The occurrence of crassulacean acid metabolism in Cymbidium (Orchidaceae) and its ecological and evolutionary implications

Crassulacean acid metabolism (CAM) is one of the photosynthetic pathways regarded as adaptations to water stress in land plants. Little is known about correlations among the level of CAM activity, environment of habitat, life form, and phylogenetic relationship of a plant group from an evolutionary perspective. We examined these relationships in 18 species of Cymbidium (Orchidaceae) because the genus shows distinctive diversification of habitats and life forms. The photosynthetic type was classed into three categories, strong CAM, weak CAM, and C₃ on the basis of CAM activity. CAM expression in Cymbidium was confined to the epiphytic and lithophytic species. Especially, all of these species from tropical to subtropical rainforest exhibited CAM activity. On the other hand, the terrestrial species always exhibited C₃ metabolism irrespective of their varied habitats. Regarding the evolution of photosynthetic characters, weak CAM was the ancestral state in Cymbidium and strong CAM and C₃ metabolism occurred subsequently. The evolution of strong CAM likely enabled Cymbidium to extend to exposed sites in tropical lowland where marked water stress exists. Further, different levels of CAM activity characterized each species and such potential plasticity of CAM may realize the radiation of Cymbidium into sites with different environmental conditions.     

Epiphytism and pollinator specialization: drivers for orchid diversity?

Epiphytes are a characteristic component of tropical rainforests. Out of the 25,000 orchid species currently known to science, more than 70% live in tree canopies. Understanding when and how these orchids diversified is vital to understanding the history of epiphytic biomes. We investigated whether orchids managed to radiate so explosively owing to their predominantly epiphytic habit and/or their specialized pollinator systems by testing these hypotheses from a statistical and phylogenetic standpoint. For the first approach, species numbers of 100 randomly chosen epiphytic and terrestrial genera were compared. Furthermore, the mean number of pollinators per orchid species within the five subfamilies was calculated and correlated with their time of diversification and species richness. In the second approach, molecular epiphytic orchid phylogenies were screened for clades with specific suites of epiphytic adaptations. Epiphytic genera were found to be significantly richer in species than terrestrial genera both for orchids and non-orchids. No evidence was found for a positive association between pollinator specialization and orchid species richness. Repeated associations between a small body size, short life cycle and specialized clinging roots of twig epiphytes in Bulbophyllinae and Oncidiinae were discovered. The development of twig epiphytism in the first group seems repeatedly correlated with speciation bursts.     

How prevalent is crassulacean acid metabolism among vascular epiphytes?

The occurrence of crassulacean acid metabolism (CAM) in the epiphyte community of a lowland forest of the Atlantic slope of Panama was investigated. I hypothesized that CAM is mostly found in orchids, of which many species are relatively small and/or rare. Thus, the relative proportion of species with CAM should not be a good indicator for the prevalence of this photosynthetic pathway in a community when expressed on an individual or a biomass basis. In 0.4 ha of forest, 103 species of vascular epiphytes with 13,099 individuals were found. As judged from the C isotope ratios and the absence of Kranz anatomy, CAM was detected in 20 species (19.4% of the total), which were members of the families Orchidaceae, Bromeliaceae, and Cactaceae. As predicted, the contribution of CAM epiphytes to the total number of individuals and to total biomass (69.6 kg ha^-1) was considerably lower (3.6% or 466 individuals and, respectively, 3.0% or 2.1 kg ha^-1).     

Four distinct trimeric forms of light-harvesting complex II isolated from the green alga Chlamydomonas reinhardtii

Photosynthesis Research - Crassulacean acid metabolism (CAM) is a specialized photosynthetic pathway present in a variety of genera including many epiphytic orchids. CAM is under circadian control...     

The role of CAM in high rainfall cloud forests: an in situ comparison of photosynthetic pathways in Bromeliaceae

Crassulacean acid metabolism (CAM), an advanced photosynthetic pathway conferring water conservation to plants in arid habitats, has enigmatically been reported in some species restricted to extremely wet tropical forests. Of these, epiphytic Bromeliaceae may possess absorbent foliar trichomes that hinder gas‐exchange when wetted, imposing further limitations on carbon dioxide (CO₂) uptake. The hypothesis that the metabolic plasticity inherent to CAM confers an ecological advantage over conventional C₃ plants, when constant rainfall and mist might inhibit gas‐exchange was investigated. Gas‐exchange, fluorometry and organic acid and mineral nutrient contents were compared for the bromeliads Aechmea dactylina (CAM) and Werauhia capitata (C₃) in situ at the Cerro Jefe cloud forest, Panama (annual rainfall > 4 m). Daily carbon gain and photosynthetic nutrient use efficiencies were consistently higher for A. dactylina, due to a greater CO₂ uptake period, recycling of CO₂ from respiration and a dynamic response of CO₂ uptake to wetting of leaf surfaces. During the dry season CAM also had water conserving and photoprotective roles. A paucity of CAM species at Cerro Jefe suggests a recent radiation of this photosynthetic pathway into the wet cloud forest, with CAM extending diversity in form and function for epiphytes.     

Impact of floral traits on the reproductive success of epiphytic and terrestrial tropical orchids

We investigated the relationship between habit, population size, floral traits and natural fruit set levels of 23 tropical orchid species of south-east Bangladesh. We showed that epiphytic orchids had lower fruit set levels than terrestrial species and that habit explained much of the variation in floral traits among the orchids. We compared our results with data from 76 other species occurring in the study area and hypothesize that a suite of floral and population characteristics present in tropical orchids combine in epiphytes to reduce their reproductive success. Characteristics which, in addition to their habit, are associated with low reproductive success are small population size, small inflorescences, non-sectile pollinia and self-incompatibility. Several of these characteristics were phylogenetically conserved and we predict that epiphytes might therefore generally have lower fruit set levels than recorded in terrestrial species. Nectar rewards are uncommon in tropical orchids and nectarless species have displays of larger flowers, which may represent an adaptation to increase pollinator attraction, although other rewards such as oils, waxes and pseudo pollen may replace nectar. We suggest that, like many temperate orchids, a high proportion of tropical orchids may lack floral rewards and be pollinated by deceit.     

Causes and consequences of high osmotic potentials in epiphytic higher plants

Past reports of the water relations of epiphytes, particularly bromeliads, indicate that tissue osmotic potentials in these tropical and subtropical plants are very high (close to zero) and are similar to values for aquatic plants. This is puzzling because several ecophysiological studies have revealed a high degree of drought stress tolerance in some of these epiphytes. The goal of this study was two-fold: (1) to increase the number of epiphytic taxa sampled for tissue osmotic potentials; and (2) to explain the apparent discrepancy in the significance of the tissue water relations and tolerance of drought stress in epiphytes. Tissue osmotic potentials of 30 species of epiphytic ferns, lycophytes, and orchids were measured in a subtropical rain forest in northeastern Taiwan. Nearly all values were less negative than -1.0 MPa, in line with all previous data for epiphytes. It is argued that such high osmotic potentials, indicative of low solute concentrations, are the result of environmental constraints of the epiphytic habitat on productivity of these plants, and that low rates of photosynthesis and transpiration delay the onset of turgor loss in the tissues of epiphytes such that they appear to be very drought-stress tolerant. Maintenance of photosynthetic activity long into drought periods is ascribed to low rates of transpiration and, hence, delayed tissue desiccation, and hydration of the photosynthetic tissue at the expense of water from the water-storage parenchyma.     

Water Relations of Tropical Epiphytes: III. EVIDENCE FOR CRASSULACEAN ACID METABOLISM

Five tropical epiphytes were examined for evidence of CrassulaceanAcid Metabolism (CAM), namely the orchids Eria velutina Lindl.,Dendrobium tortile Lindl. and Dendrobium crumenatum Sw., andthe ferns Pyrrosia adnascens (Forst.) Ching and Pyrrosia angustata(Sw.) Ching, family Polypodiaceae. Diurnal variations in leaftitratable acidity, diffusive conductance and water potentialwere measured at various levels of water stress. The three orchidsshowed typical CAM behaviour, namely large diurnal fluctuationsin leaf acidity, day-time closure and night opening of stomataand a very slow decline in water potential under stress. Theferns showed some evidence of CAM, but this was not as well-developedas had been reported for two other tropical epiphytic membersof the same family. Key words: Crassulacean acid metabolism, Tropical epiphytes, Water stress     

Epiphytism,anatomy and regressive evolution in trichomanoid filmy ferns (Hymenophyllaceae)

The few studies on the evolution of epiphytism in ferns have mostly focused on xerophytic and humus‐collecting strategies, neglecting hygrophytes that are abundant in rainforests, such as the trichomanoids (Hymenophyllaceae). Using a phylogenetic approach, we studied the acquisition of epiphytism in this lineage, with the aim of identifying ecological anatomical adaptations and verifying the regressive epiphytic ‘bryophyte‐like’ strategy previously suggested for the group. Inferred evolution of anatomy and morphology, regression and ecology (more particularly colonial epiphytism) were analysed and compared using a maximum likelihood approach. Regressive evolution of anatomy and morphology is revealed in the three clades of colonial epiphytes, probably linked to the selection of water acquisition by blades rather than by regressed roots. However, the ‘bryophyte‐like’ strategy is restricted to some taxa (especially Didymoglossum). Furthermore, a relationship is revealed between large metaxylem and climbing habit. Diversification of colonial epiphytes (and some individual epiphytes) and hemi‐epiphytism would have occurred in the upper Cretaceous and Tertiary, in accordance with the timing of diversification of modern ferns and the evolution of epiphytism in other fern families in the first angiosperm‐dominated forests. This was here performed by selecting hygrophilous strategies that are unique in vascular plants. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 573–593.     

The photosynthetic pathway of the roots of twelve epiphytic orchids with CAM leaves

The photosynthetic pathway of the roots (both the white velamentous main portions and the green, nonvelamentous tips) was investigated in twelve taxa (natural species and intergeneric hybrid cultivars) of epiphytic orchids having CAM leaves. All organs contained chlorophyll, and the a/b ratios indicate that the organs, especially the roots, are likely shade-adapted. Stable carbon isotope ratios of the tissues were near −15‰ for all organs, a value typical of obligate (constitutive) CAM plants. Values for root tissues were slightly lower (more negative) than those of the leaves. The presence of CAM in the leaves of these orchids did not ensure that their roots performed CAM photosynthesis. Further work is needed to address the questions raised in this study and to determine if the photosynthetic roots of these taxa are capable of assimilating atmospheric CO₂.     

海南霸王岭不同森林类型附生兰科植物的多样性和分布

附生兰科植物是热带林附生植物的主要类群之一,对于维持热带林生态系统的物种多样性及生态功能具有重要的作用。以海南岛霸王岭国家级自然保护区内的6种热带原始林类型(热带季雨林、低地雨林、热带针叶林、山地雨林、山地常绿林及山顶矮林)中的附生兰科植物为研究对象,通过样带调查(每个森林类型设置12个10m×50m的样带,记录每个样带内胸径(DBH)≥5cm的树木及藤本上附生兰科植物的物种名称、株数及附生位置)分析了附生兰科植物的物种多样性、附生位置及其在不同森林类型中的分布规律。结果表明:1)3.6hm2森林调查样带内共记录到附生兰科植物9634株,分属于26属60种;2)除趋势对应分析(DCA)结果表明,6种森林类型中的附生兰科植物可分成5组(其中,山地常绿林与山顶矮林内的附生兰科植物归为一组);3)分布海拔范围相临近的森林类型的附生兰科植物具有较高的相似性,山地常绿林和山顶矮林附生兰科植物的相似性最高(88.9%);4)6种森林类型中,较高海拔的3种森林类型(山地雨林、山地常绿林和山顶矮林)中,附生兰科植物的丰富度和多度均显著高于其在较低海拔的3种森林类型(热带季雨林、低地雨林和热带针叶林),其中,附生兰科植物在山地常绿林内的丰富度和多度均最高;5)热带季雨林、低地雨林、热带针叶林及山地雨林内,宿主冠区附生兰科植物的多度均高于干区;山地常绿林内两者之间无显著差异;而山顶矮林干区的附生兰科植物的多度高于冠区;6)调查木上附生兰科植物的发生率在高海拔森林类型均高于其在低海拔森林类型,各森林类型内附生兰科植物的多度及物种丰富度与宿主胸径均存在显著正相关关系。     

Drought resistance does not explain epiphytic abundance of accidental epiphytes

ABSTRACT

Background

Accidental epiphytism is common among vascular plants in forest ecosystems around the globe. A frequent observation in surveys of accidental epiphytes is the occurrence of few species with high epiphytic abundance, while most co-occurring terrestrial species are rarely found as epiphytes.     

Comparative vegetative anatomy and systematics of Cymbidium (Cymbidieae: Orchidaceae)

The genus Cymbidium (Orchidaceae) exhibits distinctive ecological diversification and occurs in terrestrial, epiphytic, and lithophytic life forms. One species, Cymbidium macrorhizon , lacks foliage leaves and has a strongly mycoparasitic existence. Correlation between habitat differentiation and anatomical characters was tested for 21 species of Cymbidium and its putative sister groups. Although hypostomaty characterizes the genus, C. canaliculatum shows amphistomaty. Ecological preference of this species indicates that amphistomaty is likely adapted to intensive insolation. Four types of subepidermal foliar sclerenchyma were found. Two forest floor species, C. goeringii and C. lancifolium as well as the mycoparasitic C. macrorhizon , do not have this sclerenchyma. In this genus, development of sclerenchyma is correlated with the degree of epiphytism. Palisade mesophyll evolved in Cymbidium section Cymbidium . As members of this section grow on isolated trees in tropical lowland forests or on rocks, the differentiation of palisade tissue is probably correlated with immigration to high light habitats. With the exception of C. macrorhizon , stegmata were found in leaves and stems of Cymbidium . Furthermore, a few epiphytic species have stegmata in their roots; this is a curious feature rarely found in vascular plants. Subterranean rhizomes characterize terrestrial species, while ageotropic roots are found in some epiphytic species. Cymbidium macrorhizon shows peculiar features such as degeneration of stomata, anomocytic stomata, and lack of stegmata and sclerenchyma. This set of character transformations is probably correlated with the evolution of mycoparasitic existence. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 2002, 138 , 383–419.     

Fruit set, nectar reward, and rarity in the Orchidaceae

A review of comparative levels of reproductive success among nectariferous and nectarless orchids worldwide was compiled from a comprehensive survey of fruit set from 117 orchid species in the literature and from our own field studies. It confirms the hypothesis that nectariferous orchids are more successful in setting fruit than are nectarless species. Overall fruit set figures for nectarless and nectariferous orchids were 19.5 and 49.3% for North America, 27.7 and 63.1% for Europe, 41.4 and 74.4% for the temperate southern hemisphere, and 11.5 and 24.9% for the tropics, demonstrating that the dichotomy is consistent across all geographical areas. On average, the provision of nectar doubles the probability of fruit set in both temperate and tropical areas, but tropical orchids are remarkable in that all (whether nectarless or nectariferous, or terrestrial or epiphytic) display low fruit productivity (<50%). Fruiting failure in the tropics may be balanced by higher productivity per capsule, since tropical orchid fruits contain on average 150 times more seeds than temperate ones. Hybridization occurs more frequently among nectarless orchids in Britain and Europe than among nectariferous ones, and there is a significant positive association between orchid rarity and lack of nectar reward in the British Isles. Sexual reproduction in the Orchidaceae is predominantly pollinator dependent, but this can sometimes be successfully circumvented by asexual seed production (agamospermy) or, more frequently, by automatic self-pollination (autogamy). The proportion of highly successful nectarless orchids from all geographic areas is very low and comparable with that of orchids offering rewards other than nectar (～14% of species in each case) emphasizing that high reproductive success is only associated with nectar reward (53% of species). It is suggested that the evolution of nectar production within the family has been the most frequent means of escaping the reproductive limitations of low pollinator visitation frequencies.     

Epiphytism in ferns: diversity and history

As for other vascular plants, numerous adaptive strategies have been selected in epiphytic ferns in order to survive in a constraining and desiccating environment and thus to prevent dehydration and/or to access to water and nutrients. Here we present some of the specializations that allow ferns to survive in this particular habitat. Some of the most spectacular epiphytic specializations are observed in the Polypodiaceae family, involving humus-collectors which entrap humus in specialized organs, and ant-plant mutualism strategies. We then address the question of epiphytism in an evolutionary context. There is little fossil evidence of vascular epiphytes. Inferring the evolution of epiphytism in extant ferns shows that diversification of major living epiphytic groups mostly occurred in the Tertiary. Finally, we focus on the Hymenophyllaceae family which provides an original example of hygrophilous epiphytic strategy that is unique in vascular plants. To cite this article: J.-Y. Dubuisson et al., C. R. Biologies 332 (2009).     

Mycorrhizal Fungi Promote Growth and Nitrogen Utilization by Dendrobium nobile (Orchidaceae)

Mycorrhizal associations play a key role in the life cycle and evolutionary history of orchids. Although most orchid species are tropical and epiphytic, their mycorrhizae are poorly understood compared with those of temperate, terrestrial orchids. To investigate the influences of such fungi on photosynthetic, epiphytic orchids, we inoculated seedlings of Dendrobium nobile with Epulorhiza sp. (S1) or Tulasnella sp. (S3). These fungi had been identified based on their morphological and molecular characters. Both S1 and S3 formed symbiotic associations with our seedlings, promoting their growth and development to various degrees. Results from signature experiments with the 15N stable isotope suggested that the utilization of organic nitrogen by orchid seedlings was significantly improved by S1, but not by S3. Dendrobine contents were significantly higher in all inoculated seedlings. Our findings demonstrate that these mycorrhizal fungi enhance plant growth, their utilization of organic nitrogen, and the accumulation of secondary metabolites in this epiphytic orchid species.     

云南哀牢山地区森林附生维管植物多样性及区系特征

附生植物作为山地森林生态系统中重要的结构性成分,在维持森林生态系统生物多样性格局、水分和养分循环等方面发挥着重要作用。本文通过野外调查、标本查阅并结合相关文献,对云南哀牢山地区附生维管植物物种组成及分布进行了系统研究。结果显示,哀牢山地区附生维管植物共有23科83属218种,其中附生蕨类和兰科植物最丰富。附生蕨类有34属93种,以附生-石生蕨类生活型占优势,其中水龙骨科17属62种,占附生蕨类的66.67%,瓦韦属(Lepisorus)和石韦属(Pyrrosia)分别有13种和10种。附生兰科植物有26属65种,其中石斛属(Dendrobium)和石豆兰属(Bulbophyllum)分别有12种和8种。该地区附生维管植物属的分布具有明显的热带性质并以热带亚洲分布居多。附生植物生长于生境因子变化剧烈、资源有限的林冠,对环境变化敏感,极易遭受破坏且破坏后难以恢复,不少附生植物具有很高的药用、观赏等价值。因此,应加强对附生维管植物这一特殊类群的保护。     

Effects of altitude and climate in determining elevational plant species richness patterns: A case study from Los Tuxtlas,Mexico

Altitudinal changes of composition and richness of montane plant assemblages are complex, depending on the taxonomic group and gradient conditions, with different factors involved that are directly altitude-dependent (e.g., temperatures, air pressure) and altitude-independent (e.g., precipitation, cloud cover, area). In order to assess the relative impacts of temperature, precipitation, air humidity, and area of altitudinal belts on plant diversity, we analyzed diversity patterns of five species-rich groups, mostly herbaceous plants, in 74 forest plots along three climatically contrasting elevational transects from humid tropical lowland vegetation up to cloud forests at Los Tuxtlas, Mexico. We recorded 278 plant species, with ferns being the most species-rich group followed by orchids, bromeliads, aroids, and piperoids. The most striking results were the contrasting patterns and model results for terrestrial and epiphytic taxa. Whereas the richness of all terrestrial species taken together did not change significantly with elevation, vascular epiphytes showed increasing species numbers with altitude. However, a number of individual terrestrial taxa showed also significant elevation-related changes: aroids showed a marked decline with hight, orchids and piperoids increased, and ferns displayed a hump-shaped pattern with highest richness in mid-altitudes. Among the epiphytes, aroids declined while most other groups increased with altitude. This distinction is relevant for projections of responses of plant communities to climate change, which will lead to increased temperatures and to changing precipitation and cloud condensation regimes and thus will likely affect terrestrial and epiphytic species in different ways.     

Stable isotopic composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect*

The foliar content of nitrogen and the relative abundances of ¹³C and ¹⁵N were analysed in vascular epiphytes collected from six sites along an altitudinal gradient from tropical dry forests to humid montane forests in eastern Mexico. The proportion of epiphyte species showing crassulacean acid metabolism (CAM) (atmospheric bromeliads, thick-leaved orchids, Cactaceae, and Crassulaceae) decreased with increasing elevation and precipitation from 58 to 6%. Atmospheric bromeliads, almost all of which had δ ¹³C values indicating CAM, were more depleted in ¹⁵N (x = ? 10·9‰ ± 2·11) than the C₃ bromeliads which form water-storing tanks ( ? 6·05‰ ± 2·26). As there was no difference in δ ¹⁵N values between C₃ and CAM orchids, the difference in bromeliads was not related to photosynthetic pathways but to different nitrogen sources. While epiphytes with strong ¹⁵N depletion appear to obtain their nitrogen mainly from direct atmospheric deposition, others have access to nitrogen in intercepted water and from organic matter decomposing on branches and in their phytotelmata. Bromeliads and succulent orchids had a lower foliar nitrogen content than thin-leaved orchids, ferns and Piperaceae. Ground-rooted hemi-epiphytes exhibited the highest nitrogen contents and δ ¹⁵N values.