Spatial variation in post-dispersal seed removal in an Atlantic forest: Effects of habitat, location and guilds of seed predators

Studies of post-dispersal seed removal in the Neotropics have rarely examined the magnitude of seed removal by different types of granivores. The relative impact of invertebrates, small rodents, and birds on seed removal was investigated in a 2,178 ha Atlantic forest fragment in southeastern Brazil. We used popcorn kernels (Zea mays-Poaceae) to investigate seed removal in a series of selective exclosure treatments in a replicated, paired design experiment that included forest understory, gaps, and forest edge sites. We recorded the vegetation around the experimental seed stations in detail in order to evaluate the influence of microhabitat traits on seed removal. Vertebrate granivores (rodents and birds) were surveyed to determine whether granivore abundance was correlated with seed removal levels. Seed removal varied spatially and in unpredictable ways at the study site. Seed encounter and seed use varied with treatments, but not with habitat type. However, seed removal by invertebrates was negatively correlated with gap-related traits, which suggested an avoidance of large gaps by granivorous ants. The abundance of small mammals was remarkably low, but granivorous birds (tinamous and doves) were abundant at the study site. Birds were the main seed consumers in open treatments, but there was no correlation between local granivorous bird abundance and seed removal. These results emphasize the stochastic spatial pattern of seed removal, and, contrary to previous studies, highlight the importance of birds as seed predators in forest habitats. (c) 2007 Elsevier Masson SAS. All rights reserved.

Granivorous birds as potentially important post-dispersal seed predators in a Brazilian forest fragment

In tropical forests, rodents exert a prominent role as post-dispersal seed predators, while other vertebrates apparently have a minor effect on seed predation. In some forest fragments in southeast Brazil, however, the density of rodents is unusually low, whereas terrestrial granivorous birds are abundant. In this study, we used seeds of a second-growth tree (Croton priscus, Euphorbiaceae) to investigate experimentally the relative importance of rodents and birds as seed predators in a forest fragment. We also estimated the density of terrestrial granivorous birds and trapped small mammals. Results indicate that, as a consequence of decreased rodent population and increased bird abundance, the latter are at least as important as the former as the main post-dispersal seed predators of C priscus. We interpret such apparent imbalance in the interaction between C priscus and their seed predators as a possible consequence of forest fragmentation.

Seed size variation in the palm Euterpe edulis and the effects of seed predators on germination and seedling survival

Intraspecific variation in seed size is common in wild plant populations and has important consequences for the reproductive success of individual plants. Multiple, often conflicting evolutionary forces mediated by biotic as well as abiotic agents may maintain such a variation. In this paper we assessed seed size variation in a population of the threatened, commercially important palm Euterpe edulis in southeast Brazil. We investigated (i) how this variation affects the probability of attack by vertebrate and invertebrate post-dispersal seed predators, and (ii) if seed size influences the outcome of seeds damaged by beetles in terms of seed germination and early survival of seedlings. Euterpe edulis seeds varied in diameter from 8.3 to 14.1 mm. Neither insects nor rodents selected the seeds they preyed upon based on seed size. Seed germination and total, shoot and root biomasses of one-year seedlings were significantly and positively affected by seed size. Root biomass and seedling survival were negatively affected by seed damage caused by a scolytid beetle (Coccotrypes palmarum) whose adults bore into seeds to consume part of the endosperm, but do not oviposit on them. Seed size had a marginally significant effect on seedling survival. Therefore, if any advantage is accrued by E. edulis individuals producing large seeds, this is because of greater seed germination success and seedling vigor. If this is so, even a relatively narrow range of variation in seed size as observed in the E. edulis population studied may translate into differential success of individual plants. (c) 2006 Elsevier SAS. All rights reserved.

Effects of frugivore impoverishment and seed predators on the recruitment of a keystone palm

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

Post dispersal weed seed predation by avian and non-avian predators

Seed predation by avian and non-avian predators was quantified in the boundaries and cropped areas of cereal fields by presenting known quantities of seed with and without exclusion cages. Predator encounter-rates with the dishes exceeded 99%. Birds removed on average 6.7% seed from the dishes during the seven-day trials compared to 51% by non-avian predators. A comparison was made of the causal factors responsible for predation of Avena fatua, Chenopodium album and Cirsium arvense seeds. A. fatua seeds were preyed most heavily by both avian and non-avian predators. Seed removal by birds was greater in the cropped area than in the field boundary, non-avian predators being generally more active in the field boundary. Seed predation by birds was greater in spring than in any other season, whilst losses to other animals were greater during autumn and winter. Although, birds were not the main seed predators in cereal fields, they may contribute to weed seed depletion, of relevance to reduced-input farming systems where herbicides use is restricted.

Effect of rodents on seed fate of five hornbill-dispersed tree species in a tropical forest in north-east India

Hornbills are important dispersers of a wide range of tree species. Many of these species bear fruits with large, lipid-rich seeds that could attract terrestrial rodents. Rodents have multiple effects on seed fates, many of which remain poorly understood in the Palaeotropics. The role of terrestrial rodents was investigated by tracking seed fate of five horn bill-dispersed tree species in a tropical forest in north-cast India. Seeds were marked inside and outside of exclosures below 6-12 parent fruiting trees (undispersed seed rain) and six hornbill nest trees (a post-dispersal site). Rodent visitors and seed removal ere monitored using camera traps. Our findings suggest that several rodent species. especially two species of porcupine were major on-site seed predators. Scatter-hoarding was rare (1.4%). Seeds at hornbill nest trees had lower survival compared with parent fruiting trees, indicating that clumped dispersal by hornbills may not necessarily improve seed survival. Seed survival in the presence and absence of rodents varied with tree species. Some species (e.g. Polyalthia simiarum) showed no difference, others (e.g. Dysoxylum binectariferum) experienced up to a 64%. decrease in survival in the presence of rodents. The differing magnitude of seed predation by rodents can have significant consequences at the seed establishment stage.

Rodent seed predation: effects on seed survival, recruitment, abundance, and dispersion of bird-dispersed tropical trees

Tropical tree species vary widely in their pattern of spatial dispersion. We focus on how seed predation may modify seed deposition patterns and affect the abundance and dispersion of adult trees in a tropical forest in India. Using plots across a range of seed densities, we examined whether seed predation levels by terrestrial rodents varied across six large-seeded, bird-dispersed tree species. Since inter-specific variation in density-dependent seed mortality may have downstream effects on recruitment and adult tree stages, we determined recruitment patterns close to and away from parent trees, along with adult tree abundance and dispersion patterns. Four species (Canarium resiniferum, Dysoxylum binectariferum, Horsfieldia kingii, and Prunus ceylanica) showed high predation levels (78.5-98.7%) and increased mortality with increasing seed density, while two species, Chisocheton cumingianus and Polyalthia simiarum, showed significantly lower seed predation levels and weak density-dependent mortality. The latter two species also had the highest recruitment near parent trees, with most abundant and aggregated adults. The four species that had high seed mortality had low recruitment under parent trees, were rare, and had more spaced adult tree dispersion. Biotic dispersal may be vital for species that suffer density-dependent mortality factors under parent trees. In tropical forests where large vertebrate seed dispersers but not seed predators are hunted, differences in seed vulnerability to rodent seed predation and density-dependent mortality can affect forest structure and composition.

Fruit and Seed Volatiles: Multiple Stage Settings, Actors and Props in an Evolutionary Play

Plants emit volatile organic compounds (VOCs) from most parts of their anatomy. Conventionally, the volatiles of leaves, flowers, fruits and seeds have been investigated separately. This review presents an integrated perspective of volatiles produced by fruits and seeds in the context of selection on the whole plant. It suggests that fruit and seed volatiles may only be understood in the light of the chemistry of the whole plant. Fleshy fruit may be viewed as an ecological arena within which several evolutionary games are being played involving fruit VOCs. Fruit odour and colour may be correlated and interact via multimodal signalling in influencing visits by frugivores. The hypothesis of volatile crypsis in the evolution of hard seeds as protection against volatile diffusion and perception by seed predators is reviewed. Current views on the role of volatiles in ant dispersal of seeds or myrmecochory are summarised, especially the suggestion that ants are being manipulated by plants in the form of a sensory trap while providing this service. Plant VOC production is presented as an emergent phenotype that could result from multiple selection pressures acting on various plant parts; the ``plant'' phenotype and VOC profile may receive significant contributions from symbionts within the plant. Viewing the plant as a holobiont would benefit an understanding of the emergent plant phenotype.

Fruit Trait Preference in Rhesus Macaques (Macaca mulatta) and its Implications for Seed Dispersal

Primates constitute 25-40 % of the frugivore biomass of tropical forests. Primate fruit preference, as a determinant of seed dispersal, can therefore have a significant impact on these ecosystems. Although the traits of fruits included in primate diets have been described, fruit trait preference has been less studied with respect to fruit availability. We examined fruit trait preference and its implications for seed dispersal in the rhesus macaque (Macaca mulatta), a dietarily flexible species and important seed disperser, at the Buxa Tiger Reserve, India. Over a year, we monitored the phenology of selected trees in the study area, observed the feeding behavior of rhesus macaques using scans and focal animal sampling, and documented morphological traits of the fruits/seeds consumed. Using generalized linear modeling, we found that the kind of edible tissue was the chief determinant of fruit consumption, with M. mulatta feeding primarily on fruits with juicy-soft pulp and acting as seed predators for those with no discernible pulp. Overall, the preferred traits were external covers that could be easily pierced by a fingernail, medium to large seeds, true stone-like seeds, and juicy-soft edible tissue, thereby implying that fruit taxa with these traits had a higher probability of being dispersed. Macaques were more selective during the high fruit availability period than the low fruit availability period, preferentially feeding on soft-skinned fruits with juicy-soft pulp. We suggest that further studies be conducted across habitats and time to understand the consistency of interactions between primates and fruits with specific traits to determine the degree of selective pressure (if any) that is exerted by primates on fruit traits.

How much Dillenia indica seed predation occurs from Asian elephant dung?

Elephants are thought to be effective seed dispersers, but research on whether elephant dung effectively protects seeds from seed predation is lacking. Quantifying rates of seed predation from elephant dung will facilitate comparisons between elephants and alternative dispersers, helping us understand the functional role of megaherbivores in ecosystems. We conducted an experiment to quantify the predation of Dillenia indica seeds from elephant dung in Buxa Reserve, India from December 2012 to April 2013. Using dung boluses from the same dung pile, we compared the number of seeds in boluses that are a) opened immediately upon detection (control boluses), b) made available only to small seed predators (<= 3 mm wide) for 1-4 months, and c) made available to all seed predators and secondary dispersers for 1-4 months. Using a model built on this experiment, we estimated that seed predation by small seed predators (most likely ants and termites) destroys between 82.9% and 96.4% of seeds in elephant dung between the time of defecation and the median germination date for D. indica. Exposure to larger seed predators and secondary dispersers did not lead to a significant additional reduction in the number of seeds per dung bolus. Our findings suggest that post-dispersal seed predation by small insects (<3 mm) substantially reduces but does not eliminate the success of elephants as dispersers of D. indica in a tropical moist forest habitat. (C) 2015 Elsevier Masson SAS. All rights reserved.

Post-dispersal seed predation of non-target weeds in arable crops

Field experiments were conducted to quantify the natural levels of post-dispersal seed predation of arable weed species in spring barley and to identify the main groups of seed predators. Four arable weed species were investigated that were of high biodiversity value, yet of low to moderate competitive ability with the crop. These were Chenopodium album, Sinapis arvensis, Stellaria media and Polygonum aviculare. Exclusion treatments were used to allow selective access to dishes of seeds by different predator groups. Seed predation was highest early in the season, followed by a gradual decline in predation over the summer for all species. All species were taken by invertebrates. The activity of two phytophagous carabid genera showed significant correlations with seed predation levels. However, in general carabid activity was not related to seed predation and this is discussed in terms of the mainly polyphagous nature of many Carabid species that utilized the seed resource early in the season, but then switched to carnivory as prey populations increased. The potential relevance of post-dispersal seed predation to the development of weed management systems that maximize biological control through conservation and optimize herbicide use, is discussed.

Post-dispersal seed predation of non-target weeds in arable crops

Field experiments were conducted to quantify the natural levels of post-dispersal seed predation of arable weed species in spring barley and to identify the main groups of seed predators. Four arable weed species were investigated that were of high biodiversity value, yet of low to moderate competitive ability with the crop. These were Chenopodium album, Sinapis arvensis, Stellaria media and Polygonum aviculare. Exclusion treatments were used to allow selective access to dishes of seeds by different predator groups. Seed predation was highest early in the season, followed by a gradual decline in predation over the summer for all species. All species were taken by invertebrates. The activity of two phytophagous carabid genera showed significant correlations with seed predation levels. However, in general carabid activity was not related to seed predation and this is discussed in terms of the mainly polyphagous nature of many Carabid species that utilized the seed resource early in the season, but then switched to carnivory as prey populations increased. The potential relevance of post-dispersal seed predation to the development of weed management systems that maximize biological control through conservation and optimize herbicide use, is discussed.

Spatio-temporal variation in seed production in three Euphorbia species and the role of animals on seed fate

Comparative studies on the reproductive biology of co-occurring related plant species have provided valuable information for the interpretation of ecological and evolutionary phenomena, with direct application in conservation management of plant populations. The aims of this thesis were to identify the causes of pre-dispersal reproductive losses in three Euphorbia species (the Mediterranean E. characias and the narrow endemics E. pedroi and E. welwitschii) and evaluate the variation of their effects in time, space and between individuals and species. Furthermore, we intended to study elaiosomes’ fatty acid profiles for the three Euphorbia and assess the role played by the elaiosome in ant attraction. Finally, we aimed to identify the major seed dispersal agents for each Euphorbia species in each site and study differences in short term seed fate due to differences in ant behaviour. The results indicated that intact seed production differed significantly between the three Euphorbia, mostly due to differences in cyathia production. Losses to pre-dispersal seed predators were proportionately larger for the endemic species which also suffered higher losses resulting in flower, fruit (in E. welwitschii) and seed abortion (in E. pedroi). The elaiosomes of E. pedroi are poor in fatty acids and for this reason seeds of this species were removed in lower proportion by mutualistic dispersers than those of their congeners, being more prone to seed predation. Two larger ant species – Aphaenogaster senilis and Formica subrufa – were responsible for a larger percentage of removals with seeds being transported at larger distances and being discarded in the vicinity of their nests following elaiosome removal. Our results highlight the role of insect-plant interactions as major determinants of seed survival for the three study plants and call for the need to include more information on insect-plant interactions in plant conservation programmes.

Bottom-up and top-down effects in a pre-dispersal seed predation system: are non-predated seeds damaged?

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

Seed dispersal and spatial distribution of Attalea geraensis (Arecaceae) in two remnants of Cerrado in Southeastern Brazil

The seed dispersal system of Attalea geraensis (Arecaceae), an acaulescent palm, was investigated during one year in two Cerrado fragments in the state of São Paulo, southeastern Brazil. A. geraensis had inflorescences and infrutescences throughout the year. Two scatter-hoarding rodents (the spiny rat, Clyomys bishopi and agoutis, Dasyptocta azarae) were identified as seed predators/dispersers, able to move seeds up to 30 in from the palms, although most of the fruits (57.5%) were dispersed less than 2 in. The removal rates were high and after 20 days, 97.2% of the fruits were removed. Fruit fate was not related to fruit mass, length and diameter. The application of Morisita's index showed a more clumped distribution of adults in the smaller fragment, probably because of the absence of agoutis. Higher seed removal by rodents in the large Cerrado remnant may decrease seed predation by beetles. (C) 2007 Elsevier Masson SAS. All rights reserved.