Soil of the nest-mound of the seed-dispersing ant,Aphaenogaster longiceps,enhances seedling growth

Although a major benefit of myrmecochory in the Australian environment is believed to be the targeting of seeds to nutrient-enriched ant nests, there is very little direct evidence for this. Here I report that, compared to control soil, soil from nest mounds of Aphaenogaster longiceps enhances the growth of seedling roots and shoots by about 50% in glasshouse trials. This benefit of nutrient-enrichment, however, probably only occurs when seeds are dispersed by ants that construct large, long-lived, nest mounds. This is very often not the case, and there is now increasing evidence that distance dispersal is often the major benefit of myrmecochory in Australia.     

Savanna fires increase rates and distances of seed dispersal by ants

Myrmecochory (seed dispersal by ants) is a prominent dispersal mechanism in many environments, and can play a key role in local vegetation dynamics. Here we investigate its interaction with another key process in vegetation dynamics—fire. We examine ant dispersal of seeds immediately before and after experimental burning in an Australian tropical savanna, one of the world’s most fire-prone ecosystems. Specifically, our study addressed the effects of burning on: (1) the composition of ants removing seeds, (2) number of seed removals, and (3) distance of seed dispersal. Fire led to higher rates of seed removal post-fire when compared with unburnt habitat, and markedly altered dispersal distance, with mean dispersal distance increasing more than twofold (from 1.6 to 3.8 m), and many distance dispersal events greater than the pre-fire maximum (7.55 m) being recorded. These changes were due primarily to longer foraging ranges of species of Iridomyrmex, most likely in response to the simplification of their foraging landscape. The significance of enhanced seed-removal rates and distance dispersal for seedling establishment is unclear because the benefits to plants in having their seeds dispersed by ants in northern Australia are poorly known. However, an enhanced removal rate would enhance any benefit of reduced predation by rodents. Similarly, the broader range of dispersal distances would appear to benefit plants in terms of reduced parent–offspring conflict and sibling competition, and the location of favourable seedling microsites. Given the high frequency of fire in Australian tropical savannas, enhanced benefits of seed dispersal by ants would apply for much of the year.     

Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory

Myrmecochory, or seed dispersal by ants, is a dispersal syndrome found among several thousand plant species occupying different ecosystems and geographical regions. Typically, ants benefit from consuming a lipid-rich appendage on the seed and in return provide seed dispersal service to the plant. Several hypotheses have been proposed to explain the selective advantage for plants resulting from myrmecochory, including directed dispersal, dispersal for distance and escape from seed predators. I contrast the evidence available in the literature for these hypotheses and distinguish the studies on the basis of ecosystem and plant growth forms. The predator-avoidance and the distance dispersal hypotheses were supported in most studies that addressed them, and the directed dispersal hypothesis was supported in about half of the studies that tested it. Multiple hypotheses were supported in most studies that tested more than one hypothesis, suggesting that the various selective advantages conferred from myrmecochory are seldom exclusive. I also review evidence for the hypothesis that plants have evolved adaptations both for selecting seed dispersers and for manipulating the behavior of those dispersers. Based on this evidence, I argue that focusing future research on the evolution of partner choice by myrmecochores and its effects on the overall plant fitness will be more fruitful than putting an emphasis on classifying the selective advantage to plants into distinct categories and test for their existence separately.     

Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone

Summary Several common plants (Chenopodiaceae) of the Australian arid zone produce diaspores that bear small and inconspicuous food bodies and are adapted for dispersal by ants. For these species, myrmecochory probably represents an adaptation for highly directional dispersal of diaspores to favorable microsites where nutrients are concentrated and possibly more accessible. Dispersal of diaspores by ants can have a pronounced effect on plant dispersion. In habitats characterized by red, crusty alluvial loam soils, myrmecochorous species grow almost exclusively on ant mounds; these same species grow in relatively continuous stands in sandy soil habitats. The flora of the Australia arid zone may contain many plant species that are adapted to use ants as dispersal agents. We consider several factors that may have promoted or facilitated the evolution of myrmecochory in arid zone plants.     

An update of the world survey of myrmecochorous dispersal distances

We update the global assessment of seed dispersal by ants and test the hypothesis that the body size of seed‐dispersing ant species varies with latitude in the same way as dispersal distance. We compiled all published data about seed dispersal distance by myrmecochory through March, 2011. We then broke the data down by vegetation type, geography and taxonomy. We also compiled data on body size (body length) of the seed‐dispersing ant species from the studies consulted. Based on 7889 observations, the mean dispersal distance was 1.99 m, although the curve has a long tail extending to 180 m. Considering the mean dispersal distance by ant species and study as independent data, the mean dispersal distance was 2.24 ± 7.19 m (n = 183). Shorter distances are associated with smaller ant species, while the tail of the dispersal curve is due to larger ant species. The mean dispersal distance of myrmecochorous seeds dispersed by ants decreased with increasing latitude, but there was no significant relationship between the body size of dispersing ant species and latitude (i.e. myrmecochorous seed‐dispersing ant species do not follow Bergmann's rule). In 1998 we made three predictions: 1) the dispersal distances of the Southern Hemisphere will decrease with as more data from mesophyllous vegetation are obtained; 2) assuming that ant nest density is higher at lower latitudes, the differences in distances between hemispheres would probably decrease with more data; and 3) numerical differences between dispersal distances in mesophyllous and sclerophyllous vegetation zones would increase with more data. The results obtained since 1998 support the only the third prediction. The dispersal distances in mesophyllous vegetation zones are shorter than in the sclerophyllous vegetation zones, and the difference between 1998 have increased. The differences in dispersal distances between hemispheres are consistent with the avoidance of parent–offspring competition (escape hypothesis).     

Dispersal for distance? Acacia ligulata seeds and meat ants Iridomyrmex viridiaeneus

Abstract Ant seed dispersal distances are typically small, averaging less than 1 m in published studies. Here, a new record (180 m) for ant seed dispersal distance is reported, and preliminary observations are made on the interaction between meat ants Iridomyrmex viridiaeneus Viehmeyer (Hymenoptera: Formicidae) and diaspores of the sandhill wattle, Acacia ligulata A. Cunn. ex Benth. (Fabaceae) in Kinchega National Park, New South Wales (NSW), Australia. Iridomyrmex viridiaeneus moved diaspores over distances of 7–180 m (mean 93.9 m) from the source trees to their nests, removed the arils underground and discarded the seeds over a 3000‐m² area surrounding the nest. A germination trial determined that the viability of discarded seeds was 40%, with 80% of the viable seeds in a dormant condition. Although the cumulative effects of I. viridiaeneus on A. ligulata recruitment require further investigation, this study and others raise the possibility that myrmecochorous systems in the Australian arid zone may be characterized by longer dispersal distances than those in other parts of the world. Long‐distance seed movement by ants lends credence to the hypothesis that distance dispersal (in contrast to directed dispersal) could be of benefit to myrmecochorous plants.     

The Benefits of Myrmecochory: A Matter of Stature

Myrmecochory, or seed dispersal by ants, occurs widely in angiosperms, and particularly in temperate forest herbs in the northern Hemisphere and sclerophyll shrubs in Mediterranean‐climate landscapes. The lipid‐rich elaiosome on the seed provides nutrition to the ants; however, how the plant benefits from myrmecochory remains unclear. Here, we provide the first comprehensive analysis of the Euphorbiaceae species in the semi‐arid Caatinga vegetation region of northeastern Brazil, and show that myrmecochory strongly associates with small plant stature, even after controlling for seed size. The association of myrmecochory with small stature suggests that the primary benefit to plants concerns distance of dispersal, which reduces parental and sibling competition.     

Why do more plant species use ants for dispersal on infertile compared with fertile soils?*

Myrmecochores are plant species that bear seeds with food-bodies adapting them for dispersal by ants. Within Australia and South Africa, myrmecochores account for a large percentage of the flora in sclerophyll vegetation on very infertile soils. On fertile soils, there are few myrmecochores and more species with fleshy fruits adapted for dispersal by vertebrates. This effect of very infertile soils may also account for the high incidence of myrmecochores in the floras of Australia and South Africa compared with other continents. The taxonomic distribution of myrmecochory shows it has evolved many times within the Australian flora. Evidence has been collected in relation to eight hypotheses that might account for the prevalence of myrmecochory on very infertile soils: (1) Myrmecochore seeds do not appear to be relocated to nutrient-enriched microsites. Seed-removing ant species relocate their nest entrances frequently; active ant nests are not nutrient-enriched; and seedlings emerging after fire are not located in nutrient-enriched soil. (2) Traffic of seed-removing ants is not greater on infertile than on fertile soils. (3) Burial to avoid predation by small mammals is not a significant factor for seeds in Australian vegetation. (4) Experiments in which diaspore traits are manipulated support the idea that a larger food body increases the likelihood that a diaspore will be taken by a seed-disperser ant species that will not eat the embryo, rather than by a seed-predator ant. However, evidence so far does not support the hypothesis that, on very infertile soils, seed-disperser ants are consistently more available than seed-predator ants. (5) Removal rates of fruits adapted for dispersal by vertebrates were, on average, two and a half times greater in vegetation on fertile soils. Birds were the main removers. Our current opinion is that the fruit-removing bird assemblage is more likely to be a consequence of the high incidence of species with vertebrate-adapted fruits, rather than the reverse. (6) Fleshy fruits are more expensive in potassium than food bodies for ants, but not in nitrogen or phosphorus. This might be a reason why fleshy fruits are uneconomic on very infertile soils. (7) Species with smaller embryo-plus-endosperm weight are relatively more likely to be adapted for dispersal by ants rather than vertebrates. However, differences in the frequency distribution of embryo-plus-endosperm weights between infertile and fertile soils are moderate in the Sydney area. An indirect association between soil fertility and dispersal mode via embryo-plus-endosperm weight cannot account for much of the difference in dispersal spectrum. (8) Species growing to less than 2 m tall are relatively more likely to be adapted for dispersal by ants rather than vertebrates, and also account for more of the flora on infertile than on fertile soils. This indirect correlation is capable of accounting for as much as 80% of the higher incidence of myrmecochory on infertile soils.     

Combining distances of ballistic and myrmecochorous seed dispersal in Adriana quadripartita (Euphorbiaceae)

The separate contributions of different vectors to net seed dispersal curves of diplochorous systems have rarely been characterised. In Australia, myrmecochory is a common seed dispersal syndrome and in the majority of such systems, seeds are initially dispersed ballistically. We measured ballistic and myrmecochorous seed dispersal distances in relation to canopies of Adriana quadripartita (Euphorbiaceae) and used a simulation model to estimate the net dispersal curve. We also compared seed removal rates and ant abundances under, and outside, plant canopies to examine how foraging patterns by ants may affect net dispersal.Overall ant abundance did not show a significant numerical response to seedfall; however, the abundance of the main seed dispersing ant, Rhytidoponera ‘metallica’ did. Despite this, seed removal rates did not differ significantly between canopy and open locations. Rhytidoponera ‘metallica’ account for 93% of observed seed dispersal events. On average, the ants dispersed seeds 1.54 m and in doing so, moved seed a mean radial distance of 0.76 m away from canopy edges. This contribution to net dispersal distance by ants is considerable since ballistic dispersal moved seeds a median distance of 7.5 cm. Our simulation model indicated that the combination of ballistic and ant seed dispersal is expected to result in seeds being transported a median net radial dispersal distance of 1.05 m from the canopy edge.Thus in this system, an important function of diplochory may simply be to move a higher proportion of seeds from under the canopy of parent plants than is possible by ballistic dispersal alone. This ‘dispersal-for-distance’ may result in reduced parent–offspring competition or may increase the probability that seeds reach rare safe sites for germination and recruitment.     

Convergent evolution of seed dispersal by ants,and phylogeny and biogeography in flowering plants: A global survey

Seed dispersal is a fundamental life history trait in plants. Although the recent surge of interest in seed dispersal by ants (myrmecochory) has added greatly to knowledge on the ecology of seed dispersal and ant–plant mutualisms, myrmecochory also represents a unique opportunity to examine the links between seed dispersal and evolution in flowering plants. Here we review the taxonomic, phylogenetic and biogeographic distribution of myrmecochory in flowering plants. Myrmecochory is mediated by elaiosomes, i.e., lipid-rich seed appendages that attract ants and serve as rewards for dispersal. We surveyed the literature for evidence of elaiosomes in angiosperm plants to estimate the global prevalence of myrmecochory. We then searched the literature for phylogenetic reconstructions to identify myrmecochorous lineages and to estimate the minimum number of independent evolutionary origins of myrmecochory. We found that myrmecochory is present in at least 11 000 species or 4.5% of all species, in 334 genera or 2.5% of all genera and in 77 families or 17% of all families of angiosperm plants. We identified at least 101, but possibly up to 147, independent origins of myrmecochory. We estimated three or more origins in 13 families and found that at least half the genera are myrmecochorous in 10 families. Most myrmecochorous lineages were Australian, South African or northern temperate (Holarctic). A mapping of families containing myrmecochorous genera on a dated angiosperm supertree showed that myrmecochory has evolved in most of the major angiosperm lineages and that it is more frequent in younger families (crown group age <80 million years) than in older ones. We suggest that the relatively low physiological and energetic costs of producing an elaiosome and the consistent selective benefits of myrmecochory (dispersal, protection from seed predators and fire, safe and nutrient-rich microsites) explain the numerous evolutionary and developmental origins of myrmecochory in angiosperm plants, and we propose that elaiosomes thus provide one of the most dramatic examples of convergent evolution in biology.     

Estimation of dispersal distance by mark-recapture experiments using traps: correction of bias caused by the artificial removal by traps

Although in mark-recapture experiments traps are useful to estimate the dispersal distance of organisms, they cause a dilemma that may be called a kind of Heisenberg effect: a large number of traps should be placed to yield a precise estimate of mean dispersal distance, while these traps shorten the mean dispersal distance itself by intercepting organisms that should have dispersed for further distances. We propose a procedure to solve this dilemma by placing traps uniformly in a lattice pattern, and by assuming a random movement and a constant rate of settlement for organisms. We applied this procedure to estimate the dispersal distance of the sugarcane wireworm Melanotus okinawensis Ohira (Coleoptera: Elateridae). The estimated mean dispersal distance was 143.8 m. Through the use of a conventional method of estimation, the mean dispersal distance was estimated to be 118.1 m. Thus, it was shown that the conventional estimate of dispersal distance was 18% smaller than the corrected estimate in our experiment.     

Mutualism vs. antagonism in introduced and native ranges: Can seed dispersal and predation determine Acacia invasion success?

Plant species introduced to new regions can escape their natural enemies but may also lose important mutualists. While mutualistic interactions are often considered too diffuse to limit plant invasion, few studies have quantified the strength of interactions in both the native and introduced ranges, and assessed whether any differences are linked to invasion outcomes. For three Acacia species adapted for ant dispersal (myrmecochory), we quantified seed removal probabilities associated with dispersal and predation in both the native (Australian) and introduced (New Zealand) ranges, predicting lower removal attributable to dispersal in New Zealand due to a relatively depauperate ant fauna. We used the role of the elaiosome to infer myrmecochory, and included treatments to measure vertebrate seed removal, since this may become an important determinant of seed fate in the face of reduced dispersal. We then tested whether differences in seed removal patterns could explain differences in the invasion success of the three Acacia species in New Zealand.Overall seed removal by invertebrates was lower in New Zealand relative to Australia, but the difference in removal between seeds with an elaiosome compared to those without was similar in both countries. This implies that the probability of a removed seed being dispersed by invertebrates was comparable in New Zealand to Australia. The probability of seed removal by vertebrates was similar and low in both countries. Differences in the invasive success of the three Acacia species in New Zealand were not explained by differences in levels of seed predation or the strength of myrmecochorous interactions. These findings suggest that interactions with ground foraging seed predators and dispersers are unlikely to limit the ability of Acacia species to spread in New Zealand, and could not explain their variable invasion success.     

Seed dispersal in Erythronium dens-canis L. (Liliaceae): variation among habitats in a myrmecochorous plant

Erythronium dens-canis is a geophyte which produces a single flower each season. The fruits produce small seeds with relatively large elaiosomes. We performed experiments to investigate primary and secondary seed dispersal mechanisms of this species in different habitats in the western part of the Cantabrian Range in northwest Spain. Sticky traps were used to measure primary dispersal of seeds up to 0.5 m from mother plants. Seed cafeteria experiments were performed in different habitats to examine the role of ants and rodents in secondary seed transport and seed predation. Our results indicate that: (a) primary seed dispersal is positively skewed (99% of seeds fall within 20 cm of the mother plant) and seed dispersal distances vary significantly among plants; (b) secondary dispersal is exclusively by myrmecochory, although the proportion of seeds removed by ants differs significantly among habitats; (c) ant species composition and abundances vary among habitats; and (d) freshly dropped seeds are more likely to be removed than seeds that have begun to dry out. We conclude that secondary dispersal of seeds is greatly influenced by habitat but not by small-scale microhabitat. This revised version was published online in June 2006 with corrections to the Cover Date.     

The costs of leaving home: ants disperse myrmecochorous seeds to low nutrient sites

Summary Leucospermum conocarpodendron (L.) Buek (Proteaceae) seedlings were excavated several months after a fire in Cape fynbos. Seedlings under burnt parental skeletons had short hypocotyls (mean 25 mm) indicating passive dispersal whereas seedlings in the open were more deeply buried (mean 48 mm) by ants. Soil nutrient concentrations at the site of germination were negatively related to depth of burial and distance from parent. Ant dispersal resulted in seedlings emerging in soils with lower nutrient concentrations than passively dispersed seeds. Tissue analysis supported the soil results with lower P content in seedlings from open (ant dispersed) sites. Seedling survival in the first year of establishment was also lower in open sites, but not significantly so. However seedlings were slightly taller in the open. The results of this study, the first on naturally occurring intraspecific variation in myrmecochory, strongly contradict current explanations for the high incidence of myrmecochory in nutrient poor environments.     

Evolution of dispersal in explicitly spatial metacommunities

We apply an evolutionary game theoretic approach to the evolution of dispersal in explicitly spatial metacommunities, using a flexible parametric class of dispersal kernels, namely 2Dt kernels, and study the resulting evolutionary dynamics and outcomes. We observe strong selective pressure on mean dispersal distance (i.e., the first moment), and weaker, but significant, one on the shape of dispersal kernel (i.e., higher moments). We investigate the effects of landscape topology and spatial heterogeneity on the resulting ‘optimal’ dispersal kernels. The shape—importantly the tail structure—and stability of evolutionarily optimal dispersal strategies are strongly affected by landscape topology or connectivity. Specifically, the results suggest that the optimal dispersal kernels in the river network topology have heavier tails and are stable, while those in the direct topology, where organisms are allowed to travel directly from one location to another, have relatively thin tails and may be unstable. We also find that habitat spatial heterogeneity enables coexistence and controls spatial distribution of distinct groups of dispersal strategies and that alteration in topology alone may not be sufficient to change such coexistence. This work provides a tool to translate environmental changes such as global climate change and human intervention into changes in dispersal behavior, which in turn may lead to important alterations of biodiversity and biological invasion patterns.     

Biogeography of Southeast Asia and the West Pacific

The biogeography of Southeast Asia and the West Pacific is complicated by the fact that these are regions on the border of two palaeocontinents that have been separated for a considerable period of time. Thus, apart from any patterns of vicariance, two general patterns relating to dispersal can be expected: a pattern of Southeast Asian elements, perhaps of Laurasian origin, expanding into Australian areas, and a reverse pattern for Australian elements, perhaps of Gondwanan origin. On top of this, both Australian and Southeast Asian elements occur in the Pacific. They dispersed there as the Pacific plate moved westward, bringing the different islands within reach of Southeast Asia and Australia. In order to reconstruct the biotic history of these areas, two large data sets consisting of both plants and animals were generated, one for each pattern, which were analysed using cladistic methods. The general patterns that emerged were weakly supported and do not allow general conclusions.     

Maintenance of high pollen dispersal in Eucalyptus wandoo, a dominant tree of the fragmented agricultural region in Western Australia

Pollen dispersal was investigated in five remnant populations of Eucalyptus wandoo, a dominant insect-pollinated tree in the fragmented agricultural region of southern Western Australia. Paternity analysis using six microsatellite loci identified a pollen source for 45% of seedlings, and the remainder were assumed to have arisen from pollen sources outside the stands. Outcrossing was variable, ranging from 52 to 89%, and long distance pollen dispersal was observed in all populations with up to 65% of pollen sourced from outside the populations over distances of at least 1 km. Modelling dispersal functions for pollination events within the two larger populations showed little difference between the four two-parameter models tested and indicated a fat-tailed dispersal curve. Similarity of direct and indirect historical estimates of gene flow indicates maintenance of gene flow at levels experienced prior to fragmentation. The study revealed extensive long distance pollen dispersal in remnant patches of trees within a fragmented agricultural landscape in the southern temperate region and highlighted the role of remnant patches in maintaining genetic connectivity at the landscape scale.     

Role of plant functional traits in determining vegetation composition of abandoned grazing land in north‐eastern Victoria,Australia

Question: In the Northern Hemisphere, species with dispersal limitations are typically absent from secondary forests. In Australia, little is known about dispersal mechanisms and other traits that drive species composition within post‐agricultural, secondary forest. We asked whether mode of seed dispersal, nutrient uptake strategy, fire response, and life form in extant vegetation differ according to land‐use history. We also asked whether functional traits of Australian species that confer tolerance to grazing and re‐colonisation potential differ from those in the Northern Hemisphere. Location: Delatite Peninsula, NE Victoria, Australia. Methods: The vegetation of primary and secondary forests was surveyed using a paired‐plot design. Eight traits were measured for all species recorded. ANOSIM tests and Non‐metric Multi‐dimensional Scaling were used to test differences in the abundance of plant attributes between land‐use types. Results: Land‐use history had a significant effect on vegetation composition. Specific leaf area (SLA) proved to be the best predictor of response to land‐use change. Primary forest species were typically myrmecochorous phanerophytes with low SLA. In the secondary forest, species were typically therophytes with epizoochorous dispersal and high SLA. Conclusions: The attributes of species in secondary forests provide tolerance to grazing suggesting that disturbance caused by past grazing activity determined the composition of these forests. Myrmecochores were rare in secondary forests, suggesting that species had failed to re‐colonise due to dispersal limitations. Functional traits that resulted in species loss through disturbance and prevented re‐colonisation were different to those in the Northern Hemisphere and were attributable to the sclerophyllous nature of the primary forest.     

Using genetic markers to estimate the pollen dispersal curve

Pollen dispersal is a critical process that shapes genetic diversity in natural populations of plants. Estimating the pollen dispersal curve can provide insight into the evolutionary dynamics of populations and is essential background for making predictions about changes induced by perturbations. Specifically, we would like to know whether the dispersal curve is exponential, thin-tailed (decreasing faster than exponential), or fat-tailed (decreasing slower than the exponential). In the latter case, rare events of long-distance dispersal will be much more likely. Here we generalize the previously developed TWOGENER method, assuming that the pollen dispersal curve belongs to particular one- or two-parameter families of dispersal curves and estimating simultaneously the parameters of the dispersal curve and the effective density of reproducing individuals in the population. We tested this method on simulated data, using an exponential power distribution, under thin-tailed, exponential and fat-tailed conditions. We find that even if our estimates show some bias and large mean squared error (MSE), we are able to estimate correctly the general trend of the curve - thin-tailed or fat-tailed - and the effective density. Moreover, the mean distance of dispersal can be correctly estimated with low bias and MSE, even if another family of dispersal curve is used for the estimation. Finally, we consider three case studies based on forest tree species. We find that dispersal is fat-tailed in all cases, and that the effective density estimated by our model is below the measured density in two of the cases. This latter result may reflect the difficulty of estimating two parameters, or it may be a biological consequence of variance in reproductive success of males in the population. Both the simulated and empirical findings demonstrate the strong potential of TWOGENER for evaluating the shape of the dispersal curve and the effective density of the population (d(e)).