Effects of frugivorous birds on seed retention time and germination in Xishuangbanna, southwest China

The dispersal of many plants depends on transportation by birds as seed dispersers. The birds play an important role in long distance seed dispersal and may also affect seed germination. However, for plants who have many bird dispersers, the influence of dominant and non-dominant dispersers on retention time （dispersal distance） and germination remains poorly understood. In this study we performed experiments with captive frugivorous birds and fruiting plant species to study the effects of dominant and non-dominant dispersers on seed retention time （SRT） and germination （seed germination percentage and germination speed）. Our study showed a great interspecific variation in the effects of frugivorous birds on both SRT and germination. Some birds enhance the germination of a given plant species, but others do not. Generally, the dominant visitors improved the seed germination and performed longer seed retention time.

Effect of frugivorous birds on the establishment of a naturally regenerating population of Chinese yew in ex situ conservation

The Chinese yew Taxus chinensis is catalogued as an endangered species in China because of the small size andsenescent status of most populations. Its lack of natural regeneration is the most important reason for its endangeredstatus. We investigated the regeneration of an ex-situ conservation population, which was introduced intothe Nanjing Botanical Garden Memorial Sun Yat-Sen in the 1950s, and evaluated the role of frugivorous birds on theestablishment of this regenerating population. Two hundred and thirteen individual yew seedlings and saplingswere found on the hillside in 2006, and the nearest seedling was found more than 10 m away from mother trees. Thespatial pattern of all seedlings and saplings occurred as a clumped distribution, which is typical for vertebratedispersedplants. Six bird species were seen ingesting whole “fruits” at yew trees in the present study and 745 visitsby avian frugivores were recorded. Red-billed blue magpie (Urocissa erythrorhyncha), Chinese bulbul (Pycnonotussinensis) and azure-winged magpie (Cyanopica cyana) were the most frequent visitors over the two years of thestudy. Comparing the flights of departure and perching habitats of the three main bird species, we inferred that U.erythrorhyncha would be the most important disperser. This regeneration population has had good developmentover the past 20 or more years;frugivorous birds have removed seeds to the hillside every year until now, and seedgermination and seedling growth continue to develop well under natural conditions. We suggest that the conservationsystem of the Chinese yew should be composed of yews, avian dispersers and habitats for seed germinationand seedling growth.

Endozoochory of frugivorous birds as potential dispersal of seed parasites from Pistacia chinesis:experimental evidence

The plant-disperser-fruit pest triads involve 3 interacting animals or groups(plants,vertebrates and seed parasites),and the dispersal of both seeds and seed parasites,which can both benefit from endozoochory via defecation or regurgitation by frugivorous vertebrates.However,we have very limited knowledge about the ecological and evolutionary consequences of these plant-disperser-fruit pest triads.Across central Northern China,several seed wasps(mainly Eurytoma plotnikov attack Pistacia chinensis fruits,and seed wasp larvae can develop,diapause and finally emerge as adults inside a seed during the following 1-3 years.In this study,we experimentally investigated whether frugivorous birds discriminated P.chinesis fruits with or without seed parasites,and whether bird endozoochory(by defecation or regurgitation)affected larval survival of seed parasites.The infestation rate by seed parasites was 37%of the P.chinesis fruit crop but with up to 48%of aborted fruits.We found that all 5 bird species can discriminate and then reject all unhealthy fruits(including aborted and insect-infested).However,4 of the 5 bird species,in particular bulbul species,consumed 15-41%of aborted and insect-infested fruits as complementary food only when these unhealthy fruits were provided.Moreover,all larva of seed parasites remained alive after bird defecation or regurgitation.In conclusion,our study demonstrates that endozoochory by frugivorous birds could lead to potential dispersal of seed parasites of P.chinensis but with a very low probability.

Bird functional traits affect seed dispersal patterns of China's endangered trees across different disturbed habitats

Background: The most dominant global threat to natural forests and their biodiversity is land-cover change, which has negative impacts on both species persistence and ecosystem functions. Land-cover change could alter animal behaviour and disrupt seed dispersal mutualisms. However, its effects on the role of bird functional traits in seed dispersal are not well studied.Methods: In the present study, we assessed the contributions of bird functional traits(behavioural traits: food habit, foraging pattern, foraging frequency, and habitat specialisation; morphological traits: weight, body length, wing length, and tail length) to both seed removal patterns and seed dispersal distances of an endangered and native tree species, Chinese yew(Taxus chinensis), in farmland, patchy habitat, and natural habitat, of southeast China.Results: We found that the ability of T. chinensis trees to form seed dispersal mutualisms with local birds varied across the different disturbed habitats. As a consequence of these mutualisms, more seeds were removed by birds from the patchy habitat than from the other two habitats. The number of seeds removed increased with bird foraging frequency. Moreover, the dispersal distance from the three habitats differed, and the longest dispersal distances were observed at both the patchy habitat and the farmland site. Seed dispersal distance increased with bird tail and wing length.Conclusions: Our results highlight the importance of bird functional traits in the seed dispersal patterns of endangered trees across disturbed forest habitats, which should be considered for tree conservation and management.

Annual periodicity of fruiting in temperate forests in Yakushima, Japan

Fruiting phenology, assessed by seed fall, in five warm- and cool-temperate forests on Yakushima Island, southern Japan, was studied for two years in one 50 m × 50 m plot and for four years in four 100 m ×50 m plots. The elevation of the plots ranged between 170 and 1200 m a.s.l. Seed fall phenology showed annual periodicity in all five plots. This was clear when assessed by the number of species but became less clear when assessed by the biomass of seed litter. Community-level annual periodicity was based on the prevalence of population-level annual periodicity and interspecific synchronization of the fruiting peak from autumn to winter. Fleshy fruits had peaks of seed fall in a wider range of months than non-fleshy fruits, since it is sometimes beneficial to bear fruit outside the community-level fruiting peaks in order to avoid interspecific competition for animal seed dispersers. No consistent effect of climatic factors on seed fall phenology was detected.

Fruit fall in five warm- and cool-temperate forests in Yakushima,Japan

Quantification of fruit fall is the only way to compare fruit food availability among different studies. This study aims to reveal the general characteristics of fruit fall in temperate forests, which should offer indispensable information for using fruit fall data as food availability for frugivores. Fruit fall in three warm-temperate and two cool-temperate forests on Yakushima, an island in southwestern Japan, were studied for two years in one cool-temperate plot of 50 m × 50 m in size and for four years in other plots of 100 m × 50 m in size. The elevations of the plots ranged 170-1200 m a.s.1. Fruit fall was highest in the lowland forests （599 and 564 DW kg·ha^-1·year^-1 and lowest in the mid-elevation forest （198 DW kg·ha^-1·year^-1）. Fleshy fruits and food-fruits for Japanese macaques constituted 3-37% and 4-87% of the total fruit fall, respectively. When only fleshy-fruit fall was compared, it was higher in the western lowland forest （222 DW kg.ha^-1.year^-1） than in any other forests （9-66 DW kg-ha^-1.year^-1）. The pulp of fleshy fruits, presumably the edible parts for frugivores, was only 1.1-12.7% of the total fi ait fall. The edible parts for Japanese macaques constituted 3-54% of the fruit fall, showing a high value where acorns are abundant. Half of the fruit-fall biomass consisted of only one or two non- fleshy-fruited species, which are usually dominant in many other temperate forests, such as Quercus and conifers. These variations agreed with the variations in occurrence of frugivorous （such as Japanese macaques）.

Subcanopy genetics —The relationship between canopy tree size and genetic variation of the savanna species <i>Pollichia campestris</i>Aiton (Illecebraceae)

In savanna vegetation, trees and their canopies provide an important, but scattered habitat. Seeds of plants growing under these nurse trees often are dispersed by animals, especially birds. In the present study, we investigated the influence of tree size and frugivore dispersal on the genetic variation of the subcanopy species Pollichia campestris, using amplified fragment length polymorphisms (AFLP). Considering the individuals under each nurse tree as subpopulations, we found the genetic variation within subpopulations to be positively correlated with the size of the respective canopy tree. Genetic variation was very low among, but high within subpopulations (ΦPT = 0.026, P = 0.18). We conclude that the low genetic variation among subpopulations is due to effective and directed dispersal (dispersal from one canopy to another) by legitimate and frugivorous dispersal agents.

Onto the sense of smell in macaws, amazons and toucans: can they use volatile cues of fruits to make foraging decisions?

Over the past decades,empirical evidence has been accumulated indicating that olfactory information plays a fundamental role in bird life history.Nonetheless,many aspects of avian olfaction remain poorly understood.Our purpose was to broaden the knowledge about the importance of the sense of smell in some neglected bird groups:psittaciformes and ramphastids,and to compare how the response varied between the species.Because of the lack of information about the use of chemical cues for locating food in fruit-eating species,we also aimed to delve into this question.We conducted a 3-choice(water/vinegar/papaya and banana juice)scent test in 5 Costa Rican native species:scarlet macaw(Ara macao),red-lored amazon(Amazona autumnalis),yellow-naped amazon(Amazona auropalliata),keel-billed toucan(Ramphastos sulfuratus),and yellow-throated toucan(Ramphastos ambiguus).Results revealed that macaws and toucans allocated significantly more time to interacting with the fruit scent container,indicating that these species can perceive the volatile chemicals emitted by ripe fruits and that they can use this information to make foraging decisions.However,amazons did not dedicate more time to interact with the fruit treatment.Our research provides thefirst evidence of the ability to exploit chemical volatile cues in macaws and toucans.

Dispersal of invasive Phytolacca americana seeds by birds in an urban garden in China

Although seed dispersal is a key process determining the regeneration and spread of invasive plant populations,few studies have explicitly addressed the link between dispersal vector behavior and seedling recruitment to gain insight into the invasion process within an urban garden context.We evaluated the role of bird vectors in the dispersal of pokeweed(Phytolacca americana),a North American herb that is invasive in urban gardens in China.Fruiting P.americana attracted both generalist and specialist bird species that fed on and dispersed its seeds.The generalist species Pycnonotus sinensis and Urocissa erythrorhyncha were the most frequent dispersers.Seedling numbers of P.americana were strongly associated with the perching behavior of frugivorous birds.If newly recruited bird species use seedling-safe perching sites,the P.americana will regenerate faster,which would enhance its invasive potential.Based on our observations,we conclude that the 2 main bird vectors,P.sinensis and U.erythrorhyncha,provide potential effective dispersal agents for P.americana.Our results highlight the role of native birds in seed dispersal of invasive plants in urban gardens.

Scatter-hoarding rodents as secondary seed dispersers of a frugivore-dispersed tree Scleropyrum wallichianum in a defaunated Xishuangbanna tropical forest, China

Local extinction or population decline of large frugivorous vertebrates as primary seed dispersers,caused by hu-man disturbance and habitat change,might lead to dispersal limitation of many large-seeded fruit trees.However,it is not known whether or not scatter-hoarding rodents as secondary seed dispersers can help maintain natural regeneration(e.g.seed dispersal)of these frugivore-dispersed trees in the face of the functional reduction or loss of primary seed dispersers.In the present study,we investigated how scatter-hoarding rodents affect the fate of tagged seeds of a large-seeded fruit tree(Scleropyrum wallichianum Arnott,1838,Santalaceae)from seed fall to seedling establishment in a heavily defaunated tropical forest in the Xishuangbanna region of Yunnan Province,in south-west China,in 2007 and 2008.Our results show that:(i)rodents removed nearly all S.wallichianum seeds in both years;(ii)a large proportion(2007,75%;2008,67.5%)of the tagged seeds were cached individually in the surface soil or under leaf litters;(iii)dispersal distance of primary caches was further in 2007(19.6±14.6 m)than that in 2008(14.1±11.6 m),and distance increased as rodents recovered and moved seeds from primary caches into subsequent caching sites;and(iv)part of the cached seeds(2007,3.2%;2008,2%)survived to the seedling stage each year.Our study suggests that by taking roles of both primary and secondary seed dispersers,scatter-hoarding rodents can play a significant role in maintaining seedling establishment of S.wallichianum,and are able to at least partly compensate for the loss of large frugivorous vertebrates in seed dispersal.

Inter-specific and intra-specific variability in fruit color preference in two species of Turdus

One of the main hypotheses proposed to explain the evolution of fruit color deals with a preference of avian frugivores for specific colors,mainly black and red,which are the most common fruit colors in many of the studied habitats.I analyzed fruit color preferences by wild birds belonging to 2 species of the highly frugivorous genus Turdus(Eurasian Blackbird Turdus merula Linnaeus,1758 and Redwing Turdus iliacus Linnaeus,1758)by means of captivity experiments with artificial fruits.Despite important within-individual(i.e.temporal)and among-individual variability,consistent patterns of species-specific color preferences emerged.Eurasian Blackbirds tended to prefer red over blue,green and black,whereas Redwings seemed to prefer black over the rest.Green was systematically avoided by both species,suggesting that it might signal unripeness of fruits.Both preferred colors have been previously reported as the most common among fleshy-fruited plants.The high variability,both within and between individuals,in preferences suggests that they can be subject to changes through experience and learning and,therefore,are not likely to drive the evolution of fruit color.The main differences between both species could be related to the most common fruit color they fed upon during the last months before capture.

Fruit availability, frugivore satiation and seed removal in 2 primate-dispersed tree species

During a mast-fruiting event we investigated spatial variability in fruit availability,consumption,and seed removal at two sympatric tree species,Manilkara bidentata and M.huberi(Sapotaceae)at Nouragues Natural Reserve,French Guiana.We addressed the question of how Manilkara density and fruits at the community level might be major causes of variability in feeding assemblages between tree species.We thus explored how the frugivore assemblages differed between forest patches with contrasting relative Manilkara density and fruiting context.During the daytime,Alouatta seniculus was more often observed in M.huberi crowns at Petit Plateau(PP)with the greatest density of Manilkara spp.and the lowest fruit diversity and availability,whereas Cebus apella and Saguinus midas were more often observed in M.bidentata crowns at both Grand Plateau(GP),with a lowest density of M.bidentata and overall greater fruit supply,and PP.Overall,nearly 53%and 15%of the M.bidentata seed crop at GP and PP,respectively,and about 47%of the M.huberi seed crop were removed,otherwise either spit out or defecated beneath trees,or dropped in fruits.Small-bodied primates concentrated fallen seeds beneath parent trees while large-bodied primate species removed and dispersed more seeds away from parents.However,among the latter,satiated A.seniculus wasted seeds under conspecific trees at PP.Variations in feeding assemblages,seed removal rates and fates possibly reflected interactions with extra-generic fruit species at the community level,according to feeding choice,habitat preferences and ranging patterns of primate species.

Plant-frugivore interactions in an intact tropical forest in north-east Thailand

Fleshy-fruited plants in tropical forests largely rely on vertebrate frugivores to disperse their seeds.Although this plant-animal interaction is typically considered a diffuse mutualism,it is fundamental as it provides the template on which tropical forest communities are structured.We applied a mutualistic network approach to investigate the relationship between small-fruited fleshy plant species and the fruit-eating bird community in an intact evergreen forest in north-east Thailand.A minimum of 53 bird species consumed fruits of 136 plant species.Plant-avian frugivore networks were highly asymmetrical,with observed networks filling 30%of all potential links.Whereas some of the missing links in the present study might be due to undersampling,forbidden links can be attributed to size constraints,accessibility and phenological uncoupling,and although the majority of missing links were unknown(58.2%),many were probably due to a given bird species being either rare or only a very occasional fruit eater.The most common frugivores were bulbuls,barbets and fairy-bluebirds,which were responsible for the majority of fruit removal from small fleshy fruited species in our system.Migratory birds seemed to be a minor component of the plant-frugivore networks,accounting for only 3%of feeding visits to fruiting trees;they filled 2%of the overall potential networks.The majority of interactions were generalized unspecific;however,Saurauia roxburghii Wall.appeared to be dependent on flowerpeckers for dispersal,while Thick-billed Pigeons were only seen to eat figs.

Does a giant tortoise taxon substitute enhance seed germination of exotic fleshy-fruited plants?

Aims The use of exotic species as taxon substitutes to restore lost ecological interactions is currently hotly debated.Aldabrachelys gigantea giant tortoises have recently been introduced to three islands in the Mascarene archipelago(Ile aux Aigrettes,Round Island and Rodrigues)to resurrect herbivory and seed dispersal functions once performed by extinct giant tortoises.However,potential unintended impacts by frugivore substitutes on native ecosystems,e.g.whether they will facilitate the germination of exotic plant species,are largely unknown.We investigated whether A.gigantea introduced to Rodrigues in 2006 could enhance the germination percentage of four widespread fleshy-fruited exotic species on the island.Using germination trials to forecast unintended impacts that could arise from the introduction of a frugivorous taxon substitute enables conservation managers to limit potential adverse negative interactions before they occur.Methods In germination trials that ran over 4 months,we investigated the effects of ingestion(gut passage and deposition in faeces)by subadult and adult A.gigantea on the germination percentage of four exotic fleshy-fruited plant species introduced to Rodrigues.We fed fruits of these plant species to sub-adult and adult A.gigantea to test how variation in age and size of the frugivore would affect seed germination.Feeding of distinctly coloured plastic pellets together with the fruits allowed us to test for individual tortoise effects on seed germination.Important Findings Ingestion by A.gigantea increased the percentage of seeds germinating of Mimusops coriacea and Lantana camara,but not percentage of germination of Veitchia merrillii or Wikstroemia indica.Seeds were more likely to germinate following ingestion by sub-adult rather than adult tortoises,which may be a consequence of the shorter gut passage time observed for sub-adults.Our results demonstrate that introduced frugivorous taxon substitutes could facilitate germination of exotic and invasive plants and highlight the need for conservation managers to weigh the risk of taxon substitutes potentially facilitating the germination and recruitment of exotic fleshy-fruited plants against the benefit of restoring lost seed dispersal functions of threatened indigenous plants.Our findings also highlight the importance of considering age and size variation in frugivores,in particular in long-lived taxa such as giant tortoises,when studying ingestion effects on the germination performance of plants.