The multiple dimensions of intraspecific variation in seed dispersal

The Sargassum beds in Gamak Bay, Korea, have deteriorated over recent decades. We conducted numerical experiments to assess the applicability of artificial reefs and longlines for seaweed forest restoration in terms of propagule dispersal. We applied hydrodynamic (Environment Fluid Dynamics Code (EFDC)), wave (Simulating Waves Nearshore (SWAN)), and particle tracking models for tidal currents, wave-induced currents, and the dispersal of the propagules, respectively. The major factors for propagule dispersal such as forcing, settling velocity w s , and release height were included, and the results of the models were analyzed using dispersal kernel, analysis of variance (ANOVA) tests, and survival rate based on bed elevation. The dispersal distance kernel was fitted to Gaussian and polynomial functions and showed higher wave impacts, whereby the mean dispersal distance was simulated 6.3 m under pure tide and increased by 14 times under the combined tide and wave condition. Propagules were found to hit the bottom intensively during a low-to-flood phase, while wave forcing enhanced vertical dispersal and hindered the intensive sinking. A two-dimensional dispersal location kernel showed that dispersal distance increased with high release heights and its direction faced the shoreline due to shallow water depth and strong wave-induced currents. ANOVA tests regarding the mean distance indicated that w s , forcing, release heights, and the combined effect of forcing and w s contributed 49.5, 20.5, 5.4, and 22.9 %, respectively, yielding a total of 72 % from w s . Adjusting the release height to extend dispersal distances led to A, C, and B locational effects, in order from lowest to highest, while survival rates were 67, 70, and 83 % for A, B, and C, respectively. From the results, we concluded that C is the most suitable locational type for restoration.

Seed dispersal by avian frugivores is one of the key processes influencing plant spatial patterns, but may fail if there is disruption of plant–frugivore mutualisms, such as decline in abundance of dispersers, fragmentation of habitat, or isolation of individual trees. We used simulation model experiments to examine the interaction between frugivore density and behaviour and the spatial arrangement of fruiting plants and its effect on seed dispersal kernels. We focussed on two New Zealand canopy tree species that produce large fruits and are dispersed predominantly by one avian frugivore ( Hemiphaga novaeseelandiae ). Although the mean seed dispersal distance decreased when trees became more aggregated, there were more frugivore flights between tree clusters, consequently stretching the tails of the dispersal kernels. Conversely, when trees were less aggregated in the landscape, mean dispersal distances increased because seeds were deposited over larger areas, but the kernels had shorter tails. While there were no statistically meaningful changes in kernel parameters when frugivore density changed, decreases in density did cause a proportional reduction in the total number of dispersed seeds. However, birds were forced to move further when fruit availability and fruit ripening were low. Sensitivity analysis showed that dispersal kernels were primarily influenced by the model parameters relating to disperser behaviour, especially those determining attractiveness based on distance to candidate fruiting trees. Our results suggest that the spatial arrangement of plants plays an important role in seed dispersal processes – although tree aggregation curbed the mean seed dispersal distance, it was accompanied by occasional long distance events, and tree dispersion caused an increase in mean dispersal distance, both potentially increasing the probability of seeds finding suitable habitats for germination and growth. Even though low frugivore densities did not cause dispersal failure, there were negative effects on the quantity of seed dispersal because fewer seeds were dispersed.

Intraspecific variation plays a pivotal role in shaping ecological dynamics. As the dispersal of seeds of most woody plants is mediated by animals, individual variation within the animal dispersers holds considerable implications for plant population and ecology. We explored how individual traits (such as sex, body mass and exploration levels) of yellow‐necked mice (Apodemus flavicollis) impact the dispersal of common oak (Quercus robur) acorns. Over 3 years, we collected data on seed fate and the specific mice responsible for their dispersal. The relationship between individual traits and seed dispersal was not static, but influenced by yearly environmental conditions. Heavier individuals tended to carry seeds farther, yet contrary to our expectations, sex had no effect on the distance of seed dispersal. Moreover, the exploration rate showed an inconsistent association with seed consumption and dispersal distance, while it positively impacted the distance of dispersal from the nearest tree. Synthesis. Our findings suggest a more nuanced role of individual traits in seed dispersal than often assumed, with noticeable annual variation significantly influencing these impacts. Consequently, it appears there is no single, universally beneficial individual type to ensure maximal benefits to plants. Rather, the traits conferring advantages in seed dispersal are dynamic, subject to change over time in response to environmental context. Read the free Plain Language Summary for this article on the Journal blog.

Seed dispersal fundamentally influences plant population and community dynamics but is difficult to quantify directly. Consequently, models are frequently used to describe the seed shadow (the seed deposition pattern of a plant population). For vertebrate-dispersed plants, animal behavior is known to influence seed shadows but is poorly integrated in seed dispersal models. Here, we illustrate a modeling approach that incorporates animal behavior and develop a stochastic, spatially explicit simulation model that predicts the seed shadow for a primate-dispersed tree species (Virola calophylla, Myristicaceae) at the forest stand scale. The model was parameterized from field-collected data on fruit production and seed dispersal, behaviors and movement patterns of the key disperser, the spider monkey (Ateles paniscus), densities of dispersed and non-dispersed seeds, and direct estimates of seed dispersal distances. Our model demonstrated that the spatial scale of dispersal for this V. calophylla population was large, as spider monkeys routinely dispersed seeds >>100 m, a commonly used threshold for long-distance dispersal. The simulated seed shadow was heterogeneous, with high spatial variance in seed density resulting largely from behaviors and movement patterns of spider monkeys that aggregated seeds (dispersal at their sleeping sites) and that scattered seeds (dispersal during diurnal foraging and resting). The single-distribution dispersal kernels frequently used to model dispersal substantially underestimated this variance and poorly fit the simulated seed-dispersal curve, primarily because of its multimodality, and a mixture distribution always fit the simulated dispersal curve better. Both seed shadow heterogeneity and dispersal curve multimodality arose directly from these different dispersal processes generated by spider monkeys. Compared to models that did not account for disperser behavior, our modeling approach improved prediction of the seed shadow of this V. calophylla population. An important function of seed dispersal models is to use the seed shadows they predict to estimate components of plant demography, particularly seedling population dynamics and distributions. Our model demonstrated that improved seed shadow prediction for animal-dispersed plants can be accomplished by incorporating spatially explicit information on disperser behavior and movements, using scales large enough to capture routine long-distance dispersal, and using dispersal kernels, such as mixture distributions, that account for spatially aggregated dispersal.

Seed dispersal is one of the most important ecosystem functions globally. It shapes plant populations, enhances forest succession, and has multiple, indirect benefits for humans, yet it is one of the most threatened processes in plant regeneration, worldwide. Seed dispersal distances are determined by the diets, seed retention times and movements of frugivorous animals. Hence, understanding how we can most effectively describe frugivore movement and behaviour with rapidly developing animal tracking technology is key to quantifying seed dispersal. To assess the current use of animal tracking in frugivory studies and to provide a baseline for future studies, we provide a comprehensive review and synthesis on the existing primary literature of global tracking studies that monitor movement of frugivorous animals. Specifically, we identify studies that estimate dispersal distances and how they vary with body mass and environmental traits. We show that over the last two decades there has been a large increase in frugivore tracking studies that determine seed dispersal distances. However, some taxa (e.g. reptiles) and geographic locations (e.g. Africa and Central Asia) are poorly studied. Furthermore, we found that certain morphological and environmental traits can be used to predict seed dispersal distances. We demonstrate that flight ability and increased body mass both significantly increase estimated seed dispersal mean and maximum distances. Our results also suggest that protected areas have a positive effect on mean seed dispersal distances when compared to unprotected areas. We anticipate that this review will act as a reference for future frugivore tracking studies, specifically to target current taxonomic and geographic data gaps, and to further explore how seed dispersal relates to key frugivore and fruit traits.

By dispersing seeds long distances, large, fruit-eating animals influence plant population spread and community dynamics. After fruit consumption, animal gut passage time and movement determine seed dispersal patterns and distances. These, in turn, are influenced by extrinsic, environmental variables and intrinsic, individual-level variables. We simulated seed dispersal by forest elephants (Loxodonta cyclotis) by integrating gut passage data from wild elephants with movement data from 96 individuals. On average, elephants dispersed seeds 5.3 km, with 89% of seeds dispersed farther than 1 km. The longest simulated seed dispersal distance was 101 km, with an average maximum dispersal distance of 40.1 km. Seed dispersal distances varied among national parks, perhaps due to unmeasured environmental differences such as habitat heterogeneity and configuration, but not with human disturbance or habitat openness. On average, male elephants dispersed seeds farther than females. Elephant behavioral traits strongly influenced dispersal distances, with bold, exploratory elephants dispersing seeds 1.1 km farther than shy, idler elephants. Protection of forest elephants, particularly males and highly mobile, exploratory individuals, is critical to maintaining long distance seed dispersal services that shape plant communities and tropical forest habitat.

The tropical tree, Platypodium elegans (Leguminosae: Papilionoideae), matures indehiscent wind-dispersed fruits containing one or, much less commonly, two seeds. Relative to single-seeded fruits, double-seeded fruits have greater wet mass, area, wingloading, and rate of descent in still air, and consequently are dispersed shorter distances under field conditions. The proximal seed of double-seeded fruits has a smaller dry mass and usually has lower and slower germination than the distal seed. Its radicle has difficulty emerging from the legume and establishing a root system, and the seedling has lower survival and slower growth. Twin seedlings arising from one fruit grow more slowly than single seedlings from doubleor single-seeded fruits, and both twins rarely survive to one year under growing house conditions. In fruit samples of equal size, more total seedlings emerge from doublethan single-seeded fruits; however, due to their lower probability of survival, double-seeded fruits have no more seedlings at one year under growing house conditions than do single-seeded fruits. Seed predation was not measured in this study. Unless multiseeded fruits more easily escape seed predation, there is no apparent evolutionary advantage to a parent of P. elegans producing multiseeded fruits. Their presence in low numbers appears to result from incomplete elimination or suppression of development of the multiple ovules after pollination. MANY TROPICAL TREES IN THE LEGUMINOSAE have winddispersed fruits. Their flowers commonly have more than one ovule, and they can produce multiseeded, indehiscent fruits. Although a large majority of their fruits are oneseeded, many species also produce a minority of multiseeded fruits. Any change in seed number per fruit has the potential to affect patterns of resource allocation to seeds and fruits, seed predation, dispersal distance, and subsequent germination and seedling survival and growth. For an herbaceous legume using ballistic dispersal, Lee (1984) showed that an increase in seed number per fruit increased the variance, but not the mean, in dispersal distance. Casper and Wiens (1981) have argued that reduced seed number per fruit is achieved by a fixed rate of ovule abortion, and perhaps enhances dispersal by wind in Ctyptantha flava. Following are the results of a study of the tropical canopy tree, Platypodium elegans J. Vogel ((Leguminosae: Papilionoideae). It produces indehiscent, wind-dispersed fruits containing either one or two seeds. The study begins by determining how this variability in seed number affects traits that define the dispersal potential of the fruits, i.e., mass, area, wind-loading, and rate of descent. Next it examines whether double-seeded fruits are dispersed shorter distances than single-seeded fruits. Finally, in a screened greenhouse, the study identifies differences between the two fruit types in seed mass and germination level, and in subsequent survival and growth of seedlings. STUDY SITE AND NATURAL HISTORY The study took place in 1980-1981 in the semideciduous lowland forest on Barro Colorado Island, Panama. Details of this biological preserve are described in Croat (1978) and Leigh et al. (1982). Platypodium elegans is a canopy tree of low abundance on the island. Its flowers have up to four ovules. Seed development usually occurs in the most distal ovule, and never in the two most proximal ovules. The legumes are obliquely oblong, up to 13 cm long and 3.6 cm wide in single-seeded fruits and 16 cm long and 4.5 cm wide in double-seeded fruits. The seed or seeds are in the distal end of the fruit. The portion of the fruit surrounding the seeds is quite thick and woody; by contrast the fruit's wing is highly vascularized and

BackgroundHundreds of millions of people get a mosquito-borne disease every year and nearly one million die. Transmission of these infections is primarily tackled through the control of mosquito vectors. The accurate quantification of mosquito dispersal is critical for the design and optimization of vector control programs, yet the measurement of dispersal using traditional mark-release-recapture (MRR) methods is logistically challenging and often unrepresentative of an insect’s true behavior. Using Aedes aegypti (a major arboviral vector) as a model and two study sites in Singapore, we show how mosquito dispersal can be characterized by the spatial analyses of genetic relatedness among individuals sampled over a short time span without interruption of their natural behaviors.ResultsUsing simple oviposition traps, we captured adult female Ae. aegypti across high-rise apartment blocks and genotyped them using genome-wide SNP markers. We developed a methodology that produces a dispersal kernel for distance which results from one generation of successful breeding (effective dispersal), using the distance separating full siblings and 2nd- and 3rd-degree relatives (close kin). The estimated dispersal distance kernel was exponential (Laplacian), with a mean dispersal distance (and dispersal kernel spread σ) of 45.2 m (95% CI 39.7–51.3 m), and 10% probability of a dispersal > 100 m (95% CI 92–117 m). Our genetically derived estimates matched the parametrized dispersal kernels from previous MRR experiments. If few close kin are captured, a conventional genetic isolation-by-distance analysis can be used, as it can produce σ estimates congruent with the close-kin method if effective population density is accurately estimated. Genetic patch size, estimated by spatial autocorrelation analysis, reflects the spatial extent of the dispersal kernel “tail” that influences, for example, the critical radii of release zones and the speed of Wolbachia spread in mosquito replacement programs.ConclusionsWe demonstrate that spatial genetics can provide a robust characterization of mosquito dispersal. With the decreasing cost of next-generation sequencing, the production of spatial genetic data is increasingly accessible. Given the challenges of conventional MRR methods, and the importance of quantified dispersal in operational vector control decisions, we recommend genetic-based dispersal characterization as the more desirable means of parameterization.

The optimal probability and distance of dispersal largely depend on the risk to end up in unsuitable habitat. This risk is highest close to the habitat's edge and consequently, optimal dispersal probability and distance should decline towards the habitat's border. This selection should lead to the emergence of spatial gradients in dispersal strategies. However, gene flow caused by dispersal itself is counteracting local adaptation. Using an individual based model we investigate the evolution of local adaptations of dispersal probability and distance within a single, circular, habitat patch. We compare evolved dispersal probabilities and distances for six different dispersal kernels (two negative exponential kernels, two skewed kernels, nearest neighbour dispersal and global dispersal) in patches of different size. For all kernels a positive correlation between patch size and dispersal probability emerges. However, a minimum patch size is necessary to allow for local adaptation of dispersal strategies within patches. Beyond this minimum patch area the difference in mean dispersal distance between center and edge increases linearly with patch radius, but the intensity of local adaptation depends on the dispersal kernel. Except for global and nearest neighbour dispersal, the evolved spatial pattern are qualitatively similar for both, mean dispersal probability and distance. We conclude, that inspite of the gene‐flow originating from dispersal local adaptation of dispersal strategies is possible if a habitat is of sufficient size. This presumably holds for any realistic type of dispersal kernel.

The process of seed dispersal that underpins ecosystem maintenance is performed by diverse arrays of fruit‐eating animals. However, seed dispersal studies are primarily focused on a subset of these animal communities that disperse seeds by endozoochory. Stomatochory (seed dispersal in which seeds are carried externally and are not swallowed) is rarely considered to be effective, despite an increasing number of taxa‐focused studies that indicate otherwise. We collated the available information on stomatochory to provide a quantitative overview of the dispersal mechanism, including plant types and fruit traits dispersed, dispersal distances and germination potential for all available taxa. We compared seed sizes dispersed, dispersal distances and germination potential with corresponding data on endozoochory for bats and primates. We also identified the main taxa dispersing seeds by stomatochory and assessed what factors influenced the distances that they carried seeds to. Stomatochoric dispersers can displace large quantities of seeds, including large seeds and those of large fruits, and over short to long distances (>1 km). Compared with similar‐sized endozoochoric dispersers, they can disperse larger seeds, but over shorter distances, on average. Similar to endozoochory, seed handling by stomatochory also improves the germination potential of dispersed seeds. Dispersal distances achieved by stomatochory were influenced by body mass, daily path length, seed width, fruit type and seed handling techniques. Five main taxonomic groups of stomatochoric dispersers were identified: bats, parrots, squirrels, corvids and Old World monkeys (cercopithecines). Parrots perform dispersal services for the largest fruits and over the longest distances. However, given the lack of research on stomatochory, it is likely other taxa are also important stomatochoric dispersers but have not been identified yet. More research attention must be directed towards seed dispersal services that are not provided by endozoochory. Many stomatochoric dispersers are common animals within communities and could be playing dominant seed dispersal roles, even without swallowing seeds. Community‐wide studies should incorporate all seed dispersal interactions, rather than focusing solely on endozoochory. This will ensure a more robust understanding of community‐wide patterns. Read the free Plain Language Summary for this article on the Journal blog.

Dispersal of organisms is a ubiquitous aspect of the natural world, with wide implications across scales and organization levels. Interest in dispersal has risen sharply over the past 30 years, mostly due to the multiple and rapid global changes ecosystems face. Among the various aspects that may characterize a dispersion event, dispersal distance is considered a key descriptor in a wide variety of studies across taxonomic groups. Typically, dispersal distances are defined in the form of dispersal kernels describing the dispersal distance distribution according to probability density functions. Although numerous methods providing dispersal data exist, there is still a lack of intuitive and comprehensive approaches and tools to estimate dispersal kernels from such data. Here we present the dispfit package, an R software application developed to fill this gap. dispfit fits and compares different families of parameterized functions to describe and predict dispersal distances. It includes 9 well-known and commonly used distributions, computes goodness-of-fit and model selection statistics, and estimate each distribution's parameters, along with their first four moments (mean, standard deviation, skewness, and kurtosis). We describe the main functions included in dispfit and provide an example to illustrate the workflow of the typical analyses performed within the package. We believe that dispfit will critically contribute to improving the modelling of species' dispersal distances, thus enhancing the understanding of the ecological and evolutionary processes involving dispersal movement.

Plant populations in fragmented ecosystems rely largely on internal dispersal by animals. To unravel the mechanisms underlying this mode of dispersal, an increasing number of experimental feeding studies is carried out. However, while physical activity is known to affect vertebrate digestive processes, almost all current knowledge on mechanisms of internal seed dispersal has been obtained from experiments with resting animals. We investigated how physical activity of the mallard Anas platyrhynchos , probably the quantitatively most important biotic dispersal agent in aquatic habitats in the entire Northern Hemisphere, affects gut passage survival and retention time of ingested plant seeds. We fed seeds of nine common wetland plants to mallards trained to subsequently swim for six hours in a flume tank at different swimming speeds (activity levels). We compared gut passage survival and retention times of seeds against a control treatment with mallards resting in a conventional dry cage. Intact gut passage of seeds increased significantly with mallard activity (up to 80% in the fastest swimming treatment compared to the control), identifying reduced digestive efficiency due to increased metabolic rates as a mechanism enhancing the dispersal potential of ingested seeds. Gut passage speed was modestly accelerated (13% on average) by increased mallard activity, an effect partly obscured by the interaction between seed retention time and probability of digestion. Gut passage acceleration will be more pronounced in digestion‐resilient seed species, thereby modulating their dispersal distances. Our findings imply that seed dispersal potential by mallards calculated from previous experiments with resting birds is highly underestimated, while dispersal distances may be overestimated for some plant species. Similar effects of physical activity on digestive efficiency of mammals suggests that endozoochorous dispersal of plant seeds by vertebrates is more effective and plays a quantitatively more important ecological role in both terrestrial and aquatic ecosystems than previously thought.

Aim We estimated the patterns of seed deposition provided by the eyed lizard, Timon lepidus, and evaluated whether these patterns can be generalized across plant species with different traits (fruit and seed size) and spatial distributions.Location Monteagudo Island, Atlantic Islands National Park (north‐western Spain).Methods We radio‐tracked seven lizards for 14 days and estimated their home ranges using fixed kernels. We also geo‐referenced all fruit‐bearing individuals of four plant species dispersed by eyed lizards in the study area (Corema album, Osyris alba, Rubus ulmifolius and Tamus communis), measured the passage time of their seeds through the lizard gut, and estimated seed predation in four habitats (bare sand, grassland, shrub and gorse). Seed dispersal kernels were estimated using a combination of these data and were combined with seed predation probability maps to incorporate post‐dispersal seed fate (‘seed survival kernels’).Results Median seed gut‐passage times were around 52–98 h, with maximum values up to 250 h. Lizards achieved maximum displacement in their home ranges within 24–48 h. Seed predation was high (80–100% of seeds in 2 months), particularly under Corema shrub and gorse. Seed dispersal kernels showed a common pattern, with two areas of preferential seed deposition, but the importance of these varied among plant species. Interspecific differences among dispersal kernels were strongly reduced by post‐dispersal seed predation; hence, seed survival kernels of the different plant species showed high auto‐ and pairwise‐correlations at small distances (< 50 m). As a result, survival to post‐dispersal seed predation increased with dispersal distance for O. alba and T. communis, but not for C. album.Main conclusions Seed dispersal by lizards was determined primarily by the interaction between the dispersers’ home ranges and the position of the fruit‐bearing plants. As a result, seed rain shared a common template, but showed considerable variation among species, determined by their specific spatial context. Seed predation increased the spatial coherence of the seed rain of the different species, but also resulted in contrasting relationships between seed survival and dispersal distance, which may be of importance for the demographic and evolutionary processes of the plants.

Frugivores are highly variable in their contribution to fruit removal in plant populations. However, data are lacking on species-specific variation in two central aspects of seed dispersal, distance of dispersal and probability of dispersal among populations through long-distance transport. We used DNA-based genotyping techniques on Prunus mahaleb seeds dispersed by birds (small- and medium-sized passerines) and carnivorous mammals to infer each seed's source tree, dispersal distance, and the probability of having originated from outside the study population. Small passerines dispersed most seeds short distances (50% dispersed <51 m from source trees) and into covered microhabitats. Mammals and medium-sized birds dispersed seeds long distances (50% of mammals dispersed seeds >495 m, and 50% of medium-sized birds dispersed seeds to >110 m) and mostly into open microhabitats. Thus, dispersal distance and microhabitat of seed deposition were linked through the contrasting behaviors of different frugivores. When the quantitative contribution to fruit removal was accounted for, mammals were responsible for introducing two-thirds of the immigrant seeds into the population, whereas birds accounted for one-third. Our results demonstrate that frugivores differ widely in their effects on seed-mediated gene flow. Despite highly diverse coteries of mutualistic frugivores dispersing seeds, critical long-distance dispersal events might rely on a small subset of large species. Population declines of these key frugivore species may seriously impair seed-mediated gene flow in fragmented landscapes by truncating the long-distance events and collapsing seed arrival to a restricted subset of available microsites.

1. Dispersal is a fundamental ecological process, so spatial models require realistic dispersal kernels. We compare five different forms for the dispersal kernel of the tansy beetle Chrysolina graminis moving between patches of its host-plant (tansy Tanacetum vulgare) in a riparian landscape. 2. Multi-patch mark-recapture data were collected every 2 weeks over 2 years within a large network of patches and from 2226 beetles. Dispersal was common (28.4% of 880 recaptures after a fortnight) and was more likely over longer intervals, out of small patches, for females and during flooding. Interpatch movement rates did not differ between years and exhibited no density dependence. Dispersal distances were similar for males and females, in both years and over all intervals, with a median dispersal distance of just 9.8 m, although a maximum of 856 m was recorded. 3. A model of dispersal, where patches competed for dispersers based on their size and distance from the beetle's source patch (scaled by the dispersal kernel) was fitted to the field data with a maximum likelihood procedure and each of five alternative kernels. The best fitting had relatively extended tails of long-distance dispersal, while Gaussian and negative exponential kernels performed worst. 4. The model suggests that females disperse more commonly than males and that both are strongly attracted to large patches but do not differ between years, which are consistent with the empirical results. Model-predicted emigration and immigration rates and dispersal phenologies match those observed, suggesting that the model captured the major drivers of tansy beetle dispersal. 5. Although negative exponential and Gaussian kernels are widely used for their simplicity, we suggest that these should not be the models of automatic choice, and that fat-tailed kernels with relatively higher proportions of long-distance dispersal may be more realistic.