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。     

金属片标签法:一种有效追踪鼠类扩散种子的方法

金属片标签法是目前一种有效追踪鼠类搬运、贮藏和扩散种子的方法。这一方法能够准确了解每个种子的来源和去向,使定量研究种子扩散和种子命运变得更准确、有效。为全面了解金属片标签法的特点,本文介绍了该方法的操作过程,包括材料选择和准备、制作、野外操作以及在追踪种子过程中的有关注意事项。     

生境对啮齿动物介导下锐齿槲栎种子命运的影响

干扰作为森林演替的驱动力,在改变森林结构和地表植被的同时也对林内动物介导下的种子扩散过程产生影响.本研究采用塑料标签标记法,选取秦岭林区不同人为干扰后形成的3种类型生境(未抚育林分、抚育3年后林分、裸地),研究啮齿动物扩散行为对不同生境类型锐齿槲栎种子命运的响应.结果表明:抚育3年后林分的种子扩散速率最大,裸地扩散速率最小.裸地的种子原地取食率显著低于未抚育(25.0%)和抚育3年后林分(36.3%),而抚育3年后林分的种子搬运后取食率显著高于未抚育林分(17.3%)和裸地(5.0%),且抚育3年后的林分中被啮齿动物分散埋藏的种子比例最高(4.3%).种子扩散距离以抚育3年后林分最大(26 m),且扩散距离显著大于裸地和未抚育林分.锐齿槲栎种子的初次扩散过程在不同生境中表现不同,其种子后期成苗率也存在差异.不同类型生境在一定程度上影响啮齿动物的觅食策略,最终导致不同的种子扩散模式和森林天然更新格局的形成.     

啮齿动物对印度栲种子扩散的效率

从2007 年11 月到2009 年11 月,在西双版纳热带雨林中选取三棵母树,在每棵树下每年释放标记印度栲种子200 粒(三年共计1 800 粒),并追踪其命运。通过调查啮齿动物搬运和分散贮藏印度栲种子的比例,以及
查贮藏种子的微生境、贮藏点大小和扩散距离,分析贮藏种子的存活情况,进而评估啮齿动物对印度栲种子扩散的效率。结果表明,啮齿动物搬运了69.3% 的印度栲种子,被搬运的种子中18% 被分散贮藏。所有被分散贮藏的种子均被埋于落叶下或埋于土壤表层,并且大部分贮藏点仅含一粒种子。种子的扩散距离从0.5 m 到43.8 m,平均距离为7.1 m,扩散距离在年间没有显著差异。2007 年(种子密度低,啮齿动物密度高) 没有种能最终存活到实验结束,而2008 和2009 年(种子密度高,啮齿动物密度低)分别有0.3% 和1.5% 的种子存活。研究表明,啮齿动物是印度栲有效的种子扩散者,但其扩散效率很大程度上取决于森林中种子的密度和啮齿动物的丰富度。     

昆虫蛀蚀对鼠类介导下的锐齿槲栎种子扩散的影响

森林鼠类的种子贮藏行为对植物的扩散和自然更新有着非常重要的影响。然而,鼠类是否具有鉴别虫蛀种子的能力还存在一定的争议。此外,鼠类的鉴别能力是否受到食物丰富度变化的影响也未见相关报道。采用标签标记法,2011年秋季(9—11月,食物丰富季节)和2012年春季(4—6月,食物匮乏季节)分别在秦岭南坡的佛坪国家级自然保护区内,调查了森林鼠类对完好和虫蛀锐齿槲栎(Quercus aliena)种子的选择差异。结果显示:1)在秋季,尽管2种类型种子的存留动态没有显著差异,但是在后期虫蛀种子的存留时间相对更长;而在春季2种类型种子的存留动态则极为显著,几乎所有的完好种子(99%)在释放后的第3天就被鼠类全部扩散,虫蛀种子的存留时间则相对较长。2)在秋季,鼠类更喜好扩散后取食完好种子;而在春季,鼠类则喜好在原地取食绝大部分的种子,并且优先取食完好种子。3)在秋季,鼠类贮藏了更多的完好种子;而在春季,尽管完好种子在释放后第1天便达到贮藏高峰,然而由于后期的大量被捕食,2种类型种子在贮藏动态上没有显示出显著差异。研究结果表明秦岭地区森林鼠类可以准确区分完好与虫蛀种子,但是食物丰富度会影响鼠类对种子的选择策略。在食物丰富的秋季,鼠类更多地选择贮藏完好种子;而在食物相对匮乏的春季,鼠类更倾向于同时取食2种类型种子。森林鼠类通过对2种类型种子的鉴别和选择,影响不同种子的命运,从而可能对种子的扩散和自然更新产生重要影响。     

电荷耦合器件荧光成象研究膜上受体扩散

冷却慢扫描电荷耦合器件照相机附在荧光显微镜上组成了一个系统,可把一系列成象进行贮存,通过标记颗粒的位置,强度以及强度分布的差别,在每幅象上可区分５００个荧光点。荧光点的运动可以跟踪,通过分析可区分不同的运动方式。在人上皮成纤维细胞上跟踪观察了流感病毒受体在膜上的侧向扩散,实验结果表示在２４℃受体存在定向扩散、随机扩散和局部随机扩散三种运动方式。扩散系数Ｄ为１０－１２ｃｍ２ｓ－１的量级     

片段化景观中壳斗科植物种子捕食和扩散模式

生境片段化伴随的面积效应和边缘效应, 可改变分散贮食动物的竞争强度、觅食行为以及隐蔽条件, 影响种子捕食和扩散模式。阐明生境片段化对多物种种子捕食和扩散的影响, 对理解片段化生境中的植物更新和生物多样性维持十分重要。该研究在浙江省千岛湖地区的岛屿和大陆上开展了针对6种壳斗科植物的种子捕食和扩散实验, 分析了物种、分散贮食动物相对多度、种子产量、岛屿大小和边缘效应如何共同影响种子命运和种子扩散距离。主要结果: (1)种子命运和扩散距离在物种间存在显著差异; (2)大陆比岛屿有更长的种子留存时间, 小岛种子留存时间最短, 岛屿内部比岛屿边缘有更长的种子留存时间; (3)物种和岛屿大小对种子原地取食率存在交互作用, 白栎(Quercus fabri)种子在大岛上有更高的原地取食率; (4)种子在小岛上有最高的扩散率, 分散贮食动物相对多度对种子扩散后贮藏率有负效应。表明在千岛湖地区, 生境片段化改变了种子捕食和扩散模式, 且面积效应对不同物种的种子捕食和扩散模式产生了不同作用, 从而影响森林群落更新和生物多样性维持。     

浙江天童国家森林公园鼠类对石栎种子的捕食和传播

研究了浙江天童国家森林公园鼠类对石栎(Lithocarpus glaber)(常绿阔叶林重要伴生种)种子的捕食和传播.共设置了带1、带2、带3(常绿阔叶林中)、带4(马尾松林中)和带5(灌丛中)5条样带及2种种子的布置方式(有无掩盖和有无标签).结果表明,社鼠(Niviventer confucianus)和针毛鼠(Niviventer fulvescens)是石栎种子潜在的捕食和传播者.损失种子可以分为3类:即Ⅰ类种子被吃,标签连着种子的残余部分;Ⅱ类种子被搬走,仅标签留在原地;Ⅲ类是标签和种子均消失.实验观察前期,种子损失量较大,随后逐渐降低;种子的日消失率在整个实验期间具有明显的波动,带2的日均消失率最高,为1.03％,带5的日均消失率最低(0.32％).3种种子命运所占比例在5个样带中存在差异,与不同样带的植被组成密切相关.有掩盖和无掩盖放置方式之间存在显著差异(P<0.05),前者的日消失率明显低于后者,而有无标签之间则无显著性差异(P>0.05).种子被鼠类搬运的最远距离为6.7 m.     

啮齿动物对秦岭松栎混交林建群种种子扩散格局的影响

森林群落中的啮齿动物对林木种子存在着一定的取食偏好性,这种偏好性会使啮齿动物形成不同的捕食和贮藏策略,从而导致林木种子形成不同的扩散格局。以秦岭中段松栎混交林建群种锐齿槲栎、油松、华山松为研究对象,采用塑料标签标记种子方法,研究啮齿动物对种子传播和扩散格局的影响。结果表明:(1)种子特征是影响啮齿动物对其进行扩散的重要因子,油松种子以其质量小、种皮薄等特点吸引啮齿动物大量捕食,其原地取食率达到83.33%,显著高于华山松和锐齿槲栎种子。(2)锐齿槲栎和华山松种子大部分被搬运一定距离后再被取食和埋藏,其中,扩散距离在1 m以内、1—3 m和5—8 m的锐齿槲栎种子分别占59.12%、18.23%和13.26%,最远扩散距离达12 m处;华山松种子扩散距离主要介于在1—3 m(37.85%)和3—5 m(23.73%),在距离5—8 m(13.56%)、8—10 m(11.86%)和大于10 m(11.30%)区间也有一定的分布,最大扩散距离为12 m。(3)啮齿动物倾向于将锐齿槲栎种子搬运至松林内取食,而将华山松种子搬运至栎林内埋藏,说明不同林分类型及其环境因素对林木种子扩散后的分布格局具有重要影响。(4)3种类型种子被啮齿动物捕食的比例以油松最大(96.90%),锐齿槲栎次之(73.57%),华山松最小(50%);次年调查时,未被捕食的种子大部分已经被取食,仅有极少数锐齿槲栎种子萌发成幼苗(1.67%)。啮齿动物的捕食和贮藏行为对林木种子扩散及其成功更新都至关重要。     

不同干扰强度生境中啮齿动物对苦槠种子的取食和扩散

在浙江省千岛湖地区,选择了受人类活动干扰较轻、中度和严重的3个生境,采用金属片标记法研究了啮齿动物对苦槠种子的取食和扩散.结果表明:在研究点捕获的取食种子的啮齿动物为针毛鼠( Niviventer fulvescens),尽管捕获的数量少,但种子被取食和扩散的速率很快,3个样地内的种子均在2d内被取食或扩散完毕;中等干扰强度的生境中,被就地取食的种子最多,占鉴别种子总数的37.8%.种子扩散距离大多<5m,最大扩散距离为24.76m,3个样地种子扩散均符合负指数分布,且样地间没有显著差异;饱满种子与虫蛀种子被就地取食与搬运后取食的命运没有显著差异,但饱满种子的最大扩散距离均显著大于虫蛀种子(P<0.05),除中等干扰样地中饱满种子与虫蛀种子平均扩散距离没有显著差异外,其余2个样地中饱满种子的平均扩散距离均显著大于虫蛀种子,显示啮齿动物对饱满种子与虫蛀种子有一定的区分能力.     

Seed dispersal of Korean pine Pinus koraiensis labeled by two different tags in a northern temperate forest, northeast China

Two types of tagging methods, i.e., a 1 × 3-cm tin tag attached to seed with a 10- to 12-cm metal wire (total weight 0.32 g) and a 2 × 4-cm white plastic tag fastened to seed with an identical metal wire (total weight 0.57 g) were used to study their effects on seed dispersal of Korean pine by small rodents. A total of 600 seeds were released to assess four main points: (1) difference in seed survival rates, (2) difference in caching behaviors of small rodents, (3) difference in dispersal distances, and (4) proportion of seed missing. The results demonstrated that seed removal for wire-plastic-tagged seeds was faster than that for wire-tin-tagged seeds. There was no apparent difference in the proportion of seeds eaten in situ (42% and 52% for wire-plastic-tagged seeds and wire-tin-tagged seeds, respectively). We found 41% and 1% of seeds were moved and hoarded for wire-plastic-tagged seeds and wire-tin-tagged seeds, respectively. However, 2.33% and 14% of seeds were missing, and their ultimate fates were not known for wire-plastic-tagged seeds and wire-tin-tagged seeds, respectively. We found the wire-plastic-tagged seeds easier to track than the wire-tin-tagged seeds due to the fact that the white plastic tags were more salient than the tin tags in field environments. The average dispersal distances were 4.11 ± 2.40 m and 3.01 ± 2.06 m for wire-plastic-tagged seeds and wire-tin-tagged seeds, respectively, and showed great difference. Despite most being eaten in situ or after removal, 41% of seeds were cached for wire-plastic-tagged seeds, much more than for wire-tin-tagged seeds. A total of 71 primary caches (123 seeds) were found for wire-plastic-tagged seeds, with the average and maximum cache sizes being 1.73 and 6, respectively. However, only three caches were found, and cache size was equal to one for wire-tin-tagged seeds. The above data suggests there is some uncertainty in different tagging methods to used track seed fates. Despite their effectiveness in helping to trace seed dispersal or movement by seed-dispersing rodents, different tagging methods—including size, color, and mass—need to be fully understand in enclosure experiments .     

Primary Seed Dispersal by Red Howler Monkeys and the Effect of Defecation Patterns on the Fate of Dispersed Seeds1

The effectiveness of a seed disperser depends on the quantity and quality of dispersal. The quality of dispersal depends in large part on factors that affect the post–dispersal fate of seeds, and yet this aspect of dispersal quality is rarely assessed. In the particular case of seed dispersal through endozoochory, the defecation pattern produced has the potential of affecting the fate of dispersed seeds and consequently, dispersal quality and effectiveness. In this study, I assessed the effects of dung presence and dung/seed densities on seed predation by rodents and secondary dispersal by dung beetles. In particular, I compared seed fates in clumped defecation patterns, as those produced by howler monkeys, with seed fates in scattered defecation patterns, as those produced by other frugivores. I also determined the prevalence of red howler monkeys (Alouatta seniculus) as seed dispersers at the plant community level in Central Amazonia by determining the number of species they dispersed in a 25–month period. I found that dung presence and amount affected rodent and dung beetle behavior. Seed predation rates were higher when dung was present, and when it was in higher densities. The same number of seeds was buried by dung beedes, in dumped versus scattered defecation patterns, but more seeds were buried when they were inside large dung–piles versus small piles. Seed density had no effect on rodent or dung beetle behavior. Results indicate that caution should be taken when categorizing an animal as a high or low quality seed disperser before carefully examining the factors that affect the fate of dispersed seeds. Red howler monkeys dispersed the seeds of 137 species during the study period, which is the highest yet reported number for an Alouatta species, and should thus be considered highly prevalent seed dispersers at the plant community level in Central Amazonian terra firme rain forests.     

The choice of seed tracking method influenced fate of beech seeds dispersed by rodents

We tracked seeds of European beech (Fagus sylvatica) dispersed by rodents in Gorzowska Forest (western Poland). We used two seed labeling methods, marking with UV-fluorescent powder and with plastic tags, to test whether using different marking methods influences results of seed tracking. The removal rates did not differ among seeds marked with UV-powder, seeds labeled with tags, and unmanipulated seeds. We found 78 % of removed seeds marked with tags, but only 25 % of UV-marked seeds. The consumption rates of tagged and UV-marked seeds were dramatically different: rodents ate 83 % of the former and 26 % of the later. The average dispersal distance was larger for seeds marked with UV-powder than for tagged seeds. Our findings suggest that the choice of seed tracking method might influence results of seed dispersal studies.     

Fruit Removal and Natural Seed Dispersal of the Brazil Nut Tree (Bertholletia excelsa) in Central Amazonia,Brazil

Experimental approaches to study seed dispersal of the Brazil nut tree have hitherto relied on exposed seeds deposited on the forest floor. Here we use a new method to study the natural dispersal by large rodents such as agoutis; tracking experimentally manipulated and tagged fruits containing individually marked seeds. Fruit manipulation did not deter agoutis from handling fruits. We found that agoutis usually moved intact fruits away from their original location below the parent tree before either hiding them or gnawing through the pericarp to access the seeds inside. Most fruits were moved to distances of 15–30 m from their original position, but some fruits could be taken as far as 60 m. A large number of seeds extracted from manipulated fruits appeared to be eaten immediately. Only 27 out of 1740 experimental seeds were found buried in shallow caches, generally within 5 m of the opened fruit. Fruit removal distance accounted for a disproportionate amount of total seed movement and seeds in the current study were dispersed significantly farther than in a previous experiment using exposed seeds, suggesting that classic dispersal experiments of this character may severely underestimate seed dispersal distances. We therefore conclude that the new method provides a more realistic and accurate approach to investigate natural seed dispersal of Brazil nuts and that the removal of fruits from underneath parent trees before being opened is the key to the significantly increased distances at which seeds are dispersed. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

The effects of kernel mass and nutrition reward on seed dispersal of three tree species by small rodents

In the present study, colored tags were fastened to individual seeds to investigate seed dispersal and seed fates of Pinus koraiensis, Corylus mandshurica, and Corylus heterophylla with different seed traits. Our aim was to determine the role of the proportion of kernel mass, caloric reward per seed, and tag color in affecting seed removal rates and seed fates. We predicted that higher proportion of kernel mass and caloric reward will favor seed removal and caching, while lower ones will facilitate seed consumption either in situ or after removal. Our results showed that the proportion of kernel mass, rather than seed size, played an important role in determining seed removal rates and seed fates. Seeds of C. heterophylla with the lowest proportion of kernel mass, regardless of their largest size and/or mass, had lower removal rates, lower level of caching but higher proportion of consumption in situ compared with P. koraiensis and C. mandshurica seeds. Seeds with higher caloric reward exhibited greater dispersal distances. Seed kernel proportion was closely correlated to seed removal rates and caching rates, while seed size and hull thickness seemed to play less important role in affecting seed dispersal, probably because the higher seed handling ability of small rodents in the experimental areas. Our investigation revealed no significant effect of tag color on seed removal rates and seed fates of the three seed species.     

Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites

A long-standing challenge in studies of seed dispersal by animal frugivores has been the characterization of the spatial relationships between dispersed seeds and the maternal plants, i.e. the seed shadow. The difficulties to track unambiguously the origin of frugivore-dispersed seeds in natural communities has been considered an unavoidable limitation of the research field and precluded a robust analysis of the direct consequences of zoochory. Here we report that the multilocus genotype at simple sequence repeat (SSR; microsatellite) loci of the woody endocarp, a tissue of maternal origin, provides an unequivocal genetic fingerprint of the source tree. By comparing the endocarp genotype against the complete set of genotypes of reproductive trees in the population, we could unambiguously identify the source tree for 82.1% of the seeds collected in seed traps and hypothesize that the remaining 17.9% of sampled seeds come from other populations. Identification of the source tree for Prunus mahaleb seeds dispersed by frugivores revealed a marked heterogeneity in the genetic composition of the seed rain in different microhabitats, with a range of 1-5 distinct maternal trees contributing seeds to a particular landscape patch. Within-population dispersal distances ranged between 0 and 316 m, with up to 62% of the seeds delivered within 15 m of the source trees. Long distance dispersal events, detected by the exclusion of all reproductive trees in the population, accounted for up to 17.9% of the seeds sampled. Our results indicate strong distance limitation of seed delivery combined with infrequent long-distance dispersal events, extreme heterogeneity in the landscape pattern of genetic makeup, and a marked mosaic of multiple parentage for the seeds delivered to a particular patch.     

Tricky to track: comparing different tagging methods for tracing beechnut dispersal by small mammals

Seed hoarding animals may distinctly impact individual fitness of plants as well as plant community dynamics in terms of differential seed consumption and seed dispersal. Addressing methodological challenges and constraints in understanding the role of seed dispersal mutualisms, we tested different seed tagging methods for relatively small seeds. We selected two study areas with dense ground vegetation, irregular terrain, and seed predator guilds with comparatively high dispersal and seed removal potential. We tested three different tagging methods, offering untagged and tagged seeds on experimental dishes: (1) wire threads with plastic flags fixed with solvent-free glue, (2) wire threads with plastic flags twisted around a beechnut, (3) and radio-transmitters fixed with solvent-free glue. Seed predators did not show any preferences for tagged or untagged seeds or for a certain tagging method at any point of time. Instead, both tagged seeds and untagged control seeds were removed from the dishes to a high degree (up to 100%) after 25–35 days. In both study areas, seeds with radio-transmitters experienced longer transport distances with a maximum of nearly 60 m and distances also differed between study areas. In one study area, higher portions of radio-tagged seeds could be recovered than for the flag-tagged seeds. Significantly more seeds tagged with radio-transmitters were cached than expected. Given the advantages and limitations of each approach, a combination of flag-tagging and radio-telemetry (not on the same seed) may be the best solution for tracking seed fate in dense vegetation or irregular terrain.     

Early fate of Myristica hypargyraea seeds dispersed by Ducula pacifica in Tonga,Western Polynesia

Abstract Although pigeons from the genus Ducula are considered among the best avian dispersers of large seeds in Asia and the Pacific, little has been documented on their role. The early fate of dispersed and undispersed seeds of the large‐seeded tree Myristica hypargyraea A. Gray was studied in order to understand the advantage of seed dispersal by the Pacific Pigeon, Ducula pacifica Gmelin in Tonga. Frequency of visits by frugivores to fruiting trees and dispersal distance of seeds were measured. Pre‐dispersal vertebrate seed predation was assessed, then post‐dispersal predation was measured over 160 days. Overall, pre‐dispersal seed predation by parrots was low but variable among trees sampled. Most seeds (54.7%) in the study area were estimated to be dispersed by D. pacifica; 79.7% of those ingested were expelled directly beneath conspecific fruiting crowns, 20% were dispersed locally and < 0.3% were dispersed more than 300 m into a different forest type. Flying foxes (Pteropus tonganus Quoy and Gaimard) dispersed very few seeds (0.7%) and all were dropped below fruiting crowns. Between 4% and 39% of dispersed and undispersed seeds were still viable, or had established seedlings after 160 days. Most seeds had been removed or killed by rats, and seed survival was highest for locally dispersed seeds (approx. 20 m from source trees and within the M. hypargyraea forest). Although D. pacifica was the only frugivore observed to disperse seeds into this higher zone of survival, overall they did not confer a great advantage to seed survival since significant numbers of seeds/seedlings also persisted under fruiting crowns (27% under crowns compared with 39% locally dispersed). Nevertheless, D. pacifica was the only vector by which seeds were regularly moved within the M. hypargyraea forest and over longer distances, and hence, D. pacifica still plays a significant role in the regeneration of M. hypargyraea.     

Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest

In Neotropical forests, mammals act as seed dispersers and predators. To prevent seed predation and promote dispersal, seeds exhibit physical or chemical defenses. Collared peccaries (Pecari tajacu) cannot eat some hard seeds, but can digest chemically defended seeds. Central American agoutis (Dasyprocta punctata) gnaw through hard‐walled seeds, but cannot consume chemically defended seeds. The objectives of this study were to determine relative peccary and agouti abundances within a lowland forest in Costa Rica and to assess how these two mammals affect the survival of large seeds that have no defenses (Iriartea deltoidea, Socratea exorrhiza), physical defenses (Astrocaryum alatum, Dipteryx panamensis), or chemical defenses (Mucuna holtonii) against seed predators. Mammal abundances were determined over 3 yrs from open‐access motion‐detecting camera trap photos. Using semi‐permeable mammal exclosures and thread‐marked seeds, predation and dispersal by mammals for each seed species were quantified. Abundances of peccaries were up to six times higher than those of agoutis over 3 yrs, but neither peccary nor agouti abundances differed across years. Seeds of A. alatum were predominantly dispersed by peccaries, which did not eat A. alatum seeds, whereas non‐defended and chemically defended seeds suffered high levels of predation, mostly by peccaries. Agoutis did not eat M. holtonii seeds. Peccaries and agoutis did not differ in the distances they dispersed seeds. This study shows that seed fates are contingent upon many factors such as seed defenses, frugivore–granivore abundances, and seed‐handling capabilities. Mammal–seed interactions are complex; the outcomes of these interactions depend on the inherent characteristics of seeds and their potential dispersers.