Dispersal of remnant endangered trees in a fragmented and disturbed forest by frugivorous birds

Most endangered plant species in a fragmented forest behave as a unique source population, with a high dependence on frugivorous birds for recruitment and persistence. In this study, we combined field data of dispersal behavior of birds and GIS information of patch attributes to estimate how frugivorous birds could affect the effective dispersal pattern of Chinese yew (Taxus chinensis) in a fragmented and disturbed forest. Nine bird species were observed to visit T. chinensis trees, with Urocissa erythrorhyncha, Zoothera dauma and Picus canus being the most common dispersers. After foraging, six disperser species exhibited different perching patterns. Three specialist species, P. canus, Turdus hortulorum, and Z. dauma stayed in the source patch, while three generalist species, U. erythrorhyncha, Hypsipetes mcclellandii, and H. castanonotus, could perch in bamboo patches and varied in movement ability due to body size. As a consequence of perching, dispersers significantly contributed to the seed bank, but indirectly affected seedling recruitment. Moreover, the recruitment of T. chinensis was also affected by patch attributes in a fragmented forest (distances to source patch, patch type, size). Our results highlighted the ability of unique source population regeneration of T. chinensis in a fragmented forest, with high dependence on both frugivorous birds and patch attributes, which should be considered in future planning for forest management and conservation.     

Consistency and reciprocity of indirect interactions between tree species mediated by frugivorous birds

Despite the recognized importance of indirect plant–plant interactions for community structure, we still need to improve our current knowledge on how their outcomes are consistent in space and time, as well as reciprocal between participating species. These caveats are especially relevant in the case of indirect interactions mediated by animals, whose behavior may show high variability. We studied consistency and reciprocity of frugivore‐mediated interactions between fleshy‐fruited trees. For three years we examined the influence of crop size and neighborhood characteristics (con‐ and heterospecific fruit abundance and forest cover) on frugivory rates on Crataegus monogyna and Ilex aquifolium, two coexisting species in the secondary forests of the Cantabrian range that share a guild of frugivorous birds. Crop size and neighborhood characteristics influenced frugivory on C. monogyna and I. aquifolium. Both con‐ and heterospecific fruit abundance affected frugivory, evidencing the occurrence of indirect interactions between trees, although the strength and sign of these effects varied between tree species as well as across years within species. By showing complex temporal patterns in the consistency and reciprocity of indirect interactions, this study emphasizes the need for multispecific, long‐term studies to assess the actual contribution of animal‐mediated plant–plant indirect interactions to community dynamics.     

西双版纳食果鸟对植物果实颜色的取食选择

黑色和红色是最主要的果实颜色.虽然食果鸟的取食选择常被假设为果实颜色特征形成的主要进化动力,但能直接支持该假说的研究案例极少.该研究选择西双版纳常见的5种食果鸟,利用试验当季常见的黑、红、黄、绿4种果实进行室内和野外环境(开阔林地、林冠下层)果实颜色选择实验.结果表明,室内试验时5种食果鸟最喜欢的果实颜色是黑色和/或红色,而野外环境下,虽然开阔林地果实被取食总量远大于林冠下层果实被取食量,但黑色和红色仍均为该两类生境中被取食最多的果实颜色.即大部分食果鸟均喜好自然界最常见的果实颜色,其喜好程度能反映研究地果实颜色组成分布格局,提示果实颜色的进化或部分来自于食果鸟取食选择的压力.     

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     

Resource selection by tropical frugivorous birds: integrating multiple interactions

Summary Resource selection is a function of interactions of organisms (competition, predation) as well as characteristics of the resource and organisms. I provide a quantitative model that integrates these factors. I use the model to predict profitability of fruits to tropical birds, but the model and its predictions are applicable to a wider array of systems and organisms. Profitability of a fruit is determined by rewards provided by the pericarp (mass and caloric yields) relative to costs (metabolic requirements, handling time, search time, behavioral interference, predator avoidance) associated with finding and eating that fruit (Fig. 1). Fruits increase in profitability with increases in fruit size until increases in handling time offset increases in pericarp mass. The fruit size at which increases in handling time offset increases in pericarp mass varies among bird species due to differences in bill and body size. Decreases in feeding rate due to decreasing numbers of fruits and increasing search time causes reduced profitability and this effect becomes more severe with decreasing fruit size and/or increasing frugivore size. Consequently, as fruit size decreases relative to frugivore size, fruit abundance becomes increasingly important to fruit selection by frugivores. However, while profitability of resources is a function of characteristics of the resources and the organisms, biological interactions can change profitability rankings; resources that may be more profitable in the absence of behavioral interference, exploitation competition, or predation risk can become less profitable in the face of these interactions. The proposed model integrates these interactions to provide predictions of resource selection and these predictions are supported by published studies.     

鸟类和蚂蚁对桃金娘种子传播的初步研究

在中国科学院鹤山丘陵综合开放试验站观察研究了鸟类和蚂蚁对桃金娘 (Rhodomyrtustomentosa)种子的传播。据野外观察和网捕法所捕鸟的情况可知 :红耳鹎 (Pycnonotusjocosus)和白头鹎 (P .sinensis)两种鸟传播桃金娘种子 ,白头鹎比红耳鹎的数量多。在网捕到的红耳鹎和白头鹎的粪便中收集到的桃金娘种子分别为 8.0± 3.0粒/只和 10 .0± 2 .0粒 /只。在显微镜下观察经过鸟消化道的桃金娘种子都没有破损。传播桃金娘种子的蚂蚁有全异巨首蚁 (Pheidologetiondiversus)和梅花山大头蚁 (Pheidolemeihuashanensis)。它们传播的最远距离分别为 4m和 5m ,平均为 1.1± 0 .0 9m和 1.3± 0 .0 7m。全异巨首蚁占样地蚂蚁个体总数的 6 0 .0 % ;梅花山大头蚁占个体总数的8.1% ;余下的为其他种蚂蚁。每个全异巨首蚁蚁巢平均贮藏桃金娘种子 195 .0± 82 .9粒 ,其中 73.2 %是完好种子。每个梅花山大头蚁蚁巢平均贮藏 2 8.8± 11.4粒种子 ,全部是完好种子。林窗、闲置的空旷地、植物群落交错带都有桃金娘实生苗。在阳光充足的全异巨首蚁和梅花山大头蚁蚁巢边也有桃金娘实生苗的存在     

Dietary specialization and fruit availability among frugivorous birds on Sulawesi

Over 20 months I collected data on the diet composition and fruit availability for 23 frugivorous bird species (pigeons, parrots, hornbills and passerines) in two lowland rain forests on Sulawesi, Indonesia. Using these data I determined species dependency on fruit, diet composition, diet breadth and the availability of their fruit resources. Fruit dependency ranged from 44 to 100% of diets across the assemblage, with significant inter-order differences reflecting shared evolutionary history within orders. By contrast, diet breadths did not differ between bird orders owing to high within-order variability, possibly as a result of species-specific foraging strategies. Overall, no significant relationship existed between fruit dependency and diet breadth, which indicated that they are not interchangeable measures of dietary specialization, but that each provided important information on dietary specialization, and enabled assessment of resource requirements and availability. The assemblage consumed the fruits of 120 species representing 40 plant families. Figs ( Ficus spp.) were of great importance across the assemblage and comprised 57% of all fruit-eating records. For hornbills, passerines and pigeons, figs accounted for substantial proportions of monthly feeding records (= 58%) and were consumed whatever the availability of other fruits. Figs were therefore a fundamental part of species' diets, possibly every month, and not merely important during times of relative scarcity of other fruit. Conservation of fig trees both inside and outside protected areas is likely to be important in maintaining healthy populations of figs and the frugivorous birds that depend on them.     

食果动物传播种子的跟踪技术

研究食果动物传播种子的主要问题之一是难以跟踪种子命运和估计种子域。到目前为止,已有不少方法用于研究食果动物与种子扩散和种子命运的关系,如直接观察法、同位素标记法、金属标记法、磁铁标记法、荧光染料法、微粒体标记法、线标法和遗传技术等。近年来,一些研究将数字编号用于种子标记,并已成为发展的主流。本文综述了以往跟踪种子命运和估计种子域的一些重要方法,并讨论了它们各自的优缺点及其应用。     

南方红豆杉的天然更新格局及食果鸟类对其种子的传播

2006年9-12月,在皖南仙寓山对南方红豆杉(Taxus chinensis var.mairei)天然更新种群的分布格局及食果鸟类对其种子的传播作用进行了研究.结果表明:天然更新种群集中分布于仙寓山海拔540 m以上面积约1.1 hm2的山坡上,与毛竹混生.共统计红豆杉1 331株,其中高度30 cm以下的幼苗1 167株,占总数的87.68%.该红豆杉种群为缓慢增长型种群,空间水平格局呈聚集分布.经过对结实母树的定点连续观察,记录到10种鸟类取食红豆杉种子,其中红嘴蓝鹊(Urocissa erythrorhyncha)、栗背短脚鹎(Hemixos castanonotus)和绿翅短脚鹎(Hypsipetes mcclellandii)为主要的取食者和传播者.食果鸟类吞入种子后,消化果肉(假种皮)后,种子随粪便排出而得以传播.野外调查中,在鸟类经常活动的地点发现带有红豆杉种子新鲜的鸟类粪便,每个含有1～2颗种子.未被鸟类取食的落果自然掉落于树冠下,假种皮被昆虫取食或腐烂,种子在母树下能正常萌发,但存活率几乎为零.因此,鸟类在该红豆杉天然种群形成中起到了重要作用,它们将种子传播至适宜萌发和生长的环境中.     

Landscape‐level tree cover predicts species richness of large‐bodied frugivorous birds in forest fragments

Large‐bodied frugivorous birds play an important role in dispersing large‐sized seeds in Neotropical rain forests, thereby maintaining tree species richness and diversity. Conversion of contiguous forest land to forest fragments is thought to be driving population declines in large‐bodied frugivores, but the mechanistic drivers of this decline remain poorly understood. To assess the importance of fragment‐level versus local landscape attributes in influencing the species richness of large‐bodied (>100 g) frugivorous birds, we surveyed 15 focal species in 22 forest fragments (2.7 to 33.6 ha, avg. = 16.0 ha) in northwest Ecuador in 2014. Fragment habitat variables included density of large trees, canopy openness and height, and fragment size; landscape variables included elevation and the proportion of tree cover within a 1 km radius of each fragment. At both the individual species level, and across the community of 12 species of avian frugivore we detected, there was higher richness and probability of presence in fragments with more tree cover on surrounding land. This tendency was particularly pronounced among some endangered species. These findings corroborate the idea that partially forested land surrounding fragments may effectively increase the suitable habitat for forest‐dwelling frugivorous birds in fragmented landscapes. These results can help guide conservation priorities within fragmented landscapes, with particular reference to retaining trees and reforesting to attain high levels of tree cover in areas between forest patches.     

Granivory rates by rodents, insects, and birds at different microsites in the Patagonian steppe

We studied the rates of seed removal by different granivores, in different microsites, at different times, in a Patagonian shrub steppe in South America. Granivory rates of exotic ( Phalaris canariensis ) and native ( Mulinum spinosum ) seed species were an order of magnitude lower than those reported for another cool desert from North America with comparable climatic conditions. Insects and rodents removed the greatest amount of seeds in comparison to birds. In general, there were no differences in seed removal across microsites, except at one sampling time (when rodents and insects removed more seeds from bare soil and beside tussocks in comparison to positions beside shrubs, while birds took similar amounts of seeds from all microsites). The length of the experiment differentially affected the granivory rate of different groups. Removal rates (per day) were significantly greater, and exhibited lower variability, when seeds were left for a longer period of time in the field (a month) than for a few days. Insects were more efficient at finding the seeds rapidly and rodents at depleting them; birds could not find or deplete many seeds in short periods of time. Rates of granivory decreased slightly but significantly as the summer progressed mainly due to a reduction of seed removal by birds and rodents but not by insects. Granivores removed an order of magnitude less native seeds than exotic seeds. These differences seemed to be related to palatability as M. spinosum seeds have more phenols, toxic concentrations of iron and copper, and lower dry matter digestibility, phosphorous, and nitrogen content, in comparison to P. canariensis seeds.     

The role of frugivorous bats in tropical forest succession

Discussion of successional change has traditionally focused on plants. The role of animals in producing and responding to successional change has received far less attention. Dispersal of plant propagules by animals is a fundamental part of successional change in the tropics. Here we review the role played by frugivorous bats in successional change in tropical forests. We explore the similarities and differences of this ecological service provided by New and Old World seed-dispersing bats and conclude with a discussion of their current economic and conservation implications. Our review suggests that frugivorous New World phyllostomid bats play a more important role in early plant succession than their Old World pteropodid counterparts. We propose that phyllostomid bats have shared a long evolutionary history with small-seeded early successional shrubs and treelets while pteropodid bats are principally dispersers of the seeds of later successional canopy fruits. When species of figs (Ficus) are involved in the early stages of primary succession (e.g. in the river meander system in Amazonia and on Krakatau, Indonesia), both groups of bats are important contributors of propagules. Because they disperse and sometimes pollinate canopy trees, pteropodid bats have a considerable impact on the economic value of Old World tropical forests; phyllostomid bats appear to make a more modest direct contribution to the economic value of New World tropical forests. Nonetheless, because they critically influence forest regeneration, phyllostomid bats make an important indirect contribution to the economic value of these forests. Overall, fruit-eating bats play important roles in forest regeneration throughout the tropics, making their conservation highly desirable.     

Diversity of seeds captured by interception exceeds diversity of seeds deposited in traps

Seed dispersal, a key process in terrestrial landscapes, is increasingly important in the face of habitat fragmentation and global climate change. Seed dispersal is also notoriously difficult to characterize, especially in species rich and spatially complex tropical forests. We contrasted assemblages of biotically dispersed seeds collected from four sites using two methods: deposition into seed traps and interception by the capture of frugivorous birds. We also compared seed deposition and interception with local fruit production. Species accumulation curves for seeds deposited in seed traps began to level off sooner than curves for seeds collected from birds captured in mist nets, and extrapolation showed significantly greater estimated species richness for seeds collected from birds than for those deposited in traps. Assemblages from birds and from traps at each site were quite different, with an abundance‐based similarity index of 0.64; this dissimilarity increases if bat‐dispersed seeds are included in the analysis. Common bird‐dispersed species were retrieved from both mist‐netted birds and from seed traps, but numerous locally fruiting understory species were recovered only from birds. We conclude that the sampling of seeds carried by birds provides a valuable complement to other methods of studying seed dispersal in species‐rich tropical forests by revealing relationships between specific dispersers and their seed plants and by creating a more complete account of species diversity of seeds being transported at a given site.     

Two-phase seed dispersal: linking the effects of frugivorous birds and seed-caching rodents

Frugivorous birds disperse the seeds of many fruit-bearing plants, but the fate of seeds after defecation or regurgitation is often unknown. Some rodents gather and scatter hoard seeds, and some of these may be overlooked, germinate, and establish plants. We show that these two disparate modes of seed dispersal are linked in some plants. Rodents removed large (>25 mg) seeds from simulated bird feces (pseudofeces) at rates of 8–50%/day and scatter hoarded them in soil. Ants (Formica sibylla) also harvested some seeds and carried them to their nests. Rodents carried seeds 2.5±3.2 m to cache sites (maximum 12 m) and buried seeds at 8±7 mm depth. Enclosure studies suggest that yellow pine chipmunks (Tamias amoenus) and deer mice (Peromyscus maniculatus) made the caches. In spring, some seeds germinated from rodent caches and established seedlings, but no seedlings established directly from pseudofeces. This form of two-phase seed dispersal is important because each phase offers different benefits to plants. Frugivory by birds permits relatively long-range dispersal and potential colonization of new sites, whereas rodent caching moves seeds from exposed, low-quality sites (bird feces on the ground surface) to a soil environment that may help maintain seed viability and promote successful seedling establishment.     

A preliminary assessment of congruence between biodiversity patterns in Afrotropical forest birds and forest mammals

Burgess, N., de Klerk, H., Fjeldsá, J., Crowe, T. & Rahbek, R. 2000. A preliminary assessment of congruence between biodiversity patterns in Afrotropical forest birds and forest mammals. Ostrich 71 (1 & 2): 286–291.

Databases compiled for forest birds and forest mammals in the Afrotropics were tested for congruence of overall patterns and hotspots of species richness and endemism. We also looked at how well a near-minimum set of priority areas for one taxon catered for the second taxon. Overall species richness and richness hotspots of forest birds were significantly correlated with those of forest mammals, as was the case for overall endemism. Endemism hotspots for forest birds and mammals were not significantly correlated. The near-minimum set for forest birds represented 136 (76.5%) forest mammal species. The near-minimum set for forest mammals represented 350 (93.62%) forest bird species. However, to represent all forest mammals three times each, 51 grids were needed in addition to the 78 chosen as a near-minimum set for forest birds, and to represent all forest birds three times each, 43 more grids were needed in addition to the 80 selected for forest mammals. There is some congruence between the patterns of richness, endemism and near-minimum sets for forest birds and mammals in the Afrotropics, but the one taxon does not provide the ideal conservation solution for the other. Further refinement of the databases used in this paper would allow for more rigorous testing of congruence between these two groups.     

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.     

南京中山植物园秋冬季鸟类对植物种子的传播作用

1999年10月20日－2000年1月20日,在南京中山植物园内随机收集鸟粪样品160份,共分离出874粒结构完整的种子和果核、3块鞘翅目昆虫残体和1块鸟类羽毛残块。已鉴定出842粒种子和果核,分属于16科20属26种（变种）。在鸟粪样品中出现频率较高的种子依次分别属于冬青（Ilex purpurea)(22.22%)、圆柏（Sabina chinensis)(11.11%)、盐肤木（Rhus chinensis)(10.63%)、朴树（Celtis sinensis)(9．18％）、爬山虎（Parthenocissus tricuspidata)(7.73%)、龙柏（S.chinensis cv.kaizuca)(7.25%)等;种子数量相对较多的植物种类主要有冬青（23．52％）、盐肤木（16．15％）、圆柏（13．54％）、爬山虎（7．96％）、龙柏（7．96％）、小果蔷薇（Rosa cymosa)(5.34%)等。除经鸟粪传播外,鸟类还通过衔取果实以及在吞食果实后将种子呕出的方式传播种子。初步发芽试验表明,鸟粪样品中的爬山虎、盐肤木的种子,以及被鸟呕出的樟树（Cinnamomum camphora)、楝树（Melia azedarach)的种子均可发芽出苗。鸟类传播种子使南京中山植物园内樟树、冬青、海桐（Pittosporum tobira)和红豆杉（Taxus chinensis)等栽培树种成功地侵入到位于植物园北缘的虎山山坡黑松（Pinus thunbergii)、枫香（Liquidambar formosana)群落、以及植物园内山溪边的枫杨（Pterocarya stenoptera)、朴树群落等生境中。鸟类对种子的传播作用扩大了南京中山植物园内那些具有肉质果实、种子具有坚硬种皮或种子包被于坚硬果核中的植物种类的分布范围,促进了它们的自然更新。     

Landscape-dependent response to predation risk by forest birds

Knowing how forest loss and associated fragmentation actually impact individual birds is essential to our understanding of consequences at the population level. We conducted a landscape-level experiment to test whether deforestation affects the trade-off between foraging and antipredatory behaviour of black-capped chickadees ( Poecile atricapilla ) in 24 landscapes (range 8–88% forest cover, 500-m radius) during two winters. At a field-forest edge in the centre of each landscape, we used the maximum distance ventured into the open by flocks to get sunflower seeds placed on the snow-covered fields, as a measure of risk-taking. In the more deforested landscapes, chickadees ventured farther (up to the maximum of 40 m) into the open. Edge density and proportion of conifers in the forest had no influence on risk-taking. However, where ad libitum food was available for a few weeks prior to the experiment (in 12 of the 24 landscapes), chickadees ventured four meters or less away from the forest edge, regardless of the level of deforestation. We conclude that landscape deforestation increases energy stress, which in turn promotes risk-taking, and may therefore increase winter mortality through greater exposure to predators.     

食果鸟类在红豆杉天然种群形成中的作用

2005年10月初至2006年2月,在南京中山植物园研究了红豆杉(Taxus chinensis)天然更新种群的分布格局,野外定点观察了鸟类对红豆杉种子的取食行为,记录了红豆杉落果的命运,分析了食果鸟类在红豆杉种群形成中的作用。结果表明:红豆杉天然更新种群集中分布于距母树群10m以外面积约0.5hm2的山坡上,全部红豆杉幼苗、幼树共213株,主要分布在中下坡;幼苗和幼树的空间水平格局符合聚集分布特征。"果实"成熟后,一部分被鸟类直接在树上取食,一部分掉落母树下地面。经过对结实母树的定点、连续观察,记录到4种鸟类取食红豆杉"果实",其中红嘴蓝鹊(Urocissa erythrorhyncha)和白头鹎(Pyc-nonotus sinensis)为主要的取食者和传播者。食果鸟类整吞"果实",消化果肉(假种皮)后,种子经消化道随粪便排出,以此过程传播种子。在取食完红豆杉"果实"后,食果鸟类多飞向坡上。坡上排水良好,有适量的荫蔽,生境适宜红豆杉种子萌发和幼苗的成长。因此,食果鸟类将种子传播至适宜萌发和生长的环境中,对该红豆杉种群的天然更新起主要作用。同时,鸟类传播对于红豆杉种群扩散、占据新的生境也有着特殊的意义。