Epiphytic Research Articles

Tree size predicts vascular epiphytic richness of traditional cultivated tea plantations in Southwestern China

Species–area relationship has been widely addressed on many plant communities, but very few have conducted on epiphytic communities. Epiphytic plants are plentiful on ancient tea trees (Camelia sinensis var. assamica) in the well-known Jingmai tea plantation area, Langcang region of Yunnan Province, SW China, and add to the plant community biodiversity. We investigated 343 tea trees with various ground diameter, canopy area, under branch height, and tree height. A total of 146 vascular epiphytic plants, belonging to 19 species in seven families were recorded from the trunk or branches of 93 (27.11%) investigated trees. We examined in situ abundance, richness, and diversity (Shannon–Weiner index) of the recorded vascular epiphytes, and their relationships to tree variables. Our results showed that the distribution (abundance, richness, and diversity) of epiphytic plants are significantly related to the canopy area (p<0.05) and basal diameter (p<0.0001) of tea trees, supporting their use as key factors and good predictor for the epiphyte’s appearance in this type of agro-ecosystems. We also concluded that the species–area relationship is a useful epiphytic species community research tool.

Dendrobium: Sources of Active Ingredients to Treat Age-Related Pathologies.

Dendrobium represents one of the most important orchid genera, ornamentally and medicinally. Dendrobiums are sympodial epiphytic plants, which is a name they are worthy of, the name coming from Greek origin: "dendros", tree, and "bios", life. Dendrobium species have been used for a thousand years as first-rate herbs in traditional Chinese medicine (TCM). They are source of tonic, astringent, analgesic, antipyretic, and anti-inflammatory substances, and have been traditionally used as medicinal herbs in the treatment of a variety of disorders, such as, nourishing the stomach, enhancing production of body fluids or nourishing Yin. The Chinese consider Dendrobium as one of the fifty fundamental herbs used to treat all kinds of ailments and use Dendrobium tonic for longevity. This review is focused on main research conducted during the last decade (2006-2016) on Dendrobium plants and their constituents, which have been subjected to investigations of their pharmacological effects involving anticancer, anti-diabetic, neuroprotective and immunomodulating activities, to report their undeniable potential for treating age-related pathologies.

Obligate plant farming by a specialized ant

Many epiphytic plants have associated with ants to gain nutrients. Here, we report a novel type of ant-plant symbiosis in Fiji where one ant species actively and exclusively plants the seeds and fertilizes the seedlings of six species of Squamellaria (Rubiaceae). Comparison with related facultative ant plants suggests that such farming plays a key role in mutualism stability by mitigating the critical re-establishment step.

Identification and Characterization of a Chloroplast-Targeted Obg GTPase in Dendrobium officinale.

Bacterial homologous chloroplast-targeted Obg GTPases (ObgCs) belong to the plant-typical Obg group, which is involved in diverse physiological processes during chloroplast development. However, the evolutionarily conserved function of ObgC in plants remains elusive and requires further investigation. In this study, we identified DoObgC from an epiphytic plant Dendrobium officinale and demonstrated the characteristics of DoObgC. Sequence analysis indicated that DoObgC is highly conserved with other plant ObgCs, which contain the chloroplast transit peptide (cTP), Obg fold, G domain, and OCT regions. The C terminus of DoObgC lacking the chloroplast-targeting cTP region, DoObgCΔ1-160, showed strong similarity to ObgE and other bacterial Obgs. Overexpression of DoObgCΔ1-160 in Escherichia coli caused slow cell growth and an increased number of elongated cells. This phenotype was consistent with the phenotype of cells overexpressing ObgE. Furthermore, the expression of recombinant DoObgCΔ1-160 enhanced the cell persistence of E. coli to streptomycin. Results of transient expression assays revealed that DoObgC was localized to chloroplasts. Moreover, we demonstrated that DoObgC could rescue the embryotic lethal phenotype of the Arabidopsis obgc-t mutant, suggesting that DoObgC is a functional homolog to Arabidopsis AtObgC in D. officinale. Gene expression profiles showed that DoObgC was expressed in leaf-specific and light-dependent patterns and that DoObgC responded to wounding treatments. Our previous and present studies reveal that ObgC has an evolutionarily conserved role in ribosome biogenesis to adapt chloroplast development to the environment.

Diet selection at three spatial scales: Implications for conservation of an endangered Hawaiian tree snail

AbstractSeveral recent studies suggest local adaptation in multiple taxa across Hawaii's steep environmental gradients. Restoration efforts in devastated tropical island ecosystems may be deficient if we lack an understanding of the interactions and dependencies in communities that occur along these gradients. Endangered Hawaiian tree snails are part of a snail–epiphyte–plant system where they graze fungi and other microbes on the leaf surface, a process difficult to observe using conventional techniques. Tree snails have undergone catastrophic decline due to introduced predators, removal by shell collectors, and human‐influenced habitat degradation. Prior to this study, little was known about the relationship among tree‐snails, their host plants, and the epiphytic microbes on which they feed. In this study, we identified scale‐dependent selection of substrates in Achatinella sowerbyana and Achatinella lila across the species’ ranges. We assessed: (1) within‐plant diet selection using high‐throughput DNA sequencing (micro‐scale); (2) among‐plant selection of tree host species (small‐scale); (3) and the influence of climate on this system (macro‐scale). Selection of substrates occurred at two scales: fungal communities in fecal samples differed in composition from those available on leaf surfaces; and at all sites, snail occurrence on Metrosideros polymorpha, a foundational forest plant, was significantly higher than expected based on availability. Habitat restoration efforts should focus on out‐planting of M. polymorpha, the preferred snail host tree, in degraded habitat. Fungal differences across sites suggest relocation efforts to predator‐free enclosures may be hindered by microbial shifts associated with geographic distance or differing environments.

Germination of seeds of New World Urostigma (Ficus) and of Morus rubra L. (Moraceae)

The New World strangler figs of the subgenus Urostigma and possibly most of the epiphytes, stranglers and banyans of the subgenera Urostiga and Ficus in the Old World bave viscid achenes. When these achenes are ingested by birds and bats they are voided without offering any apparent change in viability or in the vise id coat. Digestion of the viscid coat by soil bacteria prior to germination explains why Urostigma seeds in the New World always germinate where there is soil and organic matter as well as humidity (floor of the forest, soil-containing cracks or cavities in tree trunks and rocks). Urostigm a and mulberry ( Morus rubra ) seeds planted experimentally in sterilized soil failed to germinate, but responded favorably when inoculated with untreated soil.

Seasonal and altitude effects on the structure of arthropod communities associated with Tillandsia violacea Baker (Bromeliaceae) in a temperate forest of Mexico

The canopy of forests has been considered “the last biotic frontier,” and study of its elements is very important in explaining the global functionality in ecosystems. Epiphytic plants and arthropods are essential elements in canopy habitats, and their relationships have been studied in order to understand the high diversity in tropical forests. Nevertheless, there are few studies on this development in temperate forests. The arthropod community was studied during the rainy and dry seasons at two altitudes, and a total of 240 T. violacea plants of three sizes were collected from Abies religiosa and Quercus spp. host trees. A total of 163,043 arthropods were collected and about 200 morphospecies identified. The highest abundance was obtained during the dry season, while high diversity was found during the rainy season. There was a significant effect of plant size, host trees and collecting season on abundance and diversity, and there were seasonal variations in community composition. The community hosted on A. religiosa epiphytes showed higher abundance and density than that of Quercus.

Dieta estacional de guanacos (Lama guanicoe) y burros ferales (Equus asinus) en un ambiente semiárido de San Luis, Argentina

En la provincia de San Luis (Argentina), en un area ecotonal entre las regiones del Monte y del Chaco Seco, coexisten poblaciones de guanacos y burros asilvestrados. Dado que diferentes especies de herbivoros con masas corporales similares y viviendo en simpatria pueden estar sujetas a competencia interespecifica por alimento, se decidio determinar sus comportamientos alimentarios y analizar la existencia de solapamiento trofico. Se realizaron dos muestreos a lo largo de un ano, en estacion seca (ES) y humeda (EH), para recolectar heces de cada especie y medir la disponibilidad relativa de alimento en el ambiente. Los habitos alimentarios se evaluaron mediante analisis microhistologicos en terminos de frecuencia relativa de aparicion (FR%) de las especies vegetales en las heces. La dieta del burro mostro variacion estacional en el consumo de monocotiledoneas y se correlaciono de manera positiva con lo disponible en el ambiente durante la ES. Estuvo compuesta principalmente por pastos (75% en ES y 50% en EH), y en la epoca de lluvias aumento el consumo de epifitas del genero Tillandsia spp. (40%). La dieta del guanaco tambien presento variacion estacional y se relaciono significativamente con la oferta ambiental durante la EH. Contuvo alrededor de 60% de lenosas, con un mayor porcentaje de epifitas y cactaceas en ES que en EH. Al comparar la composicion total de las dietas, el porcentaje de similitud fue 20% en ES y 40% en EH, y se observo un valor elevado de similitud en relacion al consumo de epifitas (74%) y cactaceas (64%) en EH. El resto del ano, las dietas difirieron en composicion y proporcion de especies vegetales, por lo que se concluye que el solapamiento trofico entre burros y guanacos en el area de estudio es bajo.

Structural and Heterochronic Variations During the Early Ontogeny in Toads (Anura: Bufonidae)

Abstract: In recent decades, a renewed interest in comparative studies of embryonic ontogeny in anurans is taking place. Toad embryos are often employed as model organisms, and scarce attention has been put on interspecific variations. In this work we analyze the development of transient embryonic and larval structures in 21 species in five genera of Bufonidae. These species vary in their ovipositional mode and the type of environments where the embryos and tadpoles develop, including ponds, streams, and axils of leaves of terrestrial or epiphytic plants. Comparative anatomical studies and sequence heterochrony analyses show that primary morphological variations occur in the morphology at the tail-bud stage, the arrangement and development of the external gills, adhesive gland type and division timing, growth of the dorsal hatching gland on the head, configuration of the oral disc, emergence and development of the hind limbs, and presence of the abdominal sucker. Some of these transformations are best ex...

Species distribution and drug-resistance analysis of urinary fungal infections in older adults

Objective To analyze the detection rates, species distribution and drug-resistance of urinary fungal infection in elderly patients at Beijing Hospital from 2011 to 2013, in order to provide the basis for the reasonable clinical use of anti-epiphyte medicines. Methods Totally 263 patients with an average of 79.6 years old were collected from Beijing Hospital. The urine from freshly voided midstream or bladder puncture was collected under aseptic condition for fungal culture, then the strains of epiphytes were identified by using API 20C AUX. The drug sensitivity was tested with ATB fungus3. Results 263 strains of epiphytes were isolated from the 2 983 urine samples, of which 92 were C. tropicalis, 85 were C. glabrata, 77 were Candida albican, and 9 were other fungus candida. The rates of drug resistance to fluconazole were 14.1%(13 strains), 37.6%(32 strains) and 15.6%(12 strains), and to itraconazole were 16.3%(15 strains), 35.3%(30 strains) and 9.1%(7 strains), respectively. All of the 263 strains were not found to have drug resistance to amphotericin. Conclusions The isolation rate of urinary fungal infections is 8.8% in Beijing Hospital. The majority of the tested fungal are C. glabrata, C. tropicalis and Candida albican, the former has higher resistance rate to azoles, and the two latter have better sensitivity to azole, and all of them have the sensitivity to amphotericin. Key words: Fungus; Species distribution; Drug-resistance; Urinary system

A δ(15)N assessment of nitrogen deposition for the endangered epiphytic orchid Laelia speciosa from a city and an oak forest in Mexico.

Atmospheric nitrogen deposition poses a major threat to global biodiversity. Tropical epiphytic plants are especially at risk given their reliance on atmospheric sources of nutrients. The leaf, pseudobulb, and root carbon and nitrogen content, C:N ratio, as well as the nitrogen isotopic composition were studied for individuals of Laelia speciosa from a city and from an oak forest in Mexico. The nitrogen content of leaves was similar between the city and the oak forest, reaching 1.3±0.2% (dry mass). The δ(15)N of leaves, pseudobulbs, and roots reached 5.6±0.2‰ in the city, values found in sites exposed to industrial and vehicular activities. The δ(15)N for plant from the oak forest amounted to -3.1±0.3‰, which is similar to values measured from sites with low industrial activities. Some orchids such as Laelia speciosa produce a single pseudobulb per year, i.e., a water and nutrient storage organ, so the interannual nitrogen deposition was studied by considering the ten most recent pseudobulbs for plants from either site formed between 2003 and 2012. The C:N ratio of the ten most recent pseudobulbs from the oak forest, as well as that of the pseudobulbs formed before 2010 for plants in the city were indistinguishable from each other, averaging 132.4±6.5, while it was lower for the two most recent pseudobulbs in the city. The δ(15)N values of pseudobulbs from the oak forest averaged ‒4.4±0.1‰ for the entire series. The δ(15)N ranged from 0.1±1.6‰ for the oldest pseudobulb to 4.7±0.2‰ for the pseudobulb formed in the city from 2008 onwards. Isotopic analysis and the C:N ratio for L. speciosa revealed that rates of nitrogen deposition were higher in the city than in the forest. The δ(15)N values of series of pseudobulbs showed that it is possible to track nitrogen deposition over multiple years.

Divergent Adaptive Strategies by Two Co-occurring Epiphytic Orchids to Water Stress: Escape or Avoidance?

Due to the fluctuating water availability in the arboreal habitat, epiphytic plants are considered vulnerable to climate change and anthropogenic disturbances. Although co-occurring taxa have been observed divergent adaptive performances in response to drought, the underlying physiological and morphological mechanisms by which epiphyte species cope with water stress remain poorly understood. In the present study, two co-occurring epiphytic orchids with different phenologies were selected to investigate their drought-resistance performances. We compared their functional traits, and monitored their physiological performances in a 25-days of drought treatment. In contrast to the deciduous species Pleione albiflora, the evergreen species Coelogyne corymbosa had different root anatomical structures and higher values for saturated water content of pseudobulbs. Moreover, plants of C. corymbosa had thicker leaves and epidermis, denser veins and stomata, and higher values for leaf mass per unit area and the time required to dry saturated leaves to 70% relative water content. However, samples from that species had lower values for net photosynthetic rate (An), stomatal length and chlorophyll content per unit dry mass. Nevertheless, due to greater capacity for water storage and conservation, C. corymbosa maintained higher An, stomatal conductance (gs), and instantaneous water-use efficiency during severe drought period, and their values for leaf water potential were higher after the water stress treatment. By Day 10 after irrigation was restarted, only C. corymbosa plants recovered their values for An and gs to levels close to those calculated prior to the imposition of water stress. Our results suggest that the different performance responding to drought and re-watering in two co-occurring epiphytic orchids is related to water-related traits and these two species have divergent adaptive mechanisms. Overall, C. corymbosa demonstrates drought avoidance by enhancing water uptake and storage, and by reducing water losses while P. albiflora employs a drought escape strategy by fixing more carbon during growing season and shedding leaves and roots at dry season, leaving a dormant pseudobulb to minimize transpiration. These findings may improve our understanding of the potential effects that climate change can have on the population dynamics of different epiphytic taxa.

Normal Alkane Distributions in Soil Samples along a Lhasa‐Bharatpur Transect

AbstractWe present n‐alkane distributions in the soil samples along a transect from Lhasa on the Tibetan Plateau to Bharatpur in Nepal, which covers a large geographical area and a wide range of climatic conditions. These data allow us to assess the significance of n‐alkane distributions in different vegetation types and their relationships to temperature and precipitation. In the tropical rainforest and broadleaved forest zones, n‐alkanes exhibit a bimodal distribution pattern with dominant homologues around n‐C31 and n‐C23. The bimodal distribution of tropical rainforest n‐alkanes may be a general pattern because of the presence of many lianas, epiphytic plants, algae and the strong microbial activity and degradation involved in the postdepositional process. In the warm‐temperate mixed forest and needle‐leaved forest zones, the long‐chain alkanes have a pattern of n‐C31 &gt; n‐C33 » n‐C27. In the alpine shrub and grassland zone, although the most abundant homologue is n‐C31, relatively high n‐C23 concentrations have also been observed in some samples. The statistical results show a good correlation between n‐alkane proxies and climatic factors. The average chain length (ACL) values are positively correlated with precipitation and temperature across the transect. The carbon preference index (CPI) values show a negative correlation with temperature and precipitation along a Lhasa–Bharatpur transect. Although there is a positive relationship between ACL and temperature, it is difficult to separate the two climatic variables (temperature and precipitation) because they are well coupled in the monsoon region.

Drought and extreme temperature tolerance for Tillandsia dasyliriifolia , an epiphytic bromeliad from the northern coastal dune scrubland in Yucatan, Mexico

The ecophysiological investigations about epiphytic plants have focused on the establishment of mechanistic explanations of how plants respond to changes in their environment. The main objective of this work was to assess the drought and extreme temperature tolerance of Tillandsia dasyliriifolia individuals growing in two coastal dune scrub sites with different precipitation patterns and microhabitat distribution. This study was focused on the effect of plant size on tolerance parameters. Drought and extreme temperature tolerance were evaluated in small (S1, 9 cm) and large individuals (S2, 35 cm). Tolerance between sites was not different but varied between size classes. Tillandsia dasyliriifolia shows moderate tolerance to drought in comparison to more succulent plants. The 50% of the leaves in small plants died after 40 days of drought and after 60 days for large plants. T. dasyliriifolia also exhibits moderate tolerance to extreme temperatures tolerance, small plants tolerate a temperature range from 11 ºC to 40 ºC and the range for large plants is a little broader (9 °C to 43 °C).

Solanum clarum and S. morelliforme as Novel Model Species for Studies of Epiphytism.

The natural history of epiphytic plant species has been extensively studied. However, little is known about the physiology and genetics of epiphytism. This is due to difficulties associated with growing epiphytic plants and the lack of tools for genomics studies and genetic manipulations. In this study, tubers were generated from 223 accessions of 42 wild potato Solanum species, including the epiphytic species S. morelliforme and its sister species S. clarum. Lyophilized samples were analyzed for 12 minerals using inductively coupled plasma optical emission spectrometry. Mineral levels in tubers of S. morelliforme and S. clarum were among the highest for 10 out of the 12 elements evaluated. These two wild potato relatives are native to southern Mexico and Central America and live as epiphytes or in epiphytic-like conditions. We propose the use of S. morelliforme and S. clarum as model organisms for the study of mineral uptake efficiency. They have a short life cycle, can be propagated vegetatively via tubers or cuttings, and can be easily grown in controlled environments. In addition, genome sequence data are available for potato. Transgenic manipulations and somatic fusions will allow the movement of genes from these epiphytes to cultivated potato.

Testate Amoeba Communities of Epilithic Mosses and Lichens: New Data from Russia, Switzerland and Italy

The testate amoebae (TA) of many potential habitats around the world have been barely investigated but data on species presence and abundance is essential to answering big questions about microbial biogeography and the diversity of protist life. One such habitat lacking basic data is epilithic mosses and lichens with only a small number of samples analysed in previous studies and no systematic attempt to understand potential environmental controls. We use a large dataset (n = 81) from sites in Russia, Switzerland and Italy to demonstrate that testate amoebae in this habitat are both abundant and diverse. The community of our samples was dominated by ubiquitous taxa and differed between the northern (Russia) and southern (Switzerland and Italy) sites, perhaps due to differences in climate or air quality. Community composition, concentration and diversity were explained by moisture content but not by elevation above the ground surface and there were no significant differences between communities of mosses and lichens. Surprisingly our data showed a significant difference between communities of epiphytic and epilithic lichens in the same region sampled at the same time. Our study adds to the evidence that moisture availability is a critical factor in structuring testate amoeba communities across habitats and highlights the paucity of knowledge of TA in many environments.

Biomonitoring potential of five sympatric Tillandsia species for evaluating urban metal pollution (Cd, Hg and Pb)

The present study quantifies non essential heavy metals highly toxic for biological systems (Pb, Hg and Cd) in five autochthonous epiphytic plants from Tillandsia genus (T. recurvata, T. meridionalis, T. duratii, T. tricholepis, T. loliacea) according to different traffic levels (reference, low, medium and high polluted sites) in Asunción (Paraguay). The three metals increased in polluted sites following Pb (till 62.99 ppm in T. tricholepis) > Cd (till 1.35 ppm in T. recurvata) > Hg (till 0.36 ppm in T. recurvata) and Pb and Cd levels were directly related to traffic flow. Although the species showed similar bioaccumulation pattern (namely, higher levels of metals in polluted sites), enrichment factors (maximum EF values 37.00, 18.16, and 11.90 for Pb, Hg, and Cd, respectively) reported T. tricholepis as the most relevant bioindicator due to its wide distribution and abundance in study sites, low metal content in control site and high metal contents in polluted sites, and significant correlations with traffic density of Pb and Cd. This study emphasizes the necessity of biomonitoring air pollution in areas out of air monitoring control such as Asunción, where the high levels of metal pollution especially Pb, may represent an increment of risk for the human population inhabiting this urban area.

Diversity and floristic characteristics of vascular epiphytes in the tropical forest of Xishuangbanna

摘要: 附生植物是山地森林生态系统中重要的结构性成分。因受林冠调查技术限制, 人们对林冠附生植物知之甚 少。本文在前人有关西双版纳植物区系研究的基础上, 结合野外调查和标本资料, 对该地区附生植物的物种组成 与分布进行了整理。结果表明, 西双版纳热带森林附生维管植物共有29科134属486种, 约占全部维管植物的11%。 附生兰科是最丰富的类群(69属293种), 其中以石斛属(Dendrobium) (49种)和石豆兰属(Bulbophyllum) (48种)物种数 最多。蕨类是仅次于兰科的附生类群(13科38属97种), 其中水龙骨科(51种)占附生蕨类总数的50%以上。基于生活 史和养分来源的划分标准, 该地区48%的附生物种属于兼性附生, 其次是以兰科为主的专性附生(46%), 半附生仅 占6%。从区系上看, 西双版纳附生植物属的分布具有明显的热带亚洲性质。附生植物主要分布于资源受限的林冠 生境, 对环境变化极为敏感, 在人为干扰日益加剧的背景下, 这类植物正面临严重威胁。因此, 需要加强对西双版

全国の道路事業における希少植物の保全対策としての移植の現状と工夫：移植困難植物（着生・混合栄養・菌従属栄養）に着目して

本研究では，移植による保全の難易度が高いと考えられる種（移植困難種）について，全国 179 の道路事業の移植事例の整理・分析を通じて，移植困難種の保全に関する現状と，移植後のモニタリング結果から生活型別の活着状況を整理した．また，工夫をこらした効果的な移植方法や移植後のモニタリング手法を抽出し，整理した．

Features of CAM-cycling expressed in the dry season by terrestrial and epiphytic plants of Clusia arrudae Planchon &amp; Triana in two rupestrian savannas of southeastern Brazil in comparison to the C3-species Eremanthus glomerulatus Less.

In rupestrian savannas in southeastern Brazil Clusia arrudae Planchon & Triana in the dry season performed CAM-cycling with very little gas exchange in the early morning followed by a long depression during the rest of the day. CAM-cycling is considered as a survival strategy under drought and the productivity of the plant which is quite abundant must rely on performance of C 3 -photosynthesis in more favorable seasons. In rupestrian savannas in the Serra do Cipo (19°14′48.9″S, 43°30′36.0″W) at 1300 m a.s.l. and in the Serra de Sao Jose (21°08′S, 44°17′W) at 1010–1030 m a.s.l. in southeastern Brazil Clusia arrudae Planchon & Triana is abundant. As CAM is frequent in the genus Clusia we supposed that it would perform CAM as a drought adaptation at the very dry rupestrian savanna sites in the dry season. At the Serra do Cipo site as control we studied the obligate C3-species Eremanthus glomerulatus Less. Both species are sympatric at this site. Eremanthus glomerulatus performed C3-photosynthesis with a midday depression. The patterns of C. arrudae were completely different so that genuine C3-photosynthesis was excluded, but they were also not typical of CAM. The stomata were almost closed during the night. Some stomatal opening and net CO2 uptake occurred in the early morning hours followed by a long depression with stomatal closure throughout the rest of the day. Nevertheless, photo inhibition was limited and photosynthetic electron transport rate remained high during this time indicating that photosynthetic excitation energy was required and suggesting that CO2 assimilation was continuing behind closed stomata based on internal sources of CO2. There was some nocturnal accumulation of organic acids (malic and citric acids) which could represent a source of CO2 during the light period. Overall, the observations can be best explained by the performance of CAM-cycling by C. arrudae. However, leaf carbon gain of C. arrudae was much inferior to that of E. glomerulatus. CAM-cycling appears to be a strategy for protection from photoinhibitory damage and survival under strong conditions of drought. Steeper more vertical leaf positions observed would assist reducing overheating during stomatal closure at high irradiance. The abundance of C. arrudae suggests that the plant must have other means to sustain productivity such as full C3-photosynthesis in the more favorable seasons.