Spatial Pattern of Pindó Palm (Syagrus romanzoffiana) Recruitment in Argentinian Atlantic Forest: The Importance of Tapir and Effects of Defaunation

Hunting pressure, fragmentation and deforestation have caused global declines in animal abundance, and the consequences for plant communities are poorly understood. Many large‐seeded plants, for instance, depend on large and endangered vertebrates for seed dispersal. In some Semi‐deciduous Atlantic Forests, endangered tapirs (Tapirus terrestris) are major dispersers of pindó palms (Syagrus romanzoffiana). Here, we compare recruitment patterns of pindó palms between protected and disturbed (defaunated) Atlantic Forest areas in Argentina and evaluate the potential consequences of the lack of the main disperser for pindó palm regeneration. We analyzed the number and spatial pattern of pindó adults, offspring, and tapir dung piles within ten plots established in an area spanning tapir latrines inside Iguazú National Park and in a fragmented forest area outside the park where tapir is locally extinct. In both areas, we evaluated recruitment levels beneath 24 adult palms in circular plots centered on adult stems. We found lower pindó palm recruitment outside the park where offspring tended to be aggregated around adult palms. In contrast, in Iguazú National Park offspring were spatially associated with tapir dung‐piles, in which most offspring were registered. Recruitment under adults was higher outside the park suggesting a lower rate of seed removal in disturbed areas. Our results show that tapir dispersal promotes higher recruitment levels of pindó offspring and shapes their spatial pattern, breaking the spatial association with adult (presumably maternal) palms. These results are useful for predicting the impact of local tapir extinction on this palm.     

Seed Dispersal by Birds and Bats in Lowland Philippine Forest Successional Area

In the tropical forests of SE Asia, only a few studies have dealt with the role animal dispersal plays in early forest succession and rehabilitation, and a comparison of bird and bat dispersal is even rarer. We investigated seed dispersal by birds and bats in a successional area in the lowland dipterocarp forest of the Subic Watershed Forest Reserve (SWFR) in Luzon Island, Philippines. Using pairs of day and night traps, we collected seeds during 3 mo of wet season and 3 mo of dry season in a 1.2-ha study site. Bird-dispersed seeds predominated over those dispersed by bats in terms of both seed abundance and number of seed species. The most abundant endozoochorous seed species were significantly biased toward either bird or bat dispersal. Birds and bats appeared to compete more strongly for fruit resources during the dry season than during the wet season, and bats responded more to changes in the seasons than birds did. GLM analyses showed that the factor that had the strongest influence on overall seed distribution was the number of fleshy-fruited trees surrounding the traps, and that the distribution pattern of day-dispersed seeds was affected by more physical factors (number of trees, size of trees, presence of fleshy-fruited and conspecific trees) in the study site than the pattern of night-dispersed seeds were. Given that birds are the more important dispersers in the study site, restoration efforts in SWFR might benefit by focusing on attracting these dispersers into its degraded habitats.     

Spatial Patterns of Seed Dispersal by White-Faced Capuchins in Costa Rica: Evaluating Distant-Dependent Seed Mortality

Spatial patterns of seed dispersal are the focus of numerous theoretical examinations of endozoochory. Here, we examine the spatial pattern of seed dispersal by white-faced capuchin monkeys Cebus capucinus in Santa Rosa National Park, Costa Rica, and the neighborhood characteristics and distance variables most closely associated with seed survival and germination, and seedling survival and growth in various locations. Overall, distance to the nearest fruiting conspecific tree has the most positive, consistent effect on growth and survival variables, which supports a variation of the Janzen–Connell seed escape hypothesis.     

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.     

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.     

Brazilian Tapir Density in the Pantanal: A Comparison of Systematic Camera-Trapping and Line-Transect Surveys

The density of Brazilian tapirs ( Tapirus terrestris) was studied in the northeastern part of the Pantanal wetlands of Brazil using two simultaneous and independent methods: (1) systematic camera trapping combined with capture–recapture analysis, with camera traps spaced 1 km apart and distributed over 54 km²; and (2) line-transect sampling using an array of 12 linear transects, from 3.8 to 7.2 km long, covering the principal open and forest habitat types across the entire 1063 km² SESC Pantanal Reserve. The two methods yielded conservative density estimates of 0.58 ± 0.11 tapirs/km² (camera trapping) and 0.55 (95% CI 0.30–1.01) tapirs/km² (line transects). The study suggests that certain Pantanal habitats and sites can sustain relatively high population densities of tapirs when these animals are protected from hunting. Further testing of the camera-trapping methodology as applied to tapirs is required, particularly focusing on extending the survey period. As it represents a relatively rapid method for estimating population density, in comparison to line-transect surveys, and as it generates information simultaneously on multiple species that are conservation priorities, we recommend that camera-trapping surveys be applied more widely across a variety of Pantanal habitats and land-use categories in order to confirm the value of the vast 140,000 km² wilderness region for this vulnerable species.     

Ruminant‐mediated Seed Dispersal of an Economically Valuable Tree in Indian Dry Forests1

Ruminant‐mediated seed dispersal, an understudied process in tropical forests, was examined via Phyllanthus emblica–Axis axis interaction. A captive Axis deer regurgitated intact P. emblica seeds after retaining them in the rumen for 7–27 h. At Rajaji National Park, a considerable fraction (22%) of deer‐regurgitated P. emblica seeds germinated, although lower than unconsumed seeds (72%). The size and strength of seeds like P. emblica might ensure that ruminants regurgitate them intact instead of defecating them.     

Seed Dispersal by Primates and Implications for the Conservation of a Biodiversity Hotspot,the Atlantic Forest of South America

Primates play a fundamental role as seed dispersers, particularly in tropical rainforests. Because defaunation and fragmentation are leading several primate species to local extinction, it is fundamental to understand the role of primates as effective seed dispersers. Here we present a systematic review of studies of seed dispersal by primates in a biodiversity hotspot, the Atlantic Forest of South America, to 1) highlight gaps in our knowledge, 2) determine species richness and proportion of seed species dispersed, and 3) test the relationship between primate body size and the size of dispersed species. Our review found 79 studies of the diet of six ecospecies (Callithrix, Leontopithecus, Callicebus, Sapajus, Alouatta, Brachyteles) but only 20 of these report information on seed dispersal, and none of these are on Callithrix or Callicebus. We found a strong bias in the distribution of species and regions, with most of the studies concentrated in southeastern Brazil. All ecospecies dispersed a large proportion of the seed species they handled (72.1–93.6%). Brachyteles dispersed the highest diversity of plants (N = 73), followed by Sapajus (N = 66), Leontopithecus (N = 49), and Alouatta (N = 26). Although we found no significant relationship between primate body size and the size of seeds dispersed, Brachyteles disperse a higher diversity of large-seeded species than smaller-bodied primates. These results suggest that the local extinction of large primate species may lead to dramatic changes in the plant community, as many large-seeded plants are inaccessible to smaller arboreal frugivores. We propose guidelines for future research on primate seed dispersal to enable the evaluation of seed dispersal effectiveness and to improve our understanding of the fundamental role of primates in this key ecosystem process.     

Mind the gap! Integrating taxonomic approaches to assess ant diversity at the southern extreme of the Atlantic Forest

Understanding patterns of species diversity relies on accurate taxonomy which can only be achieved by long‐term natural history research and the use of complementary information to establish species boundaries among cryptic taxa. We used DNA barcoding to characterize the ant diversity of Iguazú National Park (INP), a protected area of the Upper Paraná Atlantic Forest ecoregion, located at the southernmost extent of this forest. We assessed ant diversity using both cytochrome c oxidase subunit 1 (COI) sequences and traditional morphological approaches, and compared the results of these two methods. We successfully obtained COI sequences for 312 specimens belonging to 124 species, providing a DNA barcode reference library for nearly 50% of the currently known ant fauna of INP. Our results support a clear barcode gap for all but two species, with a mean intraspecific divergence of 0.72%, and an average congeneric distance of 17.25%. Congruently, the library assembled here was useful for the discrimination of the ants of INP and allowed us to link unidentified males and queens to their worker castes. To detect overlooked diversity, we classified the DNA barcodes into Molecular Operational Taxonomic Units (MOTUs) using three different clustering algorithms, and compared their number and composition to that of reference species identified based on morphology. The MOTU count was always higher than that of reference species regardless of the method, suggesting that the diversity of ants at INP could be between 6% and 10% higher than currently recognized. Lastly, our survey contributed with 78 new barcode clusters to the global DNA barcode reference library, and added 36 new records of ant species for the INP, being 23 of them new citations for Argentina.     

Seed Dispersal by Kerama Deer (Cervus nippon keramae) on Aka Island,the Ryukyu Archipelago,Japan1

Endozoochorous seed dispersal by kerama deer (Cervus nippon keramae) was investigated at four sites on Aka Island, the Ryukyu Archipelago, Japan. Kerama deer feces contained seeds of 35 plant species. Most of the germinated seeds were small (1.3 ± 0.18 mm) and had a hard coat, comparable to the germinated seeds in several other studies of endozoochorous seed dispersal by herbivores. Both the numbers and species compositions of seeds differed among the four sites, reflecting differences in the food available to kerama deer among habitats. Although many graminoid seeds were found in the two open habitats (Sites A and B) and in the adjoining forest habitat (Site C), woody plant seeds dispersed endozoochorously by birds and mammals were dominant in the forest (Site D), away from the marsh. Although a majority of the graminoid species was growing in open habitats such as the marsh and open fields, few were growing in the forest. Therefore, the kerama deer spread many open‐habitat graminoid seeds to the open and forest habitats. If a high density of kerama deer persists for a long time and gaps in forests are created by browsing kerama deer or by other means, graminoid species may spread substantially on Aka Island. Therefore, it is possible that seed dispersal by forest deer contributes to the expansion of grasslands.     

Fragmentation and Alteration of Seed Dispersal Processes: An Initial Evaluation of Dung Beetles, Seed Fate, and Seedling Diversity1

Given current accelerated trends of tropical land conversion, forest fragments are being incorporated into many conservation programs. For investing in fragments to be a viable conservation strategy, forest fragments must maintain their ecological integrity over the long term. Based on fieldwork in 22 forest fragments in the crater lakes region of western Uganda and in the continuous forest of Kibale National Park, we examined (1) seed predation on experimentally dispersed seeds, (2) abundance and composition of the dung beetle community that may play a major role in removing seeds from sites of high seed predation, and (3) compared the fragments’ seedling community composition to adult tree community composition and the seedling community in continuous forest. First, the rate of seed removal at experimental stations was lower in forest fragments (85% remaining after 1 day) than at stations in the continuous forest (79% remaining) and the probability of stations being discovered by seed predators was lower in fragments (23%) than in the intact forest (41%). Second, there was a 62 percent decline in fragment dung beetle abundance. The magnitude of this decline varied among dung beetle guilds that process dung and seeds in different fashions. The abundance of large rollers that move large seeds away from sites of defecation did not differ, but medium and smaller rollers and burying beetles that process small and medium‐sized seeds were less common in the fragments than in the intact forest. Finally, we compared the seedling community composition relative to adult tree community composition by identifying all adult trees in each fragment and by sampling the composition of the seedling community. We found some evidence to suggest that there was movement of seeds among forest fragments by large‐bodied dispersers, particularly chimpanzees (Pan troglodytes) and hornbills (Ceratogymna subcylindricus).     

Poachers and Forest Fragmentation Alter Seed Dispersal,Seed Survival,and Seedling Recruitment in the Palm Attalea butyraceae,with Implications for Tropical Tree Diversity1

We examined the interaction between a palm and two bruchid beetles along with several mammal species to explore how poachers and habitat fragmentation may indirectly alter the spatial pattern of seed dispersal, seed predation, and seedling recruitment in central Panama. The large, stony endocarps of Attalea butyraceae decay slowly and bear distinctive scars when opened by rodents or beetles. We determined the final distance between endocarps and reproductive trees (which we call an ecologically effective dispersal distance), the predation status of each endocarp, and the distance between seedlings and reproductive trees. The 68 focal trees were divided among 14 sites and four levels of anthropogenic disturbance. Levels of disturbance included full protection from poachers, light and heavy pressure from poachers, and small island habitat fragments. Ecologically effective seed dispersal distances were greatest for protected sites, intermediate for lightly poached sites, and shortest for heavily poached sites and habitat fragments. Seed predation by rodents increased with distance to the nearest reproductive Attalea and was greatest for fully protected sites, intermediate for lightly poached sites, and least for heavily poached sites and habitat fragments. Seed predation by beetles reversed the patterns described for seed predation by rodents. Total seed predation by beetles and rodents combined was independent of distance, greatest for fully protected sites, and lower for poached sites and habitat fragments. Seedling densities were always greatest close to reproductive trees; however, the increase in seedling densities close to reproductive trees was minimal for fully protected sites, clearly evident for poached sites, and pronounced for habitat fragments. Increased seedling recruitment near conspecific trees may in time reduce tree diversity where humans disrupt mammal communities.     

Habitat Use and Diet of Baird's Tapirs (Tapirus bairdii) in a Montane Cloud Forest of the Cordillera de Talamanca, Costa Rica1

Results from 24 transects showed that tapirs were less abundant in areas with higher human presence. They also preferred less steep areas, especially as browsing sites. An analysis of feces showed that fibers were the largest component (40–55%) followed by leaves (10–30%) and twigs (15%). Bamboo (Chusquea spp.) was found in all samples and probably accounts for the high proportion of fibers. Twenty‐seven plant species were identified to be eaten by tapirs.     

Patterns of Seed Dispersal and Dispersal Failure in a Hawaiian Dry Forest Having Only Introduced Birds

Dry forests are among the most endangered natural communities in the Hawaiian Islands. Most have been reduced to isolated trees and small forest fragments in which native tree species reproduce poorly. The replacement of native birds by introduced generalists may be contributing to dry forest decline through modification of seed dispersal patterns. To document seed dispersal by introduced birds, we conducted foraging observations on fleshy-fruited trees and measured seed rain under trees and in adjacent open areas for 1 year in a dry forest dominated by native trees. Although trees covered only 15.2 percent of the study area, 96.9 percent of the bird-dispersed seeds were deposited beneath them. The Japanese white-eye (Zosterops japonicus) was the principal dispersal agent. Among bird-dispersed seeds, those of the invasive tree Bocconia frutescens accounted for 75 percent of all seeds collected beneath trees (14.8 seeds/m²/yr) and the invasive shrub Lantana camara accounted for 17 percent. Although nearly 60 percent of the reserve's native woody species possess fleshy fruits, introduced birds rarely disperse their seeds. Native trees accounted for <8 percent of all bird-dispersed seeds and are consequently experiencing dispersal failure by falling directly under parent trees. Smaller-seeded non-native plants, in contrast, may be benefiting from dispersal by introduced birds. Current dispersal patterns suggest that these readily disseminated non-native plants may eventually replace the remaining native flora.     

Specialization on Guadua Bamboo Seeds by Three Bird Species in the Atlantic Forest of Argentina

Most bamboos are semelparous. Their synchronous masting events occur on a cycle of 3–120 yr and represent an extremely pulsed resource for granivorous birds. Although many bird species feed occasionally on bamboo seeds, there are constraints to specializing on such a fluctuating resource and few bird species are known to specialize on bamboo seeds. Three of these bird species are endemic to the Atlantic forest of South America: the purple-winged ground-dove Claravis godefrida , buff-fronted seedeater Sporophila frontalis , and Temminck's seedeater Sporophila falcirostris . All three species are irregularly recorded in the province of Misiones, Argentina. We compared the temporal and spatial patterns of records of these birds in Misiones to masting events of the five common bamboos: yatevó Guadua trinii , takuaruzú Guadua chacoensis , takuapí Merostachys claussenii , pitinga Chusquea tenella , and takuarembó Chusquea ramosissima . All bird records coincided with times and places where Guadua bamboos ( G. trinii and G. chacoensis ) were known or estimated to have seeds. None of the bird species occurred during masting events of Merostachys or Chusquea , unless Guadua was also masting. We discuss relevant ecological and morphological features of the birds that might bear on their association with Guadua bamboos and that might be key to their conservation.     

Dispersal by cattle of salt-marsh and dune species into salt-marsh and dune communities

We investigated the spatial cohort structure of Trillium populations in old-growth cove forests in Great Smoky Mountains National Park (TN, USA). We mapped the locations of all Trillium erectum L., Trillium grandiflorum (Michaux) Salisbury, and Trillium vaseyi Harbison occurring within two 10 × 10 m sample plots at each of three old-growth sites—Anthony Creek, Cove Mountain, and Kalanu Prong. The height and life stage of each individual were recorded and a randomly selected subset was excavated for age determination. Our results suggest that Trillium populations in cove forests of the southern Appalachians display a high degree of spatial aggregation and are relatively stable, spatially, over long time periods (i.e., decades). Individual patches (aggregations of plants) within populations were typically multi-aged and no clear spatial cohort structure was observed. Surprisingly, more isolated plants (distal from large aggregations) were among the oldest plants in the population, rather than recent colonists dispersing away from parent populations. Individual species were less mingled than expected given that they share a common dispersal agent (ants). This study provides a double-baseline for Trillium population structure in old, primary forests with low browse pressure.     

Seed Dispersal by Monkeys and the Fate of Dispersed Seeds in a Peruvian Rain Forest1

Primary seed dispersal by two species of monkeys and the effects of rodents and dung beetles on the fate of dispersed seeds are described for a rain forest in southeastern Perú. During the six-month study period (June–November 1992) spider monkeys (Ateles paniscus) dispersed the seeds of 71 plant species, whereas howler monkeys (Alouatta seniculus) dispersed seeds of 14 species. Spider and howler monkeys also differed greatly in their ranging behavior and defecation patterns, and as a consequence, produced different seed rain patterns. Monkey defecations were visited by 27 species of dung beetles (Scarabaeidae). Dung beetles buried 41 percent of the seeds in the dung, but the number of seeds buried varied greatly, according to seed size. Removal rates of unburied seeds by rodents varied between 63–97 percent after 30 d for 8 plant species. The presence of fecal material increased the percentage of seeds removed by seed predators, but this effect became insignificant with time. Although seed predators found some seeds buried in dung balls (mimicking burial by dung beetles), depth of burial significantly affected the fate of these seeds. Less than 35 percent of Brosimum lactescens seeds buried inside dung balls at a depth of 1 cm remained undiscovered by rodents, whereas at least 75 percent of the seeds escaped rodent detection at a depth of 3 cm and 96 percent escaped at 5 cm. Both dung beetles and rodents greatly affected the fate of seeds dispersed by monkeys. It is thus important to consider postdispersal factors affecting the fate of seeds when assessing the effectiveness of frugivores as seed dispersers.