Secondary dispersal mechanisms of winged seeds: a review

Winged seeds, or samaras, are believed to promote the long‐distance dispersal and invasive potential of wind‐dispersed trees, but the full dispersive potential of these seeds has not been well characterised. Previous research on the ecology of winged seeds has largely focussed on the initial abscission and primary dispersal of the samara, despite it being known that the primary wind dispersal of samaras is often over short distances, with only rare escapes to longer distance dispersal. Secondary dispersal, or the movement of the seeds from the initial dispersal area to the site of germination, has been largely ignored despite offering a likely important mechanism for the dispersal of samaras to microhabitats suitable for establishment. Herein, we synthesise what is known on the predation and secondary dispersal of winged seeds by multiple dispersive vectors, highlighting gaps in knowledge and offering suggestions for future research. Both hydrochory and zoochory offer the chance for samaroid seeds to disperse over longer distances than anemochory alone, but the effects of the wing structure on these dispersal mechanisms have not been well characterised. Furthermore, although some studies have investigated secondary dispersal in samaroid species, such studies are scarce and only rarely track seeds from source to seedling. Future research must be directed to studying the secondary dispersal of samaras by various vectors, in order to elucidate fully the invasive and colonisation potential of samaroid trees.     

Population history,gene flow,and bottlenecks in island populations of a secondary seed disperser,the southern grey shrike (Lanius meridionalis koenigi)

Studying the population history and demography of organisms with important ecological roles can aid understanding of evolutionary processes at the community level and inform conservation. We screened genetic variation (mtDNA and microsatellite) across the populations of the southern grey shrike (Lanius meridionalis koenigi) in the Canary Islands, where it is an endemic subspecies and an important secondary seed disperser. We show that the Canarian subspecies is polyphyletic with L. meridionalis elegans from North Africa and that shrikes have colonized the Canary Islands from North Africa multiple times. Substantial differences in genetic diversity exist across islands, which are most likely the product of a combination of historical colonization events and recent bottlenecks. The Eastern Canary Islands had the highest overall levels of genetic diversity and have probably been most recently and/or frequently colonized from Africa. Recent or ongoing bottlenecks were detected in three of the islands and are consistent with anecdotal evidence of population declines due to human disturbance. These findings are troubling given the shrike's key ecological role in the Canary Islands, and further research is needed to understand the community‐level consequences of declines in shrike populations. Finally, we found moderate genetic differentiation among populations, which largely reflected the shrike's bottleneck history; however, a significant pattern of isolation‐by‐distance indicated that some gene flow occurs between islands. This study is a useful first step toward understanding how secondary seed dispersal operates over broad spatial scales.     

The Interplay of Habitat and Seed Type on Scatterhoarding Behavior in a Fragmented Afromontane Forest Landscape

Scatterhoarding by rodents, whereby seeds are collected and stored for later consumption, can result in seed dispersal. Seeds may be covered in litter on the forest floor (cached) or buried. This is particularly so in the Neotropics for large, nutritious seeds, and where primary dispersers are rare or missing. In African forests, contemporary anthropogenic pressures such as hunting, forest degradation, and fragmentation are contributing toward major declines in large frugivores, yet the potential for scatterhoarding to mitigate this loss is largely unknown. In this study, we used thread‐marked seed to explore the balance between seed predation and dispersal by rodents in Afromontane forest. We studied two tree species in three habitats: (1) continuous forest; (2) continuous forest edge, and (3) small, degraded riparian forest patches. We found that seed removal rates were high and almost the same in all three habitats for both tree species, but that the predation/dispersal balance differed among habitats. In continuous forest, more seeds of each species were scatterhoarded than depredated, and rates of scatterhoarding differed between the two species. In all habitats, burying seeds up to 2 cm belowground was more common than caching. Distances seeds were moved was approximately five times greater in continuous forest than in forest edge or riparian patches. We found strong evidence to suggest that the African pouched rat, Cricetomys sp. nov was responsible for the scatterhoarding.     

Exploitation of Fallen Diaspores by Ants: Are there Ant–Plant Partner Choices?

Ants frequently interact with fleshy fallen diaspores (fruits or seeds) not adapted for ant‐dispersal. Such interactions are usually considered as opportunistic, but recent evidence has indicated that these ants may differ in their effects on diaspore survival and plant recruitment. We investigated if partner choices are recognizable among genera of ants and plants, and if ant and plant traits may influence such preferences in cerrado (savanna‐like vegetation) from southeast Brazil. During a 2‐yr period, 521 ant–diaspore interactions were recorded through various methods, yielding 71 ant species and 38 plant species. Exploitation of fallen diaspores was common among several ant genera, and included carnivorous, omnivorous, and fungivorous ants. Contrary to others areas around the world, where true myrmecochory (seed dispersal by ants) is common among shrubs, ants also exploited diaspores from several cerrado trees. Plant life form, diaspore size, and ant body size did not seem to explain the pattern of interactions observed. Two subsets of preferential interactions, however, segregated fungivorous ants from another group composed of carnivorous and omnivorous ants, probably influenced by the chemical composition of the plant diaspores. Omnivorous ants usually remove the fleshy portion of diaspores on spot and probably provide limited benefits to plants. Carnivorous and fungivorous ants usually remove the whole diaspore to the nest. As each of these ant groups may influence the fitness of diaspores in different ways, there are possible subtle pathways for the evolution of partner choices between ants and these non‐myrmecochorous diaspores.     

Secondary seed dispersal by ants in Neotropical cerrado savanna: species‐specific effects on seeds and seedlings of Siparuna guianensis (Siparunaceae)

1. Most woody plant species in tropical habitats are primarily vertebrate‐dispersed, but interactions between ants and fallen seeds and fruits are frequent. This study assesses the species‐specific services provided by ants to fallen arillate seeds of Siparuna guianensis, a primarily bird‐dispersed tree in cerrado savanna. The questions of which species interact with fallen seeds, their relative contribution (versus vertebrates) to seed removal, and the potential effects on seedling establishment are investigated. 2. Seeds are removed in similar quantities in caged and control treatments, suggesting that ants are the main dispersers on the ground. Five ant species attended seeds. Pheidole megacephala (≈0.4 cm) cooperatively transported seeds, whereas the smaller Pheidole sp. removed the seed aril on spot. Large (> 1.0 cm) Odontomachus chelifer, Pachycondyla striata, and Ectatomma edentatum individually carried seeds up to 4 m. Bits of aril are fed to larvae and intact seeds are discarded near the nest entrance. 3. Overall, greater numbers of seedlings were recorded near ant nests than in control plots without nests. This effect, however, was only detected near P. megacephala and P. striata nests, where soil penetrability was greater compared with controls. Soil nutrients did not differ between paired plots. 4. This study confirms the prevalence of ant–seed interactions in cerrado and shows that ant‐derived benefits are species‐specific. Ant services range from seed cleaning on the spot to seed displacement promoting non‐random spatial seedling recruitment. Although seed dispersal distances by ants are likely to be shorter than those by birds, our study of S. guianensis shows that fine‐scale ant‐induced seed movements may ultimately enhance plant regeneration in cerrado.     

Diplochory in two Jatropha (Euphorbiaceae) species of the Monte Desert of Argentina

The potential explosive seed dispersal under controlled conditions and the dispersal by ants in natural populations are compared between two diplochoric species: Jatropha hieronymi Kuntze and J. excisa Griseb. The seeds of J. hieronymi are more than eightfold heavier than J. excisa seeds, and were explosively dispersed considerably further distances, reaching a maximum of almost 18 m. The differences in explosive dispersal distances between the two species seem to depend on both carpel wall thickness of the fruit and aerodynamic shape of the seed. Seed removal by ants was positively correlated with the presence of the elaiosome and was higher for J. excisa (83.6%) than for J. hieronymi (31.6%). Seed size was the major factor affecting the removal by ants, as only large bodied ants were able to transport the large seeds of J. hieronymi. The larger size and the higher oleic acid content of the elaiosomes of J. hieronymi seeds had no influence on the observed removal rates by ants. In contrast, ants transported the J. hieronymi seeds further distances than J. excisa seeds. Jatropha hieronymi distances achieved by both dispersal modes are in the range of the furthest distances described for a diplochorous species. Finally, the possible advantages of this dispersal mode in arid zones are discussed.     

Myrmecochorous adaptations ofCorydalis species (Papaveraceae) in southern Japan

Dispersal morphology based on the myrmecochorous adaptations for predator avoidance of sevenCorydalis species including two varieties are investigated in southern Japan. Three types of myrmecochory were distinguished: myrmecochory with autochory (diplochory), the explosive ejection of seeds followed by ant transportation; myrmecochory with vegetative reproduction, seed-transportation by ants and reproduction by tuber; and pure myrmecochory, seed-transporting by ants only. Diplochory occurs in one winter annual plant, which has explosive capsules, a smooth seed surface, a small elaiosome, long pedicels and large bracts. Myrmecochory with vegetative reproduction occurs in two perennials that reproduce by tuber, although they also produce a small number of seeds with a medium-sized elaiosome. the pedicels and bracts are medium in size. Pure myrmecochory occurs in five annuals or biennials that are characterized by a rough seed surface with a large elaiosome, comparatively high seed production, short pedicels and only small bracts. Diplochory is exhibited by only one species distributed widely throughout Japan. Myrmecochory with vegetative reproduction is exhibited by species mainly distributed in cool-temperate northern Japan, while true myrmecochory is exhibited by the majority ofCorydalis species in warm-temperate Japan.     

Rodent handling of Araucaria araucana seeds

In an intermast year of very low seed production, we studied seed handling in an Araucaria araucana (Araucariaceae) forest in Neuquén Province, Argentina. Rodents identified in 844 photographs from automatic cameras removed 589 seeds marked with small embedded magnets. Within 12 days of removal, 460 were recovered using a magnetic field locator; 79% of recoveries were from burrows and caches in litter or soil. Rodents exhibited a diversity of seed‐handling strategies and differed in their potential as dispersal agents. Seed removal was most likely between 15.00 hours and 21.00 hours, but diurnal and nocturnal visits were recorded for all species. Oligoryzomys longicaudatus (Cricetidae) was a seed predator that took 8% of marked seeds and left none whole. Chelemys macronyx (Cricetidae) and Rattus norvegicus (Muridae) removed 25% and 19% of marked seeds respectively. These two species deposited the majority of seeds in groups of 10 or more in burrow larders that were unfavourable seedling establishment sites far from daylight. Abrothrix longipilis (Cricetidae) removed 43% of seeds, scatter‐hoarded the largest percentage of whole seeds (37%), moved some seeds farther than 40 m, and left them in favourable seedling establishment sites near daylight. For all species, the number and proportion of seeds cached whole increased as more seeds were removed. Rodents, especially A. longipilis, may play an important role in regeneration of A. araucana. Seed‐handling strategies and potentially effective dispersal are discussed in terms of masting seed production.     

Interactions between Ants and Non‐myrmecochorous Fruits in Miconia (Melastomataceae) in a Neotropical Savanna

The aim of this study was to evaluate the role of ants as secondary seed dispersers of six primarily bird‐dispersed Miconia species in the cerrados of southeastern Brazil. Vertebrate exclosure and seed germination experiments were performed for M. albicans, M. alborufescens, M. corallina, M. ferruginata, M. ibaguensis, and M. irwinii. Excluding vertebrates did not significantly alter fruit removal rate for any of the Miconia species relative to open controls. Fruits on stalks and fallen fruits were removed and transported to nests mainly by species of Atta, Acromyrmex, and Ectatomma (dispersal distance ranging from 0.1 to 45.2 m), while Camponotus ants tended to be observed removing the fruit pulp (seed cleaning) where the fruits were found. Seed manipulation by Atta decreased germination of M. irwinii, but not M. ferruginata. Germination did not occur in intact fruits, and thus seed cleaning was an important service provided by the ants. Ant nest soils did not inhibit germination of any of the Miconia species, suggesting they are a good substrate for long‐lived Miconia seeds. We conclude that ant activity could have important effects on the fate of Miconia seeds adapted for bird dispersal.     

Dung Beetles Reduce Clustering of Tropical Tree Seedlings

We used manipulative field exclusion experiments to investigate the effects of dung beetles on the spatial aggregation of emerging seedlings of two tropical tree species. The results provide the first direct demonstration that tropical dung beetles reduce seedling clustering, with important implications for plant densities and demography.