersal in two dimensions, with the direction of dispersal drawn from a uniform distribution on (0, 2p) at each dispersal step, with probability of initial ant dispersal, p1 ¼ 0.74 (Ness et al., 2009) and probability of redispersal, p2 ¼ 0.93 (data herein)....

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  • ...We also explored how changes in A. rudis density affect population spread rate by varying the removal rate p1, because the removal rate of seeds depends on both the presence and abundance of A. rudis (Ness et al., 2009; Zelikova et al., 2008; Warren et al., 2010)....

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Journal ArticleDOI
J. Smallwood1
TL;DR: It was found that ant colony movement is a common phenomenon that frequently occurs in species that represent a variety of taxonomic groups and in a wide range of habitats.
Abstract: Ant nest relocation was studied in a decidous forest in the eastern U.S. Nests were located by tuna baiting and were re-checked every 2–3 weeks for continued occupation or desertion by the colonies. Nest half lives for four species were calculated and varied from 12.9 days forTapinoma sessile to 89.9 days forFormica subsericea.

111 citations


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

  • ...The seed-dispersing ant species in the European temperate forest habitats (generally Formica spp.) have nutrient-rich, long-term (often many-year) nest sites (Culver and Beattie, 1980; Gorb et al., 2000; Gorb and Gorb, 2003; Smallwood, 1982a)....

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  • ...A. rudis hibernate underground until early spring, emerge, move the entire colony to temporary dwellings within the leaf litter, and then seek more established nest sites (Talbot, 1951; Smallwood, 1982b)....

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  • ...Perhaps seeds tend to be redispersed to sunnier areas on the forest floor near the nest (Smallwood, 1982b) or scattered throughout the litter layer (Gonzalez, 1972)....

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  • ...If a colony moved (n ¼ 3; a common occurrence for A. rudis; see Culver and Beattie, 1978; Smallwood, 1982a, b), we marked the new nest location of any colony that contained tagged seeds, but we measured redispersal distance from the original location of the nest....

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  • ...The keystone disperser in eastern North American forests, A. rudis, has temporary (mean 20 days) nest locations (Culver and Beattie, 1978; Smallwood, 1982a, b) and redisperses a majority of seeds outside the nest into the surrounding leaf litter (data herein)....

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Journal ArticleDOI
TL;DR: It is suggested the relocation to Myrmica nests, rich in phosphorus, potassium and nitrogen, may result in greater survivorship of seedlings, and the hypothesis that relocation of ant-dispersed seeds into ant nests may be advantageous to the plant species involved is suggested.
Abstract: Nests of Myrmica discontinua and Formica canadensis from meadows in the vicinity of the Rocky Mountain Biological Laboratory, Colorado, USA were analysed for fifteen plant macronutrients, micronutrients and heavy metals. Nest samples were compared with control samples taken from surrounding soils. Principal components analysis and discriminant function analysis show that the nest chemistry of F. canadensis differs significantly from that of M. discontinua. Also, nest chemistry differs from that of the surrounding soils. Both kinds of nests contain elevated levels of phosphorus relative to adjacent soils, but F. canadensis nests may be deficient in the micronutrients zinc, iron and manganese. On the other hand, the nests of M. discontinua are also richer in ammonium and percent organic matter. These results are discussed with respect to the hypothesis that relocation of ant-dispersed seeds into ant nests may be advantageous to the plant species involved. It is suggested the relocation to Myrmica nests, rich in phosphorus, potassium and nitrogen, may result in greater survivorship of seedlings.

110 citations


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

  • ...” 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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  • ..., 2000; Gorb and Gorb, 2003) and for the few myrmecochore species in the western North American meadows (Beattie and Culver, 1983; Hanzawa et al., 1988)....

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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…...

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  • ...…1988; Giladi, 2006), an effect often cited as a primary benefit to plants in European temperate forests (Culver and Beattie, 1980; Gorb et al., 2000; Gorb and Gorb, 2003) and for the few myrmecochore species in the western North American meadows (Beattie and Culver, 1983; Hanzawa et al., 1988)....

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Journal ArticleDOI
TL;DR: As has been observed for some other clonal plant species, few costs were found for either sexual or asexual reproduction and Asarum canadense appears to be under unusually strong selection for seedling survival.
Abstract: 1 We report the results from a 7-year study on the patterns of reproduction and vegetative spread of Asarum canadense, conducted in replicate plots located in the understorey of early and late successional forest. 2 We recorded the spatial location, size, demographic performance and clonal fragment identity of all A. canadense ramets in our plots, as well as the position and fate of seedling recuits. We also collected detailed morphological data on patterns of clonal growth. 3 Recently germinated plants and the much larger, clonally produced daughter ramets had equal survivorship. Size also had little impact on rhizome production. Within sets of genetically identical ramets, flowering ramets were larger than non-flowering ramets. When there was an effect of habitat, ramets performed best in late successional forest. 4 Neither sexual nor asexual reproduction decreased the future performance of a ramet. Having connections to other ramets had little effect on survivorship or rhizome production, but often was associated with an increased probability of flowering. Clones with more ramets outperformed smaller clones and spread the risk of genet mortality. 5 Rhizome lengths were shorter in the high light, early successional forest, but no other clonal growth parameters differed between habitats. Empirically calibrated simulation and diffusion models indicated that the between-habitat differences in rhizome length were not great enough to affect the long-term expansion of clones. 6 Diffusion coefficients for the long-term spread by clonal growth or seed dispersal were compared for a number of species. Diffusion model results indicated that plants can disperse as far by clonal growth as they do by seed, although the values for A. canadense were 14 and 8895 cm2 year -1, respectively. 7 Asarum canadense appears to be under unusually strong selection for seedling survival. As has been observed for some other clonal plant species, few costs were found for either sexual or asexual reproduction.

109 citations


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

  • ...canadense (Canadian wild ginger) is a small, evergreen, herbaceous perennial, common in deciduous and occasionally mixed forests in eastern North America as far south as North Carolina and north into Canada (Cain and Damman, 1997; Heithaus, 1986; Offer, 1992)....

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  • ...Reproduction occurs through seed production, with approximately 10e30 seeds per reproductive plant, and clonal reproduction (Cain and Damman, 1997; Offer, 1992)....

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  • ...Life history stages were classified by Cain and Damman (1997) as seedling, yearling, lateral shoot (reproductive), and mature ramets (reproductive) (Table B.1, Appendix B)....

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  • ...A. canadense (Canadian wild ginger) is a small, evergreen, herbaceous perennial, common in deciduous and occasionally mixed forests in eastern North America as far south as North Carolina and north into Canada (Cain and Damman, 1997; Heithaus, 1986; Offer, 1992)....

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