Limited seed dispersal shapes fine-scale spatial genetic structure in a Neotropical dioecious large-seeded palm

Seed and pollen dispersal contribute to gene flow and shape the genetic patterns of plants over fine spatial scales. We inferred fine-scale spatial genetic structure (FSGS) and estimated realized dispersal distances in Phytelephas aequatorialis, a Neotropical dioecious large-seeded palm. We aimed to explore how seed and pollen dispersal shape this genetic pattern in a focal population. For this purpose, we genotyped 138 seedlings and 99 adults with 20 newly developed microsatellite markers. We tested if rodent-mediated seed dispersal has a stronger influence than insect-mediated pollen dispersal in shaping FSGS. We also tested if pollen dispersal was influenced by the density of male palms around mother palms in order to further explore this ecological process in large-seeded plants. Rodent-mediated dispersal of these large seeds occurred mostly over short distances (mean 34.76 ± 34.06 m) while pollen dispersal distances were two times higher (mean 67.91 ± 38.29 m). The spatial extent of FSGS up to 35 m and the fact that seed dispersal did not increase the distance at which male alleles disperse suggest that spatially limited seed dispersal is the main factor shaping FSGS and contributes only marginally to gene flow within the population. Pollen dispersal distances depended on the density of male palms, decreasing when individuals show a clumped distribution and increasing when they are scattered. Our results show that limited seed dispersal mediated by rodents shapes FSGS in P. aequatorialis, while more extensive pollen dispersal accounts for a larger contribution to gene flow and may maintain high genetic diversity. Abstract in Spanish is available with online material.     

Demographic spatial genetic structure of the Neotropical tree, Jacaranda copaia

We used genotypes from six microsatellite loci and demographic data from a large mapped forest plot to study changes in spatial genetic structure across demographic stages, from seed rain to seedlings, juveniles, and adult diameter classes in the Neotropical tree, Jacaranda copaia. In pairwise comparisons of genetic differentiation among demographic classes, only seedlings were significantly differentiated from the other diameter classes; F(ST) values ranged from 0.006 to 0.009. Furthermore, only seedlings showed homozygote excess suggesting biparental inbreeding in the large diameter reproductive adults. We found very low levels of relatedness in the first distance class of trees, 1-26 cm diameter (F(ij) = 0.011). However, there was a 5- to 10-fold rise in relatedness in the smallest distance class, from the smallest to the largest tree diameter classes (F(ij) = 0.110 for individuals > 56 cm diameter). A variety of non-mutually exclusive mechanisms have been invoked perviously to explain such a pattern, including natural selection, history, or nonequilibrium population dynamics. The long-term demographic data available for this species allow us to evaluate these mechanisms. Jacaranda is a fast-growing, light-demanding species with low recruitment rates and high mortality rates in the smaller diameter classes. It successfully regenerates only in large light gaps, which occur infrequently and stochastically in space and time. These factors contribute to the nonequilibrium population dynamics and observed low genetic structure in the small size classes. We conclude that the pattern of spatial genetic transitions in Jacaranda is consistent with overlapping related generations and strong but infrequent periods of high recruitment, followed by long periods of population decline.     

Intraspecific variation in seed dispersal of a Neotropical tree and its relationship to fruit and tree traits

The distribution of wind‐dispersed seeds around a parent tree depends on diaspore and tree traits, as well as wind conditions and surrounding vegetation. This study of a neotropical canopy tree, Platypodium elegans, explored the extent to which parental variation in diaspore and tree traits explained (1) rate of diaspore descent in still air, (2) distributions of diaspores dispersed from a 40‐m tower in the forest, and (3) natural diaspore distributions around the parent tree. The geometric mean rate of descent in still air among 20 parents was highly correlated with geometric mean wing loading^1/2 (r = 0.84). However, diaspore traits and rate of descent predicted less variation in dispersal distance from the tower, although descent rate⁻¹ consistently correlated with dispersal distance. Measured seed shadows, particularly their distribution edges, differed significantly among six parents (DBH range 62–181 cm) and were best fit by six separate anisotropic dispersal kernels and surveyed fecundities. Measured rate of descent and tree traits, combined in a mechanistic seed dispersal model, did not significantly explain variation among parents in natural seed dispersal distances, perhaps due to the limited power to detect effects with only six trees. Seedling and sapling distributions were at a greater mean distance from the parents than seed distributions; saplings were heavily concentrated at far distances. Variation among parents in the distribution tails so critical for recruitment could not be explained by measured diaspore or tree traits with this sample size, and may be determined more by wind patterns and the timing of abscission in relation to wind conditions. Studies of wind dispersal need to devote greater field efforts at recording the “rare” dispersal events that contribute to far dispersal distances, following their consequences, and in understanding the mechanisms that generate them.     

Effects of seed dispersal, adult tree and seedling density on the spatial genetic structure of regeneration at fine temporal and spatial scales

Several demographic factors can produce family structured patches within natural plant populations, particularly limited seed and pollen dispersal and small effective density. In this paper, we used computer simulations to examine how seed dispersal, density, and spatial distribution of adult trees and seedlings can explain the spatial genetic structure (SGS) of natural regeneration after a single reproductive event in a small population. We then illustrated the results of our simulations using genetic (isozymes and chloroplast microsatellites) and demographic experimental data from an Abies alba (silver fir) intensive study plot located in the Southern French Alps (Mont Ventoux). Simulations showed that the structuring effect of limited dispersal on seedling SGS can largely be counterbalanced by high effective density or a clumped spatial distribution of adult trees. In addition, the clumping of natural regeneration far from adult trees, which is common in temperate forest communities where gap dynamics are predominant, further decreases SGS intensity. Contrary to our simulation results, low adult tree density, aggregated spatial distribution of seedlings, and limited seed dispersal did not generate a significant SGS in our A. alba experimental plot. Although some level of long distance pollen and seed flow could explain this lack of SGS, our experimental data confirm the role of spatial aggregation (both in adult trees and in seedlings far from adult trees) in reducing SGS in natural populations.     

The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations

Seed dispersal mechanisms should have a direct impact on the genetic structure of populations. Species whose seeds are dispersed near the maternal plant (e.g. gravity or wind dispersal) or species whose seeds are deposited in clumps or patches should have more fine-scale genetic structure than species whose seeds are dispersed singly by mobile animals. Furthermore, due to the overlap of seed shadows, species with high adult densities should have less genetic structure than species with lower densities. Allozyme analyses of three tropical tree species belonging to the moist tropical forest of Barro Colorado Island, Republic of Panama, were used to describe variation in the scale and intensity of genetic structure within their populations. The genetic structure of seedlings and immature trees in the low-density, wind-dispersed species (Platypodium elegans) was the coarsest and strongest whereas genetic structure in a population of Swartzia simplex var. ochnacea (high density, bird-dispersed) was both the finest and the weakest. The genetic structure of Alseis blackiana, a high-density, wind-dispersed species was intermediate in both degree and scale. In P. elegans and A. blackiana, which had J shaped size distributions, the significant genetic structure seen in the smaller and intermediate diameter classes disappeared in the largest diameter class. The loss of genetic structure was not observed in S. simplex, a species with a more even size distribution.     

A genetic evaluation of seed dispersal in the neotropical tree Jacaranda copaia (Bignoniaceae)

Seed dispersal is a critical but poorly understood life-history stage of plants. Here we use a genetic approach to describe seed dispersal patterns accurately in a natural population of the Neotropical tree species Jacaranda copaia (Bignoniaceae). We used microsatellite genotypes from maternally derived tissue on the diaspore to identify which individual of all possible adult trees in the population was the true source of a given seed collected after it dispersed. Wind-dispersed seeds were captured in two different years in a large array of seed traps in an 84-ha mapped area of tropical forest on Barro Colorado Island, Panama. We were particularly interested in the proportion of seeds that traveled long distances and whether there was evidence for direct dispersal into gaps, which are required for successful recruitment of this pioneer tree species. Maximum likelihood procedures were used to fit single- and multiple-component dispersal kernels to the distance data. Mixture models, with separate distributions near and far, best fit the observed dispersal distances, albeit with considerable uncertainty in the tail. We discuss the results in light of different mechanisms responsible for separate distributions near the adult source and in the tail of the curve.     

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.     

Estimating seed vs. pollen dispersal from spatial genetic structure in the common ash

Spatial genetic structure was analysed with five highly polymorphic microsatellite loci in a Romanian population of common ash (Fraxinus excelsior L.), a wind-pollinated and wind-dispersed tree species occurring in mixed deciduous forests over almost all of Europe. Contributions of seed and pollen dispersal to total gene flow were investigated by analysing the pattern of decrease in kinship coefficients among pairs of individuals with geographical distance and comparing it with simulation results. Plots of kinship against the logarithm of distance were decomposed into a slope and a shape component. Simulations showed that the slope is informative about the global level of gene flow, in agreement with theoretical expectations, whereas the shape component was correlated with the relative importance of seed vs. pollen dispersal. Hence, our results indicate that insights into the relative contributions of seed and pollen dispersal to overall gene flow can be gained from details of the pattern of spatial genetic structure at biparentally inherited loci. In common ash, the slope provided an estimate of total gene dispersal in terms of Wright's neighbourhood size of Nb = 519 individuals. No precise estimate of seed vs. pollen flow could be obtained from the shape because of the stochasticity inherent to the data, but the parameter combinations that best fitted the data indicated restricted seed flow, sigmas pound 14 m, and moderate pollen flow, 70 m pound sigmap pound 140 m.     

Loss of animal seed dispersal increases extinction risk in a tropical tree species due to pervasive negative density dependence across life stages

Overhunting in tropical forests reduces populations of vertebrate seed dispersers. If reduced seed dispersal has a negative impact on tree population viability, overhunting could lead to altered forest structure and dynamics, including decreased biodiversity. However, empirical data showing decreased animal-dispersed tree abundance in overhunted forests contradict demographic models which predict minimal sensitivity of tree population growth rate to early life stages. One resolution to this discrepancy is that seed dispersal determines spatial aggregation, which could have demographic consequences for all life stages. We tested the impact of dispersal loss on population viability of a tropical tree species, Miliusa horsfieldii, currently dispersed by an intact community of large mammals in a Thai forest. We evaluated the effect of spatial aggregation for all tree life stages, from seeds to adult trees, and constructed simulation models to compare population viability with and without animal-mediated seed dispersal. In simulated populations, disperser loss increased spatial aggregation by fourfold, leading to increased negative density dependence across the life cycle and a 10-fold increase in the probability of extinction. Given that the majority of tree species in tropical forests are animal-dispersed, overhunting will potentially result in forests that are fundamentally different from those existing now.     

Combined impacts of multiple non-native mammals on two life stages of a critically endangered Neotropical tree

Despite of the widespread co-occurrence of multiple invaders, little is known on their combined ecological impacts and on their effects on different life stages of native species. We assessed the joint impacts of four non-native mammals (cattle, horse, European hare Lepus europaeus, and wild boar Sus scrofa) on seed surplus and seedling abundance of the Paraná pine (Araucaria angustifolia), a critically-endangered species of the Atlantic Forest. We found that its seeds constitute an autumn food resource for a native community richer than previously thought, with 70 bird and mammal species as confirmed or potential seed consumers, of which 40 were not previously recognized as such. We also recorded the number of uneaten seeds and seedlings at the middle-end of autumn under 520 female Paraná pine trees across the species’ distribution and identified signs of the species consuming seeds from each tree through direct observations combined with camera trapping. Most of the sampled trees (98%) were visited by at least one seed consumer species, and over 60% were visited by at least one non-native mammal. Seed surplus strongly declined in the presence of cattle, horses and wild boars, their impacts being additive, whereas the number of seedlings declined in the presence of European hares. Our results emphasize the importance of Paraná pine seeds for native fauna and the additive impact of invaders in a species-rich ecosystem. Seed predation by non-native species reduces the potential regeneration of Paraná pine forests, and may severely reduce food supply for its native consumers.     

Consequences of frugivore-mediated seed dispersal for the spatial and genetic structures of a neotropical palm

The idiosyncratic behaviours of seed dispersers are important contributors to plant spatial associations and genetic structures. In this study, we used a combination of field, molecular and spatial studies to examine the connections between seed dispersal and the spatial and genetic structures of a dominant neotropical palm Attalea phalerata. Field observation and genetic parentage analysis both indicated that the majority of A. phalerata seeds were dispersed locally over short distances (<30 m from the maternal tree). Spatial and genetic structures between adults and seedlings were consistent with localized and short-distance seed dispersal. Dispersal contributed to spatial associations among maternal sibling seedlings and strong spatial and genetic structures in both seedlings dispersed near (<10 m) and away (>10 m) from maternal palms. Seedlings were also spatially aggregated with juveniles. These patterns are probably associated with the dispersal of seeds by rodents and the survival of recruits at specific microsites or neighbourhoods over successive fruiting periods. Our cross-cohort analyses found palms in older cohorts and cohort pairs were associated with a lower proportion of offspring and sibling neighbours and exhibited weaker spatial and genetic structures. Such patterns are consistent with increased distance- and density-dependent mortality over time among palms dispersed near maternal palms or siblings. The integrative approaches used for this study allowed us to infer the importance of seed dispersal activities in maintaining the aggregated distribution and significant genetic structures among A. phalerata palms. We further conclude that distance- and density-dependent mortality is a key postdispersal process regulating this palm population.     

Long-distance seed and pollen dispersal inferred from spatial genetic structure in the very low-density rainforest tree, Baillonella toxisperma Pierre, in Central Africa

We analysed the spatial distribution of genetic diversity to infer gene flow for Baillonella toxisperma Pierre (Moabi), a threatened entomophilous pollinated and animal-dispersed Central African tree, with typically low density (5-7 adults trees/km(2)). Fifteen nuclear and three universal chloroplast microsatellites markers were used to type 247 individuals localized in three contiguous areas with differing past logging intensity. These three areas were within a natural forest block of approximately 2886 km(2) in Gabon. Expected heterozygosity and chloroplast diversity were He(nuc) = 0.570 and H(cp) = 0.761, respectively. F(IS) was only significant in one area (F(IS) = 0.076, P < 0.01) and could be attributed to selfing. For nuclear loci, Bayesian clustering did not detect discrete gene pools within and between the three areas and global differentiation (F(STnuc) = 0.007, P > 0.05) was not significant, suggesting that they are one population. At the level of the whole forest, both nuclear and chloroplast markers revealed a weak correlation between genetic relatedness and spatial distance between individuals: Sp(nuc) = 0.003 and Sp(cp) = 0.015, respectively. The extent of gene flow (σ) was partitioned into global gene flow (σ(g)) from 6.6 to 9.9 km, seed dispersal (σ(s)) from 4.0 to 6.3 km and pollen dispersal (σ(p)) from 9.8 to 10.8 km. These uncommonly high dispersal distances indicate that low-density canopy trees in African rainforests could be connected by extensive gene flow, although, given the current threats facing many seed disperser species in Central Africa, this may no longer be the case.     

Small-scale spatial structure within patterns of seed dispersal

A large proportion of dispersing propagules land near their maternal plant, even in species that have evolved structures which enhance dispersal. For these propagules, their post-dispersal spatial pattern is likely to reflect the overall shape and scale of the parental plant canopy and, especially in poorly dispersing species, aggregation of propagules on the plant prior to dispersal. Localised patterns within seed shadows are also likely to be affected by secondary movement after dispersal, leading to either more or less small-scale aggregation, depending on the mechanism. Our general aim was to study the small-scale spatial structure within patterns of seed dispersal of Raphanus raphanistrum L. to generate hypotheses about the sequence of processes and events leading to the spatial pattern of dispersal in this species. More specifically, we determined the sizes of small-scale structures within the seed shadows on the ground after dispersal and the extent to which these match the sizes of pre-dispersal aggregations within the parental canopy. Variation in plant size and shape was provided by four levels of inter-specific competition resulting from differing wheat crop densities. Positions of propagules were determined using a three-dimensional digitizer, and the data for each plant were analysed using point pattern analysis. Not surprisingly, larger plants, growing at lower plant density, had larger seed shadows, showing an overall influence of maternal plant size. The pattern of propagules exhibited significant small-scale aggregates, with similar sizes on the plant and on the ground. There was no evidence that aggregation size was greater on the ground or increased with time, but the strength of the aggregation increased with length of time on the ground.     

Ant-mediated seed dispersal contributes to the local spatial pattern and genetic structure of Globba lancangensis (Zingiberaceae)

Globba lancangensis is a typical myrmecochorous perennial herb found in southwest China. In 2002 and 2003, seed dispersal by ants was examined. Twelve ant species were recorded and found to move seeds 0.01-3.35 m. This removal promoted seed dispersal. In 2003, ant exclusion was made in 4 of 8 study plots for 1 year to practically detect the effects of ant dispersal. As a result, nearest neighbor analyses indicated that although ant dispersal could not significantly change the mean nearest neighbor distance, it obviously reduced the clustering degree of seedlings. Spatial genetic structure (SGS) of mature plants in 2003 and sequent seedlings in 2004 were investigated with intersimple sequence repeats. The whole correlagram of all individuals from 2003 showed significant positive autocorrelations between genetic and geographical distances within 4 m, suggesting a patchy structure at such short distances in the studied population. This pattern is likely associated with limited seed dispersal. The comparative analysis of fine-scale correlograms (<4 m) for ant-excluded treatment indicated lacking ants as the primary dispersers could have a similar pattern to ant dispersal presence, which is likely due to the restriction of ant dispersal distance. In conclusion, ant-mediated dispersal contributes to reduce seedling clustering degree and plays a minor role in developing and maintaining the local SGS in G. lancangensis.     

Negative density dependence of seed dispersal and seedling recruitment in a Neotropical palm

Negative density dependence (NDD) of recruitment is pervasive in tropical tree species. We tested the hypotheses that seed dispersal is NDD, due to intraspecific competition for dispersers, and that this contributes to NDD of recruitment. We compared dispersal in the palm Attalea butyracea across a wide range of population density on Barro Colorado Island in Panama and assessed its consequences for seed distributions. We found that frugivore visitation, seed removal and dispersal distance all declined with population density of A. butyracea, demonstrating NDD of seed dispersal due to competition for dispersers. Furthermore, as population density increased, the distances of seeds from the nearest adult decreased, conspecific seed crowding increased and seedling recruitment success decreased, all patterns expected under poorer dispersal. Unexpectedly, however, our analyses showed that NDD of dispersal did not contribute substantially to these changes in the quality of the seed distribution; patterns with population density were dominated by effects due solely to increasing adult and seed density.     

Agouti reintroduction recovers seed dispersal of a large-seeded tropical tree

The aim of animal reintroductions has mainly been species recovery; only few reintroduction initiatives focus on ecosystem restoration. Therefore, reintroduction consequences on ecological interactions are seldom assessed. We used the interaction between a reintroduced population of agoutis (Dasyprocta leporina) and a vulnerable tropical endemic tree (Joannesia princeps) to examine reintroduction effects on seed dispersal and seedling establishment. To test the outcomes of this interaction, we tracked seeds of J. princeps in two adjacent forest areas with and without reintroduced agoutis. We also assessed if dispersal distances affected seedling survival. To determine seed fate and dispersal distance, we used spool-and-line tracking, together with camera traps to identify dispersers. Agoutis were the only species removing J. princeps seeds, thus dispersal only occurred where agoutis had been reintroduced; in the area without agoutis, all seeds remained intact on the soil, even one year after the experiment's beginning. At the reintroduction area, most seeds were preyed upon by agoutis but 7% remained dispersed and 2% germinated after ten months. Only seeds buried by agoutis were able to germinate. Most dispersed seeds were dispersed 15 m or farther and longer dispersal distances benefited J. princeps, since seedlings farther from a conspecific adult tree had greater survival probability. Agoutis were also seen burying seeds of two other plant species; these mammals have the potential to benefit dozens of large-seeded species in our study system. Agouti reintroduction thus exemplifies the value of trophic rewilding programs to re-establish ecological interactions and restore ecosystem functioning.