Effects of bird ingestion on seed germination of two Prunus species with different fruit-ripening seasons

To evaluate the effects of ingestion by birds on seed germination under natural conditions, we carried out germination experiments in the field using seeds of two Prunus species that have different fruit-ripening seasons. Germination of seeds with the following three treatments was compared: ingested seeds, seeds excreted after feeding of fruits to birds; extracted seeds, seeds deliberately extracted from the fruit pulp; and intact fruit, seeds in untreated intact fruit. Many ingested and extracted seeds of both Prunus species germinated during the first spring, and the difference in germination percentage between ingested and extracted seeds was not significant. Many seeds in intact fruit of Prunus sargentii also germinated during the first spring, but those of Prunus ssiori did not germinate until the second spring. Pulp removal through bird ingestion enabled rapid germination for the autumn-fruiting P. ssiori, whose fruit pulp was not likely to be decomposed until the first spring. In contrast, the effects of ingestion were not striking for the summer-fruiting P. sargentii, whose fruit pulp is quickly decomposed.     

黄檗的更新特点及食果实鸟类对其种子的传播

在帽儿山实验林场和哈尔滨实验林场 ,黄檗母树下没有幼苗分布 ,不能进行天然更新 ,需要靠食果实鸟类等将果实和种子传播至远离母树的其他林下。捕食黄檗果实的食果实鸟类有 9种。其中 6种是食果肉鸟类 ,吞入果实后 ,消化果肉 ,而种子完整地随粪便排出而得以传播。其余 3种是食种子鸟类 ,没有传播作用。果实在鸟类消化道内的滞留时间达 2 0～ 30min ,具有很长的潜在传播距离。将鸟类消化后的种子与完整果实和人为去果肉种子进行萌发对比实验 ,消化后种子的累计萌发率与其余二者之间均没有显著性差异 ,说明食果实鸟类的消化 (道 )过程对种子萌发没有明显影响 ,同时证明果肉对种子萌发率没有显著影响 ,果肉中不含萌发抑制物质。黄檗提供多种鸟类以食物 ,而鸟类也同时以多种肉质果植物为食物。因此食果实鸟类和肉质果植物 (包括黄檗 )之间形成了松散的互利共生关系     

Directed vertebrate-mediated seed dispersal of a fleshy-fruited amaryllid in a heterogenous habitat

Most plants with fleshy fruits have seeds that are ingested by animals, but a less well-understood mode of seed dispersal involves fleshy fruits containing seeds that are discarded by frugivorous animals because they are too large or toxic to be ingested. We studied the seed dispersal biology of Haemanthus deformis, an amaryllid lily species found in a mosaic of bush clumps in a grassland matrix in South Africa. We asked whether seed dispersal is directed in and among bush clumps and whether germination and survival are greater for seeds dispersed to bush clumps than for those dispersed into grassland. Using camera trapping, we found that fruits are consumed mainly by birds and rodents. The pulp was removed from the seeds which were then discarded without ingestion. While many seeds were dispersed close to the parent plant, most (c. 78.5%) were dispersed further than 1 m away from the parent plant. Longer distance dispersal resulted mainly from birds flying off with fruits in their bill or from rodents engaging in scatter-hoarding behavior. Seedling survival was most successful within bush clumps as compared to grasslands and shade was identified as a primary requirement for seedling survival. Seeds from which the fruit pulp had been removed germinated faster than those in intact fruits. Haemanthus deformis deploys a system of directed seed dispersal, whereby both birds and rodents contribute to the dispersal of seeds within patchy bush clumps that are favorable for seedling survival.     

Effects of bird ingestion on seed germination of four woody species of the temperate rainforest of Chiloé island, Chile

We study the effect of ingestion by birds on seed germination and theconsequences of absence of dispersal, with the persistency of the seedsinside the fruit. We collected seeds of four woody species ofthe temperate rainforest of Chiloé: Gaultheriamucronata, Luma apiculata, Myrteolanummularia, and Myrceugenia planipes. The seedstested had the following origins: 1) Ingested seeds: seeds collected fromthe feces of birds, 2) Extracted seeds: seeds obtained directly from thefruits, and 3) Intact fruits: fruits collected directly from the plants.Germination of Myrceugenia planipes under greenhouseconditions, Luma apiculata, and Myrteolanummularia under laboratory conditions, and Gaultheriamucronata under both conditions was analyzed. We found that the seedsreach their maximum germination between 15–20 days after sowing, withthe exception of those of G. mucronata sown in the greenhouse,which showed a low germination rate. In the greenhouse assay, seeds ofG. mucronata ingested by birds, seeds extracted manuallyfrom the fruits, and seeds inside the fruits did not show significant differencesin their germination percentages. In the laboratory assays, the seeds ofG. mucronata and M. nummulariaingested by birds and the seeds extracted manually from the fruits also did not show anysignificant difference in germination. Under laboratory conditions, theseeds of L. apiculata ingested by birds presented astatistically greater percentage of germination than the seeds extracted manually.Under greenhouse conditions, seeds of M. planipes ingestedby birds did not present a statistically different germination percentage fromthose seeds extracted from the fruits. The seeds of M.planipes, and L. apiculata inside the intactfruits did not germinate. We conclude that birds do not affect the seedviability of any of the four species studied.     

Two thrush species as dispersers of Miconia prasina (Sw.) DC. (Melastomataceae): an experimental approach.

We carried out a seed germination experiment using two thrush species in captivity. We compared the number of germinated seeds and germination time of control seeds (manually removed from fruits) and ingested seeds of Miconia prasina by two bird species, Turdus albicollis and T. amaurochalinus, and also compared retention times of seeds by both thrush species. Control seeds germinated more frequently than those ingested for one species, T. albicollis. The germination time of ingested seeds by T. amaurochalinus was similar to the control seeds but seeds ingested by T. albicollis took longer to germinate than the controls. Both thrush species had a similar seed defecation pattern. The cumulative number of defecated seeds increased by 2 hours after fruit ingestion. At the end of the first 30 minutes both species had already defecated approximately 50% of the seeds ingested Our results suggest that both species could act as disperser agents of M. prasina.     

Antelope ingestion enhances germination of the marula (Sclerocarya birrea), an important African savannah tree

The marula (Sclerocarya birrea Hochst.) is an important forage and fruit tree in African savannahs. This study compared germination rate (days to germination) and success (percentage of stones that produced seedlings) among an intact control and four treatments, where fruits were (i) ingested by antelope (Cephalophinae and Neotragini), (ii) manually depulped, (iii) manually depulped and burnt and (iv) burnt intact. Measurements on three unrelated trees showed that whilst stone size differed significantly, germination success was comparable. Antelope regurgitated and expelled stones during rumination, within 16 h of ingestion. Seedling emergence commenced approximately 6 months after fruit drop when ambient temperature increased. Removal of fruit pulp increased germination rate and germination success, but moderate exposure to fire inhibited germination, especially following depulping. Germinated seeds were from significantly smaller stones than ungerminated seeds, suggesting that thicker‐walled endocarps inhibited seedling emergence. However, germination of the second seed in a stone was from larger stones in the germinated subset, possibly due to larger seed size. That antelope ingestion significantly enhanced germination over other treatments suggests that endozoochory is an important mode of seed dispersal in marulas. Appropriate fire management is therefore required in savannahs, as high‐intensity fires may limit germination and recruitment of marulas.     

Seed Germination Ecology of the Cold Desert Annual Isatis violascens (Brassicaceae): Two Levels of Physiological Dormancy and Role of the Pericarp

The occurrence of various species of Brassicaceae with indehiscent fruits in the cold deserts of NW China suggests that there are adaptive advantages of this trait. We hypothesized that the pericarp of the single-seeded silicles of Isatis violascens restricts embryo expansion and thus prevents germination for 1 or more years. Thus, our aim was to investigate the role of the pericarp in seed dormancy and germination of this species. The effects of afterripening, treatment with gibberellic acid (GA₃) and cold stratification on seed dormancy-break were tested using intact silicles and isolated seeds, and germination phenology was monitored in an experimental garden. The pericarp has a role in mechanically inhibiting germination of fresh seeds and promotes germination of nondormant seeds, but it does not facilitate formation of a persistent seed bank. Seeds in silicles in watered soil began to germinate earlier in autumn and germinated to higher percentages than isolated seeds. Sixty-two percent of seeds in the buried silicles germinated by the end of the first spring, and only 3% remained nongerminated and viable. Twenty to twenty-five percent of the seeds have nondeep physiological dormancy (PD) and 75–80% intermediate PD. Seeds with nondeep PD afterripen in summer and germinate inside the silicles in autumn if the soil is moist. Afterripening during summer significantly decreased the amount of cold stratification required to break intermediate PD. The presence of both nondeep and intermediate PD in the seed cohort may be a bet-hedging strategy.     

DORMANCY AND GERMINATION IN SEEDS OF COMMON RAGWEED WITH REFERENCE TO BEAL'S BURIED SEED EXPERIMENT

Common ragweed (Ambrosia artemisiifolia L.) was one of 19 herbaceous weedy species used by Beal in his buried viable seed experiment started in 1879. No seeds germinated during the first 35 years of the experiment when germination tests were performed in late spring, summer or early autumn. Germination did occur in seeds buried for 40 years when seeds were exhumed and tested for germination in early spring. Data obtained in more recent research provide the probable explanation for these results. Seeds of common ragweed that do not germinate in spring enter secondary dormancy by mid to late spring and will not germinate until dormancy is broken the following late autumn and winter. Thus, during the first 35 years of the experiment seeds were dormant when tested for germination, whereas seeds buried for 40 years were nondormant. Seeds buried 50 years or longer did not germinate when tested in spring, probably because they had lost viability and/or seeds germinated during burial and seedlings died.     

Large African herbivores,bruchid beetles and their interactions with Acacia seeds

This study investigated the interactions of large African herbivores and bruchid seed beetles with Acacia seeds. The germination of bruchid-infested and uninfested seeds was compaed. The effects of pod consumption by large herbivores on bruchid infestation and seed germination was also assessed. Bruchid-infested seeds did germinate, and the germination of bruchid-infested and uninfested A. tortilis, A. nilotica and A. hebeclade seeds did not differ. Pod ingestion by large herbivores lowered the bruchid infestation of consumed and defaecated seeds compared to uningested seeds. Uninfested, ingested and voided A. tortilis seeds germinated seeds. Furthermore, infested A. tortilis seeds egested by giraffe, kudu and ostrich germinated better than infested, uningested seeds. Pod ingestion by large herbivores may reduce bruchid infestation, increase Acacia seed germination and therefore increase potential Acacia seedling recruitment.     

Effects of macaque ingestion on seed destruction and germination of a fleshy-fruited tree, <Emphasis Type="Italic">Eurya emarginata</Emphasis>

Effects of macaque ingestion were examined on both seed destruction during passage through the gut and germination enhancement after defecation, using typically endozoochorous fruits of Eurya emarginata. Mechanical and chemical actions associated with the ingestion were also examined. A fruit-feeding experiment found that 4.4% of ingested seeds could pass intact through the gut of Japanese macaques. No significant difference was detected between the seed passage percentages of six Eurya emarginata trees despite individual variation in seed weight and hardness, implying that mastication is a major factor in the severe seed mortality during the gut passage. Seeds in intact fruits showed lower germination percentage and longer germination delay than seeds with the flesh removed artificially. In contrast, no enhancement in germination was observed after passage through the gut. A series of seed treatment experiments indicated that seed abrasion did not affect germination percentage, though acid and heat-exposure enhanced the germination. The two factors, severe seed destruction and germination enhancement by flesh removal, opposed each other. With the survival proportion of uningested seeds taken as 1.0, the survival proportion of ingested seeds was estimated as 0.49 with the 95% confidence interval of 0.14–1.46, which indicated no significant difference between the proportions of ingested- and uningested-seeds.     

The role of frugivorous birds in fruit removal and seed germination of the invasive alien Cotoneaster franchetii in central Argentina

Many invasive plant species have fleshy fruits that are eaten by native frugivorous birds which disperse their seeds and may facilitate their germination, playing an important role in plant invasion success. The fleshy‐fruited shrub Cotoneaster franchetii (Rosaceae) is an important invasive alien in the mountainous regions of central Argentina. To determine the role of avian frugivorous in fruit removal of this species, we conducted a frugivore exclusion experiment including bagged and unbagged branches in 75 plants of C. franchetii. At the end of the dispersal period, we compared the percentage of missing fruits (removed by birds + naturally dropped) in unbagged branches with the percentage of naturally dropped fruits in bagged branches. To assess whether any mechanism acting on seeds during their passage through bird guts (de‐inhibition by pulp removal and/or seed scarification) affects seed germination of this species, we compared percentage and speed of germination among seeds obtained from faeces of the native frugivorous Turdus chiguanco, from manually de‐pulped fruits, and from intact fruits. The percentage of missing fruits per shrub in unbagged branches was significantly higher than the percentage of naturally dropped fruits in bagged branches, suggesting that frugivorous birds play an important role in fruit removal of C. franchetii in the study area. Seeds from bird faeces and from manually de‐pulped fruits germinated in higher percentage and faster than seeds from intact fruits. Germination percentage and speed of seeds from manually de‐pulped fruits were significantly higher than those of gut‐passed seeds. These results indicate that T. chiguanco increases and accelerates seed germination of C. franchetii through pulp removal, but not through seed scarification. Overall, our findings indicate that native frugivorous birds facilitate the dispersal and germination success of C. franchetii, likely playing an important role in its invasion throughout the mountainous region of central Argentina.     

鸟类取食中国沙棘果实的方式及其对种子的传播作用

2003年9月～2004年3月,定期观察取食中国沙棘果实的鸟类及其取食方式。共记录取食中国沙棘果实的鸟类18种,其取食果实的方式主要有：1)直接在树冠上吞食果实,有时候在吞食后将种子呕出;2)将果实从树上衔走后,在栖息处吞食或啄食;3)将果实啄落至地面,然后取食果肉和种子,留下果皮;4)啄破果皮,吸食果肉,留下果皮及种子;5)从顶端将果皮啄破后,仅取食里面的种子。不同的取食方式决定了它们对沙棘种子的传播作用不同。收集鸟粪便中的种子与完整的干果实及人工剥离果肉和内果皮的种子做萌发对比实验,结果表明,鸟类消化道过程对种子的萌发有一定影响,但萌发率仍较高。沙棘为多种鸟类提供食物,而鸟类则为沙棘传播种子,它们之间形成一种互利关系。     

Role of temperature in the germination ecology of three summer annual weeds

Summary Ambrosia artemisiifolia L., Chenopodium album L., and Amaranthus retroflexus L. are three summer annual weeds that occur in disturbed habitats. In nature, the peak germination season for A. artemisiifolia and C. album is in early to mid-spring, while in A. retroflexus the peak germination season is late spring to early summer. Furthermore, seeds of A. artemisiifolia germinate only in spring, while seeds of C. album and A. retroflexus germinate throughout the summer. In an attempt to explain the differential germination behavior of these three species in nature, changes in their germination responses to temperature during burial in a non-heated greenhouse from October 1974 to October 1975 were monitored. A high percentage of the seeds of all three species after-ripened during winter. Seeds of A. artemisiifolia and C. album germinated at temperatures characteristic of those in the field in early and mid-spring, but seeds of A. retroflexus required the higher temperatures of late spring and early summer for germination. Seeds of all three species germinated to higher percentages in light than in darkness. Non-dormant seeds of A. artemisiifolia that did not germinate in spring entered secondary dormancy. On the other hand, seeds of C. album and A. retroflexus that did not germinate when temperatures first became favorable for germination, did not enter secondary dormancy and, thus, retained the ability to germinate at summer field temperatures during summer. Thus, temporal differences in the germination behavior of these three species are caused by the differential reaction of the seeds to temperature during the annual temperature cycle.     

Fruits foraging patterns and seed dispersal effect of frugivorous birds on Hippophae rhamnoides sinensis

Behaviors of 18 species of birds eating fruits of Hippophae rhamnoides spp.sinensis were observed from September 2003 to March 2004.Their foraging patterns were found to be very different and Can be divided into five classes:(1)direct swallowing the fruits on crown of the shrubs and sometimes regurgitating seeds soon after;(2)carrying the fruits to their perching sites and swallowing;(3)pecking the fruits from the shrubs to the ground,eating pulp and seeds but leaving pericarp;(4)pecking through the pericarp,eating pulp and leaving pericarp and seeds;(5)pecking through the pericarp on the top of fruits,and only eating seeds.These foraging patterns have different effects on seed dispersal of H.rhamnoides spp.sinensis.The germination experiment of three groups of seeds(seeds from feces,dry fruits and extracted seeds from dry fruits)was carried out.Although ingestion processes of birds had some adverse effects on the seed germination of H.rhamnoides spp.sinensis,the seeds from feces still have a relatively higher germination ratio.H.rhamnoides spp.sinensis provides food to a variety of frugivorous birds.and the birds disperse its seeds.Thus,a mutually beneficial relationship between the bird and the seed is formed.     

Fruits foraging patterns and seed dispersal effect of frugivorous birds on Hippophae rhamnoides sinensis

Behaviors of 18 species of birds eating fruits of Hippophae rhamnoides spp. sinensis were observed from September 2003 to March 2004. Their foraging patterns were found to be very different and can be divided into five classes: (1) direct swallowing the fruits on crown of the shrubs and sometimes regurgitating seeds soon after; (2) carrying the fruits to their perching sites and swallowing; (3) pecking the fruits from the shrubs to the ground, eating pulp and seeds but leaving pericarp; (4) pecking through the pericarp, eating pulp and leaving pericarp and seeds; (5) pecking through the pericarp on the top of fruits, and only eating seeds. These foraging patterns have different effects on seed dispersal of H. rhamnoides spp. sinensis. The germination experiment of three groups of seeds (seeds from feces, dry fruits and extracted seeds from dry fruits) was carried out. Although ingestion processes of birds had some adverse effects on the seed germination of H. rhamnoides spp. sinensis, the seeds from feces still have a relatively higher germination ratio. H. rhamnoides spp. sinensis provides food to a variety of frugivorous birds, and the birds disperse its seeds. Thus, a mutually beneficial relationship between the bird and the seed is formed. __________ Translated from Chinese Journal of Ecology, 2005, 24(6): 635–638 [译自: 生态学杂志, 2005, 24(6): 635–638]     

The effect of frugivory on postdispersal seed removal and germination in the pantropical forest tree Antiaris toxicaria Leschenault

The quality of seed treatment by frugivores has an effect on seed removal after dispersal, seed germination and tree recruitment. We provide information on postdispersal seed removal, germination and subsequent recruitment in tropical forest tree species Antiaris toxicaria in Ghana. We tested whether postdispersal seed removal and germination rates were differentially affected by the following seed treatments: seeds that were spat out by monkeys with all fruit pulp removed and spitting seeds with fruit pulp partially removed as observed in some birds and bats. We used seeds of intact ripened fruits as control. Frugivore seed treatment and distance from bole affected seed removal patterns, whereas intact seeds were significantly removed from all seed stations. The germination success was greater for seeds that were spat out by monkeys and poor for seeds with fruit pulp partially removed and intact fruits. More recruits were recorded at the edge of the adult A. toxicaria canopy radius. There was weak relationship (r² = 0.042) between the number of recruits and distance away from the adult tree. Results suggest that the subsequent recruitment in tropical forest tree species may be enhanced by some frugivore fruit‐handling behaviour where fruit pulp is removed from the seeds without destroying the seeds.     

GERMINATION ECOLOGY OF PHACELIA DUBIA VAR. DUBIA IN TENNESSEE GLADES

The germination characteristics of a population of the winter annual Phacelia dubia (L.) Trel. var. dubia from the middle Tennessee cedar glades were investigated in an attempt to define the factor(s) regulating germination in nature. Factors considered were changes in physiological response of the seeds (after-ripening), temperature, age, light and darkness, and soil moisture. At seed dispersal (late May to early June), approximately 50 % of the seeds were non-dormant but, would germinate only at low temperatures (10–15 C). As the seeds aged from June to September, there was an increase in rate and total percent of germination at 10, 15, and 20 C, and the maximum temperature for germination increased to 25 C. Little or no germination occurred at the June, July, and August temperatures in 0- to 2-month-old seeds, even in seeds on soil that was kept continuously moist during this 3-month period. At the September, October, and November temperatures 3- to 5-month-old seeds germinated to high percentages. In all experiments seeds germinated better at a 14-hr photoperiod than in constant darkness. Inability of 0- to 2-month-old seeds to germinate at high summer temperatures allows P. dubia dubia to pass the dry summer in the seed stage, while increase in optimum and maximum temperatures for germination during the summer permits seeds to germinate in late summer and early fall when conditions are favorable for seedling survival and eventual maturation.     

Frugivory and seed dispersal of golden lion tamarin (Leontopithecus rosalia (Linnaeus, 1766)) in a forest fragment in the Atlantic Forest, Brazil

The influence of the golden lion tamarin (Leontopithecus rosalia) as a seed disperser was studied by monitoring two groups of tamarins from December 1998 to December 2000 (871.9 hours of observations) in a forest fragment in south-east Brazil. The tamarins consumed fruits of 57 species from at least 17 families. They ingested the seeds of 39 species, and 23 of these were put to germinate in the laboratory and/or in the field. L. rosalia is a legitimate seed disperser because the seeds of all species tested germinated after ingestion, albeit some in low percentages. These primates do not show a consistent effect in final seed germination, because they benefit some species while damaging others. Feces were examined for seeds that had been preyed upon or digested.     

Ingestion by an endemic frugivore enhances seed germination of endemic plant species but decreases seedling survival of exotics

Aim To test whether ingestion by endemic frugivores differentially affects the seed germination time, germination percentage and seedling survival of endemic, native and exotic fleshy fruited plant species, and to identify the principal processes and attributes driving such effects. Location Round Island, Mauritius. Methods We conducted a germination and seedling survival experiment for 3 months to test whether ingestion (gut passage and deposition in faeces) by the endemic Telfair’s skink (Leiolopisma telfairii) had a differential effect on the germination time, germination percentage and seedling survival of two endemic, four native and two exotic fleshy fruited plant species. To assess the importance of factors involved in the ingestion process, we used a factorial design with gut passage (gut‐passed vs. not gut‐passed), depulping (whole fruit vs. manually depulped seed) and the presence of faecal material (faeces vs. without faeces). In addition, the roles of species‐specific traits, seed size and deposition density (average number of seeds per faeces) were examined. Results Exotic species had a higher germination percentage than indigenous (native and endemic) species when not ingested. Following skink ingestion, there was no longer a difference, as ingestion enhanced germination percentage most in endemic species. The exotic species still germinated faster overall than the indigenous species, despite ingestion accelerating the germination time of endemics. However, ingestion strongly reduced seedling survival of the exotic species, while having no negative effect on the survival of indigenous seedlings. Overall, ingested indigenous seeds were more likely to germinate and the seedlings more likely to survive than ingested exotic seeds and seedlings. Seed size, deposition density and the removal of fruit pulp by either manual depulping or gut passage were important predictors of germination time, germination percentage and seedling survival. Main conclusions These endemic frugivores can enhance the competitiveness of endemic compared with exotic fleshy fruited plants at the critical germination and seedling establishment stage. Consequently, conservation and restoration of mutualistic endemic plant–animal interactions may be vital to mitigating the degradation of habitats invaded by exotic plants, which is of particular relevance for island ecosystems in which large numbers of endemics are threatened by exotic invaders.     

五蕊寄生种子萌发特性

采用室内与野外实验相结合的方法,对五蕊寄生（Dendrophthoe pentandra）种子萌发特性以及鸟类消化过程对其种子萌发的影响进行研究。结果表明：五蕊寄生种子对温度和光照较敏感,与黑暗条件相比,光照能显著提高种子的萌发率;20℃为种子萌发的最适温度,萌发率达53.8%,高温35℃及低温10℃均不利于种子萌发。研究发现纯色啄花鸟（Dicaeum concolor）是该植物的主要食果者,种子外的果肉不是限制种子萌发的关键因素,人为去除果肉并不能提高种子的萌发率,但可缩短种子萌发的时间,果实通过纯色啄花鸟类肠道消化后,随着粪便排出的种子萌发率显著提高（达69%）,暗示纯色啄花鸟在五蕊寄生的种子萌发过程中具有重要的作用。