SciCombinator

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Concept: Seed dispersal

174

Human-mediated dispersal is known as an important driver of long-distance dispersal for plants but underlying mechanisms have rarely been assessed. Road corridors function as routes of secondary dispersal for many plant species but the extent to which vehicles support this process remains unclear. In this paper we quantify dispersal distances and seed deposition of plant species moved over the ground by the slipstream of passing cars. We exposed marked seeds of four species on a section of road and drove a car along the road at a speed of 48 km/h. By tracking seeds we quantified movement parallel as well as lateral to the road, resulting dispersal kernels, and the effect of repeated vehicle passes. Median distances travelled by seeds along the road were about eight meters for species with wind dispersal morphologies and one meter for species without such adaptations. Airflow created by the car lifted seeds and resulted in longitudinal dispersal. Single seeds reached our maximum measuring distance of 45 m and for some species exceeded distances under primary dispersal. Mathematical models were fit to dispersal kernels. The incremental effect of passing vehicles on longitudinal dispersal decreased with increasing number of passes as seeds accumulated at road verges. We conclude that dispersal by vehicle airflow facilitates seed movement along roads and accumulation of seeds in roadside habitats. Dispersal by vehicle airflow can aid the spread of plant species and thus has wide implications for roadside ecology, invasion biology and nature conservation.

Concepts: Plant, Transport, Seed, Walking, Vehicle, Automobile, The Road, Seed dispersal

71

Invasive vertebrate predators are directly responsible for the extinction or decline of many vertebrate species, but their indirect impacts often go unmeasured, potentially leading to an underestimation of their full impact. When invasives extirpate functionally important mutualists, dependent species are likely to be affected as well. Here, we show that the invasive brown treesnake, directly responsible for the extirpation of forest birds from the island of Guam, is also indirectly responsible for a severe decline in plant recruitment as a result of disrupting the fruit-frugivore mutualism. To assess the impact of frugivore loss on plants, we compare seed dispersal and recruitment of two fleshy-fruited tree species on Guam and three nearby islands with intact disperser communities. We conservatively estimate that the loss of frugivorous birds caused by the brown treesnake may have caused a 61-92% decline in seedling recruitment. This case study highlights the potential for predator invasions to cause indirect, pervasive and easily overlooked interaction cascades.

Concepts: Plant, Symbiosis, Vertebrate, Plant morphology, Extinction, Invasive species, Mutualism, Seed dispersal

29

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.

Concepts: Metabolism, Africa, Nitrogen, Primate, New World, Lemur, Ring-tailed Lemur, Seed dispersal

17

The seeds of most heterotrophic plants, commonly referred to as dust seeds, are typically dispersed in the air like dust particles. Therefore, little attention has been paid to how seeds of heterotrophic plants are dispersed, owing to the notion that wind dispersal is the dominant strategy. However, inconspicuous but fleshy, indehiscent fruit can be observed in distantly related plants that have independently evolved full heterotrophy. Here I investigated the seed dispersal system in three unrelated fully heterotrophic plants with fleshy, indehiscent fruits (Yoania amagiensis, Monotropastrum humile and Phacellanthus tubiflorus) by direct observation, a differential exclusion experiment of fruit feeders and investigation on seed viability through the digestive tract. The present study revealed that camel crickets are the major seed disperser in three achlorophyllous plants in the study population. This represents the first evidence of seed dispersal by camel crickets in any angiosperm species. These heterotrophic plants grow in the understorey of densely vegetated forests where wind is probably an ineffective seed dispersal agent. Life-history traits of the achlorophyllous plants associated with heterotrophic lifestyles, such as colonization of dark understorey habitats and dust seeds, could facilitate independent recruitment of the novel endozoochorous seed dispersal system by camel crickets.

Concepts: Plant, Fruit, Seed, Legume, Plant morphology, Biological dispersal, Nut, Seed dispersal

15

Anthropogenic activity is driving population declines and extinctions of large-bodied, fruit-eating animals worldwide. Loss of these frugivores is expected to trigger negative cascading effects on plant populations if remnant species fail to replace the seed dispersal services provided by the extinct frugivores. A collapse of seed dispersal may not only affect plant demography (i.e., lack of recruitment), but should also supress gene flow via seed dispersal. Yet little empirical data still exist demonstrating the genetic consequences of defaunation for animal-dispersed plant species. Here, we first document a significant reduction of seed dispersal distances along a gradient of human-driven defaunation, with increasing loss of large- and medium-bodied frugivores. We then show that local plant neighbourhoods have higher genetic similarity, and smaller effective population sizes when large seed dispersers become extinct (i.e., only small frugivores remain) or are even partially downgraded (i.e., medium-sized frugivores providing less efficient seed dispersal). Our results demonstrate that preservation of large frugivores is crucial to maintain functional seed dispersal services and their associated genetic imprints, a central conservation target. Early signals of reduced dispersal distances that accompany the Anthropogenic defaunation forecast multiple, cascading effects on plant populations.

Concepts: Evolution, Biology, Plant, Demography, Population, Extinction, Biological dispersal, Seed dispersal

14

Many large species have declined worldwide due to habitat fragmentation and poaching. The defaunation of large frugivores and the consequent reductions of seed dispersal services may have immediate effects on plant demography. Yet, the lasting effects of frugivore defaunation on microevolutionary processes of the plants they disperse remain understudied. We tested if the loss of large seed dispersers can lead to microevolutionary changes of a tropical palm. We show that frugivore defaunation is the main driver of changes in allelic frequency among populations. Turnover of alleles accounted for 100% of dissimilarity in allelic frequencies of individuals between defaunated and non-defaunated forests; and individuals from defaunated sites are 1.5 times more similar genetically than those found in pristine sites. Given that sizeable fractions of the palm fruit crops remain undispersed in defaunated sites due to lack of large-bodied frugivores, this distinct pattern of gene pool composition of early recruits may reveal strong dispersal limitation for specific genotypes, or collapses of gene flow between fragmented areas, or both. Because most of tropical tree species rely on seed dispersal by vertebrates, our results show that defaunation has a lasting effect on microevolutionary processes, with potential consequences for persistence under scenarios of environmental change.

Concepts: Gene, Genetics, Genotype, Allele, Evolution, Species, Plant, Seed dispersal

13

Seed ingestion by frugivorous vertebrates commonly benefits plants by moving seeds to locations with fewer predators and pathogens than under the parent. For plants with high local population densities, however, movement from the parent plant is unlikely to result in ‘escape’ from predators and pathogens. Changes to seed condition caused by gut passage may also provide benefits, yet are rarely evaluated as an alternative. Here, we use a common bird-dispersed chilli pepper (Capsicum chacoense) to conduct the first experimental comparison of escape-related benefits to condition-related benefits of animal-mediated seed dispersal. Within chilli populations, seeds dispersed far from parent plants gained no advantage from escape alone, but seed consumption by birds increased seed survival by 370% - regardless of dispersal distance - due to removal during gut passage of fungal pathogens and chemical attractants to granivores. These results call into question the pre-eminence of escape as the primary advantage of dispersal within populations and document two overlooked mechanisms by which frugivores can benefit fruiting plants.

Concepts: Plant, Population, Population density, Fruit, Seed, Plant morphology, Capsicum, Seed dispersal

5

The extinction of large frugivores has consequences for the recruitment of large-seeded plants with potential lasting effects on carbon storage in tropical rainforests. However, previous studies relating frugivore defaunation to changes in carbon storage ignore potential compensation by redundant frugivores and the effects of seed predators on plant recruitment. Based on empirical data of the recruitment success of a large-seeded hardwood tree species (Cryptocarya mandioccana, Lauraceae) across a defaunation gradient of seed dispersers and predators, we show that defaunation increases both seed dispersal limitation and seed predation. Depending on the level of seed predator loss, plant recruitment is reduced by 70.7-94.9% as a result of the loss of seed dispersers. The loss of large seed predators increases the net seed mortality by 7-30% due to the increased abundance of small granivorous rodents. The loss of large seed dispersers can be buffered by the compensatory effects of smaller frugivores in seed removal, but it is not sufficient to prevent a decrease in plant recruitment. We show that the conservation of both seed predators and dispersers is necessary for the recruitment of large-seeded plants. Since these plants contribute substantially to carbon stocks, defaunation can jeopardize the maintenance of tropical forest carbon storage.

Concepts: Plant, Ecology, Tree, Fruit, Plant reproduction, Seed predation, Seed dispersal, Frugivore

3

Species interactions, both mutualistic and antagonistic, are widely recognized as providing important ecosystem services. Fruit-eating animals influence plant recruitment by increasing germination during gut passage and moving seeds away from conspecifics. However, relative to studies focused on the importance of frugivores for plant population maintenance, few studies target frugivores as ecosystem service providers, and frugivores are underappreciated as ecosystem service providers relative to other mutualists such as pollinators. Here we use an accidental experiment to elucidate the role of seed dispersal by frugivores for maintaining a culturally and economically important plant, the donne' sali chili (Capsicum frutescens) in the Mariana Islands. One of the islands (Guam) has lost nearly all of its native forest birds due to an invasive snake (Boiga irregularis), whereas nearby islands have relatively intact bird populations. We hypothesized that frugivore loss would influence chili recruitment and abundance, which could have economic and cultural impacts. By using video cameras, we confirmed that birds were the primary seed dispersers. We used captive bird feeding trials to obtain gut-passed seeds to use in a seedling emergence experiment. The experiment showed that gut-passed seeds emerged sooner and at a higher proportion than seeds from whole fruits. Consistent with our findings that birds benefit chilies, we observed lower chili abundance on Guam than on islands with birds. In a survey questionnaire of island residents, the majority of residents reported an association between the wild chili and local cultural values and traditions. In addition, we identified a thriving market for chili products, suggesting benefits of wild chilies to people in the Marianas both as consumers and producers. Our study therefore documents seed dispersal as both a cultural and a supporting ecosystem service. We provide a comprehensive case study on how seed-dispersed plants decline in the absence of their disperser, and how to apply mixed-methods in ecosystem service assessments. Furthermore, we suggest that scientists and resource managers may utilize fruit-frugivore mutualisms concerning socially valuable plants to gather support for frugivore and forest conservation efforts. This article is protected by copyright. All rights reserved.

Concepts: Plant, Ecology, Fruit, Seed, Plant morphology, Mariana Islands, Guam, Seed dispersal

3

Plant secondary metabolites (SMs) acting as defensive chemicals in reproductive organs such as fruit tissues play roles in both mutualistic and antagonistic interactions between plants and seed dispersers/predators. The directed-deterrence hypothesis states that SMs in ripe fruits deter seed predators but have little or no effect on seed dispersers. Indeed, studies have demonstrated that birds are able to cope with fruit SMs whereas rodents are deterred by them. However, this mechanism was only demonstrated at the class level, i.e., between birds and mammals, based on differences in the vanilloid receptors. Here we present experimental and behavioral data demonstrating the use of the broad-range, class-independent “mustard oil bomb” mechanism in Ochradenus baccatus fruits to force a behavioral change at an ecological timescale, converting rodents from seed predators to seed dispersers. This is achieved by a unique compartmentalization of the mustard oil bomb, causing activation of the system only upon seed and pulp coconsumption, encouraging seed dispersal via seed spitting by rodents. Our findings demonstrate the power of SMs to shift the animal-plant relationship from predation to mutualism and provide support for the directed-deterrence hypothesis at the intraspecific level, in addition to the interspecific level.

Concepts: Plant, Predation, Symbiosis, Fruit, Seed, Plant morphology, Nut, Seed dispersal