Pollination services of Africanized honey bees and native Melipona beecheii to buzz‐pollinated annatto (Bixa orellana L.) in the neotropics

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Evidence for mutualism between a flower-piercing carpenter bee and ocotillo: use of pollen and nectar by nesting bees

Abstract.

• 1 Carpenter bees (Xylocopa californica arizonensis) in west Texas, U.S.A., gather pollen and ‘rob’ nectar from flowers of ocotillo (Fouquieria splendens). When common, carpenter bees are an effective pollen vector for ocotillo. We examined ocotillo's importance as a food source for carpenter bees.
• 2 The visitation rate of carpenter bees to ocotillo flowers in 1988 averaged 0.51 visits/flower/h and was 4 times greater than that of queen bumble bees (Bombus pennsylvanicus sonorus), the next most common visitor. Nectar was harvested thoroughly and pollen was removed from the majority of flowers. Hummingbird visits were rare.
• 3 Pollen grains from larval food provisions were identified from sixteen carpenter bee nests. On average, 53% of pollen grains sampled were ocotillo, 39% were mesquite (Prosopis glandulosa), and 8% were Zygophyllaceae (Larrea tridentata or Guaiacum angustifolium). Carpenter bee brood size averaged 5.8 per nest.
• 4 We measured the number of flowers, and production of pollen and nectar per flower by mature ocotillo plants, as well as the quantity of pollen and sugar in larval provisions. An average plant produced enough pollen and nectar sugar to support the growth of eight to thirteen bee larvae. Ocotillo thus has the potential to contribute significantly to population growth of one of its key pollinators.
• 5 Although this carpenter bee species, like others, is a nectar parasite of many plant species, it appears to be engaged in a strong mutualism with a plant that serves as both a pollen and as a nectar source during carpenter bee breeding periods.

     

Flower‐visitor networks only partially predict the function of pollen transport by bees

Mutualistic networks display distinct structural and organizational features such as nestedness, power‐law degree distribution and asymmetric dependencies. Attention is now focused on how these structural properties influence network function. Most plant‐pollinator networks are constructed using records of animals contacting flowers, which is based on the assumption that all visitors to flowers are pollinators; however, animals may visit flowers as nectar robbers, florivores, or to prey upon other visitors. To differentiate potential pollinator interactions from other interaction types, we examined individual bees that had visited flowers to detect if they carried pollen. Using these data, we constructed visitation and pollen‐transport networks for a spinifex‐dominated arid zone grassland. To determine how the structure of the visitation network reflects pollen transport, we compared the two networks using a null model approach to account for differences in network size. Differences in number of species, nestedness and connectance observed between the visitation and pollen‐transport networks were within expected ranges generated under the null model. The pollen‐transport network was more specialized, had lower interaction evenness, and fewer links compared to the visitation network. Almost half the number of species of the visitation network participated in the pollen‐transport network, and one‐third of unique visitation interactions resulted in pollen transport, highlighting that visitation does not always result in pollination. Floral visitor data indicate potential pollen transporters, but inferring pollination function from visitation networks needs to be performed cautiously as pollen transport resulted from both common and rare interactions, and depended on visitor identity. Although visitation and pollen‐transport networks are structurally similar, the function of all species cannot be predicted from the visitation network alone. Considering pollen transport in visitation networks is a simple first step towards determining pollinators from non‐pollinators. This is fundamental for understanding how network structure relates to network function.     

An affordable apparatus for fine‐controlled emulation of buzzing frequencies of bees for the testing hypothesis in buzz interactions

The buzzing foraging behavior of female bees for pollen harvesting called the attention of early pollination biologists. Flower types that demand this buzzing behavior comprise about 20,000 species of different and phylogenetically unrelated plant taxa, suggesting that it had independently evolved many times among the flowering plants. Between the late 1970s and early 1980s, theoretical papers had modeled the energetics of buzz pollination, but, up to this moment, no hypothesis was experimentally tested concerning the theoretical basis of the energetics of buzz pollination. We present a cost‐effective and simple apparatus, including a digital and highly accurate frequency generator, and a device for the transference of buzz‐frequency energy to the receptive floral unity. The receptive floral unities may comprise the entire or partial androecium, or the tubular corolla, or, in some cases, the whole flower. This apparatus can be easily used in both laboratory and field conditions of research, as natural air currents are avoided, and the response of pollen liberation can be quantitatively measured by pollen grain counts that can be captured by adhesion in slide poured with an isosmotic lactate–glycerol media. The maximum displacement of the hardwire beam/claw system was 0.1170 ± 0.0006 mm @ 150 Hz; 0.021 ± 0.003 mm @ 250 Hz; 0.010 ± 0.001 mm @ 350 Hz; 0.0058 ± 0.0001 mm @ 450 Hz; and 0.0082 ± 0.0005 mm @ 550 Hz. Hypothesis contrasting frequency emission and pollen liberation measured as pollen grain counts may be tested in a species flower type by simple linear regression if pollen counts are normally distributed, or ordinal logistic regression, with non‐normal counts. The comparison among different flower‐type requirements can be tested through appropriate statistical methods for both normally and non‐normally distributed pollen grain counts.     

HT proteins contribute to S‐RNase‐independent pollen rejection in Solanum

Plants have mechanisms to recognize and reject pollen from other species. Although widespread, these mechanisms are less well understood than the self‐incompatibility (SI) mechanisms plants use to reject pollen from close relatives. Previous studies have shown that some interspecific reproductive barriers (IRBs) are related to SI in the Solanaceae. For example, the pistil SI proteins S‐RNase and HT protein function in a pistil‐side IRB that causes rejection of pollen from self‐compatible (SC) red/orange‐fruited species in the tomato clade. However, S‐RNase‐independent IRBs also clearly contribute to rejecting pollen from these species. We investigated S‐RNase‐independent rejection of Solanum lycopersicum pollen by SC Solanum pennellii LA0716, SC. Solanum habrochaites LA0407, and SC Solanum arcanum LA2157, which lack functional S‐RNase expression. We found that all three accessions express HT proteins, which previously had been known to function only in conjunction with S‐RNase, and then used RNAi to test whether they also function in S‐RNase‐independent pollen rejection. Suppressing HT expression in SC S. pennellii LA0716 allows S. lycopersicum pollen tubes to penetrate farther into the pistil in HT suppressed plants, but not to reach the ovary. In contrast, suppressing HT expression in SC. Solanum habrochaites LA0407 and in SC S. arcanum LA2157 allows S. lycopersicum pollen tubes to penetrate to the ovary and produce hybrids that, otherwise, would be difficult to obtain. Thus, HT proteins are implicated in both S‐RNase‐dependent and S‐RNase‐independent pollen rejection. The results support the view that overall compatibility results from multiple pollen–pistil interactions with additive effects.     

Buzz-pollination in Neotropical bees:genus-dependent frequencies and lack of optimal frequency for pollen release

Over 50 genera of bees release pollen from flower anthers using thoracic vibrations,a phenomenon known as buzz-pollination.The efficiency of this process is directly affected by the mechanical properties of the buzzes,namely the duration,amplitude,and frequency.Nonetheless,although the effects of the former two properties are well described,the role of buzz frequency on pollen release remains unclear.Furthermore,nearly all of the existing studies describing vibrational properties of natural buzz-pollination are limited to bumblebees(Bombus)and carpenter bees(Xvlocopa)constraining our current understanding of this behavior and its evolution.Therefore,we attempted to minimize this shortcoming by testing whether flower anthers exhibit optimal frequency for pollen release and whether bees tune their buzzes to match these(optimal)frequencies.If true,certain frequencies will trigger more pollen release and lighter bees will reach buzz frequencies closer to this optimum to compensate their smaller buzz amplitudes.Two strategies were used to test these hypotheses:(i)the use of(artificial)vibrational playbacks in a broad range of buzz frequencies and amplitudes to assess pollen release by tomato plants(Solarium Ivcopersicum L.)and(ii)the recording of natural buzzes of Neotropical bees visiting tomato plants during pollination.The playback experiment indicates that although buzz frequency does affect pollen release,no optimal frequency exists for that.In addition,the recorded results of natural buzz-pollination reveal that buzz frequencies vary with bee genera and are not correlated with body size.Therefore,neither bees nor plants are tuned to optimal pollen release frequencies.Bee frequency of buzz-pollination is a likely consequence of the insect flight machinery adapted to reach higher accelerations,while flower plant response to buzz-pollination is the likely result of its pollen granular properties.     

RiceAntherNet: a gene co‐expression network for identifying anther and pollen development genes

In plants, normal anther and pollen development involves many important biological events and complex molecular regulatory coordination. Understanding gene regulatory relationships during male reproductive development is essential for fundamental biology and crop breeding. In this work, we developed a rice gene co‐expression network for anther development (RiceAntherNet) that allows prediction of gene regulatory relationships during pollen development. RiceAntherNet was generated from 57 rice anther tissue microarrays across all developmental stages. The microarray datasets from nine rice male sterile mutants, including msp1‐4, ostdl1a, gamyb‐2, tip2, udt1‐1, tdr, eat1‐1, ptc1 and mads3‐4, were used to explore and test the network. Among the changed genes, three clades showing differential expression patterns were constructed to identify genes associated with pollen formation. Many of these have known roles in pollen development, for example, seven genes in Clade 1 (OsABCG15, OsLAP5, OsLAP6, DPW, CYP703A3, OsNP1 and OsCP1) are involved in rice pollen wall formation. Furthermore, Clade 1 contained 12 genes whose predicted orthologs in Arabidopsis have been reported as key during pollen development and may play similar roles in rice. Genes in Clade 2 are expressed earlier than Clade 1 (anther stages 2–9), while genes in Clade 3 are expressed later (stages 10–12). RiceAntherNet serves as a valuable tool for identifying novel genes during plant anther and pollen development. A website is provided ( https://www.cpib.ac.uk/anther/riceindex.html ) to present the expression profiles for gene characterization. This will assist in determining the key relationships between genes, thus enabling characterization of critical genes associated with anther and pollen regulatory networks.     

Airborne conifer pollen grains are rarely deposited on stigmas of coflowering insect‐pollinated angiosperms

Although plant species with either animal or wind pollination modes are widespread and usually sympatric in nature, the degree of pollen interference from wind‐pollinated species on animal‐pollinated species remains little known. Conifer trees generally release a huge number of pollen grains into the air, floating into our noses and sometimes causing an allergic response. Here we document airborne pollen from two conifers (Pinus densata Mast. and Picea likiangensis (Franch.) E. Pritz.) deposited on the stigmas of eight coflowering insect‐pollinated angiosperms over 2 years in a mountainous forest community, in Shangri‐La, southwest China. Pollen density in the air as well as conifer pollen deposited onto stigmas at short and long distances from the airborne pollen source were quantified. Our results showed that conifer pollen as a proportion of total stigmatic pollen loads in the insect‐pollinated plants varied from 0.16% to 8.67% (3.16% ± 0.41%, n = 735) in 2016 and 0.66% to 5.38% (2.87% ± 0.86%, n = 180), and pollen quantity per unit area was closely related to that of airborne pollen in the air. Conifer pollen deposition on stigmas of insect‐pollinated species decreased greatly with increased distance from the pollen source. In the 10 plant species flowering in summer after conifer pollen release had finished, heterospecific pollen deposited on these stigmas came mainly from other insect‐pollinated flowers, with little contribution from airborne conifer pollen. The results indicate that there might be little interference with coflowering angiosperms by airborne pollen from dominant conifers in natural communities.     

Generalized food deception: colour signals and efficient pollen transfer in bee‐pollinated species of Eulophia (Orchidaceae)

Non‐rewarding plants use a variety of ruses to attract their pollinators. One of the least understood of these is generalized food deception, in which flowers exploit non‐specific food‐seeking responses in their pollinators. Available evidence suggests that colour signals, scent and phenology may all play key roles in this form of deception. Here we investigate the pollination systems of five Eulophia spp. (Orchidaceae) lacking floral rewards. These species are pollinated by bees, notably Xylocopa (Anthophorinae, Apidae) or Megachile (Megachilidae) for the large‐flowered species and anthophorid (Anthophorinae, Apidae) or halictid (Halictidae) bees for the small‐flowered species. Spectra of the lateral petals and ultraviolet‐absorbing patches on the labella are strongly contrasting in a bee visual system, which may falsely signal the presence of pollen to bees. All five species possess pollinarium‐bending mechanisms that are likely to limit pollinator‐mediated self‐pollination. Flowering times extend over 3–4 months and the onset of flowering was not associated with the emergence of pollinators, some of which fly year round. Despite sharing pollinators with other plants and lacking rewards that would encourage fidelity, the Eulophia spp. exhibited relatively high levels of pollen transfer efficiency compared with other rewarding and deceptive orchids. We conclude that the study species employ generalized food deception and exploit food‐seeking bees. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 713–729.     

Characterization of pollen and bacterial community composition in brood provisions of a small carpenter bee

Many insects obtain gut microbes from their diet, but how a mother's foraging patterns influence the microbes found in her offspring's food remains an open question. To address this gap, we studied a bee that forages for pollen from multiple species of plants and may therefore acquire diverse bacteria from different plants. We tested the hypothesis that pollen diversity correlates with bacterial diversity by simultaneously characterizing these two communities in bee brood provisions for the first time. We used deep sequencing of the plant RBCL gene and the bacterial 16S rRNA gene to characterize pollen and bacterial diversity. We then tested for associations between pollen and bacterial species richness and community composition, as well as co‐occurrence of specific bacteria and pollen types. We found that both pollen and bacterial communities were extremely diverse, indicating that mother bees visit a wide variety of flowers for pollen and nectar and subsequently bring a diversity of microbes back into their nests. Pollen and bacterial species richness and community composition, however, were not correlated. Certain pollen types significantly co‐occurred with the most proportionally abundant bacteria, indicating that the plants these pollen types came from may serve as reservoirs for these bacteria. Even so, the overall diversity of these communities appears to mask these associations at a broader scale. Further study of these pollen and bacteria associations will be important for understanding the complicated relationship between bacteria and wild bees.     

Types of pollen dispersal units in orchids,and their consequences for germination and fertilization

The various pollen dispersal units (PDU) found in orchids are discussed together with possible evolutionary trends and the consequences for germination and fertilization. Orchids with monad and tetrad pollen form more complex dispersal units by means of pollenkitt, elastoviscin, a callosic wall, common walls or a combination of these. Evolutionary trends include (1) from pollenkitt to elastoviscin; (2) from monad to tetrads and multiples of tetrads; (3) from partially dehydrated (<30 %) to partially hydrated (>30 %) pollen; and (4) from monad pollen to PDUs with many pollen grains. The biological consequences concern both male and female reproductive systems. Some features of the male side are present in all orchids irrespective of the pollen dispersal unit, whereas other characters are found only in orchids with pollinia; the same applies for the female counterpart. Pollen grains of orchids with pollinia germinate at least 24 h after pollination because the pollen grains/tetrads must swell and make space for the growth of pollen tubes.