Beta Diversity of Plant-Pollinator Networks and the Spatial Turnover of Pairwise Interactions

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

Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape

Mediterranean landscapes comprise a complex mosaic of different habitats that vary in the diversity of their floral communities, pollinator communities and pollination services. Using the Greek Island of Lesvos as a model system, we assess the biodiversity value of six common habitats and measure ecosystemic 'health' using pollen grain deposition in three core flowering plants as a measure of pollination services. Three fire-driven habitats were assessed: freshly burnt areas, fully regenerated pine forests and intermediate age scrub; in addition we examined oak woodlands, actively managed olive groves and groves that had been abandoned from agriculture. Oak woodlands, pine forests and managed olive groves had the highest diversity of bees. The habitat characteristics responsible for structuring bee communities were: floral diversity, floral abundance, nectar energy availability and the variety of nectar resources present. Pollination services in two of our plant species, which were pollinated by a limited sub-set of the pollinator community, indicated that pollination levels were highest in the burnt and mature pine habitats. The third species, which was open to all flower visitors, indicated that oak woodlands had the highest levels of pollination from generalist species. Pollination was always more effective in managed olive groves than in abandoned groves. However, the two most common species of bee, the honeybee and a bumblebee, were not the primary pollinators within these habitats. We conclude that the three habitats of greatest overall value for plant-pollinator communities and provision of the healthiest pollination services are pine forests, oak woodland and managed olive groves. We indicate how the highest value habitats may be maintained in a complex landscape to safeguard and enhance pollination function within these habitats and potentially in adjoining agricultural areas. (c) 2005 Elsevier Ltd. All rights reserved.

Response of plant-pollinator communities to fire: changes in diversity, abundance and floral reward structure

Globally, plant-pollinator communities are subject to a diverse array of perturbations and in many temperate and semi-arid systems fire is a dominant structuring force. We present a novel and highly integrated approach, which quantifies, in parallel, the response to fire of pollinator communities, floral communities and floral reward structure. Mt Carmel, Israel is a recognised bee-flower biodiversity hotspot, and using a chronosequence of habitats with differing post-fire ages, we follow the changes in plant-pollinator community organisation from immediately following a burn until full regeneration of vegetation. Initially, fire has a catastrophic effect on these communities, however, recovery is rapid with a peak in diversity of both flowers and bees in the first 2 years post-fire, followed by a steady decline over the next 50 years. The regeneration of floral communities is closely matched by that of their principal pollinators. At the community level we quantify, per unit area of habitat, key parameters of nectar and pollen forage known to be of importance in structuring pollinator communities. Nectar Volume, nectar water content, nectar concentration and the diversity of nectar foraging niches are all greatest immediately following fire with a steady decrease as regeneration proceeds. Temporal changes in energy availability for nectar, pollen, total energy (nectar + pollen) and relative importance of pollen to nectar energy show a similar general decline with site age, however, the pattern is less clear owing to the highly patchy distribution of floral resources. Changes in floral reward structure reflect the general shift from annuals (generally low-reward open access flowers) to perennials (mostly high-reward and restricted access flowers) as post-fire regeneration ensues. The impact of fire on floral communities and their associated rewards have clear implications for pollinator community structure and we discuss this and the role of other disturbance factors on these systems.

The effects of cattle grazing on plant-pollinator communities in a fragmented Mediterranean landscape

The main aims of this study were to assess grazing impacts on bee communities in fragmented mediterranean shrubland (phrygana) and woodland habitats that also experience frequent wildfires, and to explain the mechanisms by which these impacts occur. Fieldwork was carried out in 1999 and 2000 on Mount Carmel, in northern Israel, a known hot-spot for bee diversity. Habitats with a range of post-burn ages and varying intensities of cattle grazing were surveyed by transect recording, grazing levels, and the diversity and abundance of both flowers and bees were measured. The species richness of both bees and flowers were highest at moderate to high grazing intensities, and path-analysis indicated that the effects of both grazing and fire on bee diversity were mediated mainly through changes in flower diversity, herb flowers being more important than shrubs. The abundance of bees increased with intensified grazing pressure even at the highest levels surveyed. Surprisingly though, changes in bee abundance at high grazing levels were not caused directly by changes in flower cover. The variation in bee abundance may have been due to higher numbers of solitary bees from the family Halictidae in grazed sites, where compacted ground (nesting resource) and composites (forage resource) were abundant. The effects of grazing on plants were clearest in the intermediate-aged sites, where cattle inhibited the growth of some of the dominant shrubs, creating or maintaining more open patches where light-demanding herbs could grow, thus allowing a diverse flora to develop. Overall, bee communities benefit from a relatively high level of grazing in phrygana. Although bee and flower diversity may decrease under very heavy grazing, the present levels of grazing on Mount Carmel appear to have only beneficial effects on the bee community.

Natural history of an ant-plant-butterfly interaction in a Neotropical savanna

Non-myrmecophilous lepidopteran larvae using plants bearing ant attractants such as extrafloral nectaries are good models for studying morphological and behavioural mechanisms against ant predation. Udranomia spitzi (Hesperiidae) is a butterfly whose larvae feed on leaves of Ouratea spectabilis (Ochnaceae), a plant with extrafloral nectaries. We described the early stages of U. spitzi, and used field observations and experiments to investigate the defensive strategies of caterpillars against predatory ants. Larvae pass through five instars and pupation occurs inside larval leaf shelters. Ant-exclusion experiments revealed that the presence of ants did not affect significantly caterpillar survival. Predation experiments showed that vulnerability to ant predation decreased with increase in larval size. The present study showed that predatory ants are not as relevant as demonstrated for other systems, and also illustrates how observational data and field experiments can contribute to a better understanding of the biology and ecology of a species of interest.

Where Is My Food? Brazilian Flower Fly Steals Prey from Carnivorous Sundews in a Newly Discovered Plant-Animal Interaction

A new interaction between insects and carnivorous plants is reported from Brazil. Larvae of the predatory flower fly Toxomerus basalis (Diptera: Syrphidae: Syrphinae) have been found scavenging on the sticky leaves of several carnivorous sundew species (Drosera, Droseraceae) in Minas Gerais and São Paulo states, SE Brazil. This syrphid apparently spends its whole larval stage feeding on prey trapped by Drosera leaves. The nature of this plant-animal relationship is discussed, as well as the Drosera species involved, and locations where T. basalis was observed. 180 years after the discovery of this flower fly species, its biology now has been revealed. This is (1) the first record of kleptoparasitism in the Syrphidae, (2) a new larval feeding mode for this family, and (3) the first report of a dipteran that shows a kleptoparasitic relationship with a carnivorous plant with adhesive flypaper traps. The first descriptions of the third instar larva and puparium of T. basalis based on Scanning Electron Microscope analysis are provided.

Plant connectivity underlies plant-pollinator-exploiter distributions in Ficus petiolaris and associated pollinating and non-pollinating fig wasps

Peer reviewed

独花兰和扇脉杓兰的传粉生态学

兰科植物精巧的花部结构及其独特的传粉机制为自然选择理论和异花受粉优势学说提供了强有力的证据。开展兰科植物的传粉生态学研究对进一步探讨植物进化中的一些关键问题（如生殖隔离、物种形成、适应和繁育系统进化等）具有重要意义。本文通过对独花兰 (Changnienia amoena) 和扇脉杓兰 (Cypripedium japonicum) 两种兰科植物进行植物与传粉者之间关系、种内形态变异、花粉散布等方面的研究，探讨其适应进化方式、传粉系统的进化趋势，同时为开发适用的分子标记，在独花兰中初步摸索和探讨了微卫星标记的分离。主要研究结果如下： 1. 濒危植物独花兰的传粉生态学 在神农架2个地点进行了连续2年的野外观测和实验。结果表明，独花兰是一种自交亲和、需要昆虫传粉的欺骗性植物。在2个地点独花兰的传粉者种类不同，在龙门河三条熊蜂 (Bombus (Diversobombus) trifasciatus) 是主要传粉者，在关门山仿熊蜂 (B. (Tricornibombus) imitator) 是唯一的传粉者。尽管它们出现的丰度和觅食行为不同，但其传粉行为和携粉部位非常相同，因此，可以看作是一个功能群（functional group）。从种群水平上看，开花个体的分布式样不是显著的偏斜曲线图，传粉者的有效访问主要集中在开花的前、中期。由于没有花蜜，传粉者在花内停留的时间很短，花粉块输出和传粉发生在熊蜂劳而无获的访问、退出花时。自然条件下，独花兰的结实率很低，只有6%-12%，并呈现明显的年份和地点变化。传粉者限制是结实率低的主要原因。与同亚族近缘种布袋兰相比，分布于中国中部的独花兰受冰期的影响很小，其传粉环境相对稳定，在进化历史中，形成了一种稳定的传粉系统。本研究结果纠正了前人对独花兰繁殖方式的错误认识，并为其保护策略的制订提供了重要资料。 2. 独花兰种群大小、传粉者访问和花粉流 为了检验独花兰种群大小、空间格局与传粉者访问之间的关系，连续2年对10个独花兰种群的花粉块输出和输入进行了统计分析，同时对花粉块进行标记研究其散布式样。结果显示，花粉块输出比例与种群大小之间关系在2003年呈显著负相关，但在2004年这种负相关关系不显著。尽管独花兰的空间分布格局在不同种群不同，但传粉者的访问除了在有蜂巢的种群为聚集式访问外，其余种群内均为随机访问式样。花粉块的散布式样呈尖峰态分布，多数花粉块散布很短的距离，少数散布较远。花粉块的平均散布距离在龙门河为7.3 m，在关门山为10.6 m。由于各种群之间相隔很远，种群之间花粉块交流受到限制，很少有种群外的花粉块输入。花粉块传递只在种群内近缘个体中进行，有可能导致种内遗传或形态分化。 3. 独花兰种内形态变异及其适应意义 对庐山、新宁和神农架3个地点15个独花兰自然种群的形态变异进行了研究，探讨了形态多样性水平和地理变异式样及其可能的适应机制。结果表明，在物种水平上独花兰形态性状存在丰富的变异。单因素方差分析显示3个地区间多个形态性状存在极显著差异（P<0.01），UPGMA聚类分析也表明这3个地区分别形成明显不同的分支，说明3个地区种群植物形态已经出现分化。在神农架地区，龙门河和关门山两个地点间出现明显的形态分化，而这两个地点的传粉者在形体大小表现出显著差异。适合度与形态性状之间的相关性分析显示，独花兰种内形态分化是以传粉者为媒介的自然选择作用的结果。移栽实验显示，本地传粉者对本地和移栽种群花的访问表现出一定的选择性。 4. 扇脉杓兰的传粉生态学研究 与独花兰同域分布、花期不遇的扇脉杓兰是杓兰属的一个特殊类群，具有典型“Japonicum”型唇瓣类型。对神农架6个种群连续两年野外观测和实验结果表明，扇脉杓兰是一种自交亲和、需要昆虫传粉的欺骗性植物。在种群水平上开花个体的分布式样呈显著的偏斜曲线图，在短时间内迅速到达盛花期。扇脉杓兰的传粉者是三种熊蜂，其访问频次很低，访问时间很短，有效访问主要集中在开花的前、中期。自然结实率只有4.3％－8.5％，人工授粉实验证明，传粉者限制是结实率低的主要原因，且传粉者限制程度在花期不同阶段和不同地点存在差异。对欺骗性植物聚集生长、开花有利于吸引传粉者这一假说进行检验，结果显示，克隆群丛大小与传粉者有效访问（花粉块输出比例）呈弱负相关关系。聚集生长的结实率与分散生长的没有显著差异，说明繁殖成功与开花个体的密度无关。扇脉杓兰的花粉集结为未蜡质化的花粉块，是杓兰属中粘质花粉和蜡质花粉块的中间进化类型。传粉生态学和形态学证据显示C. acaule和扇脉杓兰是东亚-北美间断分布的姐妹种对。 5. 独花兰微卫星位点的分离 为了深入研究独花兰种群的基因流和交配系统，用Dynabeads和选择性杂交法分离微卫星位点、筛选引物。首先将基因组DNA用合适的内切酶消化为400-1000 bp大小的片段，然后用生物素标记的简单重复寡核苷酸序列做探针与其杂交，杂交复合物用抗生链霉素蛋白包裹的磁珠吸附，经过一系列洗脱、沉淀，得到富含重复片段的DNA，然后在进行克隆、测序，利用SSR两侧翼区设计引物，经过多态性分析可得到微卫星标记。结果显示，35个克隆序列中18个（51.4％）含有重复片段（SSRs），说明用Dynabeads富集效率明显高于传统方法。到目前为止所得引物共4对。这一实验方法的探索为以后分离杓兰属等兰科植物微卫星位点、进而进行群体遗传学研究奠定了一定的基础。

四川黄龙沟兰科植物多样性及影响繁殖成功的生态因子

植物生态学特性诸如植物的分布特征、与生境的关系、生物学特性、繁殖成功特点及其影响因素等方面的详细资料是研究珍稀植物种群结构和动态以及开展保育生物学研究的基础。 黄龙沟草本植物群落具有较为丰富的植物种类。在所调查样方中(N=662)共有维管植物124种，分属于37科91属，有54个中国特有种。其中兰科植物多达21属33种，中国特有种有12个，新种一个。如此众多的地生兰科植物聚集在面积不到1平方千米的沟内，而且部分兰科植物种类在沟内形成优势草本群落，这在中国地生兰的分布区域中是不多见的。大多数物种，包括兰科植物在内，出现的频率都较小，并且分布不均匀。种间关联分析和相关分析表明黄龙沟优势兰科植物可以分为两组。一组包括无苞杓兰、黄花杓兰、二叶根茎兰、广布小碟兰、少花鹤顶兰和西藏杓兰，主要分布在光线充足但又具有一定遮阴条件的环境中;另一组包括筒距兰、沼兰、珊瑚兰、小斑叶兰、布袋兰、小花舌唇兰和小叶对叶兰，它们主要分布于荫蔽的环境中。这些兰科植物在组内大多呈现显著的正相关关系，组间大多呈现显著的负相关关系，说明黄龙沟兰科植物在资源利用方式上可能产生了分化。 黄龙沟兰科植物主要分布在两种生境中，即钙化滩流地和一小片森林中。在这两种生境中微环境条件以及兰科植物的种类组成、数量特征和分布格局的差异都很大。钙化滩流地的兰科植物种类数目和每个样方中包含的兰科植物种类数目都比森林生境中的高。钙化滩流地中发现有30种兰科植物，六种最为常见的是无苞杓兰、黄花杓兰、西藏杓兰、广布小碟兰、二叶根茎兰和少花鹤顶兰，它们的密度与树木盖度呈负相关关系。森林生境中有21种兰科植物分布，其中筒距兰和斑叶兰出现最多，其密度与树木盖度呈正相关关系。光照强度可能对兰科植物的分布起到重要的决定作用。兰科植物彼此之间对繁殖成功以及植株间建立的相互促进作用以及土壤中高的钙含量很可能是形成黄龙沟兰科植物多样性的重要原因，而钙化滩流地中的溪流对建立和维持兰科植物生存所必须的稳定环境条件起到至关重要的作用，如果随意改变水流的方向或减少水流的流量，将给某些兰科植物带来灾难性的后果。 黄龙沟钙化滩流地中斑块的大小对物种数（含兰科植物）具有强烈的影响，即斑块越大，所包含的物种数量越多。物种-面积关系符合幂函数方程S=cAZ的规律。中等尺度的斑块(1-10 m2)包含的物种数（含兰科植物）的增长速度最快，而在斑块面积大于10 m2时，物种数增长速度最小。 少花鹤顶兰是多年生、多次结实的具有克隆能力的地生兰科植物，是中国特有种。黄龙沟少花鹤顶兰每个花序的平均花朵数为3(1-7)朵。叶和花的形态指标在年季间无显著变异。2005-2007年3年间的开花物候没有明显的差异，花期始于6月中旬，于7月底至8月初结束，持续约6-7周，80-90%的花在7月初的开花高峰期开放，属花集中开放模式。花寿命与是否授粉密切相关，成功授粉的花寿命比没有授粉的花寿命短。少花鹤顶兰是自交亲和的，但其结实完全依赖于两种熊蜂的传粉，不存在自动自花授粉和无融合生殖现象。柱头可授性和花粉活力可维持15天左右。繁殖成功率年季间的变化很大，并表现出逐年下降的趋势，花粉移走率为18-51%，自然结实率为10-36%。繁殖成功与开花物候之间的关系不显著，但与某一特定时刻的开花数量（密度）有关。生境对少花鹤顶兰的形态和繁殖成功率有显著的影响。在荫蔽生境中的个体比开阔地中的个体大，但繁殖成功率却低于开阔地的。花序密度（丛的大小）对少花鹤顶兰繁殖成功的影响比较复杂，不同大小的丛，对花粉移走率的影响格局和方式不同，而对结实率几乎没有影响。花序大小对繁殖成功率没有显著的影响。花位置对繁殖成功的影响在不同大小的丛中具有不同的格局，在最小的丛中，花位置对雄性和雌性繁殖成功的影响都很显著，但在最大丛中都不显著。边缘效应对少花鹤顶兰和广布小碟兰的繁殖成功有显著的影响，花粉移走率和结实率均随离栈道的距离增加而增加。在离栈道10米以内的植株受到的影响最为严重。这种影响可能是由边缘效应和在栈道上的游客共同作用下，对传粉者产生了干扰，导致传粉者的行为改变所引起的。如果这种边缘效应是一个普遍现象的话，那么在进行自然保护区设计时，应该对这种效应加以重视。

Micromorphology of the labellum and structure of the osmophore in a group of closely related species of the sexually deceptive Orchid genus Ophrys (orchidaceae)

Tese de doutoramento, Biologia (Biologia Celular), Universidade de Lisboa, Faculdade de Ciências, 2016

The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction

There is growing evidence of a substantial decline in pollinators within Europe and North America, most likely caused by multiple factors such as diseases, poor nutrition, habitat loss, insecticides, and environmental pollution. Diesel exhaust could be a contributing factor to this decline, since we found that diesel exhaust rapidly degrades floral volatiles, which honey bees require for flower recognition. In this study, we exposed eight of the most common floral volatiles to diesel exhaust in order to investigate whether it can affect volatile mediated plant-pollinator interaction. Exposure to diesel exhaust altered the blend of common flower volatiles significantly: myrcene was considerably reduced, β-ocimene became undetectable, and β-caryophyllene was transformed into its cis-isomer isocaryophyllene. Proboscis extension response (PER) assays showed that the alterations of the blend reduced the ability of honey bees to recognize it. The chemically reactive nitrogen oxides fraction of diesel exhaust gas was identified as capable of causing degradation of floral volatiles.

Habitat heterogeneity and pollinators: Bees in fragmented landscapes (Hymenoptera : Apidae)

This text presents the main studies that report the effect of habitat degradation upon plant-pollinator interactions and the importance of the presence of native vegetation remnants to pollinators, which leads to the need for conservation measures.