Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad

Abstract This article deals with the physiological ecology of the Bromeliaceae, a large neotropical family containing both terrestrial and epiphytic forms, as well as many species with crassulacean acid metabolism (CAM). The article is in two parts. In the first, we review what is known of the occurrence of CAM and C₃ species in the Bromeliaceae. The photosynthetic pathways are discussed in the context of the major taxonomic divisions within the family and the great diversity of bromeliad life-forms. Of the three subfamilies, the Pitcairnioideae contain both C₃ and CAM species and are essentially all terrestrial. In contrast, the Tillandsioideae are entirely epiphytic or saxicolous, with CAM species being restricted to the genus Tillandsia, And in the Bromelioideae all species show CAM, but terrestrial and epiphytic forms are found in about equal numbers. The evidence suggests that both CAM and the epiphytic habit arose more than once in the family's evolutionary history. In the second part we consider the photosynthetic ecology of the various bromeliad life-forms in more detail using the specific example of Trinidad (West Indies). CAM bromeliads tend to be centred on the drier regions of the island and C₃ forms on the wetter areas. However, at any one site there is a marked vertical stratification of species within the forest profile. Based on the known habitat preferences of the bromeliads, six contrasting sites were selected for field studies in Trinidad. These ranged from arid coastal scrub to montane rain forest, the vegetational and climatic characteristics of which are described here. The constancy of δ¹³C values (carbon-isotope ratios) for individual CAM species in these markedly different habitats emphasized the need for ecophysiological studies to characterize environmental effects on CO₂ assimilation and transpiration. The following papers in this series present the results of a comparative investigation of gas exchange and leaf water relations of CAM and C₃ bromeliads in situ at the various sites.     

Ecological patterns in theBromeliaceae of the lomas formations of Coastal Chile and Peru

Studies of geographic distribution and physiological adaptations in theBromeliaceae of coastal Chile and Peru provide insights into the ecological patterns of habit selection and speciation. The hyperarid coastal Atacama and Peruvian Deserts along the Pacific coast of South America contain a surprisingly rich flora of bromeliad species. These include representatives of all threeBromeliaceae subfamilies: two terrestrialBromelioideae and two terrestialPitcairnioideae, all with rooted growth morphologies, and 14 species ofTillandsioideae (allTillandsia) with epiphytic and unrooted, terrestraial representatives. TheBromelioideae are represented by two species ofPuya Molina, one each in Peru and Chile. ThePitcairnioideae are represented by two genera,Deuterocohnia andPitcairnia, with one species each. The 14Tillandsia species are distributed in five subgenera which have successfully invaded the coastal deserts, and include both widespread and local endemics with xeromorphic adaptations. All theTillandsia species are epiphytic in the broad sense, but in addition to growing on plants, they are found growing on rocks (i.e. saxicolous or epilithic). Six species (T. purpurea, T. latifolia, T. capillaris, T. marconae, T. werdermanii, andT. landbeckii) have evolved a highly specialized substrate ecology where they grow essentially unrooted on sand (i.e. epiarenic). Nowhere in the world are bromeliads more dominant or have more biomass than in these coastal species growing on sand. Many of these species grow at the absolute limits of vascular plant tolerance, with the entire community consisting of a singleTillandsia species. Rooted, terrestrial bromeliads in the coastal lomas formations (allPitcairnioideae) include CAM, C₃, and C₃-CAM flexible taxa in their metabolic systems, the CAM species growing in the most arid sites along the coast and C₃ species growing in the most mesic habitats within the center of the coastal fog belt where fog moisture input is highest. All of the epiphyticTillandsia species of the coastal desert region utilize CAM metabolism entirely or in part. At least two species,T. latifolia andT. tragophoba, utilize a flexible C₃-CAM mode of carbon fixation. Whereas most of the desert-inhabitingTillandsia species have relatively narrow leaves covered by water absorbing trichomes on their surface,T. multiflora in northern Peru andT. tragophoba in northern Chile are tank-forming species where the bases of the leaves form a water-containing reservoir. The occurrence of the latter as a local endemic in hyperarid northern Chile is remarkable since it occurs thousands of kilometers south of its closest potential relatives in the central Andes.     

Elevational gradients in species richness and endemism of selected plant groups in the central Bolivian Andes

I analyzed the distribution of Acanthaceae, Araceae, Bromeliaceae, Cactaceae, Melastomataceae, and Pteridophyta in 62 vegetation plots of 400 m² along an elevational transect between 500 m and 2450 m, and at a nearby lowland site in western Santa Cruz department, Bolivia. These groups were selected because they are physiognomically distinctive, have high species numbers, are comparatively easy to identify, adequately reflect overall floristic relationships, include a wide range of life forms, and are small. The transect was located in the Tucumano-Boliviano biogeographic zone and included drought-deciduous (<850–1000 m), mixed evergreen (850–1000 m to 1800 m), and evergreen Podocarpus-dominated (>1800 m) forests. Elevational patterns of species richness were group-specific and probably related to the ecophysiological properties of each group. Species richness in Pteridophyta and Melastomataceae was correlated with moss cover (i.e., humidity), with elevation (i.e., temperatures) in Acanthaceae and epiphytic Bromeliaceae, with potential evapotranspiration (i.e., ecosystem productivity) in Araceae, and with light availability at ground level in terrestrial Bromeliaceae and Cactaceae. Community endemism generally increased with elevation, but showed a maximum at 1700 m for terrestrial Pteridophyta, and a nonsignificant decline for epiphytic Bromeliaceae and Cactaceae. Endemism was higher for terrestrial than for epiphytic taxa, and was lower among Pteridophyta compared to all other groups, reflecting different dispersal ability among taxonomic and ecological groups. Elevational zonation, tested against a null-model of random distribution of elevational limits, revealed a significant accumulation of upper and lower elevational range boundaries at 900–1050 m and at 1500–1850 m, corresponding to the elevational limits of the main physiognomic vegetation types.     

Crassulacean acid metabolism photosynthesis in Bromeliaceae: an evolutionary key innovation

Crassulacean acid metabolism (CAM) is a photosynthetic pathway that significantly increases water use efficiency in plants. It has been proposed that CAM photosynthesis, which evolved from the ancestral C3 pathway, has played a role in the diversification of some prominent plant groups because it may have allowed them to colonize and successfully spread into arid or semi‐arid environments. However, the hypothesis that CAM photosynthesis constitutes an evolutionary key innovation, thereby enhancing diversification rates of the clades possessing it, has not been evaluated quantitatively. We tested whether CAM photosynthesis is a key innovation in the Bromeliaceae, a large and highly diversified plant family that has successfully colonized arid environments. We identified five pairs of sister groups with and without the CAM feature, including 31 genera and over 2000 species. In all five cases, the clades with CAM photosynthesis were more diverse than their C3 counterparts. We provide quantitative evidence that the evolution of CAM photosynthesis is significantly associated with increased diversification in Bromeliaceae and thus constitutes an evolutionary key innovation. We also found preliminary evidence of an association between the CAM pathway and growth habit in bromeliads, with terrestrial species being more likely to show CAM photosynthesis than epiphytic species. To our knowledge, this is the first case of a physiological attribute shown to be a key innovation in plants. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 480–486.     

Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms,habitat preference and the occurrence of CAM

Summary An investigation was carried out into the photosynthetic pathways of the complete bromeliad flora of Trinidad (West Indies). Carbon-isotope ratios (¹³C values) were used to distinguish obligate C₃ and crassulacean acid metabolism (CAM) species. Measurements were also carried out on some species in the field to test for day-night changes in leaf titratable acidity.A wide range of ¹³C values was found. The obligate CAM species had values of -10 to -20 and the obligate C₃ species of -23 to -35 CAM was found (a) in the majority of Tillandsia spp. (Tillandsioideae) and (b) in all species of Bromelioideae. The other genera of the Tillandsioideae appeared to be at least predominantly C₃. One species, Guzmania monostachia var. monostachia, was identified as a C₃-CAM intermediate, and others may well exist in the Trinidad flora. The influence of factors such as source CO₂, photosynthetic photon flux density and ambient humidity in determining the ¹³C values is discussed.The taxonomic distribution of C₃ and CAM species within the Bromeliaceae is analyzed in terms of the life-forms and ecological types recognized by Pittendrigh (1948). The most xerophytic species (the light-demanding atmospherics) all show CAM and are restricted to the drier parts of the island. Most of the species with waterstoring tanks have a wide geographic distribution: these include light-demanding C₃ plants and less light-demanding CAM plants. The shade-tolerant bromeliads, which show a requirement for high ambient humidity, are all C₃ plants. We discuss the phylogenetic origins of CAM and the epiphytic habit in the Bromeliaceae.     

Juvenile tank-bromeliads lacking tanks: do they engage in CAM photosynthesis?

In the epiphytic tillandsioids, Guzmania monostachia, Werauhia sanguinolenta, and Guzmania lingulata (Bromeliaceae), juvenile plants exhibit an atmospheric habit, whereas in adult plants the leaf bases overlap and form water-holding tanks. CO₂ gas-exchange measurements of the whole, intact plants and δ¹³C values of mature leaves demonstrated that C₃ photosynthesis was the principal pathway of CO₂ assimilation in juveniles and adults of all three species. Nonetheless, irrespective of plant size, all three species were able to display features of facultative CAM when exposed to drought stress. The capacity for CAM was the greatest in G. monostachia, allowing drought-stressed juvenile and adult plants to exhibit net CO₂ uptake at night. CAM expression was markedly lower in W. sanguinolenta, and minimal in G. lingulata. In both species, low-level CAM merely sufficed to reduce nocturnal respiratory net loss of CO₂. δ¹³C values were generally less negative in juveniles than in adult plants, probably indicating increased diffusional limitation of CO₂ uptake in juveniles.     

Photosynthetic pathway and morphological functional types in the vegetation from North-Beijing agro-pastoral ecotone, China

Photosynthetic pathways (C₃, C₄, and CAM) and morphological functional types were identified for the species from vegetation in agro-pastoral ecotone, North Beijing. 792 vascular plant species (nearly half of the total species in the ecotone), in 66 families and 317 genera, were identified with C₃, C₄, and CAM photosynthesis (Table 1). 710 species (90 % of the identified species in Table 1) in 268 genera and 64 families were found with C₃ photosynthesis, 68 species (9 % of the total identified species) in 40 genera and 7 families with C₄ photosynthesis, and 14 species in 4 genera and 1 family with CAM photosynthesis. Gramineae is the leading family with C₄ photosynthesis (43 species), Cyperaceae ranks the second (16 species) followed by Chenopodiaceae (5 species). The significant increase of C₄ proportion (C₄/total species) with land deterioration suggested the plants of this type are remarkably responsive to land use in the ecotone. 792 species were classified into nine morphological functional types and the changes of most of these types (e.g. perennial forbs (PEF), annual grasses (ANG), and annual forbs (ANF)) were consistent with habitats and vegetation dynamics in the agro-pastoral ecotone. Hence the photosynthetic pathways, combined with the morphological functional types, are efficient indications for studying the linkage between species and ecosystems in the ecotone.     

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.     

Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae)

Summary The heterophyllous epiphyte Tillandsia deppeana exhibits an atmospheric habit as a juvenile and a tank form as an adult. Both juveniles and adults utilize C₃ photosynthesis. This is the first report of an atmospheric form of Tillandsia which does not exhibit CAM. Photosynthetic saturation occurred at approximately 10% of full sunlight in both forms, but the adults exhibited greater rates of photosynthesis at all levels of irradiance. The adults also had a higher and broader photosynthetic temperature optimum than did the juveniles. The adults transpired at greater rates than the juveniles; however, the water use efficiencies of both forms were similar and were high for C₃ plants. In both forms the photosynthetic rate decreased in response to a decrease in humidity. After 8 days without water the juveniles were able to fix CO₂ throughout the day. The adults, however, exhibited a net loss of CO₂ on the second day without water and thereafter. These results indicate that the water-conservative atmospheric juvenile of T. deppeana is well adapted to establishment in the epiphytic habitat.     

Occurrence of arbuscular mycorrhizal fungi in bromeliad species from the tropical Atlantic forest biome in Brazil

The mycorrhizal status of epiphytic, rupicolous, and terrestrial bromeliad species from the Brazilian Atlantic Rain Forest has been examined. Roots of 13 species of bromeliads were analyzed for the presence of mycorrhizal structures such as arbuscules, hyphae, and vesicles as well as other fungal structures. Rhizosphere soil was sampled to identify arbuscular mycorrhizal fungal (AMF) species associated only with terrestrial bromeliad species. Most specimens collected were epiphytic bromeliads in the genera Aechmea, Bilbergia, Nidularium, Tillandsia, and Vriesea. Differentiating structures of AMF were found in only three species of bromeliads. The pattern of mycorrhizal colonization was mainly internal, and external mycelium and arbuscules were observed only in the terrestrial Nidularium procerum. Root endophytes with dark brown septate mycelium, thin external hyphae, and Rhizoctonia-like sclerotia were also detected in some root segments. A total of ten spore morphotypes were recovered from the rhizosphere of N. procerum, with Acaulospora mellea, A. foveata, and Glomus sp. being the most common species recovered. Our study demonstrated that most of the epiphytic species are not associated with AMF. We attribute this mainly to the exposed bare root conditions found in epiphytic bromeliads.     

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.     

Carbon isotope composition and mode of photosynthesis in Clusia species from Mexico

The neotropical genus Clusia comprises arborescent species exhibiting Crassulacean Acid Metabolism (CAM) as was first reported for a Mexican species, Clusia lundellii. Here, the occurrence of CAM photosynthesis was studied in 20 species of Clusia, 18 from Mexico, and 2 from Guatemala, using leaf carbon isotopic composition. In most species, samples from individuals collected in different locations were analyzed. CAM was present in at least 11 species, eight of which contained specimens with δ¹³C values less negative than −20.0 ‰, indicating strong CAM (C. chanekiana, C. flava, C. lundellii, C. mexicana, C. quadrangula, C. rosea, C. suborbicularis, and C. tetra-trianthera). δ¹³C was highly variable in some species, but CAM expression was not correlated to life form (epiphytic, hemiepiphytic, terrestrial) or habitat. CAM specimens were not collected at altitudes above 1 700 m a.s.l.     

CAM photosynthesis in submerged aquatic plants

Crassulacean acid metabolism (CAM) is a CO₂-concentrating mechanism selected in response to aridity in terrestrial habitats, and, in aquatic environments, to ambient limitations of carbon. Evidence is reviewed for its presence in five genera of aquatic vascular plants, includingIsoëtes, Sagittaria, Vallisneria, Crassula, andLittorella. Initially, aquatic CAM was considered by some to be an oxymoron, but some aquatic species have been studied in sufficient detail to say definitively that they possess CAM photosynthesis. CO₂-concentrating mechanisms in photosynthetic organs require a barrier to leakage; e.g., terrestrial C₄ plants have suberized bundle sheath cells and terrestrial CAM plants high stomatal resistance. In aquatic CAM plants the primary barrier to CO₂ leakage is the extremely high difrusional resistance of water. This, coupled with the sink provided by extensive intercellular gas space, generates daytime CO₂(pi) comparable to terrestrial CAM plants. CAM contributes to the carbon budget by both net carbon gain and carbon recycling, and the magnitude of each is environmentally influenced. Aquatic CAM plants inhabit sites where photosynthesis is potentially limited by carbon. Many occupy moderately fertile shallow temporary pools that experience extreme diel fluctuations in carbon availability. CAM plants are able to take advantage of elevated nighttime CO2 levels in these habitats. This gives them a competitive advantage over non-CAM species that are carbon starved during the day and an advantage over species that expend energy in membrane transport of bicarbonate. Some aquatic CAM plants are distributed in highly infertile lakes, where extreme carbon limitation and light are important selective factors. Compilation of reports on diel changes in titratable acidity and malate show 69 out of 180 species have significant overnight accumulation, although evidence is presented discounting CAM in some. It is concluded that similar proportions of the aquatic and terrestrial floras have evolved CAM photosynthesis. AquaticIsoëtes (Lycophyta) represent the oldest lineage of CAM plants and cladistic analysis supports an origin for CAM in seasonal wetlands, from which it has radiated into oligotrophic lakes and into terrestrial habitats. Temperate Zone terrestrial species share many characteristics with amphibious ancestors, which in their temporary terrestrial stage, produce functional stomata and switch from CAM to C₃. Many lacustrineIsoëtes have retained the phenotypic plasticity of amphibious species and can adapt to an aerial environment by development of stomata and switching to C₃. However, in some neotropical alpine species, adaptations to the lacustrine environment are genetically fixed and these constitutive species fail to produce stomata or loose CAM when artificially maintained in an aerial environment. It is hypothesized that neotropical lacustrine species may be more ancient in origin and have given rise to terrestrial species, which have retained most of the characteristics of their aquatic ancestry, including astomatous leaves, CAM and sediment-based carbon nutrition.     

Comparative ecophysiology of CAM and C3 bromeliads. III. Environmental influences on CO2 assimilation and transpiration

Abstract Field measurements of the gas exchange of epiphytic bromeliads were made during the dry season in Trinidad in order to compare carbon assimilation with water use in CAM and C₃ photosynthesis. The expression of CAM was found to be directly influenced by habitat and microclimate. The timing of nocturnal CO₂ uptake was restricted to the end of the dark period in plants found at drier habitats, and stomatal conductance in two CAM species was found to respond directly to humidity or temperature. Total night-time CO₂ uptake, when compared with malic-acid formation (measured as the dawn-dusk difference in acidity, ΔH⁺), could only account for 10–40% of the total ΔH⁺ accumulated. The remaining malic acid must have been derived from the refixation of respired CO₂ (recycling). Within the genus Aechmea (12 samples from four species), recycling was significantly correlated with night temperature at the six sample sites. Recycling was lowest in A. fendleri (54% of ΔH⁺ derived from respired CO₂), a CAM bromeliad with little water-storage parenchyma that is restricted to wetter, cooler regions of Trinidad. Gas-exchange rates of C₃ bromeliads were found to be similar to those of the CAM bromeliads, with CO₂ uptake from 1 to 3 μmol m^?2 s^?1 and stomatal conductances generally up to 100 mmol m^?2 s^?1. The midday depression of photosynthesis occurred in exposed habitats, although photosynthetically active radiation (PAR) limited photosynthesis in shaded habitats. CO₂ uptake of the C₃ bromeliad Guzmania lingulata was saturated at around 500 μmol m^?2 s^?1 PAR, suggesting that epiphytic plants found in the shaded forest understorey are shade-tolerant rather than shade-demanding. Transpiration ratios (TR) during CO₂ fixation in CAM (Phase I and IV) and C₃ bromeliads were compared at different sites in order to assess the efficiency of water utilization. For the epiphytes displaying marked uptake of CO₂, TR were found to be lower than many previously published values. In addition, the average TR values were very similar for dark CO₂ uptake in CAM (42 ± 41, n= 12), Phase IV of CAM (69 ± 36, n= 3) and for C₃ photosynthesis (99 ± 73, n= 4) in these plants. It appears that recycling of respired CO₂ by CAM bromeliads and efficient use of water in all phases of CO₂ uptake are physiological adaptations of bromeliads to arid microclimates in the humid tropics.     

Size-Dependent Variation of Carbon and Nitrogen Isotope Abundances in Epiphytic Bromeliads

Abstract: While atmospheric species of bromeliads have narrow leaves, densely covered with water‐absorbing trichomes throughout their life cycles, many tank bromeliads with broad leaves, forming phytotelmata, go through an atmospheric juvenile phase. The effect of the different habits and the phase change in tank‐forming bromeliads on water and nutrient relations was investigated by analysing the relationship between plant size, C/N ratios and the natural abundance of ¹³C and ¹⁵N in five epiphytic bromeliad species or morphospecies of a humid montane forest in Xalapa, Mexico. The atmospheric species Tillandsia juncea and T. butzii exhibited full crassulacean acid metabolism, with δ¹³C values (mean ‐ 15.3 ‰ and ‐ 14.7 ‰, respectively) independent of size. In Tillandsia species with C₃ photosynthesis, δ¹³C decreased with increasing plant size, indicating stronger drought stress in juveniles. The increase of the C/N ratio with size suggests that, at least in heteroblastic bromeliads, the availability of water is more limiting during early growth, and that limitations of nitrogen supply become more important later on, when water stored in the tank helps to bridge dry periods, reducing water shortage. δ¹⁵N values of the two atmospheric species were very negative (‐ 12.6 ‰ and ‐ 12.2 ‰, respectively) and did not change with plant size. Tank‐forming bromeliads had less negative δ¹⁵N values (c ‐ 6 ‰), and, in species with atmospheric juveniles and tank‐forming adults, δ¹⁵N values increased significantly with plant size. These differences do not appear to be an effect of the isotopic composition of N sources, but rather reflect N availability and limitation and stress‐induced changes in ¹⁵N discrimination.     

Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae

Leaf economic and hydraulic theories have rarely been applied to the ecological differentiation of speciose herbaceous plant radiations. The role of character trait divergences and network reorganization in the differentiation of the functional types in the megadiverse Neotropical Bromeliaceae was explored by quantifying a range of leaf economic and hydraulic traits in 50 diverse species. Functional types, which are defined by combinations of C₃ or Crassulacean acid metabolism (CAM) photosynthesis, terrestrial or epiphytic habits, and non‐specialized, tank‐forming or atmospheric morphologies, segregated clearly in trait space. Most classical leaf economic relationships were supported, but they were weakened by the presence of succulence. Functional types differed in trait‐network architecture, suggesting that rewiring of trait‐networks caused by innovations in habit and photosynthetic pathway is an important aspect of ecological differentiation. The hydraulic data supported the coupling of leaf hydraulics and gas exchange, but not the hydraulic safety versus efficiency hypothesis, and hinted at an important role for the extra‐xylary compartment in the control of bromeliad leaf hydraulics. Overall, our findings highlight the fundamental importance of structure–function relationships in the generation and maintenance of ecological diversity.     

C3 photosynthesis in the gametophyte of the epiphytic CAM fern Pyrrosia longifolia (Polypodiaceae)

Sporophytes of some epiphytic species in the fern genus Pyrrosia exhibit Crassulacean acid metabolism (CAM), generally considered to be a derived physiological response to xeric habitats. Because these species alternate between independent sporophytic and gametophytic generations yet only the sporophyte has been characterized physiologically, experiments were conducted to determine the photosynthetic pathways present in mature sporophytes, immature sporophytes, and gametophytes of Pyrrosia longifolia. Diurnal CO₂ exchange and malic acid fluctuations demonstrated that although the mature sporophytes exhibited CAM, only C₃ photosynthesis occurred in the gametophytes and young sporophytes. Consideration of the above results and those from previous studies, as well as the life cycle of ferns, indicates that the induction of CAM probably occurs at a certain developmental stage of the sporophyte and/or following exposure to stress. Elucidation of the precise mechanisms underlying this C₃-CAM transition awaits further research.     

CRASSULACEAN ACID METABOLISM IN THE GESNERIACEAE

The occurrence of the Crassulacean acid metabolism (CAM) was studied in four epiphytic species of the Gesneriaceae: two neotropical species, Codonanthe crassifolia and Columnea linearis, and two paleotropical species, Aeschynanthus pulcher and Saintpaulia ionantha. Gas exchange parameters, enzymology, and leaf anatomy, including mesophyll succulence and relative percent of the mesophyll volume occupied by airspace, were studied for each species. Codonanthe crassifolia was the only species to show nocturnal CO₂ uptake and a diurnal organic acid fluctuation. According to these results, Codonanthe crassifolia shows CAM-cycling under well-watered conditions and when subjected to drought, it switches to CAM-idling. Other characteristics, such as leaf anatomy, mesophyll succulence, and PEP carboxylase and NADP malic enzyme activity, indicate attributes of the CAM pathway. All other species tested showed C₃ photosynthesis. The most C₃-like species is Columnea linearis, according to the criteria tested in this investigation. The other two species show mesophyll succulence and relative percent of the leaf volume occupied by airspace within the CAM range, but no other characters of the CAM pathway. The leaf structure of certain genera of the Gesneriaceae and of the genus Peperomia in the Piperaceae are similar, both having an upper succulent, multiple epidermis, a medium palisade of one or a few cell layers, and a lower, succulent spongy parenchyma not too unlike CAM photosynthetic tissue. We report ecophysiological similarities between these two distantly related families. Thus, the occurrence of CAM-cycling may be more common among epiphytic species than is currently known.