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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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BookDOI
01 Jan 2003
TL;DR: The myrmecochorous syndrome is a major explanatory factor in the decline in the ability of ants to remove diaspores from ant nests and the dispersal systems used for this removal are poorly understood.
Abstract: Introduction: an historical background.- 1. The myrmecochorous syndrome.- 2. Diaspore removal by ants.- 3. Factors influencing diaspore removal.- 4. Effect of the ant species complex on diaspore removal.- 5. Diaspore transporting by ants.- 6. Seed flow in ant territories.- 7. Secondary relocation of diaspores from ant nests.- 8. Comparative analysis of plant dispersal systems by ants: diaspore concentration and redistribution.- 9. Ecological implications of myrmecochory.- 10. Interactions between ants and non-myrmecochorous plants.- 11. Methods for studying myrmecochory.- Conclusions and outlook.- References.

102 citations


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

  • ..., 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....

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  • ...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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  • ...In these studies, understory herbs experience reduced competition and densitydependent effects at relatively short distances from the parent (and each other) due to ant dispersal (Heithaus, 1986; Higashi et al., 1989; Kalisz et al., 1999; Giladi, 2006; Gorb and Gorb, 2003)....

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  • ...) 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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  • ...…(Heithaus, 1986) for Sanguinaria canadensis seeds by A. rudis, but we provide the first documentation of the extent of redispersal and its consequences for spatial population dynamics in eastern North American forests (though there are many examples in European forests; see Gorb and Gorb, 2003)....

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Journal ArticleDOI
TL;DR: It was found that seed removals decreased with elevation, but seed dispersal distance did not depend on elevation, and was dominated by one species, A. rudis, which occurred at every site and removed the vast majority of all observed seeds in this study.
Abstract: Seed dispersal by ants is ecologically important and geographically widespread as 20-50% of all herbaceous species in eastern deciduous forests are dispersed by ants, but we know little about how or why such interactions vary geographically. In this paper, we examined variation in seed dispersal by ants along an extensive elevational gradient (256-2025 m) in the Great Smoky Mountains National Park, USA. Specifically, we asked whether variation in ant community composition affected seed removals and seed dispersal distance of Trillium undulatum and Hexastylis arifolia, two common understory herbs found throughout the southern Appalachian Mountains. We also examined variation in myrmecochore abundance, specifically Trillium spp. and H. arifolia, along the same elevational gradient. Measures of ant community and climate variables strongly covaried with elevation, while Trillium species richness and abundance did not. We found that seed removals decreased with elevation, but seed dispersal distance did not depend on elevation. The most impor- tant variables predicting seed removals were average annual temperature and the abundance of Aphaenogaster rudis, both of which varied along the elevational gradient. Seed dispersal by ants did not depend on ant community composition, but was dominated by one species, A. rudis, which occurred at every site and removed the vast majority of all observed seeds in this study. Though the ant fauna in the Great Smoky Mountains National Park is diverse, dispersal of T. undulatum and H. arifolia, and likely other myrmecochores, is driven by one ant species, A. rudis.

81 citations

Journal ArticleDOI
01 Mar 1989-Oikos
TL;DR: The relatively short-distance dispersal of T. tschonoskii seeds by ants is sufficient to reduce seedling mortality, by reducing competition between seedlings; and that this is the primary advantage of myrmecochory in this species.
Abstract: Trillium tschonoskii Maxim. is a myrmecochorous perennial herb which grows in single-species stands in the cool temperate broad-leaved deciduous woodland of Hokkaido, northern Japan. Its many-seeded fruit initially falls close to the parent, over 50% within 20 cm. Ants, principally Myrmica ruginodis and Aphaenogaster japonica, transport seeds to their nests, a mean distance of 64 cm. The nests are overdispersed and short-lived, and are no richer in nitrogen or phosphorus than surrounding soils. There are proportionally more older (3-leaved) than younger (1-leaved) juvenile Trillium plants at distances > 60 cm from the nearest parent plant than at 0-30 or 30-60 cm. This indicates that the relatively short-distance dispersal of T. tschonoskii seeds by ants is sufficient to reduce seedling mortality, by reducing competition between seedlings; and that this is the primary advantage of myrmecochory in this species. This contrasts with previous studies, involving ant species with longer-lived nests, where the main advantage to the plant is nutrient-enhanced seedling microsites.

81 citations


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

  • ...…have shown that an increase in local seed density decreases the survival and growth of seedlings and adults of H. arifolia (Giladi, 2004; Gonzalez, 1972) as well as for other temperate forest myrmecochores (Culver and Beattie, 1980; Heithaus, 1986; Higashi et al., 1989; Kalisz et al., 1999)....

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  • ...arifolia (Giladi, 2004; Gonzalez, 1972) as well as for other temperate forest myrmecochores (Culver and Beattie, 1980; Heithaus, 1986; Higashi et al., 1989; Kalisz et al., 1999)....

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  • ...In these studies, understory herbs experience reduced competition and densitydependent effects at relatively short distances from the parent (and each other) due to ant dispersal (Heithaus, 1986; Higashi et al., 1989; Kalisz et al., 1999; Giladi, 2006; Gorb and Gorb, 2003)....

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Journal ArticleDOI
01 Feb 1982-Ecology
TL;DR: Field and laboratory experiments were conducted to determine if competition or reduced nest insolation, which acts to reduce internal nest temperature, could act as cues triggering colony emigrations, and the effect of increased food supply and artificial shade on the emigration rate.
Abstract: Aphaenogaster rudis is a common ant in eastern United States forests that exhibits a high rate of colony relocation to new nest sites, even in the absence of nest disturbances. Field and laboratory experiments were conducted to determine if competition or reduced nest insolation, which acts to reduce internal nest temperature, could act as cues triggering colony emigrations. The field experiments tested the effect of increased food supply and artificial shade on the emigration rate. Laboratory experiments tested the effect of increased aggressive encounters with another ant species on emigration rate. Reduction in nest insolation resulted in a dramatic increase in the probability of emigration. Competition resulted in nest relocations only when it involved the invasion of the A. rudis nest site by another ant species. Changes in the amount of available food had no demonstrable effect on the probability of relocation although such changes did affect the intensity and direction of foraging activity. Seasonal trends in emigratory behavior were also observed. Emigration rate in A. rudis reached a maximum in midsummer. Also, the effect of artificially shading nests on emigration rate was the greatest in early summer and significantly less in spring and late summer.

70 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: The hypothesis that the invasive ant Pachycondyla chinensis disrupts ant-seed dispersal mutualisms by displacing native ant species, especially the keystone mutualist Aphaenogaster rudis, while failing to disperse seeds itself is tested.
Abstract: By disrupting the structure of native ant assemblages, invasive ants can have effects across trophic levels Most studies to date, however, have focused on the impacts just two species (Linepithema humile and Solenopsis invicta) The impacts of many other invasive ant species on ecological processes in their introduced range are unknown In this study we tested the hypothesis that the invasive ant Pachy- condyla chinensis disrupts ant-seed dispersal mutu- alisms by displacing native ant species, especially the keystone mutualist Aphaenogaster rudis, while fail- ing to disperse seeds itself In a paired design we measured the impact of P chinensis on the native ant-plant seed dispersal mutualism The number of A rudis workers was 96% lower in invaded than in intact plots, and the number of seeds removed was 70% lower in these plots Finally, in invaded plots the abundance of Hexastylis arifolia, a locally abundant myrmecochorous plant, was 50% lower than in plots where P chinensis was absent A parsimonious interpretation of our results is that P chinensis causes precipitous declines in the abundance of A rudis within invaded communities, thereby dis- rupting the ant-plant seed dispersal mutualisms and reducing abundances of ant-dispersed plants In sum, the magnitude of the effects of P chinensis on seed dispersal is quantitatively similar to that documented for the intensively studied invasive Argentine ant We suggest that more studies on the impacts of less- studied invasive ant species on seed dispersal mutu- alisms may increase our knowledge of the effects of these invaders on ecosystem function

62 citations


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

  • ..., 2011) and invasive species (Rodriguez-Cabal et al., 2011), which may decrease A....

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  • ...…of eastern North American myrmecochores on A. rudis for dispersal may lead to significant effects on the population spread rate of myrmecochores due to the sensitivity of A. rudis to the effects of climate change (Warren et al., 2011) and invasive species (Rodriguez-Cabal et al., 2011)....

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  • ...In addition, the keystone disperser is sensitive to climate change (Warren et al., 2011) and invasive species (Rodriguez-Cabal et al., 2011), which may decrease A. rudis abundance, which will diminish the overall spread rate of myrmecochores, marginalize the effect of redispersal on spread rates,…...

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  • ...rudis abundance, which will diminish the overall spread rate of myrmecochores, marginalize the effect of redispersal on spread rates, and may lead to the decline of the myrmecochore population (Rodriguez-Cabal et al., 2011)....

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  • ...…and invasive species (Rodriguez-Cabal et al., 2011), which may decrease A. rudis abundance, which will diminish the overall spread rate of myrmecochores, marginalize the effect of redispersal on spread rates, and may lead to the decline of the myrmecochore population (Rodriguez-Cabal et al., 2011)....

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