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Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species.

ABSTRACT: Seed dispersal distance (SDD) critically influences the survival of seedlings, spatial patterns of genetic diversity within plant populations, and gene flow among plant populations. In animal-dispersed species, foraging behavior and movement patterns determine SDD. Direct observations of seed dispersal events by animals in natural plant populations are mostly constrained by the high mobility and low visibility of seed dispersers. Therefore, diverse alternative methods are used to estimate seed dispersal distance, but direct comparisons of these approaches within the same seed dispersal system are mostly missing.We investigated two plant species with different life history traits, Leonia cymosa and Parkia panurensis, exclusively dispersed by two tamarin species, Saguinus mystax and Leontocebus nigrifrons. We compared SDD estimates obtained from direct observations, genetic identification of mother plants from seed coats, parentage analysis of seedlings/saplings, and phenomenological and mechanistic modeling approaches.SDD derived from the different methods ranged between 158 and 201 m for P. panurensis and between 178 and 318 m for L. cymosa. In P. panurensis, the modeling approaches resulted in moderately higher estimates than observations and genotyping of seed coats. In L. cymosa, parentage analysis resulted in a lower estimate than all other methods. Overall, SDD estimates for P. panurensis (179 ± 16 m; mean ± SD) were significantly lower than for L. cymosa (266 ± 59 m; mean ± SD).Differences among methods were related to processes of the seed dispersal loop integrated by the respective methods (e.g., seed deposition or seedling distribution). We discuss the merits and limitations of each method and highlight the aspects to be considered when comparing SDD derived from different methodologies. Differences among plant species were related to differences in reproductive traits influencing gut passage time and feeding behavior, highlighting the importance of plant traits on animal-mediated seed dispersal distance.

SUBMITTER: Gelmi-Candusso TA

PROVIDER: S-EPMC6706201 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species.

Gelmi-Candusso Tiziana A TA Bialozyt Ronald R Slana Darja D Zárate Gómez Ricardo R Heymann Eckhard W EW Heer Katrin K

Ecology and evolution 20190725 16

Seed dispersal distance (SDD) critically influences the survival of seedlings, spatial patterns of genetic diversity within plant populations, and gene flow among plant populations. In animal-dispersed species, foraging behavior and movement patterns determine SDD. Direct observations of seed dispersal events by animals in natural plant populations are mostly constrained by the high mobility and low visibility of seed dispersers. Therefore, diverse alternative methods are used to estimate seed d ...[more]

PMID: 31462995

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Project description:BackgroundLong-distance seed dispersal (LDD) has strong impacts on the spatiotemporal dynamics of plants. Large animals are important LDD vectors because they regularly transport seeds of many plant species over long distances. While there is now ample evidence that behaviour varies considerably between individual animals, it is not clear to what extent inter-individual variation in behaviour alters seed dispersal by animals.MethodsWe study how inter-individual variation in the movement and feeding behaviour of one of Europe's largest herbivores (the red deer, Cervus elaphus) affects internal seed dispersal (endozoochory) of multiple plant species. We combine movement data of 21 individual deer with measurements of seed loads in the dung of the same individuals and with data on gut passage time. These data serve to parameterize a model of passive dispersal that predicts LDD in three orientations (horizontal as well as upward and downward in elevation).With this model we investigate to what extent per-seed probabilities of LDD and seed load vary between individuals and throughout the vegetation period (May-December). Subsequently, we test whether per-seed LDD probability and seed load are positively (or negatively) correlated so that more mobile animals disperse more (or less) seeds. Finally, we examine whether non-random associations between per-seed LDD probability and seed load affect the LDD of individual plant species.ResultsThe studied deer dispersed viable seeds of at least 62 plant species. Deer individuals varied significantly in per-seed LDD probability and seed loads. However, more mobile animals did not disperse more or less seeds than less mobile ones. Plant species also did not differ significantly in the relationship between per-seed LDD probability and seed load. Yet plant species differed in how their seed load was distributed across deer individuals and in time, and this caused their LDD potential to differ more than twofold. For several plant species, we detected non-random associations between per-seed LDD probability and seed load that generally increased LDD potential.ConclusionsInter-individual variation in movement and feeding behaviour means that certain deer are substantially more effective LDD vectors than others. This inter-individual variation reduces the reliability of LDD and increases the sensitivity of LDD to the decline of deer populations. Variation in the dispersal services of individual animals should thus be taken into account in models in order to improve LDD projections.

Project description:BackgroundFunctional redundancy has been debated largely in ecology and conservation, yet we lack detailed empirical studies on the roles of functionally similar species in ecosystem function. Large bodied frugivores may disperse similar plant species and have strong impact on plant recruitment in tropical forests. The two largest frugivores in the neotropics, tapirs (Tapirus terrestris) and muriquis (Brachyteles arachnoides) are potential candidates for functional redundancy on seed dispersal effectiveness. Here we provide a comparison of the quantitative, qualitative and spatial effects on seed dispersal by these megafrugivores in a continuous Brazilian Atlantic forest.Methodology/principal findingsWe found a low overlap of plant species dispersed by both muriquis and tapirs. A group of 35 muriquis occupied an area of 850 ha and dispersed 5 times more plant species, and 13 times more seeds than 22 tapirs living in the same area. Muriquis dispersed 2.4 times more seeds in any random position than tapirs. This can be explained mainly because seed deposition by muriquis leaves less empty space than tapirs. However, tapirs are able to disperse larger seeds than muriquis and move them into sites not reached by primates, such as large forest gaps, open areas and fragments nearby. Based on published information we found 302 plant species that are dispersed by at least one of these megafrugivores in the Brazilian Atlantic forest.Conclusions/significanceOur study showed that both megafrugivores play complementary rather than redundant roles as seed dispersers. Although tapirs disperse fewer seeds and species than muriquis, they disperse larger-seeded species and in places not used by primates. The selective extinction of these megafrugivores will change the spatial seed rain they generate and may have negative effects on the recruitment of several plant species, particularly those with large seeds that have muriquis and tapirs as the last living seed dispersers.

Project description:Fauna-mediated ecosystem service provision (e.g. seed dispersal) can be difficult to quantify and predict because it is underpinned by the shifting niches of multiple interacting organisms. Such interactions are especially complex in tropical ecosystems, including endangered peat forests of Central Borneo, a biodiversity hot spot and home to the critically endangered orangutan (Pongo pygmaeus wurmbii). We combined studies of the digestive physiology of captive orangutans in Australia with detailed field studies of wild orangutans in the Natural Laboratory of Peat-Swamp Forest of Sabangau, Central Kalimantan, Indonesia. By measuring the gut transit time (TT) of indigestible seed mimics (beads) in captivity and applying this as a temporal constraint to movement data of wild orangutans, we developed a mechanistic, time-explicit spatial model to project the seed dispersal patterns by these large-bodied, arboreal frugivores. We followed seven orangutans and established home range kernels using Time Local Convex Hull (T-LoCoH) modelling. This allowed us to model individual orangutan movements and to adjust these models according to gut transit times to estimate seed dispersal kernels. Female movements were conservative (core ranges of 55 and 52 ha in the wet and dry seasons, respectively) and revisitation rates to the same location of n = 4 in each 24-h block. Male movements were more unpredictable, yielding fragmented core ranges and revisitation rates to the same location of only 1.2 times each 24 h; males also demonstrated large disjunctions where they moved rapidly over long distances and were frequently lost from view. Seed dispersal kernels were nested predictably within the core ranges of females, but not males. We used the T-LoCoH approach to analyse movement ecology, which offered a powerful tool to predict the primary deposition of seeds by orangutans, thereby providing a reliable method for making a priori predictions of seed dispersal dynamics by other frugivores in novel ecosystems.

Project description:Restricted gene flow may lead to the loss of genetic diversity and higher genetic differentiation among populations, but the genetic consequences of megafauna extinction for plant populations still remain to be assessed. We performed a phylogenetic-independent meta-analysis across 102 Neotropical plants to test the hypothesis that plant species with megafaunal seed dispersal syndrome have a lower genetic diversity and a higher genetic differentiation than those without it. We classified as megafauna-dependent plant species those that potentially relied only on megafauna to seed dispersal, and as megafauna-independent those that relied on megafauna and other seed dispersers. Our data comprised 98 studies using microsatellite markers. We found no statistical difference in genetic diversity and differentiation between plants with megafauna and non-megafauna seed dispersal syndrome, although the statistical power to detect differences in genetic differentiation was low. Moreover, we found no statistical difference between megafauna-dependent and megafauna-independent plant species. We then used generalized linear mixed models and phylogenetic generalized least square models to investigate the effects of megafaunal seed dispersal syndromes and reproductive traits on variation in genetic diversity and genetic differentiation. We found no effect of megafaunal syndrome, rather, reproductive traits, such as pollination mode, mating, and breeding systems, showed significant effects. Our findings show that the genetic studies of Neotropical plants performed so far show no difference in genetic diversity and differentiation in plants with megafaunal compared to those with non-megafaunal seed dispersal syndromes. Our results also provide evidence pointing out that plant species with megafaunal seed dispersal syndromes may have used different strategies to counterbalance the extinction of their mutualistic megafauna dispersers, such as the dispersal by extant mammals that may promote long-distance seed dispersal. Our results also reinforce the importance of pollination to long-distance gene flow in Neotropical plants.

Dataset Information

Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species.

Publications

Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species.

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