Spatio-temporal variation of seed rain between urban and rural fragments of humid tropical forests / Variación espacio-temporal de la lluvia de semillas entre fragmentos urbanos y rurales de bosques tropicales húmedos

Introduction: The type of land use surrounding the remnants of tropical forest may generate changes in the characteristics of plant populations and communities. Consequently, there may be a significant reduction in processes of pollination and diasporas dispersion. Therefore, causing changes in some parameters of seed rain. Objective: To characterize and compare seed density, species richness, floristic composition, habit, dispersal syndrome, and successional category of seed rain between urban and rural fragments of Atlantic Forest, in the 2015 and 2016 weather seasons. Methods: The study areas were defined after mapping and quantification of urban and rural occupations around the remnants, based on satellite images. In each fragment, were installed 36 collectors of 0.25 m2. The material was collected monthly during two consecutive years. Results: Seed rain richness was higher in the urban fragment during the rainy season in the two years, whereas it was similar between the fragments in the dry season. The seed density in the rural fragment was higher than in the urban during the rainy season; did not vary in urban between years or between seasons; and it was higher in the rural fragment in the rainy season of one year. There was a difference in the floristic composition of the seed rain between the fragments along time. The variations in the functional attributes of habit, dispersal syndrome, and successional category, were explained by the variables fragment, season, and year. Conclusions: Differences in the characteristics of the seed rain between the fragments might reflect the spatial and temporal heterogeneity, due to the diverse uses of the soil and external pressures (anthropogenic actions) present in the surroundings of the forest fragments and temporal variation in precipitation.

Introducción: El tipo de uso del suelo que rodea los remanentes de bosque tropical puede generar cambios en las características de las poblaciones y comunidades vegetales. En consecuencia, puede haber una reducción significativa en los procesos de polinización y dispersión de las diásporas. Por lo tanto, provocando cambios en algunos parámetros de la lluvia de semillas. Objetivo: Caracterizar y comparar la densidad de semillas, la riqueza de especies, la composición florística, el hábito, el síndrome de dispersión y la categoría sucesional de la lluvia de semillas entre fragmentos urbanos y rurales de Mata Atlántica, en las estaciones climáticas del 2015 y 2016. Métodos: Las áreas de estudio se definieron luego del mapeo y cuantificación de las ocupaciones urbanas y rurales alrededor de los remanentes, con base en imágenes satelitales. En cada fragmento se instalaron 36 colectores de 0.25 m2. El material fue recolectado mensualmente durante dos años consecutivos. Resultados: La riqueza de lluvia de semillas fue mayor en el fragmento urbano durante la estación lluviosa en los dos años, mientras que fue similar entre los fragmentos en la estación seca. La densidad de semillas en el fragmento rural fue mayor que en el urbano durante la estación lluviosa; no varió en urbano entre años o entre estaciones; y fue mayor en el fragmento rural en la estación lluviosa del primer año. Hubo una diferencia en la composición florística de la lluvia de semillas entre los fragmentos a lo largo del tiempo. Las variaciones en los atributos funcionales de hábito, síndrome de dispersión y categoría sucesional, fueron explicadas por las variables fragmento, estación y año. Conclusiones: Las diferencias en las características de la lluvia de semillas entre los fragmentos podrían reflejar la heterogeneidad espacial y temporal, debido a los diversos usos del suelo y presiones externas (acciones antropogénicas) presentes en el entorno de los fragmentos de bosque y variación temporal de la precipitación.

Trade-offs between diaspore dispersal and dormancy within a spike of the invasive annual grass Aegilops tauschii.

MAIN CONCLUSION: Differences in dispersal and dormancy of heteromorphic diaspores of Aegilos tauschii may increase its flexibility to invade/occupy weedy unpredictable habitats by spreading risk in space and time. In plant species that produce dimorphic seeds, there often is a negative relationship between dispersal and dormancy, with high dispersal-low dormancy in one morph and low dispersal-high dormancy in the other, which may function as a bet-hedging strategy that spreads the risk of survival and ensures reproductive success. However, the relationship between dispersal and dormancy and its ecological consequences in invasive annual grasses that produce heteromorphic diaspores is not well studied. We compared dispersal and dormancy responses of diaspores from the basal (proximal) to the distal position on compound spikes of Aegilops tauschii, an invasive grass with heteromorphic diaspores. Dispersal ability increased and degree of dormancy decreased as diaspore position on a spike increased from basal to distal. There was a significant positive correlation between length of awns and dispersal ability, and awn removal significantly promoted seed germination. Germination was positively correlated with GA concentration and negatively correlated with ABA concentration, and the ABA: GA ratio was high in seeds with low germination/high dormancy. Thus, there was a continuous inverse-linear relationship between diaspore dispersal ability and degree of dormancy. This negative relationship between diaspore dispersal and degree of dormancy at different positions on a spike of Aegilops tauschii may facilitate seedling survival in space and time.

Fruit Physiology through Signaling Processes: Latest Advances and Future Challenges.

Fruits are unique to flowering plants and confer a selective advantage to these species by facilitating seed maturation and dispersal [...].

Environmental morphing enables informed dispersal of the dandelion diaspore.

Animal migration is highly sensitised to environmental cues, but plant dispersal is considered largely passive. The common dandelion, Taraxacum officinale, bears an intricate haired pappus facilitating flight. The pappus enables the formation of a separated vortex ring during flight; however, the pappus structure is not static but reversibly changes shape by closing in response to moisture. We hypothesised that this leads to changed dispersal properties in response to environmental conditions. Using wind tunnel experiments for flow visualisation, particle image velocimetry, and flight tests, we characterised the fluid mechanics effects of the pappus morphing. We also modelled dispersal to understand the impact of pappus morphing on diaspore distribution. Pappus morphing dramatically alters the fluid mechanics of diaspore flight. We found that when the pappus closes in moist conditions, the drag coefficient decreases and thus the falling velocity is greatly increased. Detachment of diaspores from the parent plant also substantially decreases. The change in detachment when the pappus closes increases dispersal distances by reducing diaspore release when wind speeds are low. We propose that moisture-dependent pappus-morphing is a form of informed dispersal allowing rapid responses to changing conditions.

Plant-defense mimicry facilitates rapid dispersal of short-lived seeds by hornets.

Rates of seed dispersal have rarely been considered important. Here, we demonstrate through field observations and experiments that rapid dispersal is essential for the unusually short-lived seeds of Aquilaria sinensis (agarwood; Thymelaeaceae), which desiccate and die within hours of exposure by fruit dehiscence in the hot, dry forest canopy in tropical southwest China. We show that three species of Vespa hornets remove most seeds within minutes of exposure. The hornets consume only the fleshy elaiosomes and deposit most seeds in damp shade, where they can germinate, a mean of 166 m from the parent tree. Electrophysiological assays and field experiments demonstrate that the hornets are attracted by highly volatile short-carbon-chain (C5-C9) compounds, including aldehydes, ketones, alcohols, and acids, emitted from the dehiscent fruit capsule. These attractive fruit volatiles share 14 of 17 major electrophysiologically active compounds with those emitted from herbivore-damaged leaves, which attract predators, including hornets. Rapid seed dispersal thus appears to have been achieved in this species by the re-purposing of a rapid indirect defense mechanism. We predict that rapid seed dispersal by various mechanisms will be more widespread than currently documented and suggest that volatile attractants are more effective in facilitating this than visual signals, which are blocked by vegetation.

Global wind patterns shape genetic differentiation, asymmetric gene flow, and genetic diversity in trees.

Wind disperses the pollen and seeds of many plants, but little is known about whether and how it shapes large-scale landscape genetic patterns. We address this question by a synthesis and reanalysis of genetic data from more than 1,900 populations of 97 tree and shrub species around the world, using a newly developed framework for modeling long-term landscape connectivity by wind currents. We show that wind shapes three independent aspects of landscape genetics in plants with wind pollination or seed dispersal: populations linked by stronger winds are more genetically similar, populations linked by directionally imbalanced winds exhibit asymmetric gene flow ratios, and downwind populations have higher genetic diversity. For each of these distinct hypotheses, partial correlations between the respective wind and genetic metrics (controlling for distance and climate) are positive for a significant majority of wind-dispersed or wind-pollinated genetic data sets and increase significantly across functional groups expected to be increasingly influenced by wind. Together, these results indicate that the geography of both wind strength and wind direction play important roles in shaping large-scale genetic patterns across the world's forests. These findings have implications for various aspects of basic plant ecology and evolution, as well as the response of biodiversity to future global change.

The effect of lizards on the dispersal and germination of Capparis spinosa (Capparaceae).

Seed dispersal is a key component of the interactions between plants and animals. There is little research on the effects of lizard seed dispersal, which is more common on islands than elsewhere. In this study, the effects of the passage of Capparis spinosa seeds through Teratoscincus roborowskii lizard digestive tracts on the seed coats, water uptake rates and germination rates were investigated. In addition, the spatial patterns of fecal deposition by lizards in various microhabitats were assessed. Our results showed that the mean retention time (MRT) of mealworms was significantly longer than that of C. spinosa seeds in both adult and juvenile lizards. The defecation rate of C. spinosa tended to be lower than that of mealworms, which might be beneficial for seed dispersal. It was determined that the longer MRT of C. spinosa seeds enhanced the permeability of the seed coats, which promoted fast water uptake, broke seed dormancy and increased the seed germination rate. Furthermore, the seeds that passed through the digestive tracts of lizards were deposited in favorable germination microhabitats. By enhancing seed germination and depositing intact and viable seeds in safe potential recruitment sites, the lizard T. roborowskii acts, at least qualitatively, as an effective disperser of C. spinosa.

Frugivory Specialization in Birds and Fruit Chemistry Structure Mutualistic Networks across the Neotropics.

AbstractThe interaction between fruit chemistry and the physiological traits of frugivores is expected to shape the structure of mutualistic seed dispersal networks, but it has been understudied compared with the role of morphological trait matching in structuring interaction patterns. For instance, highly frugivorous birds (i.e., birds that have fruits as the main component of their diets), which characteristically have fast gut passage times, are expected to avoid feeding on lipid-rich fruits because of the long gut retention times associated with lipid digestion. Here, we compiled data from 84 studies conducted in the Neotropics that used focal plant methods to record 35,815 feeding visits made by 317 bird species (155 genera in 28 families) to 165 plant species (82 genera in 48 families). We investigated the relationship between the degree of frugivory of birds (i.e., how much of their diet is composed of fruit) at the genus level and their visits to plant genera that vary in fruit lipid content. We used a hierarchical modeling of species communities approach that accounted for the effects of differences in body size, bird and plant phylogeny, and spatial location of study sites. We found that birds with a low degree of frugivory (e.g., predominantly insectivores) tend to have the highest increase in visitation rates as fruits become more lipid rich, while birds that are more frugivorous tend to increase visits at a lower rate or even decrease visitation rates as lipids increase in fruits. This balance between degree of frugivory and visitation rates to lipid-poor and lipid-rich fruits provides a mechanism to explain specialized dispersal systems and the occurrence of certain physiological nutritional filters, ultimately helping us to understand community-wide interaction patterns between birds and plants.

Ecological correlates of species' roles in highly invaded seed dispersal networks.

Ecosystems with a mix of native and introduced species are increasing globally as extinction and introduction rates rise, resulting in novel species interactions. While species interactions are highly vulnerable to disturbance, little is known about the roles that introduced species play in novel interaction networks and what processes underlie such roles. Studying one of the most extreme cases of human-modified ecosystems, the island of O'ahu, Hawaii, we show that introduced species there shape the structure of seed dispersal networks to a greater extent than native species. Although both neutral and niche-based processes influenced network structure, niche-based processes played a larger role, despite theory predicting neutral processes to be predominantly important for islands. In fact, ecological correlates of species' roles (morphology, behavior, abundance) were largely similar to those in native-dominated networks. However, the most important ecological correlates varied with spatial scale and trophic level, highlighting the importance of examining these factors separately to unravel processes determining species contributions to network structure. Although introduced species integrate into interaction networks more deeply than previously thought, by examining the mechanistic basis of species' roles we can use traits to identify species that can be removed from (or added to) a system to improve crucial ecosystem functions, such as seed dispersal.

Oilbirds disperse large seeds at longer distance than extinct megafauna.

The extinction of megafauna in the Neotropics is thought to have reduced the potential of large seeds to be dispersed over long distances by endozoochory (ingestion by animals), but some seed dispersal systems have not been considered. We describe the role of oilbirds (Steatornis caripensis) as seed dispersers, in terms of seed width and dispersal distance (using GPS tracking devices), and we compare with data reported for other animals. Oilbirds dispersed seeds up to 29 mm wide, with a mean dispersal distance of 10.1 km (range 0-47.6 km). Some components of seed dispersal by oilbirds are outliers compared to that of other frugivores, such as the relationship between maximum seed width and body weight (however, few other extant specialized frugivores are also outliers). Estimates of mean dispersal distance by oilbirds are the largest reported, and we confirm that some living frugivores currently fulfil roles of seed dispersers and ecosystem services previously assumed to be only performed by extinct species.

Interspecific interactions among functionally diverse frugivores and their outcomes for plant reproduction: A new approach based on camera-trap data and tailored null models.

The study of plant-frugivore interactions is essential to understand the ecology and evolution of many plant communities. However, very little is known about how interactions among frugivores indirectly affect plant reproductive success. In this study, we examined direct interactions among vertebrate frugivores sharing the same fruit resources. Then, we inferred how the revealed direct interspecific interactions could lead to indirect (positive or negative) effects on reproductive success of fleshy fruited plants. To do so, we developed a new analytical approach that combines camera trap data (spatial location, visitor species, date and time, activity) and tailored null models that allowed us to infer spatial-temporal interactions (attraction, avoidance or indifference) between pairs of frugivore species. To illustrate our approach, we chose to study the system composed by the Mediterranean dwarf palm, Chamaerops humilis, the Iberian pear tree, Pyrus bourgaeana, and their shared functionally diverse assemblages of vertebrate frugivores in a Mediterranean area of SW Spain. We first assessed the extent to which different pairs of frugivore species tend to visit the same or different fruiting individual plants. Then, for pairs of species that used the same individual plants, we evaluated their spatial-temporal relationship. Our first step showed, for instance, that some prey frugivore species (e.g. lagomorphs) tend to avoid those C. humilis individuals that were most visited by their predators (e.g. red foxes). Also, the second step revealed temporal attraction between large wild and domestic frugivore ungulates (e.g. red deer, cows) and medium-sized frugivores (e.g. red foxes) suggesting that large mammals could facilitate the C. humilis and P. bourgaeana exploitation to other smaller frugivores by making fruits more easily accessible. Finally, our results allowed us to identify direct interaction pathways, that revealed how the mutualistic and antagonistic relations between animal associates derived into indirect effects on both plants seed dispersal success. For instance, we found that large-sized seed predators (e.g. ungulates) had a direct positive effect on the likelihood of visits by legitimate seed dispersers (e.g. red foxes) to both fleshy fruited plants. Then, seed predators showed an indirect positive effect on the plants' reproductive success. Our new analytical approach provides a widely applicable framework for further studies on multispecies interactions in different systems beyond plant-frugivore interactions, including plant-pollinator interactions, the exploitation of plants by herbivores, and the use of carcasses by vertebrate scavengers.

Extreme drought alters progeny dispersal unit properties of winter wild oat (Avena sterilis L.).

MAIN CONCLUSION: The dead husk is a vital component of the dispersal unit whose biochemical properties can be modified following exposure to drought. This might affect seed performance and fate, soil properties and consequently plant biodiversity. We investigated the effects of extreme drought on the dispersal unit (DU) properties of winter wild oat (Avena sterilis L.) in the Mediterranean ecosystems focusing on a commonly ignored component of the DU, namely the dead floral bracts (husk). DUs were collected from a climate change experimental research station in the Judean Hills, Israel, simulating extreme drought and from two additional sites differing in the rainfall amounts. Our results showed that drought conditions significantly affected A. sterilis reproductive traits displaying reduced DUs and caryopses weights. The husk contributes profoundly to seed performance showing that germination from the intact DUs or the intact florets 1 was higher, faster and more homogenous compared to naked caryopses; no effect of drought on germination properties was observed. The husk stored hundreds of proteins that retain enzymatic activity and multiple metabolites including phytohormones. Changes in rainfall amounts affected the composition and levels of proteins and other metabolites accumulated in the husk, with a notable effect on abscisic acid (ABA). The husk of both control and drought plants released upon hydration substances that selectively inhibited other species seed germination as well as substances that promoted microbial growth. Our data showed that the dead husk represents a functional component of the DU that have been evolved to nurture the embryo and to ensure its success in its unique habitat. Furthermore, drought conditions can modify husk biochemical properties, which in turn might affect seed performance and fate, soil microbiota and soil fertility and consequently plant species diversity.

Frugivore-fruit size relationships between palms and mammals reveal past and future defaunation impacts.

Mammalian frugivores are critical seed dispersers, but many are under threat of extinction. Futhermore, the impact of past and future defaunation on plant assemblages has yet to be quantified at the global scale. Here, we integrate palm and mammalian frugivore trait and occurrence data and reveal a global positive relationship between fruit size and frugivore body size. Global variation in fruit size is better explained by present-day frugivore assemblages than by Late Pleistocene assemblages, suggesting ecological and evolutionary reorganization after end-Pleistocene extinctions, except in the Neotropics, where some large-fruited palm species may have outlived their main seed dispersers by thousands of years. Our simulations of frugivore extinction over the next 100 years suggest that the impact of defaunation will be highest in the Old World tropics, and an up to 4% assemblage-level decrease in fruit size would be required to maintain the global body size-fruit size relationship. Overall, our results suggest that while some palm species may be able to keep pace with future defaunation through evolutionary changes in fruit size, large-fruited species may be especially vulnerable to continued defaunation.

Viburnum tinus Fruits Use Lipids to Produce Metallic Blue Structural Color.

Viburnum tinus is an evergreen shrub that is native to the Mediterranean region but cultivated widely in Europe and around the world. It produces ripe metallic blue fruits throughout winter [1]. Despite its limited fleshy pulp [2], its high lipid content [3] makes it a valuable resource to the small birds [4] that act as its seed-dispersers [5]. Here, we find that the metallic blue appearance of the fruits is produced by globular lipid inclusions arranged in a disordered multilayer structure. This structure is embedded in the cell walls of the epicarp and underlaid with a dark layer of anthocyanin pigments. The presence of such large, organized lipid aggregates in plant cell walls represents a new mechanism for structural coloration and may serve as an honest signal of nutritional content.

Phenotypic plasticity in diaspore production of a amphi-basicarpic cold desert annual that produces polymorphic diaspores.

Phenotypic plasticity has been studied in diaspore-dimorphic species, but no such study has been done on a diaspore-polymorphic species. Our aim was to determine the effects of abiotic and biotic factors on phenotypic plasticity of the diaspore-polymorphic cold desert annual Ceratocarpus arenarius. Plants produced from dispersal units near the soil surface (a, basicarps) and at the middle (c) and upper (f) parts of the plant canopy were subjected to different levels of soil moisture, nutrient supply and intramorph and intermorph densities. Different levels of these biotic and abiotic factors resulted in significant variation in total plant mass, diaspore mass, mass allocation to stem and reproductive organs and total number and proportion of morphs a, c and f on an individual. The effect of stress on number and mass of a dispersal unit morph varied by treatment, with dispersal unit f having the highest CV and dispersal unit a the lowest. The success of this diaspore polymorphic species in its rainfall-unpredictable environment likely is enhanced by plasticity in production of the different types of diaspores.

Environmental context determines the limiting demographic processes for plant recruitment across a species' elevational range.

Plant recruitment is a multi-stage process determining population dynamics and species distributions. Still, we have limited understanding of how the successive demographic processes depend on the environmental context across species' distributional ranges. We conducted a large-scale transplant experiment to study recruitment of Pinus cembra over six years. We quantified the effects of environmental conditions on four demographic processes and identified the most limiting across and beyond the pines' elevational range over several years. Realized transition probabilities of the demographic processes varied substantially across the species' distributional range. Seed deposition decreased from the lower to the upper elevational range margin by 90%, but this reduction was offset by increased seed germination and seedling survival. Dispersal limitation at the upper range margin potentially stems from unsuitable seed caching conditions for the animal seed disperser, whereas increased seed germination might result from enemy escape from fungal pathogens and favourable abiotic conditions at the upper range margin. Our multi-year experiment demonstrates that environmental context is decisive for the local relevance of particular demographic processes. We conclude that experimental studies identifying the limiting demographic processes controlling species distributions are key for projecting future range dynamics of plants.

Small vertebrates are key elements in the frugivory networks of a hyperdiverse tropical forest.

The local, global or functional extinction of species or populations of animals, known as defaunation, can erode important ecological services in tropical forests. Many mutualistic interactions, such as seed dispersal of large seeded plants, can be lost in large continuous forests due to the rarity of large-bodied mammalian frugivores. Most of studies that try to elucidate the effects of defaunation on seed dispersal focused on primates or birds, and we lack a detailed understanding on the interactions between ground-dwelling fauna and fleshy fruits. Using camera traps in forest areas with different degrees of defaunation, we described the organization of frugivory networks involving birds, mammals and plants. We recorded 375 frugivory interactions between 21 frugivores and 150 fruiting trees of 30 species of fleshy fruit plants in six sites in continuous Atlantic forest of Brazil. We found that small frugivores-particularly small rodents and birds-were responsible for 72% of the events of frugivory. Large frugivores, such as tapirs and peccaries, were responsible for less than 21% of frugivory events. Our results indicate that the interactions between flesh fruiting plants and frugivores are dominated by small frugivores, an indication of a functional loss of large frugivores in this endangered biome.

Large River Effect or Frozen Kinetics: How Complex Nonlinear Living Systems Solve Optimization Problems.

In this paper, we introduce general idea of trajectories attraction in phase space, which is very common phenomenon for the processes in the Nature. We start from a rather general biological example of natural selection, where adaptation to the environmental conditions can be described as attraction of some population distribution in the phenotype space to a center of ecological niche. The niche is mathematically represented as the "survival coefficient" which in turn can be linked to a kind of energy potential. This link between biological and physical approaches may be very useful for solution of a wide range of biological problems. In particular, we discuss an evolution in complex potential with a lot of valleys in a multi-dimensional space accompanied by the so-called large river effect, which corresponds to an extremely slow evolution of some, normally close to final, stages of the adaptation. This effect is related to the practically important states of the "frozen kinetics" which accompanies extremely wide spectrum of phenomena and allows understanding different physical and biological processes.

Seed ejection mechanism in an Oxalis species.

With millions of years' evolution, plants and fungi have developed a variety of ballistic dispersal structures for seeds or spores. One typical example is the catapult of an Oxalis sp., which can realize a consecutive seed ejection by triggering only one seed. If the protrusion on an aril, a specialized outgrowth covering a seed, is disturbed, cracks would occur and cause the opening of the aril. Subsequently, the whole aril snaps and transforms its stored strain energy to eject the inside seed with an optimal launching angle. Once the first seed is triggered, its curly aril will contact the next seed's protrusion and induce its firing. This chain effect will further trigger the remaining seeds in turns, within 0.1 s. Inspired by this phenomenon, we invented a bionic ejection device to launch projectiles with high efficiency. This exploration is promising for a number of applications, such as drug delivery and oil displacement.

Is dispersal mode a driver of diversification and geographical distribution in the tropical plant family Melastomataceae?

Species of plants with different life history strategies may differ in their seed dispersal mechanisms, impacting their distribution and diversification patterns. Shorter or longer distance dispersal is favored by different dispersal modes, facilitating (or constraining) population isolation, which can, in turn, impact speciation and species range sizes. While these associations are intuitive, few studies have explicitly tested these hypotheses for large clades of angiosperms. The plant family Melastomataceae is found on disparate habitats with different dispersal modes, representing a good model to address these questions. In this study, we reconstruct the phylogeny of Melastomataceae and gather data on their dispersal mode and range size to test the impact of dispersal mode on diversification and range size evolution. We found that abiotic dispersal is ancestral in the family, while biotic dispersal evolved multiple times. Species richness distribution is very similar across dispersal modes, although abiotically dispersed species tend to be relatively more diverse in seasonal environments. Range sizes across dispersal modes are not significantly different, although biotically dispersed species have slightly wider distributions. Model comparisons indicate that factors other than dispersal mode might have driven diversification heterogeneity. We did not find evidence for the role of dispersal mode driving diversification rates or range size in the Melastomataceae, suggesting a complex macroevolutionary scenario for this diverse angiosperm family. The bulk of changes to biotic dispersal coinciding with an increase in passerine diversification suggests a possible "past" key innovation in Melastomataceae. Future studies should investigate the role of other diversification drivers in the family and the relatively higher diversity of abiotically dispersed species in open habitats.