Defaunation changes leaf trait composition of recruit communities in tropical forests in French Guiana.

Hunting impacts tropical vertebrate populations, causing declines of species that function as seed dispersers and predators, or that browse seedlings and saplings. Whether and how the resulting reductions in seed dispersal, seed predation, and browsing translate to changes in the tree composition is poorly understood. Here, we assess the effect of defaunation on the functional composition of communities of tree recruits in tropical rainforests in French Guiana. We selected eight sites along a gradient of defaunation, caused by differences in hunting pressure, in otherwise intact old-growth forests in French Guiana. We measured shifts in functional composition by comparing leaf and fruit traits and wood density between tree recruits (up to 5 cm diameter at breast height) and adults, and tested whether and how these compositional shifts related to defaunation. We found a positive relationship with defaunation for shifts in specific leaf area, a negative relationship for shifts of leaf toughness and wood density, and a weak relationship for shifts in fruit traits. Our results suggest that the loss of vertebrates affects ecological processes such as seed dispersal and browsing, of which browsing remains understudied. Even though these changes sometimes seem minor, together they result in major shifts in forest composition. These changes have long-term ramifications that may alter forest dynamics for generations.

Site and species contribution to ß-diversity in terrestrial mammal communities: Evidence from multiple Neotropical forest sites.

In a scenario where escalating human activities lead to several environmental changes and, consequently, affect mammal abundance and distribution, ß-diversity may increase due to differences among sites. Using the ecological uniqueness approach, we analyzed ß-diversity patterns of ground-dwelling mammal communities recorded through comprehensive camera trap monitoring within eight tropical forests protected areas in Mesoamerica and South America under variable landscape contexts. We aimed to investigate whether the contribution of single sites (LCBD) and single species (SCBD) to overall ß-diversity could be explained by community metrics and environmental variables, and by species metrics and biological traits, respectively. Total ß-diversity was also partitioned into species replacement and richness difference. We related LCBD to species richness, total relative abundance, functional indices, and environmental variables (tree basal area, protected area size, NDVI, and precipitation seasonality), and SCBD to species naïve occupancy, relative abundance, and morphoecological traits via beta regression. Our findings showed that LCBD was primarily explained by variation in species richness, rather than relative abundance and functional metrics. Protected area size and tree basal area were also important in explaining variation in LCBD. SCBD was strongly related to naïve occupancy and relative abundance, but not to biological traits, such as body mass, trophic energy level, activity cycle, and taxonomic category. Local ß-diversity was a result of species replacements and to a lesser extent differences in species richness. Our approach was useful in examining and comparing the ecological uniqueness among different sites, revealing the regional scale current status of mammal diversity. High LCBD values comprised sites embedded within smaller habitat extents, hosting lower tree basal areas, and harboring low species richness. SCBD showed that relatively ubiquitous species that occur at variable abundances across sites contributed most to ß-diversity.

Tick Microbiomes in Neotropical Forest Fragments Are Best Explained by Tick-Associated and Environmental Factors Rather than Host Blood Source.

The composition of tick microbiomes varies both within and among tick species. Whether this variation is intrinsic (related to tick characteristics) or extrinsic (related to vertebrate host and habitat) is poorly understood but important, as microbiota can influence the reproductive success and vector competence of ticks. We aimed to uncover what intrinsic and extrinsic factors best explain the microbial composition and taxon richness of 11 species of neotropical ticks collected from eight species of small mammals in 18 forest fragments across central Panama. Microbial richness varied among tick species, life stages, and collection sites but was not related to host blood source. Microbiome composition was best explained by tick life stage, with bacterial assemblages of larvae being a subset of those of nymphs. Collection site explained most of the bacterial taxa with differential abundance across intrinsic and extrinsic factors. Francisella and Rickettsia were highly prevalent, but their proportional abundance differed greatly among tick species, and we found both positive and negative cooccurrence between members of these two genera. Other tick endosymbionts (e.g., Coxiella and Rickettsiella) were associated with specific tick species. In addition, we detected Anaplasma and Bartonella in several tick species. Our results indicate that the microbial composition and richness of neotropical ticks are principally related to intrinsic factors (tick species and life stage) and collection site. Taken together, our analysis informs how tick microbiomes are structured and can help anchor our understanding of tick microbiomes from tropical environments more broadly.IMPORTANCE Blood-feeding arthropod microbiomes often play important roles in disease transmission, yet the factors that structure tick microbial communities in the Neotropics are unknown. Utilizing ticks collected from live animals in neotropical forest fragments, this study teases apart the contributions of intrinsic and extrinsic tick-associated factors on tick microbial composition as well as which specific microbes contribute to differences across tick species, tick life stages, the mammals they fed on, and the locations from where they were sampled. Furthermore, this study provides revelations of how notable tick-associated bacterial genera are interacting with other tick-associated microbes as well as the forest animals they encounter.

Increased terrestriality in a Neotropical primate living on islands with reduced predation risk.

An arboreal lifestyle is thought to be central to primate origins, and most extant primate species still live in the trees. Nonetheless, terrestrial locomotion is a widespread adaptation that has arisen repeatedly within the primate lineage. The absence of terrestriality among the New World monkeys (Platyrrhini) is thus notable and raises questions about the ecological pressures that constrain the expansion of platyrrhines into terrestrial niches. Here, we report the results of a natural experiment, comparing patterns of terrestrial behavior in white-faced capuchin monkeys (Cebus capucinus imitator) living on two islands off the Pacific coast of Panama that lack mammalian predators (island sites) with the behavior of capuchins at three sites in central Panama with more intact predator communities (mainland sites). Surveys with camera traps revealed increased terrestriality in island vs. mainland sites. Capuchin detection rates were higher, the range of party sizes observed was larger, and individuals engaged in a wider range of terrestrial behaviors on the islands lacking mammalian predators. Furthermore, females carrying infants were frequently photographed on the ground at the island sites, but never at the mainland sites. These findings support the long-standing hypothesis that predators constrain the exploitation of terrestrial niches by primates. These results are also consistent with the hypothesis that arboreal locomotion imposes costs that primates will avoid by walking on the ground when predation risk is low.

Effectiveness of Panama as an intercontinental land bridge for large mammals.

Habitat fragmentation is a primary driver of wildlife loss, and establishment of biological corridors is a common strategy to mitigate this problem. A flagship example is the Mesoamerican Biological Corridor (MBC), which aims to connect protected forest areas between Mexico and Panama to allow dispersal and gene flow of forest organisms. Because forests across Central America have continued to degrade, the functioning of the MBC has been questioned, but reliable estimates of species occurrence were unavailable. Large mammals are suitable indicators of forest functioning, so we assessed their conservation status across the Isthmus of Panama, the narrowest section of the MBC. We used large-scale camera-trap surveys and hierarchical multispecies occupancy models in a Bayesian framework to estimate the occupancy of 9 medium to large mammals and developed an occupancy-weighted connectivity metric to evaluate species-specific functional connectivity. White-lipped peccary (Tayassu pecari), jaguar (Panthera onca), giant anteater (Myrmecophaga tridactyla), white-tailed deer (Odocoileus virginianus), and tapir (Tapirus bairdii) had low expected occupancy along the MBC in Panama. Puma (Puma concolor), red brocket deer (Mazama temama), ocelot (Leopardus pardalis), and collared peccary (Pecari tajacu), which are more adaptable, had higher occupancy, even in areas with low forest cover near infrastructure. However, the majority of species were subject to ≥1 gap that was larger than their known dispersal distances, suggesting poor connectivity along the MBC in Panama. Based on our results, forests in Darien, Donoso-Santa Fe, and La Amistad International Park are critical for survival of large terrestrial mammals in Panama and 2 areas need restoration.

Efectividad de Panamá como un Puente Terrestre Intercontinental para Mamíferos Mayores Resumen La fragmentación del hábitat es un causante primario de la pérdida de biodiversidad, y el establecimiento de corredores biológicos es una estrategia común para mitigar este problema. El Corredor Biológico Mesoamericano (CBM) es un ejemplo notable que pretende conectar áreas boscosas protegidas entre México y Panamá para permitir la dispersión y flujo genético de organismos del bosque. El funcionamiento del CBM se ha cuestionado debido a que la degradación de los bosques en Centroamérica continúa, pero no se dispone de estimaciones confiables de la ocurrencia de especies. Los mamíferos grandes son indicadores adecuados del funcionamiento de los bosques tropicales Por lo tanto evaluamos su estado de conservación en el Istmo de Panamá, la sección más angosta del CBM. Utilizamos muestreos con cámaras trampa y modelos de ocupación para múltiples especies bajo un modelo Bayesiano para estimar la ocupación de 9 especies de mamíferos medianos a grandes, y desarrollamos una métrica de conectividad ponderada por la ocupación para evaluar la conectividad funcional para cada especie. El puerco de monte (Tayassu pecari), jaguar (Panthera onca), hormiguero gigante (Myrmecophaga tridactyla), venado cola blanca (Oidocoileus virginianus), y tapir (Tapirus bairdii) presentaron una ocupación baja en el CBM en Panamá. El puma (Puma concolor), venado corzo (Mazama temama), ocelote (Leopardus pardalis) y el saino (Pecari tajacu), que son más adaptables, presentaron mayor ocupación, aún en áreas con poca cobertura boscosa, cercanas a infraestructura. Sin embargo, la mayoría de las especies estuvo sujeta a ≥ 1 vacío que era mayor que sus distancias de dispersión conocidas, lo que sugiere una conectividad pobre a lo largo del CBM en Panamá. Basados en nuestros resultados, los bosques de Darién, Donoso-Santa Fé y el Parque Internacional La Amistad son críticos para la supervivencia de mamíferos terrestres grandes en Panamá mientras que 2 áreas requieren restauración.

Prey availability and temporal partitioning modulate felid coexistence in Neotropical forests.

Carnivores have long been used as model organisms to examine mechanisms that allow coexistence among ecologically similar species. Interactions between carnivores, including competition and predation, comprise important processes regulating local community structure and diversity. We use data from an intensive camera-trapping monitoring program across eight Neotropical forest sites to describe the patterns of spatiotemporal organization of a guild of five sympatric cat species: jaguar (Panthera onca), puma (Puma concolor), ocelot (Leopardus pardalis), jaguarundi (Herpailurus yagouaroundi) and margay (Leopardus wiedii). For the three largest cat species, we developed multi-stage occupancy models accounting for habitat characteristics (landscape complexity and prey availability) and models accounting for species interactions (occupancy estimates of potential competitor cat species). Patterns of habitat-use were best explained by prey availability, rather than habitat structure or species interactions, with no evidence of negative associations of jaguar on puma and ocelot occupancy or puma on ocelot occupancy. We further explore temporal activity patterns and overlap of all five felid species. We observed a moderate temporal overlap between jaguar, puma and ocelot, with differences in their activity peaks, whereas higher temporal partitioning was observed between jaguarundi and both ocelot and margay. Lastly, we conducted temporal overlap analysis and calculated species activity levels across study sites to explore if shifts in daily activity within species can be explained by varying levels of local competition pressure. Activity patterns of ocelots, jaguarundis and margays were similarly bimodal across sites, but pumas exhibited irregular activity patterns, most likely as a response to jaguar activity. Activity levels were similar among sites and observed differences were unrelated to competition or intraguild killing risk. Our study reveals apparent spatial and temporal partitioning for most of the species pairs analyzed, with prey abundance being more important than species interactions in governing the local occurrence and spatial distribution of Neotropical forest felids.

Local host-tick coextinction in neotropical forest fragments.

Ticks are obligatory parasites with complex life cycles that often depend on larger bodied vertebrates as final hosts. These traits make them particularly sensitive to local coextinction with their host. Loss of wildlife abundance and diversity should thus lead to loss of tick abundance and diversity to the point where only generalist tick species remain. However, direct empirical tests of these hypotheses are lacking, despite their relevance to our understanding of tick-borne disease emergence in disturbed environments. Here, we compare vertebrate and tick communities across 12 forest islands and peninsulas in the Panama Canal that ranged 1000-fold in size (2.6-2811.3 ha). We used drag sampling and camera trapping to directly assess the abundance and diversity of communities of questing ticks and vertebrate hosts. We found that the abundance and species richness of ticks were positively related to those of wildlife. Specialist tick species were only present in fragments where their final hosts were found. Further, less diverse tick communities had a higher relative abundance of the generalist tick species Amblyomma oblongoguttatum, a potential vector of spotted fever group rickettsiosis. These findings support the host-parasite coextinction hypothesis, and indicate that loss of wildlife can indeed have cascading effects on tick communities. Our results also imply that opportunities for pathogen transmission via generalist ticks may be higher in habitats with degraded tick communities. If these patterns are general, then tick identities and abundances serve as useful bioindicators of ecosystem health, with low tick diversity reflecting low wildlife diversity and a potentially elevated risk of interspecific disease transmission via remaining host species and generalist ticks.

Carrion fly-derived DNA metabarcoding is an effective tool for mammal surveys: Evidence from a known tropical mammal community.

Metabarcoding of vertebrate DNA derived from carrion flies has been proposed as a promising tool for biodiversity monitoring. To evaluate its efficacy, we conducted metabarcoding surveys of carrion flies on Barro Colorado Island (BCI), Panama, which has a well-known mammal community, and compared our results against diurnal transect counts and camera trapping. We collected 1,084 flies in 29 sampling days, conducted metabarcoding with mammal-specific (16S) and vertebrate-specific (12S) primers, and sequenced amplicons on Illumina MiSeq. For taxonomic assignment, we compared blast with the new program protax, and we found that protax improved species identifications. We detected 20 mammal, four bird, and one lizard species from carrion fly metabarcoding, all but one of which are known from BCI. Fly metabarcoding detected more mammal species than concurrent transect counts (29 sampling days, 13 species) and concurrent camera trapping (84 sampling days, 17 species), and detected 67% of the number of mammal species documented by 8 years of transect counts and camera trapping combined, although fly metabarcoding missed several abundant species. This study demonstrates that carrion fly metabarcoding is a powerful tool for mammal biodiversity surveys and has the potential to detect a broader range of species than more commonly used methods.

Cascading effects of defaunation on the coexistence of two specialized insect seed predators.

Identification of the mechanisms enabling stable coexistence of species with similar resource requirements is a central challenge in ecology. Such coexistence can be facilitated by species at higher trophic levels through complex multi-trophic interactions, a mechanism that could be compromised by ongoing defaunation. We investigated cascading effects of defaunation on Pachymerus cardo and Speciomerus giganteus, the specialized insect seed predators of the Neotropical palm Attalea butyracea, testing the hypothesis that vertebrate frugivores and granivores facilitate their coexistence. Laboratory experiments showed that the two seed parasitoid species differed strongly in their reproductive ecology. Pachymerus produced many small eggs that it deposited exclusively on the fruit exocarp (exterior). Speciomerus produced few large eggs that it deposited exclusively on the endocarp, which is normally exposed only after a vertebrate handles the fruit. When eggs of the two species were deposited on the same fruit, Pachymerus triumphed only when it had a long head start, and the loser always succumbed to intraguild predation. We collected field data on the fates of 6569 Attalea seeds across sites in central Panama with contrasting degrees of defaunation and wide variation in the abundance of vertebrate frugivores and granivores. Speciomerus dominated where vertebrate communities were intact, whereas Pachymerus dominated in defaunated sites. Variation in the relative abundance of Speciomerus across all 84 sampling sites was strongly positively related to the proportion of seeds attacked by rodents, an indicator of local vertebrate abundance. SYNTHESIS: We show that two species of insect seed predators relying on the same host plant species are niche differentiated in their reproductive strategies such that one species has the advantage when fruits are handled promptly by vertebrates and the other when they are not. Defaunation disrupts this mediating influence of vertebrates and strongly favours one species at the expense of the other, providing a case study of the cascading effects of defaunation and its potential to disrupt coexistence of non-target species, including the hyperdiverse phytophagous insects of tropical forests.

Interspecific associations in seed arrival and seedling recruitment in a Neotropical forest.

Contagious seed dispersal refers to the tendency for some sites to receive many dispersed seeds while other sites receive few dispersed seeds. Contagious dispersal can lead to interspecific associations in seed arrival, and this in turn might lead to interspecific associations in seedling recruitment. We evaluate the extent of spatially contagious seed arrival, the frequency of positive interspecific associations in seed arrival, and their consequences for seedling recruitment at the community level in a tropical moist forest. We quantified seed arrival to 200 passive seed traps for 28 yr of weekly censuses and seedling recruitment to 600 1-m2 quadrats for 21 yr of annual censuses on Barro Colorado Island, Panama. We assessed whether spatially contagious seed dispersal was more important among zoochorous species than among anemochorous species, increased in importance with similarity in fruiting times, and led to interspecific associations in seed arrival and seedling recruitment. We controlled adult seed source associations statistically to evaluate predicted relationships. We found that spatially contagious seed arrival was widespread among zoochorous species, but also occurred among anemochorous species when the strong, consistent trade winds were present. Significant interspecific associations in seed arrival were more likely for pairs of species with zoochorous seeds and similar fruiting times and persisted through seedling recruitment. Thus, interspecifically contagious seed dispersal affects local species composition and alters the mixture of interspecific interactions through the seed, germination, and early seedling stages in this forest. Future investigations should consider the implications of interspecific association at the regeneration stages documented here for later life stages and species coexistence.

Host body size and the diversity of tick assemblages on Neotropical vertebrates.

Identifying the factors that influence the species diversity and distribution of ticks (Acari: Ixodida) across vertebrate host taxa is of fundamental ecological and medical importance. Host body size is considered one of the most important determinants of tick abundance, with larger hosts having higher tick burdens. The species diversity of tick assemblages should also be greater on larger-bodied host species, but empirical studies testing this hypothesis are lacking. Here, we evaluate this relationship using a comparative dataset of feeding associations from Panama between 45 tick species and 171 host species that range in body size by three orders of magnitude. We found that tick species diversity increased with host body size for adult ticks but not for immature ticks. We also found that closely related host species tended to have similar tick species diversity, but correcting for host phylogeny did not alter the relationships between host body size and tick species diversity. The distribution of tick species was highly aggregated, with approximately 20% of the host species harboring 80% of all tick species, following the Pareto principle or 20/80 Rule. Thus, the aggregated pattern commonly observed for tick burdens and disease transmission also holds for patterns of tick species richness. Our finding that the adult ticks in this system preferentially parasitize large-bodied host species suggests that the ongoing anthropogenic loss of large-bodied vertebrates is likely to result in host-tick coextinction events, even when immature stages feed opportunistically. As parasites play critical roles in ecological and evolutionary processes, such losses may profoundly affect ecosystem functioning and services.

Host specificity in a diverse Neotropical tick community: an assessment using quantitative network analysis and host phylogeny.

BACKGROUND: Host specificity is a fundamental determinant of tick population and pathogen transmission dynamics, and therefore has important implications for human health. Tick host specificity is expected to be particularly high in the tropics, where communities of ticks, hosts and pathogens are most diverse. Yet the degree to which tropical tick species are host-specific remains poorly understood. Combining new field data with published records, we assessed the specificity of tick-host associations in Panama, a diverse Neotropical region. METHODS: The resulting dataset includes 5,298 adult ticks belonging to 41 species of eight genera that were directly collected from 68 vertebrate host species of 17 orders. We considered three important aspects of tick host specificity: (i) the relative ecological importance of each host species (structural specificity); (ii) relatedness among host species (phylogenetic specificity); and (iii) spatial scale-dependence of tick-host relationships (geographical specificity). Applying quantitative network analyses and phylogenetic tools with null model comparisons, we assessed the structural and phylogenetic specificity across three spatial scales, ranging from central Panama to countrywide. Further, we tested whether species-rich tick genera parasitized a wider variety of hosts than species-poor genera, as expected when ticks specialize on different host species. RESULTS: Most tick species showed high structural and/or phylogenetic specificity in the adult stage. However, after correcting for sampling effort, we found little support for geographical specificity. Across the three scales, adult ticks tended to be specific to a limited number of host species that were phylogenetically closely related. These host species in turn, were parasitized by tick species from distinct genera, suggesting switching among distantly related hosts is common at evolutionary timescales. Further, there was a strong positive relationship between the taxonomic richness of the tick genera and that of their hosts, consistent with distinct tick species being relatively specific to different host species. CONCLUSIONS: Our results indicate that in the adult stage, most ticks in the diverse Neotropical community studied are host specialists. This contrasts with earlier assessments, but agrees with findings from other host-parasite systems. High host specificity in adult ticks implies high susceptibility to local tick-host co-extirpation, limited ability to colonize new habitats and limited potential for interspecific pathogen transmission.

Indirect interactions among tropical tree species through shared rodent seed predators: a novel mechanism of tree species coexistence.

The coexistence of numerous tree species in tropical forests is commonly explained by negative dependence of recruitment on the conspecific seed and tree density due to specialist natural enemies that attack seeds and seedlings ('Janzen-Connell' effects). Less known is whether guilds of shared seed predators can induce a negative dependence of recruitment on the density of different species of the same plant functional group. We studied 54 plots in tropical forest on Barro Colorado Island, Panama, with contrasting mature tree densities of three coexisting large seeded tree species with shared seed predators. Levels of seed predation were far better explained by incorporating seed densities of all three focal species than by conspecific seed density alone. Both positive and negative density dependencies were observed for different species combinations. Thus, indirect interactions via shared seed predators can either promote or reduce the coexistence of different plant functional groups in tropical forest.

Negative density dependence of seed dispersal and seedling recruitment in a neotropical palm.

Negative density dependence (NDD) of recruitment is pervasive in tropical tree species. We tested the hypotheses that seed dispersal is NDD, due to intraspecific competition for dispersers, and that this contributes to NDD of recruitment. We compared dispersal in the palm Attalea butyracea across a wide range of population density on Barro Colorado Island in Panama and assessed its consequences for seed distributions. We found that frugivore visitation, seed removal and dispersal distance all declined with population density of A. butyracea, demonstrating NDD of seed dispersal due to competition for dispersers. Furthermore, as population density increased, the distances of seeds from the nearest adult decreased, conspecific seed crowding increased and seedling recruitment success decreased, all patterns expected under poorer dispersal. Unexpectedly, however, our analyses showed that NDD of dispersal did not contribute substantially to these changes in the quality of the seed distribution; patterns with population density were dominated by effects due solely to increasing adult and seed density.

Viability of small seeds found in feces of the Central American tapir on Barro Colorado Island, Panama.

Tapirs are known as effective dispersers of large-seeded tree species, but their role in dispersing small-seeded plant species has yet to be established. Tapir feces have been reported to contain large numbers of small seeds, but whether these are viable has rarely been evaluated. We determined the abundance and viability of small seeds in feces of Central American tapir (Tapirus bairdii) on Barro Colorado Island, Panama. A total of 72 fecal samples were collected opportunistically from 4 tapir latrine sites. Seeds were manually extracted from feces and classified by size. Seed viability was estimated by opening each seed and examining for the presence of at least 1 intact firm white endosperm. In total, we obtained 8166 seeds of at least 16 plant species. Small-seeded species dominated, with 96% of all seeds found measuring <5 mm. The canopy tree Laetia procera was the most abundant species in the samples. Of all small seeds found, 69% contained an intact endosperm and appeared viable. This suggests that small seeds, like large seeds, often pass through the digestive tract of T. bairdii intact. Thus, tapirs potentially serve as effective dispersers of a wide range of small-seeded plant species.

Amblyomma tapirellum (Acari: Ixodidae) collected from tropical forest canopy.

Free-ranging ticks are widely known to be restricted to the ground level of vegetation. Here, we document the capture of the tick species Amblyomma tapirellum in light traps placed in the forest canopy of Barro Colorado Island, central Panama. A total of forty eight adults and three nymphs were removed from carbon dioxide-octenol baited CDC light traps suspended 20 meters above the ground during surveys for forest canopy mosquitoes. To our knowledge, this represents the first report of questing ticks from the canopy of tropical forests. Our finding suggests a novel ecological relationship between A. tapirellum and arboreal mammals, perhaps monkeys that come to the ground to drink or to feed on fallen fruits.

Directed seed dispersal towards areas with low conspecific tree density by a scatter-hoarding rodent.

Scatter-hoarding animals spread out cached seeds to reduce density-dependent theft of their food reserves. This behaviour could lead to directed dispersal into areas with lower densities of conspecific trees, where seed and seedling survival are higher, and could profoundly affect the spatial structure of plant communities. We tested this hypothesis with Central American agoutis and Astrocaryum standleyanum palm seeds on Barro Colorado Island, Panama. We radio-tracked seeds as they were cached and re-cached by agoutis, calculated the density of adult Astrocaryum trees surrounding each cache, and tested whether the observed number of trees around seed caches declined more than expected under random dispersal. Seedling establishment success was negatively dependent on seed density, and agoutis carried seeds towards locations with lower conspecific tree densities, thus facilitating the escape of seeds from natural enemies. This behaviour may be a widespread mechanism leading to highly effective seed dispersal by scatter-hoarding animals.

Thieving rodents as substitute dispersers of megafaunal seeds.

The Neotropics have many plant species that seem to be adapted for seed dispersal by megafauna that went extinct in the late Pleistocene. Given the crucial importance of seed dispersal for plant persistence, it remains a mystery how these plants have survived more than 10,000 y without their mutualist dispersers. Here we present support for the hypothesis that secondary seed dispersal by scatter-hoarding rodents has facilitated the persistence of these large-seeded species. We used miniature radio transmitters to track the dispersal of reputedly megafaunal seeds by Central American agoutis, which scatter-hoard seeds in shallow caches in the soil throughout the forest. We found that seeds were initially cached at mostly short distances and then quickly dug up again. However, rather than eating the recovered seeds, agoutis continued to move and recache the seeds, up to 36 times. Agoutis dispersed an estimated 35% of seeds for >100 m. An estimated 14% of the cached seeds survived to the next year, when a new fruit crop became available to the rodents. Serial video-monitoring of cached seeds revealed that the stepwise dispersal was caused by agoutis repeatedly stealing and recaching each other's buried seeds. Although previous studies suggest that rodents are poor dispersers, we demonstrate that communities of rodents can in fact provide highly effective long-distance seed dispersal. Our findings suggest that thieving scatter-hoarding rodents could substitute for extinct megafaunal seed dispersers of tropical large-seeded trees.

Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm.

Natural enemies, especially host-specific enemies, are hypothesised to facilitate the coexistence of plant species by disproportionately inflicting more damage at increasing host abundance. However, few studies have assessed such Janzen-Connell mechanisms on a scale relevant for coexistence and no study has evaluated potential top-down influences on the specialized pests. We quantified seed predation by specialist invertebrates and generalist vertebrates, as well as larval predation on these invertebrates, for the Neotropical palm Attalea butyracea across ten 4-ha plots spanning 20-fold variation in palm density. As palm density increased, seed attack by bruchid beetles increased, whereas seed predation by rodents held constant. But because rodent predation on bruchid larvae increased disproportionately with increasing palm density, bruchid emergence rates and total seed predation by rodents and bruchids combined were both density-independent. Our results demonstrate that top-down effects can limit the potential of host-specific insects to induce negative-density dependence in plant populations.