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.     

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.     

Interactions between spatial and temporal scales in the evolution of dispersal rate

The evolution of dispersal rate is studied with a model of several local populations linked by dispersal. Three dispersal strategies are considered where all, half or none of the offspring disperse. The spatial scale (number of patches) and the temporal scale (probability of local extinction) of the environment are critical in determining the selective advantage of the different dispersal strategies. The results from the simulations suggest that an interaction between group selection and individual selection results in a different outcome in relation to the spatial and temporal scales of the environment. Such an interaction is able to maintain a polymorphism in dispersal strategies. The maintenance of this polymorphism is also scale-dependent. This study suggests a mechanism for the short-term evolution of dispersal, and provides a testable prediction of this hypothesis, namely that loss of dispersal abilities should be more frequent in spatially more continuous environments, or in temporally more stable environments. This revised version was published online in July 2006 with corrections to the Cover Date.     

Intertwined effects of defaunation,increased tree mortality and density compensation on seed dispersal

Contemporary defaunation has profound ecological consequences ranging from local or even global co-extinctions of interacting species to the loss of ecosystem functions and services critical for humanity. Other components of global change (climate change, introduced pests, land use changes) are also harming ecosystem functioning by augmenting tree mortality worldwide. Defaunation and increased tree mortality often coincide in many human-altered ecosystems but whether they interact, leading to non-additive effects on ecosystem functioning, remains largely unknown. However, under some ecological circumstances, the decline or extirpation of one species due to defaunation can be neutralized by increases in the abundance of some functionally similar species (i.e. ‘density compensation’). We combined long-term field data with individual-based modelling to investigate the potential interactive effects of seed disperser loss, increased tree mortality and density compensation on seed dispersal in a heterogeneous landscape. Our simulation experiments showed that both stressors markedly limit not only the quantity of seed dispersal but also its quality since the impact on seed dispersal strongly varied among habitat types that differ strikingly in suitability for tree establishment. Density compensation had a marked positive effect on seed dispersal which, however, was largely limited under increased tree mortality. The combined negative effects of defaunation and increased tree mortality on seed dispersal were lower than the expected additive effect. This highlights the need to account for the joint operation of multiple stressors to accurately predict the impacts of global change on the link between biodiversity and ecosystem functioning.     

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.     

Rapid recovery of genetic diversity of stomatopod populations on Krakatau: temporal and spatial scales of marine larval dispersal

Although the recovery of terrestrial communities shattered by the massive eruption of Krakatau in 1883 has been well chronicled, the fate of marine populations has been largely ignored. We examined patterns of genetic diversity in populations of two coral reef-dwelling mantis shrimp, Haptosquilla pulchella and Haptosquilla glyptocercus (Stomatopoda: Protosquillidae), on the islands of Anak Krakatau and Rakata. Genetic surveys of mitochondrial cytochrome oxidase c (subunit 1) in these populations revealed remarkably high levels of haplotypic and nucleotide diversity that were comparable with undisturbed populations throughout the Indo-Pacific. Recolonization and rapid recovery of genetic diversity in the Krakatau populations indicates that larval dispersal from multiple and diverse source populations contributes substantially to the demographics of local populations over intermediate temporal (tens to hundreds of years) and spatial scales (tens to hundreds of kilometres). Natural experiments such as Krakatau provide an excellent mechanism to investigate marine larval dispersal and connectivity. Results from stomatopods indicate that marine reserves should be spaced no more than 50-100 km apart to facilitate ecological connectivity via larval dispersal.     

Effects of seed dispersal on spatial genetic structure in populations of Rutidosis leptorrhychoides with different levels of correlated paternity

Rutidosis leptorrynchoides is a perennial forb endemic to grasslands and grassy woodlands in southeastern Australia. Studies of seed dispersal, spatial genetic structure and clonality were carried out in four populations around the Canberra region that varied in levels of correlated paternity to examine: (1) whether R. leptorrhynchoides populations exhibit fine-scale spatial genetic structure and whether this varies between populations as a function of correlated paternity; (2) whether there is a correlation between seed dispersal distance and genetic relatedness within populations; and (3) whether clonal reproduction occurs in this species and to what degree this could account for the observed spatial genetic structure. The results show that there is variation in the magnitude and extent of spatial genetic structure between R. leptorrhynchoides populations. The three larger populations, with low to moderate full-sib proportions, showed significant patterns of coancestry between plants over scales of up to one metre, whereas the smallest population, with a high full-sib proportion, had erratically high but non-significant coancestry values. The observed patterns of genetic clumping could be explained by a combination of limited seed dispersal and correlated mating owing to limited mate availability resulting from the species' sporophytic self-incompatibility system. Clonality does not appear to be an important factor contributing to genetic structure in this species.     

Primate seed dispersal leaves spatial genetic imprint throughout subsequent life stages of the Neotropical tree Parkia panurensis

Key message

The Neotropical tree Parkia panurensis shows a spatial genetic structure from the seed to the adult stage that is most likely the outcome of the seed dispersal provided by primates.

Abstract

Seed dispersal and pollination determine the gene flow within plant populations. In addition, seed dispersal creates the template for subsequent stages of plant recruitment. Therefore, the question arises whether and how seed dispersal affects the spatial genetic structure (SGS) of plant populations. In this study, we used microsatellites to analyse the SGS of the Neotropical tree Parkia panurensis (Fabaceae). This plant species is a major food resource for primates and its seeds are mainly dispersed by primates. Seeds were collected during behavioural observations of a tamarin mixed-species troop in north-eastern Peru. Additionally, leaf samples of juveniles and of adults trees of this species were collected throughout the home range of the tamarin troop. A significant SGS for embryos (located within the dispersed seeds) and for non-reproductive plants are found up to a distance of 300 m. This matches the distance within which most seeds are dispersed. In the adult stage, the scale of a significant SGS is reduced to 100 m. While we cannot explain this scale reduction, our study provides the first evidence that primate seed dispersal does influence the SGS of a tropical tree species.     

Avian seed dispersal and seedling distribution of the endangered tree species,Taxus chinensis,in patchy habitats

Background: There is limited understanding about bird dispersal behaviour and seedling distribution of endangered tree species in patchy environments, although these processes are important for plant species persistence.

Aims: We tested how patch features affected bird behaviour and seed dispersal, and thus seedling distribution of the endangered Chinese yew tree (Taxus chinensis).

Methods: In the present study, we combined field data of bird dispersal behaviour and GIS-based information to elucidate the influence of spatial features of habitat patches on bird dispersal behaviour, and the resulting effects on the seedling distribution of the endangered Chinese yew in two patchy habitats.

Results: Our results showed that the only seed source patch could attract eight bird species for dispersal at the two sites. Post-foraging movements of bird dispersers was strongly related to both topography and the relative locations of habitat patches. Yew seedlings aggregated only at the seed source and bamboo recruitment patches, which was affect by both the spatial distribution of recruitment patches and patch use by dispersers.

Conclusions: Our results emphasise that bamboo patches in both patchy environments provide the necessary conditions for germination of yew seeds, and the post-foraging behaviour of dispersers determines seed deposited in these patches. Our study highlights the importance of the dispersal behaviour of frugivorous birds in the successful regeneration and colonisation of yew populations in patchy habitats.     

Effects of dung and seed size on secondary dispersal,seed predation,and seedling establishment of rain forest trees

Seeds dispersed by tropical, arboreal mammals are usually deposited singly and without dung or in clumps of fecal material. After dispersal through defecation by mammals, most seeds are secondarily dispersed by dung beetles or consumed by rodents. These post-dispersal, plant-animal interactions are likely to interact themselves, as seeds buried by dung beetles are less likely to be found by rodents than unburied seeds. In a series of three experiments with seeds of 15 species in central Amazonia (Brazil), we determined (1) how presence and amount of dung associated with seeds influences long-term seed fate and seedling establishment, (2) how deeply dung beetles bury seeds and how burial depth affects seedling establishment, and (3) how seed size affects the interaction between seeds, dung beetles, and rodents. Our overall goal was to understand how post-dispersal plant-animal interactions determine the link between primary seed dispersal and seedling establishment. On average, 43% of seeds surrounded by dung were buried by dung beetles, compared to 0% of seeds not surrounded by dung (n=2,156). Seeds in dung, however, tended to be more prone than bare seeds to predation by rodents. Of seeds in dung, probability of burial was negatively related to seed size and positively related to amount of dung. Burial of seeds decreased the probability of seed predation by rodents three-fold, and increased the probability of seedling establishment two-fold. Mean burial depth was 4 cm (0.5–20 cm) and was not related to seed size, contrary to previous studies. Probability of seedling establishment was negatively correlated with burial depth and not related to seed size at 5 or 10 cm depths. These results illustrate a complex web of interactions among dung beetles, rodents, and dispersed seeds. These interactions affect the probability of seedling establishment and are themselves strongly tied to how seeds are deposited by primary dispersers. More generally, our results emphasize the importance of looking beyond a single type of plant-animal interaction (e.g., seed dispersal or seed predation) to incorporate potential effects of interacting interactions.     

Effects of kin-structured seed dispersal on the genetic structure of the clonal dioecious shrub ilex leucoclada

Nonrandom patterns of gene dispersal have been identified as possible causes of genetic structuring within populations. Attempts to model these patterns have generally focused solely on the effects of isolation by distance, but the processes involved are more complex than such modeling suggests. Here, we extend considerations of gene dispersal processes beyond simple isolation by distance effects by directly evaluating the effects of kin-structured gene dispersal mediated by the group dispersal of related seeds within fruits (i.e., kin-structured seed dispersal) by birds on genetic structure in Ilex leucoclada, a clonal dioecious shrub. To examine the genetic structure patterns, we established two 30x30 m plots (one with immature soils in old-growth forest and one in secondary forest, designated IM and SC, respectively) with different I. leucoclada stem densities. In these two plots 145 and 510 stems were found, representing 78 and 85 genets, respectively, identified by analyzing their genotypes at eight microsatellite loci. The clonal structure was stronger in the SC plot than in the IM plot. Correlograms of coancestry for genets in both plots exhibited significant, positive, high values in the shortest distance class, indicating the presence of strong genetic structure. However, Sp statistics revealed that the pattern of the genetic structure differed between the plots. In addition, to estimate the family structure within fruits, we sampled forty fruits, in total, from 15 randomly selected plants in the area around the IM and SC plots, and found that 80% of the fruits were multiseeded and 42-100% of the multiseeded fruits contained at least one pair of full sibs. Simulations based on these estimates demonstrated that the group dispersal of related seeds produced through correlated mating both within and across fruits, but not unstructured half-sib dispersal, could generate the observed magnitude and trends of genetic structure found in the IM plot. Furthermore, in addition to kin-structured seed dispersal, isolation by distance processes is also likely to promote genetic substructuring in the SC plot. After discussing possible ecological factors that may have contributed to the observed genetic structure, we contrast our results with those predicted by general isolation by distance models, and propose that kin-structured seed dispersal should promote some evolutionary phenomena, and thus should be incorporated, where appropriate, in models of gene dispersal in natural plant populations.     

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.     

Consequences of frugivore diversity for seed dispersal, seedling establishment and the spatial pattern of seedlings and trees

Many plants depend on frugivorous animals for the dispersal of their seeds. However, it is only poorly known whether regional differences in frugivore diversity have consequences for seed dispersal, seedling establishment, and the spatial distribution of seedlings and trees. This comparative study of seed dispersal investigated the consequences of regional differences in frugivore diversity for two tree species of the genus Commiphora. C. harveyi was studied in South Africa where avian frugivore diversity is high, C. guillaumini was studied in Madagascar where the avian frugivore community is depauperate. At both study sites, the percentages of handled and dispersed seeds in Commiphora trees were quantified by fruit traps, and visitation rates, seed handling rates and dispersal rates were quantified for each animal species for two consecutive years. Seedlings were mapped and the spatial distribution of trees quantified. At both study sites, fruits were mainly eaten by birds. The total percentage of dispersed seeds in South Africa was significantly higher than in Madagascar (70.8% vs. 7.9%) because there was a lack of effective dispersers that swallowed seeds in Madagascar. Seed dispersal benefit, i.e. the increase in the probability of becoming established as a seedling away from parent trees due to dispersal was much higher in Madagascar (80 times higher probability) compared to South Africa (6 times higher). Corresponding with the different dispersal percentages, seedlings in South Africa were found at relatively large distances from the nearest Commiphora tree (median distance=21.0 m), whereas in Madagascar seedlings were found mostly under and close to the nearest Commiphora tree (median distance=0.9 m). Finally, Commiphora trees in the Malagasy study site were clumped, but were more randomly distributed in the South African study site. These results suggest that regional differences in frugivore diversity and behaviour strongly affect seed dispersal of trees, seedling establishment and the spatial distribution of seedlings and trees.     

Mating system,pollen and propagule dispersal,and spatial genetic structure in a high-density population of the mangrove tree Kandelia candel

Mangrove tree species form ecologically and economically important forests along the tropical and subtropical coastlines of the world. Although low intrapopulation genetic diversity and high interpopulation genetic differentiation have been detected in most mangrove tree species, no direct investigation of pollen and propagule dispersal through paternity and/or parentage analysis and spatial genetic structure within populations has been conducted. We surveyed the mating system, pollen and propagule dispersal, and spatial genetic structure in a natural population of Kandelia candel, one of the typical viviparous mangrove tree species, using nuclear and chloroplast microsatellite markers. High diversity and outcrossing rates were observed. Paternity and parentage analysis and modelling estimations revealed the presence of an extremely short-distance component of pollen and propagule dispersal (pollen: 15.2 ± 14.9 m (SD) by paternity analysis and 34.4 m by modelling; propagule: 9.4 ± 13.8 m (SD) by parentage analysis, and 18.6 m by modelling). Genetic structure was significant at short distances, and a clumped distribution of chloroplast microsatellite genotypes was seen in K. candel adults. We conclude that the K. candel population was initiated by limited propagule founders from outside by long-distance dispersal followed by limited propagule dispersal from the founders, resulting in a half-sib family structure.     

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.     

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.     

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.