Seed Dispersal Phenology and Germination Characteristics of a Drought-Prone Vegetation in Southeastern Brazil

Seed germination is determined by the environmental conditions typical of a habitat and also by the geographical origin of the source species pool. During the Quaternary, Brazilian Atlantic Rain Forest species expanded their distribution into the sandy coastal plains (restingas). Periods of water shortage, however, are frequent in the sandy substrate of the restinga. We investigated whether the germination characteristics of restinga species are more related to their biogeographical origin in the humid forest or to water shortage on sandy substrates. We characterized the seed dispersal phenology of a restinga community and conducted experiments to determine the water requirements for seed germination and the short-term seed dehydration sensitivity of different species. Species shed seeds throughout the year in the restinga. When subjected to Ψ=−0.37 MPa, seed germination percentage decreased and germination time increased in six of ten species when compared with Ψ=0 MPa. Most species showed high seed moisture content (MC>40 %) at seed dispersal. Seeds took 3–17 d to dehydrate when subjected to relative humidity≤76 percent and only two of eight species had seeds sensitive to short-term dehydration. Thus, rather than a specific set of germination characteristics related to humid or dry habitats, we gathered evidence to show that the germination characteristics of restinga species represent a multiplicity of responses that may be found in both kinds of habitat.     

Seed Dispersal by Golden-headed Lion Tamarins Leontopithecus chrysomelas in Southern Bahian Atlantic Forest, Brazil

Seed dispersal by small primates may be particularly relevant in areas where populations of larger frugivores have been reduced or extinguished by hunting and/or habitat disturbance. In this context, the aim of this study was to evaluate the role of the golden-headed lion tamarin Leontopithecus chrysomelas as a seed disperser in Atlantic forest remnants in Brazil. To this end, we opportunistically collected feces deposited during observations on the feeding behavior of two groups of golden-headed lion tamarins ranging in the degraded areas of the Una Biological Reserve, Bahia, Brazil, from February 2006 to January 2007. We collected 587 fecal samples, of which 524 contained seeds from 24 plant species, distributed over 13 families. Disregarding seeds of<3 mm, the majority of seeds recovered were bromeliad seeds. In general, ingestion of seeds by golden-headed lion tamarins did not improve the germination proportion or decrease the germination delay of seeds, with the exception of Aechmea spp. seeds. The tamarins encountered different habitats during their daily activity period, while feeding and defecating. Consequently, some seeds were transported to different habitats including disturbed areas. Thus, the role of seed dispersal in combination with the daily movement pattern of L. chrysomelas contributes to the persistence of fruit plants and epiphyte species and to the natural regeneration process within Atlantic forest remnants.     

Frugivory and Seed Dispersal by Four Species of Primates in Madagascar's Eastern Rain Forest1

In the unique faunal assemblage of the Malagasy rain forest, lemurs appear to play particularly important roles as seed-dispersing frugivores. A three-month study of feeding ecology and seed dispersal by four species of lemurs in Madagascar's eastern rain forest found that three species, Eulemur rubriventer, Eulemur fulvus, and Varecia variegata were seed dispersers, and the fourth, Propithecus diadema, was a seed predator. In germination trials, seeds passed by lemurs sprouted significantly faster and in greater numbers than those not passed by lemurs. Analysis of fruit morphologies of 69 local plant taxa producing fleshy fruits during the study period found that these fruits fell into two well-defined color categories that correlated significantly with fruit size. Seventy seven percent of fleshy fruits greater than 10 mm in diameter were colored green, brown, tan, purplish, or black, while all fruits less than 10 mm in diameter were colored red, yellow, orange, pink, blue, or white. Three introduced exotic plant species provided exceptions to this pattern, producing fruits which were larger than 10 mm and pink or orange. Fruits chosen by the primates in this study were usually larger than 10 mm in diameter and were in nearly all cases colored green, brown, tan, purplish, red, or some combination of these colors. Morphological traits shared by fruits of multiple plant taxa in the diets of seed-dispersing lemurs suggest possible coevolved relationships between Malagasy rain forest plants and lemurs.     

Evidence for Seed Dispersal by Rodents in Tropical Montane Forest in Africa

Seed dispersal by rodents has been understudied in Africa. Based on seed‐removal experiments, the presence of seeds in burrows and caches, cotyledon burial of seedlings, and images from camera traps, we provide evidence that rodents (Cricetomys kivuensis) remove and hoard large seeds of Carapa grandiflora in Nyungwe National Park, Rwanda.     

Mammalian Frugivores With Different Foraging Behavior Can Show Similar Seed Dispersal Effectiveness

Frugivores with disparate foraging behavior are considered to vary in their seed dispersal effectiveness (SDE). Measured SDEs for gibbons and macaques for a ‘primate‐fruit’ were comparable despite the different foraging and movement behavior of the primates. This could help facilitate fruit trait convergence in diverse fruit–frugivore networks.     

Effectiveness of Mistletoe Seed Dispersal by Tyrant Flycatchers in a Mixed Andean Landscape

The dependence of mistletoes on few dispersers and the directed dispersal they provide is well known, yet no recent work has quantified either the effectiveness of these ‘legitimate’ dispersers, or the extent of redundancy among them. Here, I use the seed dispersal effectiveness (SDE) framework to analyze how birds (Mionectes striaticollis and Zimmerius bolivianus) contribute to mistletoe (Struthanthus acuminatus and Phthirusa retroflexa) infection in traditional mixed plantations within a humid montane forest in Bolivia. I calculated SDE for each bird–mistletoe pair and for the disperser assemblage, by estimating both the quantity and the quality of dispersal. The quantity of dispersal was measured as: (1) disperser abundance; (2) frequency of visits; and (3) number of seeds dispersed per visit, and the quality of dispersal was measured as: (1) germination percentage and speed of germination of seeds regurgitated by birds; and (2) the concordance of deposited seeds and seedling distribution patterns with adult mistletoe distribution at three scales (habitat, host, and microhabitat). Dispersers were not redundant: the more generalist species M. striaticollis dispersed more seeds, but provided lower quality seed dispersal, whereas the mistletoe specialist Z. bolivianus provided low‐quantity and high‐quality seed dispersal. Whereas S. acuminatus benefited more from the SDE of Z. bolivianus, P. retroflexa benefited from the complementary seed dispersal provided by both birds. These results demonstrate how sympatric mistletoes that share the same disperser assemblage may develop different relationships with specific vectors, and describe how the services provided by two different dispersers (one that provides high‐quality and one that provides high‐quantity dispersal) interact to shape spatial patterns of plants.     

The Relative Contribution of Specialists and Generalists to Mistletoe Dispersal: Insights from a Neotropical Rain Forest

Mistletoes rely on birds for seed dispersal, but the presumed importance of mistletoe‐specialist frugivores has not been critically examined nor compared with generalist frugivores and opportunistic foragers. The contribution of these three groups was compared directly by quantifying bird visitation to fruiting mistletoe plants ( Oryctanthus occidentalis: Loranthaceae) at Barro Colorado Island, Panama, and by comparing these results with proportions calculated from other empirical studies of mistletoe visitation conducted elsewhere. After more than 100 h of timed watches, 23 bird species were recorded visiting eight heavily infected host trees ( Luehea seemannii: Tiliaceae). Eight of these species visited mistletoe, of which five (all tyrannids) consumed mistletoe fruit. Although two mistletoe specialist frugivores ( Tyrannulus elatus and Zimmerius vilissimus) removed most fruit (73%), more than a quarter was consumed by one generalist frugivore ( Mionectes oleagineus) and two opportunists ( Myiozetetes cayanensis and Myiozetetes similis). Post consumption behaviour varied: the specialists flew from mistletoe to mistletoe, the generalist rested in the subcanopy and understory, and the opportunists spent most time hawking insects and resting high in the canopy. Integrating these data with previous work, the dietary specialization, short gut passage rate and strict habitat preferences of mistletoe specialists suggests that their services relate primarily to intensification and contagious dispersal, while species with broader diets are more likely to visit uninfected trees and establish new infections. The presumed importance of mistletoe‐specialist frugivores was not supported and mistletoes are considered to be comparable to many other bird‐dispersed plants, relying on both specialist and generalist frugivores, while opportunists may be disproportionately important in long‐distance dispersal.     

Fruit Removal and Natural Seed Dispersal of the Brazil Nut Tree (Bertholletia excelsa) in Central Amazonia,Brazil

Experimental approaches to study seed dispersal of the Brazil nut tree have hitherto relied on exposed seeds deposited on the forest floor. Here we use a new method to study the natural dispersal by large rodents such as agoutis; tracking experimentally manipulated and tagged fruits containing individually marked seeds. Fruit manipulation did not deter agoutis from handling fruits. We found that agoutis usually moved intact fruits away from their original location below the parent tree before either hiding them or gnawing through the pericarp to access the seeds inside. Most fruits were moved to distances of 15–30 m from their original position, but some fruits could be taken as far as 60 m. A large number of seeds extracted from manipulated fruits appeared to be eaten immediately. Only 27 out of 1740 experimental seeds were found buried in shallow caches, generally within 5 m of the opened fruit. Fruit removal distance accounted for a disproportionate amount of total seed movement and seeds in the current study were dispersed significantly farther than in a previous experiment using exposed seeds, suggesting that classic dispersal experiments of this character may severely underestimate seed dispersal distances. We therefore conclude that the new method provides a more realistic and accurate approach to investigate natural seed dispersal of Brazil nuts and that the removal of fruits from underneath parent trees before being opened is the key to the significantly increased distances at which seeds are dispersed. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

Movement Patterns of a Native and Non‐native Frugivore in Hawaii and Implications for Seed Dispersal

Avian frugivores historically played important roles as seed dispersers across the Hawaiian Islands, but presently, the ‘ōma‘o (Myadestes obscurus) is the only extant native frugivore in the wild on the Island of Hawaii. During recent decades, the introduced generalist Japanese White‐eye (Zosterops japonicus) has become the most common bird in Hawaii. The movements of avian frugivores largely dictate how far seeds get dispersed and into what kinds of microhabitats. This study compares the movement patterns and diet of the ‘ōma‘o to the Japanese White‐eye to understand how a native differs from a non‐native frugivore in the type and distances of seeds dispersed. Radiotelemetry was conducted on nine ‘ōma‘o and nine Japanese White‐eyes in a system of natural forest fragments (kīpuka) created by lava flows. Japanese White‐eyes disperse seeds approximately twice as far as ‘ōma‘o; during the time of gut passage, ‘ōma‘o move a mean distance of 98.1 m, and Japanese White‐eyes move 170.1–194.8 m. However, the ‘ōma‘o disperses the seeds of at least seven different native fruit species compared with two dispersed by Japanese White‐eyes. Japanese White‐eyes were found to disperse seeds smaller than 1.5 mm, whereas the ‘ōma‘o dispersed seeds up to 6 mm in diameter. Despite their ecological differences, both birds distribute certain seeds within and among kīpuka and likely facilitate primary succession of fruiting plants in the young lava matrix. However, this study suggests that if the ‘ōma‘o were extirpated, a smaller‐bodied generalist cannot entirely substitute for the ecological role played by the native frugivore.     

Lowland tapirs facilitate seed dispersal in degraded Amazonian forests

The forests of southeastern Amazonia are highly threatened by disturbances such as fragmentation, understory fires, and extreme climatic events. Large‐bodied frugivores such as the lowland tapir (Tapirus terrestris) have the potential to offset this process, supporting natural forest regeneration by dispersing a variety of seeds over long distances to disturbed forests. However, we know little about their effectiveness as seed dispersers in degraded forest landscapes. Here, we investigate the seed dispersal function of lowland tapirs in Amazonian forests subject to a range of human (fire and fragmentation) and natural (extreme droughts and windstorms) disturbances, using a combination of field observations, camera traps, and light detection and ranging (LiDAR) data. Tapirs travel and defecate more often in degraded forests, dispersing much more seeds in these areas [9,822 seeds per ha/year (CI_95% = 9,106; 11,838)] than in undisturbed forests [2,950 seeds per ha/year (CI_95% = 2,961; 3,771)]. By effectively dispersing seeds across disturbed forests, tapirs may contribute to natural forest regeneration—the cheapest and usually the most feasible way to achieve large‐scale restoration of tropical forests. Through the dispersal of large‐seeded species that eventually become large trees, such frugivores also contribute indirectly to maintaining forest carbon stocks. These functions may be critical in helping tropical countries to achieve their goals to maintain and restore biodiversity and its ecosystem services. Ultimately, preserving these animals along with their habitats may help in the process of natural recovery of degraded forests throughout the tropics. Abstract in Portuguese is available with online material.     

Behavioral and Social Structure Effects on Seed Dispersal Curves of a Forest‐Interior Bulbul (Pycnonotidae) in a Tropical Evergreen Forest

Movement patterns of animals can vary dramatically as a function of their reproductive cycle or social structure; however, little is known about how changes in the social structure of dispersers affect patterns of seed dispersal. We examined the movement patterns of the forest‐dwelling and cooperatively breeding Puff‐throated Bulbul (Alophoixus pallidus) in relation to different stages of their reproductive cycle, time of day, and group size, to determine potential impacts on the shape and scale of dispersal curves generated using a combination of gut passage time and displacement distance data. There were significant differences in dispersal distances depending on group size, season (breeding, non‐breeding), incubation (vs. other times of the year), and time of the day. The estimated median seed dispersal distance was 28 m. The median dispersal distances produced by birds in larger groups were longer than those of smaller groups (29 m vs. 25 m). During the breeding season, median dispersal distances were longer than during the non ‐ breeding season (31 m vs. 25 m), but the median dispersal distances were significantly shorter during incubation than during outside incubation (24 m vs. 28 m). The median dispersal distance produced in the early morning (30 m) was also longer than that of other times of the day (23 m late morning, 28 m early afternoon, and 26 m late afternoon). This study suggests that various aspects of an animal's behavior are likely to have significant effects on seed shadows and that this may vary significantly even among individuals of the same species.     

Mating Behavior Drives Seed Dispersal by the Long‐wattled Umbrellabird Cephalopterus penduliger

Frugivores exhibit considerable variation in the seed dispersal services they provide. Understanding what drives these differences is a key goal for ecologists because of the central role seed dispersal plays in shaping ecological and genetic diversity in plant populations. The lek‐mating system of the Long‐wattled Umbrellabird (Cephalopterus penduliger) provides a powerful lens to examine how mating behavior may impact seed dispersal outcomes. As in all lek‐breeding species, male Umbrellabirds congregate in traditional sites (leks) to display, whereas females are solitary and visit leks only rarely. This study demonstrates how differences in mating behavior between the sexes drive distinctive seed movement and deposition patterns by male vs. female Umbrellabirds. Using radio tracking and gut retention trials, we documented divergent movement patterns between the sexes that are directly attributable to mating behavior differences. These movement differences led males to disperse seeds long distances from source trees and to deposit the majority of seeds they ingested within the lek; females dispersed seeds shorter distances and more evenly across the landscape. We empirically confirmed that the density of dispersed seeds was higher in leks than in control areas outside the lek, yet found no evidence that this higher density of seeds in leks reduced probability of seedling establishment. This research not only provides a mechanistic explanation for long dispersal distances and high levels of genetic diversity previously reported for seeds in Umbrellabird leks, but also highlights the importance of explicitly considering behavior in studies of animal‐mediated seed dispersal.     

Effects of an Epiphytic Orchid on Arboreal Ant Community Structure in Panama

Epiphytes are conspicuous structural elements of tropical forest canopies. Individual tree crowns in lowland forests may support more than 30 ant species, yet we know little about the effects of epiphytes on ant diversity. We examined the composition of arboreal ant communities on Annona glabra trees and their interactions with the epiphytic orchid Caularthron bilamellatum in Panama. We surveyed the ants on 73 trees (45 with C. bilamellatum and 28 lacking epiphytes) and recorded their nest sites and behavioral dominance at baits. We found a total of 49 ant species (in 20 genera), ranging 1–9 species per tree. Trees with C. bilamellatum had higher average (±SD) ant species richness (4.2±2.28) than trees without epiphytes (2.7±1.21). Hollow pseudobulbs (PBs) of C. bilamellatum were used as nest sites by 32 ant species, but only 43 percent of suitable PBs were occupied. Ant species richness increased with PB abundance in trees, but nest sites did not appear to be a limiting resource on A. glabra. We detected no close association between ants and the orchid. We conclude that higher ant species richness in the presence of the orchid is due to bottom‐up effects, especially the year‐round supply of extrafloral nectar. The structure of ant communities on A. glabra partly reflects interference competition among behaviorally dominant species and stochastic factors, as observed in other forests.     

A Multi-Forest Comparison of Dietary Preferences and Seed Dispersal by <Emphasis Type="BoldItalic">Ateles</Emphasis> spp

Investigations of coevolutionary relationships between plants and the animals that disperse their seeds suggest that disperser-plant interactions are likely shaped by diffuse, rather than species-to-species, coevolution. We studied the role of dietary plasticity in shaping the potential for diffuse coevolution by comparing dietary fruit preferences and seed dispersal by 3 species of spider monkeys (Ateles spp.) in 4 moist forests in Colombia, Ecuador, Panama, and Surinam. In all forests, spider monkeys were highly frugivorous and preyed upon seeds of few species. We estimated dietary use of fruiting taxa based on absolute consumption and preference, which accounts for resource availability. Of the 59 genera that comprised the 20 most frequently consumed genera summed in each forest, only 3—Brosimum (Moraceae), Cecropia (Cecropiaceae) and Virola (Myristicaceae)—ranked within the top 20 at every forest. Most genera were within the 20 most frequently consumed at only 1 or 2 forests. Based on preferences, only 4 genera ranked in the 20 most-preferred in all 4 forests: Brosimum, Cecropia, Ficus (Moracae), and Virola. Patterns in fruit consumption and preference at the familial level were similar in that only 2 families—Myristicaceae and Moraceae—were in the 10 most-consumed or most-preferred in all 4 forests. Interforest variation in plant specific composition and abundances and supra-annual fruiting phenologies, combined with dietary flexibility of Ateles spp., may partly explain these patterns. Our results suggest that variation in plant community structure strongly influences dietary preferences, and hence, seed dispersal by spider monkeys. Thus, diffuse coevolution in spider monkey-plant relationships may be limited to few taxa at the generic and familial levels.     

Seed germination and dormancy traits of forbs and shrubs important for restoration of North American dryland ecosystems

• In degraded dryland systems, native plant community re‐establishment following disturbance is almost exclusively carried out using seeds, but these efforts commonly fail. Much of this failure can be attributed to the limited understanding of seed dormancy and germination traits.
• We undertook a systematic classification of seed dormancy of 26 species of annual and perennial forbs and shrubs that represent key, dominant genera used in restoration of the Great Basin ecosystem in the western United States. We examined germination across a wide thermal profile to depict species‐specific characteristics and assessed the potential of gibberellic acid (GA₃) and karrikinolide (KAR₁) to expand the thermal germination envelope of fresh seeds.
• Of the tested species, 81% produce seeds that are dormant at maturity. The largest proportion (62%) exhibited physiological (PD), followed by physical (PY, 8%), combinational (PY + PD, 8%) and morphophysiological (MPD, 4%) dormancy classes. The effects of chemical stimulants were temperature‐ and species‐mediated. In general, mean germination across the thermal profile was improved by GA₃ and KAR₁ for 11 and five species, respectively. We detected a strong germination response to temperature in freshly collected seeds of 20 species. Temperatures below 10 °C limited the germination of all except Agoseris heterophylla, suggesting that in their dormant state, the majority of these species are thermally restricted.
• Our findings demonstrate the utility of dormancy classification as a foundation for understanding the critical regenerative traits in these ecologically important species and highlight its importance in restoration planning.

     

Massive Seed Predation of Pseudobombax grandiflorum (Bombacaceae) by Parakeets Brotogeris versicolurus (Psittacidae) in a Forest Fragment in Brazil1

Here we report massive seed predation of Pseudobombax grandiflorum (Bombacaceae) by Botogeris versicolurus (Psittacidae) in a forest fragment in Brazil. The intensity of seed predation was very high when compared to other studies in continuous forest, perhaps resulting from a scarcity of resources in such areas. This scarcity may limit the range of parrot's diet to a few plant species. It suggests that studies of Psittacidae seed predation may be important for conservation of some plants in fragments.     

Seed dispersal and realized gene flow of two forest orchids in a fragmented landscape

• Species with vast production of dust‐like windborne seeds, such as orchids, should not be limited by seed dispersal. This paradigm, however, does not fit recent studies showing that many sites suitable for orchids are unoccupied and most seeds land close to their maternal plant. To explore this issue, we studied seed dispersal and gene flow of two forest orchid species, Epipactis atrorubens and Cephalanthera rubra, growing in a fragmented landscape of forested limestone hills in southwest Bohemia, Czech Republic.
• We used a combination of seed trapping and plant genotyping methods (microsatellite DNA markers) to quantify short‐ and long‐distance dispersal, respectively. In addition, seed production of both species was estimated.
• We found that most seeds landed very close to maternal plants (95% of captured seeds were within 7.2 m) in both species, and dispersal distance was influenced by forest type in E. atrorubens. In addition, C. rubra showed clonal reproduction (20% of plants were of clonal origin) and very low fruiting success (only 1.6% of plants were fruiting) in comparison with E. atrorubens (25.7%). Gene flow was frequent up to 2 km in C. rubra and up to 125 km in E. atrorubens, and we detected a relatively high dispersal rate among regions in both species.
• Although both species occupy similar habitats and have similar seed dispersal abilities, C. rubra is notably rarer in the study area. Considerably low fruiting success in this species likely limits its gene flow to longer distances and designates it more sensitive to habitat loss and fragmentation.