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.     

The Pollinators of the Malagasy Star Orchids Angraecum sesquipedale,A. sororium and A. compactum and the Evolution of Extremely Long Spurs by Pollinator Shift

The pollination process of the extremely long-spurred orchids Angraecum sesquipedale and A. sororium is described and documented here for the first time. The pollinaria and viscidia load was examined in moths captured in central and south Madagascar. Visits to orchids by hawkmoths were rarely observed in the field and were therefore systematically recorded in large flight tents using a night-vision video technique and flashlight photography. Angraecum sesquipedale in Fort Dauphin is pollinated by Xanthopan morgani praedicta and A. sororium on Mt. Angavokely by Coelonia solani. By combining a deep nectar spur of extraordinary length with a protruding labellum functioning as a landing platform, these orchids overcome the moth's stereotypic swing-hovering flight thus enabling full insertion of the long tongue. Angraecum compactum in Forêt d'Ambohitantely is pollinated by both the shorter and longer-tongued forms of Panogena lingens which never swing-hover but is also exploited by X. morgani and C. solani with wastage of pollinaria. The duration of tongue insertion, nectar exploitation and tongue withdrawal were analyzed: legitimate and illegitimate visitors differ in their time budget and approach to the flower. Nectar volume, nectar level and sugar concentration of A. sesquipedale and A. sororium were compared with the nectar requirements of the pollinating hawkmoths. The evolution of very long spurs in these orchids is likely to have involved a series of pollinator shifts. The orchids adapted to different hawkmoth species with increasingly long tongues which primarily evolved to avoid predator attacks during visits to less specialized flowers. This “pollinator shift” model modifies the classical “coevolutionary race” model. The relevance of the taxon Angraecum bosseri Senghas is questioned.     

The phenology of gender in homogamous flowers: temporal change in the residual sex function of flowers of Oil-seed Rape (Brassica napus)

1. We investigated the phenology of the male and female sexual functions in flowers of Oil-seed Rape ( Brassica napus ) that were exposed to pollinators in an experimental garden. The female 'residual sex function' (RSF) of flowers was measured by hand-pollinating with genetically marked pollen in order to determine the proportion of ovules that remained available for fertilization by incoming pollen. Male RSF was measured by estimating the proportion of pollen grains that remained in dehiscing anthers.
2. Following flower opening, an average flower's male and female sexual functions each required for completion c. 13 h of exposure to pollinators. One hour after opening, c. 50% of a flower's ovules were unavailable to incoming pollen whereas only c. 10% of pollen was removed. Therefore, a flower's sexual function was predominantly female for the first hour and predominantly male thereafter.
3. We found a fairly close correspondence between the proportion of the stigma covered with pollen and the depletion of female RSF.
4. On average, floral senescence occurred after c. 14·5 h of exposure to pollinators. Our observations are fairly consistent with a simple, economic model of optimal senescence time because the flowers remained open for approximately the same length of time as was necessary for the completion of their sexual functions.
5. A flower's senescence was hastened when pollen was removed from the anthers, but not when pollen was deposited on the stigma.
6. When flowers were either left undisturbed or hand-pollinated, senescence occurred after c. 24 h. Pollen removal caused senescence after c. 13 h, which also approximated the longevity of flowers in the experimental garden. Apparently, pollen removal governed floral longevity under field conditions.     

兰科新种巾唇兰的花粉团发育及分类学意义

巾唇兰属是我国新记录属,近十余年来先后在我国南方发现了两种,包括在云南发现的新种——巾唇兰（Pennilabium yunnanense）。利用解剖镜和石蜡切片技术观察了巾唇兰具有分类学意义的花形态特征和花粉团发育的胚胎学特征,结果如下。成熟花的合蕊柱短,无蕊柱足;花粉块由2个球形花粉团、粘盘和粘盘柄组成。在花药发育早期,花药原基分化出一对侧生并列药室;在小孢子母细胞时期,每个小孢子囊在两个药室相邻的内花药壁处分化出一段不贯穿药室的不育隔膜组织。在花药发育过程中,该隔膜组织逐渐被吸收降解,到花粉成熟时形成2个开口朝内的孔裂花粉团。发育成熟的花药壁共有4层,发育类型为单子叶型,绒毡层为单核、腺质型。在小孢子母细胞进入减数分裂阶段,表皮细胞变窄出现了降解,中层和绒毡层细胞也逐渐被吸收和降解;花药成熟时,花药壁仅剩下残缺的表皮和纤维状加厚明显的药室内壁。小孢子母细胞通过同时型胞质减数分裂形成小孢子四分体,其排列方式主要为正四面体形和左右对称,成熟花粉为2细胞型。本文从形态发育角度澄清了巾唇兰花粉团特征的描述,讨论了其花粉团发育特征的分类学意义,为兰科花药发育多样性提供了新资料。     

Phylogeny and radiation of pollination systems in DISA (Orchidaceae)

We studied the patterns of adaptive radiation in Disa, a large orchid genus in southern Africa. A cladogram for 27 species was constructed using 44 morphological characters. Pollination systems were then mapped onto the phylogeny in order to analyze pathways of floral evolution. Shifts from one pollination system to another have been a major feature of the evolutionary diversification of Disa. Unlike many plant genera that are pollinated mainly by a single group of insects, radiation in Disa has encompassed nearly all major groups of pollinating insects; in all, 19 different specialized pollination systems have been found in the 27 species included in this analysis. Another striking pattern is the repeated evolution of broadly similar pollination systems in unrelated clades. For example, butterfly-pollinated flowers have evolved twice; showy deceptive flowers pollinated by carpenter bees, twice; long-spurred flowers pollinated by long-tongued flies, four times; night-scented flowers pollinated by moths, three times; and self-pollination, three times. This suggests that a few dominant pollinator species in a region may be sufficient to generate diversification in plants through repeated floral shifts that never retrace the same pathways.     

Transfer of pollinaria on birds’ feet: a new pollination system in orchids

We report the discovery of a new mechanism of pollination in orchids: transfer of pollinaria on the feet of birds. Observations carried out in South Africa and Malawi showed that the orchids Disa chrysostachya Sw. and Disa satyriopsis Kraenzl. are pollinated by sunbirds. Pollinaria of these orchids become attached firmly to the birds toes when they perch on the tall narrow inflorescences which are packed tightly with numerous small orange flowers. Birds typically perch on the lower part of an inflorescence while reaching up to feed on nectar in flowers on the upper part, but occasionally reverse this position to probe the lower flowers. The nectar is contained within a short bulbous spur with a narrow entrance that permits entrance of a sunbirds slender tongue. Contrary to expectation, the pollination mechanism in D. chrysostachya is remarkably efficient with about 6.1% of pollen reaching stigmas on other plants and fruit set occurring in 95% of flowers at one site. Birds seldom move their feet once perched, thus minimizing the incidence of self-pollination, either within or between flowers on an inflorescence.     

Phenotype–fitness relationships and pollen-transfer efficiency of five orchid species with different pollination strategies

Premise

Deceptive pollination, a fascinating mechanism that independently originated in several plant families for benefiting from pollinators without providing any reward, is particularly widespread among orchids. Pollination efficiency is crucial in orchids due to the aggregated pollen in a pollinarium, which facilitates pollen transfer and promotes cross-pollination as pollinators leave after being deceived.

Methods

In this study, we compiled data on reproductive ecology from five orchid species with different pollination strategies: three deceptive-strategy species (shelter imitation, food deception, sexual deception), one nectar-rewarding species, and one shelter-imitation but spontaneously selfing species. We aimed to compare the reproductive success (female fitness: fruit set; male fitness: pollinarium removal) and pollination efficiency of species representing these strategies. We also investigated pollen limitation and inbreeding depression among the pollination strategies.

Results

Male and female fitness were strongly correlated in all species but the spontaneously selfing species, which had high fruit set and low pollinarium removal. As expected, pollination efficiency was highest for the rewarding species and the sexually deceptive species. Rewarding species had no pollen limitation but did have high cumulative inbreeding depression; deceptive species had high pollen limitation and moderate inbreeding depression; and spontaneously selfing species did not have pollen limitation or inbreeding depression.

Conclusions

Pollinator response to deception is critical to maintain reproductive success and avoid inbreeding in orchid species with non-rewarding pollination strategies. Our findings contribute to a better understanding of the trade-offs associated with different pollination strategies in orchids and highlight the importance of pollination efficiency in orchids due to the pollinarium.

     

Chloroplast DNA and the determination of species status in the Disa tripetaloides complex (Orchidaceae), and its relationships to three species Racemosae, section Disa

Disa cardinalis and three populations within the D. tripetaloides species complex contain variation in their chloroplast DNA (cpDNA) variability. All four taxa possessed unique cpDNAs and sequence divergence values ranged from 0.34 to 1.03%. A phylogeny of these genomes was reconstructed, along with the genomes of three other species, D. racemosa, D. uniflora and D. venosa, all of which are also section Disa and series RAcemosae, to determine the relationship of these closely related species to the D. tripetaloides complex. A phylogeny of the taxa using morphological data was also reconstructed. Outgroup comparison was made with D. sagittalis, a member of section Coryphaea. Although the molecular and morphological data were not completely congruent, both data types revealed D. cardinalis, rather than D. tripetaloides ssp. aurata, to be more closely allied with D. tripetaloides ssp. tripetaloides, suggesting that D. tripetaloides ssp. aurata should be elevated to species rank. Additionally, the high sequence divergence observed between the Natal and Cape populations, coupled with their geographical isolation and alternate flowering seasons, suggests that these two D. tripetaloides ssp. tripetaloides populations may, in fact, be more appropriately ranked as subspecies.     

开花式样对传粉者行为及花粉散布的影响

理解植物花的特征可以从单花特征和群体特征两个层次入手。开花式样是植物的花在群体上的特征体现, 通过在开花数目、开花类型以及花的排列上的变化, 不同的开花式样对传粉者具有不同的吸引力, 影响昆虫在植株上的活动, 使花粉运动的方向发生相应变化, 从而影响着植物最终的交配结果。此外开花式样随环境改变也会发生一些变化。本文介绍了开花式样研究的进展, 对开花数目、开花类型以及花的排列等3个方面的已有研究进行了分别阐述, 并提出开花式样研究应更多地考虑影响传粉的各种因素。     

Evidence for Bastesian mimicry in a butterfly-pollinated orchid

Observations in the Cape Province, South Africa, showed that Disa ferruginea (Orchidaceae) is dependent on a single butterfly species— Meneris tulbaghia (Nymphalidae: Satyrinae)—for pollination. The flowers of D. ferruginea contain no food reward and, instead, appear to secure pollinator visits by imitating flowers which are nectar sources for the butterfly. A red-flowered form of D. ferruginea appears to mimic the red nectar-producing flowers of Tritoniopsis triticea (Iridaceae) in the south-western Cape, while an orange-flowered form of D. ferruginea appears to mimic the orange nectar-producing flowers of Kniphofia uvaria (Asphodelaceae) in the Langeberg Mountains. Reflectance spectra of the orchid's flowers closely match those of its putative models. Analysis of foraging movements of the butterfly in a mixed stand of D. ferruginea and T. triticea indicated that it does not discriminate between the nectarless orchid and the nectar-producing model. Populations of D. ferruginea which are sympatric with T. triticea have relatively high levels of pollination and fruit production, compared with populations where the orchid grows alone. Although other studies have reported relatively low fecundity in deceptive orchids, pollination and fruiting success in D. ferruginea compares favourably with a nectar-producing congener, Disa uniflora , which is also pollinated solely by M. tulbaghia.     

Which food‐mimic floral traits and environmental factors influence fecundity in a rare orchid,Calanthe yaoshanensis?

Orchid species that are food mimics produce fewer fruits than species offering rewards, but few studies have shown the impact of environmental factors (e.g. anthropogenic activity, frost and herbivores) on their reproductive success over several seasons. In this study, we focused on the sole population of the endangered Calanthe yaoshanensis as it secretes no nectar. We investigated its floral biology, fruit set rates and prevailing environmental factors over three seasons (2008–2010). Mechanical self‐pollination did not occur in C. yaoshanensis, but hand‐selfed and crossed flowers produced equal numbers of fruit. However, seed viability and embryo size were significantly higher in cross‐pollinated fruits maximizing embryonic fitness. Large hoverflies (Syrphidae) and Bombus patagiatus (gynes) were the only pollinarium vectors, but they often failed to disperse pollinaria. We interpret the temporary retention of the anther cap over the pollinarium as an adaptation lowering self‐pollination. Insect‐mediated rates of pollinarium removal were always higher than rates of pollinia deposition on stigmas. Over 3 years, natural rates of pollinarium removal differed significantly, whereas natural rates of fruit set were not significantly different (< 22%). Climate, herbivory and anthropogenic collections also inhibited some fruit set and maturation. Both biotic and abiotic factors appear to lower the fecundity of this endangered population. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 421–433.     

14种石斛属(兰科)植物的花粉团形态及分类学意义

利用体式显微镜和扫描电镜观察了14种石斛的花粉团形态及其表面纹饰超微特征,为该属的物种划分和系统演化提供花粉形态证据。解剖镜下,14种石斛的花药里有4枚花粉团,表面金黄油亮呈蜡质,质地坚硬。根据每种石斛的4枚花粉团的总体轮廓形态和大小,可分为3种形态(心形、近心形和长心形)和4种类型(极小花粉团,小花粉团,大花粉团和超大花粉团)。根据单个花粉团边界轮廓的曲直,可将其分为4种类型(月牙型、弓型、棍状和米粒型)。扫描电镜下,14种石斛的花粉团表面纹饰类型有5种(光滑平整型、光滑带丝状突起型、光滑不平整型、粗网纹状型和皱波状型),在广东石斛和球花石斛的花粉团表面观察到晶体的存在。花粉团的形态大小和外壁纹饰特征在种间变化明显,对澄清石斛属的分类学问题有一定意义。     

Anther cap retention prevents self-pollination by elaterid beetles in the South African orchid Eulophia foliosa

BACKGROUND AND AIMS: Pollination by insects that spend long periods visiting many flowers on a plant may impose a higher risk of facilitated self-pollination. Orchids and asclepiads are particularly at risk as their pollen is packaged as pollinia and so can be deposited on self-stigmas en masse. Many orchids and asclepiads have adaptations to limit self-deposition of pollinia, including gradual reconfiguration of pollinaria following removal. Here an unusual mechanism--anther cap retention--that appears to prevent self-pollination in the South African orchid Eulophia foliosa is examined. METHODS: Visits to inflorescences in the field were observed and pollinators collected. Visitation rates to transplanted inflorescences were compared between a site where putative pollinators were abundant and a site where they were rare. Anther cap retention times were determined for removed pollinaria and atmospheric vapour pressure deficit was recorded concurrently. Anther cap anatomy was examined using light microscopy. KEY RESULTS: Eulophia foliosa is pollinated almost exclusively by Cardiophorus obliquemaculatus (Elateridae) beetles, which remain on the deceptive inflorescences for on average 301 s (n = 18). The anther cap that covers the pollinarium is retained for an average of 512 s (n = 24) after pollinarium removal by beetles. In all populations measured, anther cap dimensions are greater than those of the stigmatic cavity, thus precluding the deposition of self-pollinia until after the anther cap has dropped. An anatomical investigation of this mechanism suggests that differential water loss from regions of the anther cap results in opening of the anther cap flaps. This is supported by observations that as atmospheric vapour pressure deficits increased, the duration of anther cap retention was reduced. CONCLUSIONS: Flowers of E. foliosa are specialized for pollination by elaterid beetles. Retention of anther caps for a period exceeding average visit times by beetles to inflorescences appears to prevent facilitated self-pollination in E. foliosa effectively.