Standard yet unusual mechanisms of long-distance dispersal: seed dispersal of Corymbia torelliana by bees

Mellitochory, seed dispersal by bees, has been implicated in long-distance dispersal of the tropical rain forest tree, Corymbia torelliana (Myrtaceae). We examined natural and introduced populations of C. torelliana for 4 years to determine the species of bees that disperse seeds, and the extent and distance of seed dispersal. The mechanism of seed dispersal by bees was also investigated, including fruit traits that promote dispersal, foraging behaviour of bees at fruits, and the fate of seeds. The fruit structure of C. torelliana , with seed presented in a resin reward, is a unique trait that promotes seed dispersal by bees and often results in long-distance dispersal. We discovered that a guild of four species of stingless bees, Trigona carbonaria, T. clypearis, T. sapiens , and T. hockingsi, dispersed seeds of C. torelliana in its natural range. More than half of the nests found within 250 m of fruiting trees had evidence of seed transport. Seeds were transported minimum distances of 20–220 m by bees. Approximately 88% of seeds were dispersed by gravity but almost all fruits retained one or two seeds embedded in resin for bee dispersal. Bee foraging for resin peaked immediately after fruit opening and corresponded to a peak of seed dispersal at the hive. There were strong correlations between numbers of seeds brought in and taken out of each hive by bees ( r =  0.753–0.992, P  < 0.05), and germination rates were 95 ± 5%. These results showed that bee-transported seeds were effectively dispersed outside of the hive soon after release from fruits. Seed dispersal by bees is a non-standard dispersal mechanism for C. torelliana, as most seeds are dispersed by gravity before bees can enter fruits. However, many C. torelliana seeds are dispersed by bees, since seeds are retained in almost all fruits, and all of these are dispersed by bees.     

荒漠孑遗植物裸果木种子时空扩散特性

裸果木(Gymnocarpos przewalskii)是亚洲中部荒漠区少有的第三纪孑遗物种,由于气候变化及人为干扰,其自然种群分布范围不断缩小。种子扩散作为植物生活史过程中的重要阶段,不仅对物种生存及其多样性至关重要,还影响物种分布范围和局部丰度。2015年和2016年分别在新疆哈密地区,采用布设种子收集器的方法,对其自然种群种子扩散的时空动态进行了定点连续观测。结果表明:该物种于当年6月上旬开始扩散,2015年略早于2016年。每年种子扩散持续时间约两个月,扩散趋势为单峰曲线,且呈集中大量扩散的模式,扩散高峰期与当年初次月降水高峰期吻合;在顺风的正南和东南方向上,种子扩散密度大且距离远;种子扩散主要集中在母株冠幅下,随着距母株距离的增加,种子扩散密度减少,二者间存在极显著的负相关性(P0.01),由于裸果木枝条繁多,对风力强度起到了一定的阻碍作用,可能是造成种子集中扩散在母株下的原因。裸果木种子扩散受外界环境(降水、风向)和自身因素等方面的影响,当种子在大量降水前完成扩散,将有利于种子在适宜的微生境萌发,是对多风、干旱的恶劣生境的一种长期适应。     

The importance of long-distance dispersal in biodiversity conservation

Dispersal is universally considered important for biodiversity conservation. However, the significance of long‐ as opposed to short‐distance dispersal is insufficiently recognized in the conservation context. Long‐distance dispersal (LDD) events, although typically rare, are crucial to population spread and to maintenance of genetic connectivity. The main threats to global biodiversity involve excessive LDD of elements alien to ecosystems and insufficient dispersal of native species, for example, because of habitat fragmentation. In this paper, we attempt to bridge the gap in the treatment of LDD by reviewing the conservation issues for which LDD is most important. We then demonstrate how taking LDD into consideration can improve conservation management decisions.     

Tracing the origin of Gulf Coast Phragmites (Poaceae): A story of long-distance dispersal and hybridization

? Premise of the study: Long-distance dispersal can affect speciation processes in two opposing ways. Dispersal can promote geographic isolation or it can bring together geographically distant and distantly related genotypes, thus counteracting local differentiation. We used the Gulf Coast of North America (GC), a "hot spot" of reed diversity and evolutionary dynamics, as a model system to study the diversification processes within the invasive, cosmopolitan, polyploid grass Phragmites. ? Methods: Genetic diversity was studied using collections representing all species of the genus and from all continents (except Antarctica). A range of molecular markers, including chloroplast and nuclear sequences, microsatellites, and AFLPs, was analyzed to detect DNA variation from the population to the species level and to infer phylogenetic relationships across continents. ? Key results: An interspecific hybrid, Phragmites mauritianus × P. australis, and four P. australis cp-DNA haplotypes from Africa, Europe, and North America have been dispersed to the GC and interbreed with each other. ? Conclusions: Long-distance dispersal and weak breeding barriers appear to be recurring phenomena, not only in the GC, but worldwide. We present data strongly suggesting that interspecific hybridization and introgression among different Phragmites species take place and appear to have contributed significantly to the diversification processes within the genus. Hence, the application of traditional species concepts within Phragmites might be inappropriate.     

Timing and spatial patterning of seed dispersal and redistribution in a South American warm desert

We measured newly-produced seeds entering the soil (Potential Seed Bank) to assess the timing and spatial patterning of Phase I dispersal in the central Monte desert, Argentina. Rates of forb- (6.13 mg m^-2 d^-1) and shrub-seed input (48.9 mg m^-2 d^-1) were maximum in early summer. The rate of grass-seed input, instead, was similar in early and late summer (7 to 8 mg m^-2 d^-1). About 90% of forb- and shrub-seed mass entered the habitat through protected (i.e., under canopy) areas, whereas 70% of grass-seed mass did so through exposed areas. Adult plant location and the uneven impact of wind on shrub, forb and grass seeds may explain such patterns.We also compared the Potential Seed Bank with the soil seed bank in the following spring (Realized Seed Bank). Seeds that form transient banks in other ecosystems (e.g., shrub seeds of the genus Larrea, or perennial grass seeds like those of Pappophorum and Trichloris) prevailed in the Potential Seed Bank. Some annual forb seeds, instead, appeared to form a more persistent seed bank, and prevailed in the Realized Seed Bank (e.g., Chenopodium). Horizontal redistribution did not affect the spatial patterning of forb and shrub seeds, but produced a more homogeneous distribution of grass seeds in the habitat. The impact of wind could explain the redistribution pattern of grass seeds. Finally, we found almost 80% of total seeds in the top 2 cm of soil. The smallest grass and forb seeds (Sporobolus and Descurainia) as well as some medium-sized and large forb seeds (e.g., Glandularia, Sphaeralcea, Phacelia) were able to reach deeper soil layers in the central Monte desert.     

High diversity of oilseed rape pollen clouds over an agro-ecosystem indicates long-distance dispersal

Abstract Estimating the frequency of long-distance pollination is important in cultivated species, particularly to assess the risk of gene transfer following the release of genetically modified crops. For this purpose, we estimated the diversity and origin of fertilizing pollen in a 10 x 10 km French oilseed rape production area. First, the cultivar grown in each field was identified through surveys to farmers and using microsatellite markers. Examination of the seed set in fields indicated high rates of seed contamination (8.7%) and pollination from other sources (5%). Then, male-sterile plants were scattered over the study area and their seed genotyped using the same markers. Most pollination was local: 65% of the seeds had a compatible sire in the closest field, i.e. at 50 or 300 m depending on site, but the nearest compatible field was found more than 1000 m away for 13% of the seeds. To assess the diversity of fertilizing pollen, each seed was assigned to the nearest putative siring cultivar. The observed diversity of pollen was then compared to that predicted by simulations using three empirical dispersal models with increasing proportion of long-distance pollination. The diversity was sensitive to the dispersal kernel used in the simulations, fatter-tailed functions predicting higher diversities. The dispersal kernel that was more consistent with our data predicted more long-distance dispersal than the exponential function.     

Temporal and spatial patterns of seed dispersal in two Cistus species (Cistaceae)

Cistus species are obligate seeding, early colonizers that follow disturbance, particularly fire, in Mediterranean ecosystems. We studied seed release, seed dispersal and soil seed populations in stands of Cistus ladanifer and C. libanotis. Seed release started in mid- to late summer (C. ladanifer) or in early autumn (C libanotis), and continued for a very extended period: 8-10 months in C. ladanifer, and for a mean of 16 months in C. libanotis. The xerochastic capsules of both species released seeds by successive dehiscence of the locules. All capsules begin to dehisce simultaneously at the start of the seed release period, but in C. libanotis capsule fragmentation replaced dehiscence early in the seed release period. In plants of both species, seed shadows were characterized by a peak of density beneath the plant canopy and a very short tail of much lower densities, indicating that seeds are concentrated beneath mother plants when dispersed. Nevertheless, in late May, at the onset of the fire season, soil seed densities beneath plant canopies were low compared with densities expected from seed shadows, but were apparently high enough to allow recovery of the stands if a disturbance, such as fire, had taken place. Seed-eating Bruchidae in summer and granivorous ants during the seed release period were apparently the main causes of seed losses. Results suggest that in both Cistus species, the staggered seed release could constitute an efficient risk-reducing trait. The plant pool of seeds existing throughout most of the year could be a relevant component of Cistus seed banks.     

Impact of the spatial uncertainty of seed dispersal on tree colonization dynamics in a temperate forest

An aggregated distribution of dispersed seeds may influence the colonization process in tree communities via inflated spatial uncertainty. To evaluate this possibility, we studied 10 tree species in a temperate forest: one primarily barochorous, six anemochorous and two endozoochorous species. A statistical model was developed by combining an empirical seed dispersal kernel with a gamma distribution of seedfall density, with parameters that vary with distance. In the probability density, the fitted models showed that seeds of Fagaceae (primarily barochorous) and Betulaceae (anemochorous) were disseminated locally (i.e. within 60 m of a mother tree), whereas seeds of Acer (anemochorous) and endozoochorous species were transported farther. Greater fecundity compensated for the lower probability of seed dispersal over long distances for some species. Spatial uncertainty in seedfall density was much greater within 60 m of a mother tree than farther away, irrespective of dispersal mode, suggesting that seed dispersal is particularly aggregated in the vicinity of mother trees. Simulation results suggested that such seed dispersal patterns could lead to sites in the vicinity of a tree being occupied by other species that disperse seeds from far away. We speculate that this process could promote coexistence by making the colonization rates of the species more similar on average and equalizing species fitness in this temperate forest community.     

Increases in air temperature can promote wind-driven dispersal and spread of plants

Long-distance dispersal (LDD) of seeds and pollen shapes the spatial dynamics of plant genotypes, populations and communities. Quantifying LDD is thus important for predicting the future dynamics of plants exposed to environmental changes. However, environmental changes can also alter the behaviour of LDD vectors: for instance, increasing air temperature may enhance atmospheric instability, thereby altering the turbulent airflow that transports seed and pollen. Here, we investigate temperature effects on wind dispersal in a boreal forest using a 10-year time series of micrometeorological measurements and a Lagrangian stochastic model for particle transport. For a wide range of dispersal and life history types, we found positive relations between air temperature and LDD. This translates into a largely consistent positive effect of +3°C warming on predicted LDD frequencies and spread rates of plants. Relative increases in LDD frequency tend to be higher for heavy-seeded plants, whereas absolute increases in LDD and spread rates are higher for light-seeded plants for which wind is often an important dispersal vector. While these predicted increases are not sufficient to compensate forecasted range losses and environmental changes can alter plant spread in various ways, our results generally suggest that warming can promote wind-driven movements of plant genotypes and populations in boreal forests.     

A first step towards inferring levels of long-distance dispersal during past expansions

Improving the realism of spatially explicit demographic models is important for better inferring the history of past populations and for understanding the genetic bases of adaptation and speciation. One particular type of demographic event to take into account is long-distance dispersal (LDD). The goals of this study are to explore the impact of various levels of LDD on genetic diversity and to show to what extent LDD levels can be correctly inferred from multilocus data sets using an approximate Bayesian computation approach. We therefore incorporated LDD into a 2D stepping stone forward simulation framework coupled to a coalescent backward simulation step to generate genetic diversity at 100 microsatellite markers under various demographic conditions relevant to recent human evolution. Our results confirm that LDD considerably increases genetic diversity within demes and decreases levels of diversity between demes. By controlling the spatial occurrence of LDD, it appears that LDD events occurring during a phase of range expansion into new territories are more important in maintaining genetic diversity than those occurring in the wake of the expansion or when colonization is over. We also show that it is possible to infer whether LDD has occurred during a range expansion, but our results suggest that one can only approximately estimate the extent of LDD based on genetic summary statistics.     

Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations

There is accumulating evidence that individuals leave their natal area and select a breeding habitat non-randomly by relying upon information about their natal and future breeding environments. This variation in dispersal is not only based on external information (condition dependence) but also depends upon the internal state of individuals (phenotype dependence). As a consequence, not all dispersers are of the same quality or search for the same habitats. In addition, the individual's state is characterized by morphological, physiological or behavioural attributes that might themselves serve as a cue altering the habitat choice of conspecifics. These combined effects of internal and external information have the potential to generate complex movement patterns and could influence population dynamics and colonization processes. Here, we highlight three particular processes that link condition-dependent dispersal, phenotype-dependent dispersal and habitat choice strategies: (1) the relationship between the cause of departure and the dispersers' phenotype; (2) the relationship between the cause of departure and the settlement behaviour and (3) the concept of informed dispersal, where individuals gather and transfer information before and during their movements through the landscape. We review the empirical evidence for these processes with a special emphasis on vertebrate and arthropod model systems, and present case studies that have quantified the impacts of these processes on spatially structured population dynamics. We also discuss recent literature providing strong evidence that individual variation in dispersal has an important impact on both reinforcement and colonization success and therefore must be taken into account when predicting ecological responses to global warming and habitat fragmentation.     

A simulation model of plant invasion: long-distance dispersal determines the pattern of spread

Mechanisms and consequences of biological invasions are a global issue. Yet, one of the key aspects, the initial phase of invasion, is rarely observed in detail. Data from aerial photographs covering the spread of Heracleum mantegazzianum (Apiaceae, native to Caucasus) on a local scale of hectares in the Czech Republic from the beginning of invasion were used as an input for an individual-based model (IBM), based on small-scale and short-time data. To capture the population development inferred from the photographs, long-distance seed dispersal, changes in landscape structures and suitability of landscape elements to invasion by H. mantegazzianum were implemented in the model. The model was used to address (1) the role of long-distance dispersal in regional invasion dynamics, and (2) the effect of land-use changes on the progress of the invasion. Simulations showed that already small fractions of seed subjected to long-distance dispersal, as determined by systematic comparison of field data and modelling results, had an over-proportional effect on the spread of this species. The effect of land-use changes on the simulated course of invasion depends on the actual level of habitat saturation; it is larger for populations covering a high proportion of available habitat area than for those in the initial phase of invasion. Our results indicate how empirical field data and model outputs can be linked more closely with each other to improve the understanding of invasion dynamics. The multi-level, but nevertheless simple structure of our model suggests that it can be used for studying the spread of similar species invading in comparable landscapes.     

Costs and benefits of non‐random seed release for long‐distance dispersal in wind‐dispersed plant species

The dispersal ability of plants is a major factor driving ecological responses to global change. In wind‐dispersed plant species, non‐random seed release in relation to wind speeds has been identified as a major determinant of dispersal distances. However, little information is available about the costs and benefits of non‐random abscission and the consequences of timing for dispersal distances. We asked: 1) to what extent is non‐random abscission able to promote long‐distance dispersal and what is the effect of potentially increased pre‐dispersal risk costs? 2) Which meteorological factors and respective timescales are important for maximizing dispersal? These questions were addressed by combining a mechanistic modelling approach and field data collection for herbaceous wind‐dispersed species. Model optimization with a dynamic dispersal approach using measured hourly wind speed showed that plants can increase long‐distance dispersal by developing a hard wind speed threshold below which no seeds are released. At the same time, increased risk costs limit the possibilities for dispersal distance gain and reduce the optimum level of the wind speed threshold, in our case (under representative Dutch meteorological conditions) to a threshold of 5–6 m s^–1. The frequency and predictability (auto‐correlation in time) of pre‐dispersal seed‐loss had a major impact on optimal non‐random abscission functions and resulting dispersal distances. We observed a similar, but more gradual, bias towards higher wind speeds in six out of seven wind‐dispersed species under natural conditions. This confirmed that non‐random abscission exists in many species and that, under local Dutch meteorological conditions, abscission was biased towards winds exceeding 5–6 m s^–1. We conclude that timing of seed release can vastly enhance dispersal distances in wind‐dispersed species, but increased risk costs may greatly limit the benefits of selecting wind conditions for long‐distance dispersal, leading to moderate seed abscission thresholds, depending on local meteorological conditions and disturbances.     

Propagule dispersal and the scales of marine community process

Benthic marine organisms are characterized by a bipartite life history in which populations of sedentary adults are connected by oceanic transport of planktonic propagules. In contrast with the terrestrial case, where ‘long distance dispersal’ (LDD) has traditionally been viewed as a process involving rare events, this creates the possibility for large numbers of offspring to travel far relative to the spatial scale of adult populations. As a result, the concept of LDD must be examined carefully when applied in a marine context. Any measure of LDD requires reference to an explicit ‘local’ scale, often defined in terms of adult population demography, habitat patchiness, or the average dispersal distance. Terms such as ‘open’ and ‘closed’ are relative, and should be used with caution, especially when compared across different taxa and systems. We use recently synthesized data on marine propagule dispersal potential and the spread of marine invasive species to draw inferences about average and maximum effective dispersal distances for marine taxa. Foremost, our results indicate that dispersal occurs at a wide range of scales in marine communities. The nonrandom distribution of these scales among community members has implications for marine community dynamics, and for the implementation of marine conservation efforts. Second, in agreement with theoretical results, our data illustrate that average and extreme dispersal scales do not necessarily covary. This further confounds simple classifications of ‘short’ and ‘long’ dispersers, because different ecological processes (e.g. range expansion vs. population replenishment) depend on different aspects of the dispersal pattern (e.g. extremes vs. average). Our findings argue for a more rigorous quantitative view of scale in the study of marine dispersal processes, where relative terms such as ‘short’ and ‘long’, ‘open’ and ‘closed’, ‘retained’ and ‘exported’ are defined only in conjunction with explicit definitions of the scale and process of interest. This shift in perspective represents an important step towards unifying theoretical and empirical studies of dispersal processes in marine and terrestrial systems.