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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
01 Aug 1992-Ecology
TL;DR: Influences of ant behavior on short— and long—term fate of elaiosome—bearing seeds were investigated in fire—prone sclerophyll vegetation neary Sydney, New South Wales by measuring dispersal distances, seed predation within ant nests, and seed burial.
Abstract: Influences of ant behavior on short— and long—term fate of elaiosome—bearing seeds were investigated in fire—prone sclerophyll vegetation neary Sydney, New South Wales. The short—term fate of seeds was assessed by measuring dispersal distances, seed predation within ant nests, and seed burial. Most seeds were taken directly to ant nests. The mean dispersal distance was 1.1 m (range 0.06—11 m). Seed predation by three ant species was measured by feeding known quantities of seeds and inedible seed mimics, made from plastic beads, into nests. Nests were excavated 2, 7, and 30 d later to recover seeds and beads. The recovery rate of beads estimated the disappearance rate of seeds from nests due to factors other than predation. Pheidole sp. 1 appeared to eat most seeds soon after collection but also stored some seeds in small caches within the nest. Both Rhytidoponera "metallica" and Aphaenogaster longiceps removed most seeds for the nest intact (the elaiosome having been consumed) and discarded them on the su...

204 citations


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

  • ...In a similar manner to other studies of seed fate within the nest (see Culver and Beattie, 1980; Hanzawa et al., 1988; Heithaus et al., 2005; Hughes and Westoby, 1992), we placed up to 50 marked A. canadense seeds near the nest entrance and observed the seeds’ removal by A. rudis to be sure all…...

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  • ...In a similar manner to other studies of seed fate within the nest (see Culver and Beattie, 1980; Hanzawa et al., 1988; Heithaus et al., 2005; Hughes and Westoby, 1992), we placed up to 50 marked A....

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Journal ArticleDOI
TL;DR: It is shown that positive interactions among resource competitors can produce species-rich model communities supported by a single limiting resource and that focusing on the net interaction between species may conceal important coexistence mechanisms when species simultaneously engage in both antagonistic and positive interactions.
Abstract: Although positive interactions between species are well documented, most ecological theory for investigating multispecies coexistence remains rooted in antagonistic interactions such as competition and predation. Standard resource-competition models from this theory predict that the number of coexisting species should not exceed the number of factors that limit population growth. Here I show that positive interactions among resource competitors can produce species-rich model communities supported by a single limiting resource. Simulations show that when resource competitors reduce each others' per capita mortality rate (e.g. by ameliorating an abiotic stress), stable multispecies coexistence with a single resource may be common, even while the net interspecific interaction remains negative. These results demonstrate that positive interactions may provide an important mechanism for generating species-rich communities in nature. They also show that focusing on the net interaction between species may conceal important coexistence mechanisms when species simultaneously engage in both antagonistic and positive interactions.

192 citations


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

  • ...Evidence continues to grow that facilitation, and more specifically mutualism, increases biological diversity and shapes the structure of ecological communities (Gross, 2008; Lengyel et al., 2009)....

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Journal ArticleDOI
TL;DR: A statistical difference exists between dispersal curves from the Northern hemisphere and the Southern hemisphere, and it is hypothesize that this difference is related to the myrmecological communities from both types of vegetation: dispersing ants from sclerophyllous vegetation would have smaller nest densities and/or bigger foraging areas than dispersing ant from mesic environments.
Abstract: . Myrmecochorous dispersal distances are reviewed; the seed dispersal curve generated by ants shows a characteristic peak at short distances and a long tail, a shape suited to small densities of safe sites. Mean global distance is of 0.96 m (n= 2524) with a range of 0.01–77 m. Data have been broken down by geography (Northern hemisphere v. Southern hemisphere), taxonomy (ant subfamilies) and ecology (vegetation: sclerophyllous v. mesophyllous). Although a statistical difference exists between dispersal curves from the Northern hemisphere and the Southern hemisphere, this may be an artefact of lack of data from mesophyllous myrmecochores from this hemisphere. The four ant subfamilies do show also numerical differences but could not be subjected to statistical analysis. A difference between the shape of dispersal curve for sclerophyllous myrmecochores and mesophyllous myrmecochores has also been detected. We hypothesize that this difference is related to the myrmecological communities from both types of vegetation: dispersing ants from sclerophyllous vegetation would have smaller nest densities and/or bigger foraging areas than dispersing ants from mesic environments.

181 citations


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

  • ...rudis redisperses a majority of seeds, w93%, from the nest at distances comparable to measures of primary dispersal (see Culver and Beattie, 1978; Giladi, 2004; Gómez and Espadaler, 1998; Kalisz et al., 1999; Zelikova et al., 2008)....

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  • ...The reported average distances of primary dispersal distance of seeds by A. rudis range from 50 to 100 cm (Culver and Beattie, 1978; Giladi, 2004; Gómez and Espadaler, 1998; Kalisz et al., 1999; Zelikova et al., 2008)....

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  • ...Overall, the data indicate A. rudis redisperses a majority of seeds, w93%, from the nest at distances comparable to measures of primary dispersal (see Culver and Beattie, 1978; Giladi, 2004; Gómez and Espadaler, 1998; Kalisz et al., 1999; Zelikova et al., 2008)....

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Journal ArticleDOI
13 May 2009-PLOS ONE
TL;DR: Myrmecochory provides the best example to date for a consistent effect of any mutualism on large-scale diversification in angiosperm plants, and diversification rates were substantially higher in ant-dispersed plants than in their non-myRMecochorous relatives.
Abstract: Background: The extraordinary diversification of angiosperm plants in the Cretaceous and Tertiary periods has produced an estimated 250,000–300,000 living angiosperm species and has fundamentally altered terrestrial ecosystems. Interactions with animals as pollinators or seed dispersers have long been suspected as drivers of angiosperm diversification, yet empirical examples remain sparse or inconclusive. Seed dispersal by ants (myrmecochory) may drive diversification as it can reduce extinction by providing selective advantages to plants and can increase speciation by enhancing geographical isolation by extremely limited dispersal distances. Methodology/Principal Findings: Using the most comprehensive sister-group comparison to date, we tested the hypothesis that myrmecochory leads to higher diversification rates in angiosperm plants. As predicted, diversification rates were substantially higher in ant-dispersed plants than in their non-myrmecochorous relatives. Data from 101 angiosperm lineages in 241 genera from all continents except Antarctica revealed that ant-dispersed lineages contained on average more than twice as many species as did their non-myrmecochorous sister groups. Contrasts in species diversity between sister groups demonstrated that diversification rates did not depend on seed dispersal mode in the sister group and were higher in myrmecochorous lineages in most biogeographic regions. Conclusions/Significance: Myrmecochory, which has evolved independently at least 100 times in angiosperms and is estimated to be present in at least 77 families and 11 000 species, is a key evolutionary innovation and a globally important driver of plant diversity. Myrmecochory provides the best example to date for a consistent effect of any mutualism on largescale diversification.

178 citations


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

  • ...Elaiosomes have evolved tens of times in themonocots (Dunn et al., 2007) and over a hundred times in the angiosperms more generally (Lengyel et al., 2009, 2010)....

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  • ...Evidence continues to grow that facilitation, and more specifically mutualism, increases biological diversity and shapes the structure of ecological communities (Gross, 2008; Lengyel et al., 2009)....

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Journal ArticleDOI
TL;DR: This work reviews how IDE models are formulated, how they are parameterized, and how they can be analyzed to project spread rates and the impact of those rates to changes in model parameters on invasion risk.
Abstract: All else being equal, the faster an invading species spreads, the more dangerous its invasion. The projection of spread rate therefore ought to be a central part of the determination of invasion risk. Originally formulated in the 1970s to describe the spatial spread of advantageous alleles, integrodifference equation (IDE) models have since been co-opted by population biologists to describe the spread of populations. More recently, they have been modified to include population structure and environmental variability. We review how IDE models are formulated, how they are parameterized, and how they can be analyzed to project spread rates and the sensitivity of those rates to changes in model parameters. For illustrative purposes, we apply these models to Cytisus scoparius, a large shrub in the legume family that is considered a noxious invasive species in eastern and western North America, Chile, Australia, and New Zealand.

177 citations


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

  • ...where I0 is the modified Bessel function of the first kind and zeroth order (Neubert and Parker, 2004; Lewis et al., 2006)....

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  • ...Thenwe can estimate the moment generating function with the directional empirical moment generating function, MENðsÞ ¼ 1 N XN i¼1 I0ðsriÞ; 0 s < N (A.5) where I0 is the modified Bessel function of the first kind and zeroth order (Neubert and Parker, 2004; Lewis et al., 2006)....

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  • ...The dispersal kernel for primary dispersal is the convolution of the autochorous dispersal kernel and the measured initial dispersal kernel of seed dispersal from the parent to the nest (Neubert and Parker, 2004)....

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