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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: In this article, the authors examine two facets of niche expansion via ant-mediated seed dispersal: (1) increased utilization of resources along resource gradients and (2) escape from unfavourable density-dependent conditions.
Abstract: Summary 1. Whereas classic niche theory is based on the contraction of the niche via negative interactions, facilitative niche theory suggests that mutualisms can expand the niche via positive interactions. Specifically, animal-mediated seed dispersal can expand the utilization of physical space by plants and allow greater access to resources and other environmental requirements. Ant-mediated dispersal of plant propagules (myrmecochory) is a common mutualism throughout the world, particularly in the deciduous forests of the eastern United States where this research is conducted. 2. We examine two facets of niche expansion via ant-mediated seed dispersal: (1) increased utilization of resources along resource gradients and (2) escape from unfavourable density-dependent conditions. 3. We test these assumptions by introducing Hexastylis arifolia seeds in cafeteria-style bait stations along abiotic gradients (moisture, temperature, light) for removal by key seed dispersers from the ant genus Aphaenogaster. We also examine plant aggregation along the same gradients. 4. Ant-mediated dispersal services decrease significantly with increasing soil moisture and ultimately fail at levels that are demonstratively within the plant’s niche optima; further, the decline in dispersal services is correlated with increasing plant aggregation, suggesting that enemy escape also falters at relatively high levels of soil moisture. 5. Synthesis. Facilitated propagule dispersal fails to expand the Hexastylis arifolia niche in either enhanced resource utilization or decreased density dependence as the niche requirements for the ant disperser are nested within those for the plant. The strength of this interaction varies across space and time, and in doing so may undermine attempts to predict future distributions. Further, given that myrmecochores are typically poor dispersers, the incomplete niche overlap between the plant and its facilitator makes this plant guild particularly susceptible to climatic change if each participant responds individually to shifting environmental conditions.

43 citations


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

  • ...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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  • ...…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., 2009)....

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Journal ArticleDOI
01 Dec 1989-Ecology
TL;DR: Two co-occurring deciduous forest myrmecochores, Asarum canadense and Jeffersonia diphylla, release their seeds at approximately the same time, and therefore potentially compete for ants as dispersers, and frequency-dependent dispersal is discussed.
Abstract: Two co-occurring deciduous forest myrmecochores, Asarum canadense and Jeffersonia diphylla, release their seeds at approximately the same time, and therefore potentially compete for ants as dispersers. Within a single woodlot, we placed seeds of both species inside a dense Jeffersonia population away from Asarum plants, inside a dense Asarum population away from Jeffersonia plants, and in a site where plants of neither species occurred. No preference was exhibited by ants where natural populations were absent. Preference at the other two sites was frequency dependent: ants preferred seeds of the introduced species. Species preferred by ants have higher seed and seedling survival because by being carried into ant nests they escape predation and avoid nutrient deficiency. Implications of frequency-dependent dispersal are discussed. rum and Jeffersonia). Both species are spring-flower- ing, clonal, perennial herbs whose seeds are dispersed by several species of ants. Both species release their seeds at approximately the same time in early June. Asarum bears its flowers at ground level. Once ripe, the six-celled capsule dehisces and ants can then begin extracting seeds from it. The fruiting capsule of Jeffer- sonia is borne on a leafless stalk. The top of the capsule functions as a lid formed by a fissure in the ovary wall. At maturity the lid opens and the distal end of the peduncle bends, spilling seeds to the ground. Predation by rodents on seeds within capsules, and after capsule dehiscence, may be quite heavy on both species, and occurs primarily at night (Heithaus 1981, Smith et al. 1986). The seeds of both species bear a fleshy elaiosome. Previous work on other species has shown that elaio- somes are rich in lipids, elicit seed-carrying behavior by ants, and provide a nutritional reward for them

41 citations


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

  • ...at SciVerse ScienceDirect Contents lists available Acta Oecologica journal homepage: www.elsevier .com/locate/actoec Original article Redispersal of seeds by a keystone ant augments the spread of common wildflowers Judith E. Canner a,*, Robert R. Dunn b, Itamar Giladi c, Kevin Gross a aBiomathematics Graduate Program, Department of Statistics, North Carolina State University, Campus Box 8203, Raleigh, NC 27695, USA bDepartment of Biology and Keck Center for Behavioral Biology, North Carolina State University, Campus Box 7617, Raleigh, NC 27695, USA cDepartment of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel a r t i c l e i n f o Article history: Received 22 September 2011 Accepted 20 February 2012 Available online 14 March 2012 Keywords: Redispersal Myrmecochory Aphaenogaster rudis Population spread rate Plant benefits Temperate forest * Corresponding author....

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  • ...We conducted our study of seed redispersal in Lake Raleigh (Quay)Woods, a mixed pine-hardwood forest located onw97 acres of Centennial Campus, North Carolina State University, Raleigh, NC, USA....

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  • ...Flowering begins in late March and early April and fruiting occurs late May and early June in North Carolina (Smith et al., 1989; personal observation)....

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  • ...The seeds of A. canadense are about 3e5 mm in length, narrowly ovate, with an elaiosome running the entire length of the seed, and a mean dry mass of 6.8 mg (mean fresh mass of 14.2 mg) (Smith et al., 1989)....

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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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Journal ArticleDOI
TL;DR: This paper concerns populations of the ant Aphaenogaster rudis Emery studied at St. Charles County, Missouri, during 1947–1949, giving together a year-around picture of their nesting conditions, maturing of brood, and hibernation.
Abstract: This paper concerns populations of the ant Aphaenogaster rudis Emery studied at St. Charles County, Missouri, during 1947–1949. All collections were made in the autumn, winter, and spring, and thus the paper supplements a summer study of Aphaenogaster rudis made by A. E. Headley in northern Ohio (Headley, 1949), giving together a year-around picture of their nesting conditions, maturing of brood, and hibernation.

40 citations


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

  • ...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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  • ...A. rudis nests are small and temporary (Culver and Beattie, 1978; Smallwood, 1982a, 1982b) and are in logs, under rocks, in the leaf litter, or below ground in temperate deciduous forests (Talbot, 1951)....

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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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  • ...rudis nests are small and temporary (Culver and Beattie, 1978; Smallwood, 1982a, 1982b) and are in logs, under rocks, in the leaf litter, or below ground in temperate deciduous forests (Talbot, 1951)....

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Journal ArticleDOI
TL;DR: Results provide some of the first experimental evidence of the diverse direct and indirect effects of ants on both above and belowground processes in forest ecosystems and demonstrate the potential consequences of losing an important seed dispersing ant species for the plants they disperse.
Abstract: Ants are ubiquitous members of most forest communities, where they disperse seeds, prey on other species, and influence the flow of nutrients. Their effects are often described as substantial, but few studies to date have simultaneously examined how the presence of ants affects both above and belowground processes. In this study, we experimentally reduced ant abundance in a suite of deciduous forest plots in northern Georgia, USA to assess the effects of ants on the spatial distribution of a common understory plant species, Hexastlylis arifolia, the structure of soil mesofaunal communities, and soil nitrogen dynamics. Over the course of several years, the removal of ants led to significant spatial aggregation of H. arifolia seedlings near the parent plant, most likely due to the absence of the keystone seed dispersal species, Aphaenogaster rudis. Seedling emergence was higher in ant removal plots, but seedling aggregation did not affect first or second year seedling mortality. Ammonium concentrations were 10× higher in ant removal plots relative to control plots where ants were present in the first year of the study, but this increase disappeared in the second and third years of the study. The effects of ant removal on the soil mesofauna were mixed: removal of ants apparently did not affect the abundance of Collembola, but the abundance of oribatid mites was significantly higher in ant removal plots by year two of the study. Taken together, these results provide some of the first experimental evidence of the diverse direct and indirect effects of ants on both above and belowground processes in forest ecosystems and demonstrate the potential consequences of losing an important seed dispersing ant species for the plants they disperse.

38 citations


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

  • ...Therefore, the increase in dispersal distance and potential decrease in seedling density due to redispersal ought to augment myrmecochore population fitness, though this is difficult to assess given the length of time to reproduction in some myrmecochores (Zelikova et al., 2011)....

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Book
31 Aug 2003
TL;DR: The myrmecochorous syndrome as mentioned in this paper was first identified by ants in the early 1970s and was later identified as a major cause of diaspore removal in non-myrmecchorous plants.
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.

38 citations