A new rain-operated seed dispersal mechanism in Bertolonia mosenii (Melastomataceae), a Neotropical rainforest herb

Although widespread among fungi, lichens, liverworts, and mosses, seed dispersal mechanisms operated by rain are unusual among flowering plants. Generally speaking, two mechanisms are involved in seed dispersal by rains: the splash-cup and the springboard. Here we describe a new seed dispersal mechanism operated by rain in a Neotropical rainforest herb Bertolonia mosenii Cogniaux (Melastomataceae). The study was carried out at the lowland Atlantic rainforest, southeastern Brazil. We experimentally demonstrate that rain is necessary to release the seeds from the capsules through what we call squirt-corner seed dispersal mechanism: when a raindrop strikes the mature fruit, the water droplet forces the seeds outward to the angles (corners) of the triangular capsule and the seeds are released. As far as we know squirt-corner represents a new rain-operated seed dispersal mechanism, and a novel seed dispersal mode both for Melastomataceae and for flowering plants from Neotropical forests.

Seed dispersal of Attalea phalerata (Palmae) by Crested caracaras (Caracara plancus) in the Pantanal and a review of frugivory by raptors

We observed Crested caracaras (Caracara plancus) consuming and dispersing fruits of the palm Attalea phalerata at Pantanal, Brazil. We reviewed the literature of seed dispersal by raptors and suggest that raptors may affect seed dispersal by three different paths: secondary seed dispersal by preying on frugivorous birds, primary seed dispersal of ornithocoric fruits and primary seed dispersal of large, lipid-rich fruits. The latter path may be an important long-distance seed dispersal mechanism for large seeds.

Frugivory and Seed Dispersal by Northern Pigtailed Macaques (Macaca leonina), in Thailand

Tropical rain forest conservation requires a good understanding of plant-animal interactions. Seed dispersal provides a means for plant seeds to escape competition and density-dependent seed predators and pathogens and to colonize new habitats. This makes the role and effectiveness of frugivorous species in the seed dispersal process an important topic. Northern pigtailed macaques (Macaca leonina) may be effective seed dispersers because they have a diverse diet and process seeds in several ways (swallowing, spitting out, or dropping them). To investigate the seed dispersal effectiveness of a habituated group of pigtailed macaques in Khao Yai National Park, Thailand, we examined seed dispersal quantity (number of fruit species eaten, proportion in the diet, number of feces containing seeds, and number of seeds processed) and quality (processing methods used, seed viability and germination success, habitat type and distance from parent tree for the deposited seeds, and dispersal patterns) via focal and scan sampling, seed collection, and germination tests. We found thousands of seeds per feces, including seeds up to 58 mm in length and from 88 fruit species. Importantly, the macaques dispersed seeds from primary to secondary forests, via swallowing, spitting, and dropping. Of 21 species, the effect of swallowing and spitting was positive for two species (i. e., processed seeds had a higher % germination and % viability than control seeds), neutral for 13 species (no difference in % germination or viability), and negative (processed seeds had lower % germination and viability) for five species. For the final species, the effect was neutral for spat-out seeds but negative for swallowed seeds. We conclude that macaques are effective seed dispersers in both quantitative and qualitative terms and that they are of potential importance for tropical rain forest regeneration. © 2013 Springer Science+Business Media New York.

Functional Redundancy and Complementarities of Seed Dispersal by the Last Neotropical Megafrugivores

Background: Functional 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 Findings: We 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/Significance: Our 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. © 2013 Bueno et al.

Specialized Seed Dispersal in Epiphytic Cacti and Convergence with Mistletoes

Mistletoes represent the best example of specialization in seed dispersal, with a reduced assemblage of dispersal agents. Specific dispersal requirements mediated by the specificity of seed deposition site have apparently led to the evolution of such close relationships between mistletoes and certain frugivores. Here, we provide evidences for another case of specialization involving epiphytic cacti in the genus Rhipsalis, and small Neotropical passerines Euphonia spp., which also act as the main seed dispersers of mistletoes in the family Viscaceae. With field observations, literature search, and observations on captive birds, we demonstrated that Rhipsalis have specific establishment requirements, and euphonias are the most effective dispersers of Rhipsalis seeds in both quantitative and qualitative aspects, potentially depositing seeds onto branches of host plants. We interpret the similar dispersal systems of Rhipsalis and Viscaceae mistletoes, which involve the same dispersal agents, similar fruit morphologies, and fruit chemistry as convergent adaptive strategies that enable seeds of both groups to reach adequate microsites for establishment in host branches. © 2013 by The Association for Tropical Biology and Conservation.

Seed dispersal by the lek-forming white-bearded manakin (Manacus manacus, Pipridae) in the Brazilian Atlantic forest

The movement patterns of males, females and juveniles of lekking species often differ due to differences in the commitment to lek activities, which may lead to differences in the spatial distribution and dispersal distances of seeds they eat. By sampling seeds in three lek and non-lek areas of the white-bearded manakin (Manacus manacus), we tested whether this lekking species increased the abundance and species richness of seeds in lek areas and, at a finer scale, in 21 displaying courts within lek areas. Combining data on seed defecation or regurgitation rates by free-ranging individuals, the number of seeds in droppings or regurgitations of mist-netted birds, and the distances travelled by birds equipped with radio-transmitters, we estimated the potential spatial distribution of seeds generated by six resident males and six females or juveniles during the morning peak of lek activity and when lek activity decreased in the afternoon. There was no difference in the species richness (46 and 44 morphospecies, respectively) and abundance of seeds (15.4 ± 7.3 seeds and 14.0 ± 1.1 seeds, respectively) between lek and non-lek areas. Within leks both parameters increased in courts (45 spp., 17.6 ± 14 seeds) compared with non-court sites (22 spp., 1.9 ± 1.8 seeds), likely as a consequence of the longer time spent by resident males in perches in or near display courts. Distances moved by juveniles and females per 60-min period (183 ± 272 m) were greater than resident males (42.6 ± 22.0 m) in the mornings, while the opposite happened in the afternoons (55.2 ± 40.7 m and 157 ± 105 m, respectively). We conclude that the spatial aggregation of seeds in lek areas of M. manacus occurs at the court level, and the spatial distribution of deposited seeds varies with manakin lekking status and the daily period of foraging. © Cambridge University Press 2013.

Frugivory and seed dispersal by tapirs: an insight on their ecological role

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Reconstructing past ecological networks: the reconfiguration of seed-dispersal interactions after megafaunal extinction

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Partitioning the relative contribution of one-phase and two-phase seed dispersal when evaluating seed dispersal effectiveness

Seed dispersal effectiveness (SDE) is a conceptual framework that aims at quantifying the contribution of seed dispersal vectors to plant fitness. While it is well recognized that diplochorous dispersal systems, characterized by two successive dispersal steps performed by two different vectors (Phase I=primary seed dispersal and Phase II=secondary seed dispersal) which are common in temperate and tropical regions, little attention has been given to distinguishing the relative contribution of one-phase and two-phase dispersal to overall SDE. This conceptual gap probably results from the lack of a clear methodology to include Phase II dispersal into the calculation of SDE and to quantify its relative contribution. We propose a method to evaluate the relative contribution of one-phase and two-phase dispersal to SDE and determine whether two seed dispersers are better than one. To do so, we used the SDE landscape and an extension of the SDE landscape, the Phase II effect landscape, which measures the direction and magnitude of the Phase II dispersal effect on overall SDE. We used simulated and empirical data from a diplochorous dispersal system in the Peruvian Amazon to illustrate this new approach. Our approach provides the relative contribution of one-phase SDE (SDE1) and two-phase SDE (SDE2) to overall SDE and quantifies how much SDE changes with the addition of Phase II dispersal. Considering that the seed dispersal process is context dependent so that Phase II depends on Phase I, we predict the possible range of variation of SDE according to the variation of the probability of Phase II dispersal. In our specific study system composed of two primate species as primary dispersal vectors and different species of dung beetles as secondary dispersal vectors, the relative contribution of SDE1 and SDE2 to overall SDE varied between plant species. We discuss the context dependency of the Phase II dispersal and the potential applications of our approach. This extension to the conceptual framework of SDE enables quantitative evaluation of the effect of Phase II dispersal on plant fitness and can be easily adapted to other biotic and/or abiotic diplochorous dispersal systems.

The importance of landscape structure for seed dispersal in rain forest fragments

Questions What are the main features of the seed rain in a fragmented Atlantic forest landscape? Can seed rain species attributes (life form, dispersal mode, successional status) relate to the spatial arrangement (size and number of fragments, edge density and presence of corridor) of forest fragments in the landscape? How does the rain forest landscape structure affect the seed rain? Location Atlantic rainforest, Sao Paulo State, Southeastern Brazil. Methods Seed rain samples were collected monthly throughout 1yr, counted, identified and classified according to species dispersal mode, successional status and life form. Seed rain composition was compared with woody species near the seed traps. Relationships between seed rain composition and landscape spatial arrangement (fragment area, presence of corridor, number of fragments in the surroundings, proximity of fragments, and edge density) were tested using canonical correspondence analysis (CCA). Results We collected 20142 seeds belonging to 115 taxa, most of them early successional and anemochorous trees. In general, the seed rain had a species composition distinct from that of the nearby forest tree community. Small isolated fragments contained more seeds, mainly of anemochorous, epiphytic and early-successional species; large fragments showed higher association with zoochorous and late-successional species compared to small fragments. The CCA significantly distinguished the species dispersal mode according to fragment size and isolation, anemochorous species being associated to small and isolated fragments, and zoochorous species to larger areas and fragment aggregation. Nevertheless, a gradient driven by proximity (PROX) and edge density (ED) segregated lianas (in the positive extremity), early successional and epiphyte species (in the negative end); large fragments were positively associated to PROX and ED. Conclusions The results highlight the importance of the size and spatial arrangement of forest patches to promote habitat connectivity and improve the flux of animal-dispersed seeds. Landscape structure controls seed fluxes and affects plant dispersal capacity, potentially influencing the composition and structure of forest fragments. The seed rain composition may be used to assess the effects of landscape spatial structure on plant assemblages, and provide relevant information for biodiversity conservation.

Influence of pollination and seed dispersal on the genetic population structure of two Commiphora species in Madagascar and South Africa

Pollination and seed dispersal are important ecological processes for the regeneration of plant populations and both vectors for gene exchange between plant populations. For my thesis, I studied the pollination ecology of the South African tree Commiphora harveyi (Burseraceae) and compared it with C. guillauminii from Madagascar. Both species have low visitation rates and a low number of pollinating insect species, resulting in a low fruit set. While their pollination ecology is very similar, they differ in their seed dispersal with a low seed dispersal rate in the Malagasy and a high seed dispersal rate in the South African species. This should be reflected in a stronger genetic differentiation among populations in the Malagasy than in the South African species. My results, based on AFLP markers, contradict these expectations, the overall differentiation was lower in the Malagasy (FST = 0.05) than in the South African species (FST = 0.16). However, at a smaller spatial scale (below 3 km), the Malagasy species was genetically more strongly differentiated than the South African species, which was reflected by the high inter-population variance within the sample site (C. guillauminii: 72.2 - 85.5 %; C. harveyi: 8.4 - 14.5 %). This strong differentiation could arise from limited gene flow, which was confirmed by spatial autocorrelation analyses. The shape of the autocorrelogram suggested that gene exchange between individuals occurred only up to 3 km in the Malagasy species, whereas up to 30 km in the South African species. These results on the genetic structure correspond to the expectations based on seed dispersal data. Thus, seed dispersal seems to be a key factor for the genetic structure in plant populations on a local scale.

Frugivores, seed dispersal and tree regeneration along a human disturbance gradient in East African tropical rainforests

Samenausbreitung und Regeneration von Bäumen sind wichtig für den langfristigen Bestand von Baum- und Frugivorengemeinschaften in tropischen Regenwäldern. Zunehmende Rohdung und Degradation gefährden den Ablauf dieser mutualistischen Prozesse in diesem Ökosystem. Um den Einfluss von kleinräumiger menschlicher Störung auf die Frugivorengemeinschaft und die zentralen Ökosystemprozesse Samenausbreitung und Regeneration zu erforschen, habe ich 1) die Frugivorengemeinschaft und die Samenausbreitungsrate von Celtis durandii (Ulmaceae) und 2) den Zusammenhang zwischen Baumarten mit fleischigen Früchten, Frugivoren und der Etablierung von Keimlingen dieser Baumarten in unterschiedlich stark gestörten Flächen dreier ostafrikanischer tropischer Regenwälder untersucht. Insgesamt konnte ich 40 frugivore Vogel- und Primatenarten in den drei untersuchten Waldgebieten nachweisen. Auf gering gestörten Flächen wurden mehr Frugivore als auf stark gestörten Flächen aufgenommen. Auch die Beobachtungen an C. durandii ergaben mehr frugivore Besucher in Bäumen auf gering gestörten als auf stark gestörten Flächen. Dies führte zu einer marginal signifikant höheren Samenausbreitungsrate auf den gering gestörten Flächen. Diese Ergebnisse waren auf regionaler Ebene in allen drei untersuchten Wäldern konsistent. Dies zeigt, dass kleinräumige Störung einen umfassenderen negativen Einfluss auf Frugivore und ihre Funktion als Samenausbreiter hat als zuvor angenommen. Bei der Vegetationserfassung nahm ich 131 verschiedene Baumarten mit fleischigen Früchten in den drei Regenwäldern auf. Kleinräumige menschliche Störung erhöhte den Artenreichtum dieser Baumarten marginal signifikant, hatte jedoch keinen direkten Einfluss auf die Frugivorendichte und den Artenreichtum von Keimlingen dieser Baumarten. Der Artenreichtum von Baumarten mit fleischigen Früchten zeigte einen marginal signifikant positiven Einfluss auf die Frugivorendichte, allerdings nicht auf die Keimlinge. Allerdings führte die Dichte der Frugivoren zu signifikant erhöhtem Artenreichtum der Keimlinge. Folglich scheint kleinräumige Störung die Keimlingsetablierung indirekt durch erhöhten Baumartenreichtum und erhöhte Frugivorendichte zu beeinflussen. Die Frugivorendichte hatte einen größeren Einfluss auf die Waldregeneration als kleinräumige Störung und Baumartenreichtum. Demnach scheint kleinräumige menschliche Störung sowohl positive als auch negative Effekte auf Samenausbreitung und Regeneration zu haben. Somit sind weitere Studien notwendig, die den Einfluss von kleinräumiger menschlicher Störung auf Mutualismen tropischer Regenwälder aufklären.

Gastropod Seed Dispersal: An Invasive Slug Destroys Far More Seeds in Its Gut than Native Gastropods

Seed dispersal is one of the most important mechanisms shaping biodiversity, and animals are one of the key dispersal vectors. Animal seed dispersal can directly or indirectly be altered by invasive organisms through the establishment of new or the disruption of existing seed dispersal interactions. So far it is known for a few gastropod species that they ingest and defecate viable plant seeds and consequently act as seed dispersers, referred to as gastropodochory. In a multi-species experiment, consisting of five different plant species and four different gastropod species, we tested with a fully crossed design whether gastropodochory is a general mechanism across native gastropod species, and whether it is altered by the invasive alien slug species Arion lusitanicus. Specifically, we hypothesized that a) native gastropod species consume the seeds from all tested plant species in equal numbers (have no preference), b) the voracious invasive alien slug A. lusitanicus – similarly to its herbivore behaviour – consumes a higher amount of seeds than native gastropods, and that c) seed viability is equal among different gastropod species after gut passage. As expected all tested gastropod species consumed all tested plant species. Against our expectation there was a difference in the amount of consumed seeds, with the largest and native mollusk Helix pomatia consuming most seeds, followed by the invasive slug and the other gastropods. Seed damage and germination rates did not differ after gut passage through different native species, but seed damage was significantly higher after gut passage through the invasive slug A. lusitanicus, and their germination rates were significantly reduced.