Influence of light,dark, temperature and drought on metabolite and ion composition in nectar and nectaries of an epiphytic bromeliad species (Aechmea fasciata)

• Research into the influence of stress factors, such as drought, different temperatures and/or varied light conditions, on plants due to climate changes is becoming increasingly important. Epiphytes, like many species of the Bromeliaceae, are particularly affected by this, but little is known about impacts on nectar composition and nectary metabolism.
• We investigated the influence of drought, different temperatures and light–dark regimes on nectar and nectaries of the epiphytic bromeliad species, Aechmea fasciata, and also the influence of drought with the terrestrial bromeliad, Billbergia nutans. The content of sugars, amino acids and ions in nectar and nectaries was analysed using HPLC. In addition, the starch content and the activities of different invertases in nectaries were determined.
• Compositions of nectar and nectaries were hardly influenced, neither by light nor dark, nor by different temperatures. In contrast, drought revealed changes in nectar volumes and nectar sugar compositions in the epiphytic bromeliad as well as in the terrestrial bromeliad. In both species, the sucrose‐to‐hexose ratio in nectar decreased considerably during the drought period. These changes in nectar sugar composition do not correlate with changes in the nectaries. The total sugar, amino acid and ion concentrations remained constant in nectar as well as in nectaries during the drought period.
• Changes in nectar composition or in the production of floral pollinator rewards are likely to affect plant–pollinator interactions. It remains questionable how far the adaptations of the bromeliads to drought and diverse light or temperature conditions are still sufficient.

     

Distribution and Flowering Ecology of Bromeliads along Two Climatically Contrasting Elevational Transects in the Bolivian Andes1

We compared the diversity, taxonomic composition, and pollination syndromes of bromeliad assemblages and the diversity and abundance of hummingbirds along two climatically contrasting elevational gradients in Bolivia. Elevational patterns of bromeliad species richness differed noticeably between transects. Along the continuously wet Carrasco transect, species richness peaked at mid‐elevations, whereas at Masicurí most species were found in the hot, semiarid lowlands. Bromeliad assemblages were dominated by large epiphytic tank bromeliads at Carrasco and by small epiphytic, atmospheric tillandsias at Masicurí. In contrast to the epiphytic taxa, terrestrial bromeliads showed similar distributions across both transects. At Carrasco, hummingbird‐pollination was the most common pollination mode, whereas at Masicurí most species were entomophilous. The proportion of ornithophilous species increased with elevation on both transects, whereas entomophily showed the opposite pattern. At Carrasco, the percentage of ornithophilous bromeliad species was significantly correlated with hummingbird abundance but not with hummingbird species richness. Bat‐pollination was linked to humid, tropical conditions in accordance with the high species richness of bats in tropical lowlands. At Carrasco, mixed hummingbird/bat‐pollination was found especially at mid‐elevations, i.e., on the transition between preferential bat‐pollination in the lowlands and preferential hummingbird‐pollination in the highlands. In conclusion, both richness patterns and pollination syndromes of bromeliad assemblages varied in distinct and readily interpretable ways in relation to environmental humidity and temperature, and bromeliad pollination syndromes appear to follow the elevational gradients exhibited by their pollinators.     

Genetic effects of tank-forming bromeliads on the associated invertebrate community in a tropical forest ecosystem

Within the area of community genetics there is an expanding volume of literature demonstrating how within-species genetic variation in temperate trees can have important effects on structuring animal and plant communities. The influence of intraspecific genetic variation on associated communities in relatively more complex ecosystems is only starting to be appreciated. Within tropical forests, epiphytic bromeliad plants often grow high in the canopy and create unique nutrient-rich microhabitats on which many invertebrate and vertebrate species depend. We investigated the influence of within-species genetic variation in the bromeliad Aechmea bracteata on the invertebrate microhabitat community. We found that more genetically similar bromeliad plants were host to more similar communities of juvenile-stage invertebrates, but not adult invertebrates. We discuss possible mechanisms for this, including differential survival and active female oviposition choice. Our work shows that the impact of within-species genetic variation on associated ecological communities may be more general than previously considered. These results agree with recent research suggesting that within-species genetic variation may perform a supporting ecosystem service for maintaining community and ecological processes.     

Do trails affect relative abundance estimates of rainforest frogs and lizards?

The selection of a sampling protocol is critical to study amphibian and reptile communities and in many instances researchers have combined the use of visual encounter surveys (VES) conducted on trails and off trails. The effect of human‐made trails on relative abundance estimates of amphibians and reptiles has been assessed in a few temperate locations, but data are lacking for tropical sites. Our study was designed to address this issue by comparing abundance estimates of frogs and lizards on and off trails in a lowland rainforest in south‐eastern Perú. We used nocturnal VES to sample frogs and lizards along transects established on trails and off trails in two different forest types. We found that the observed relative abundance estimates of frogs and lizards were affected by the location of transects (on trail vs. off trail) and the type of forest (floodplain forest vs. terra firme forest). We also found an interaction between the two main effects, indicating that the effect of transect location with respect to trails varies as a function of habitat. Observed frog abundances were higher on trails than off trails, indicating that studies that include VES on trails will bias relative abundance estimates in contrast to studies that include only VES off trails. We suggest that transects should be established only off trails, especially for monitoring studies because trail use by humans can have a strong influence on observed animal abundance.     

The Stability of Invertebrate Communities in Bromeliad Phytotelmata in a Rain Forest Subject to Hurricanes

Communities of invertebrate animals in lower canopy and saxicolous tank bromeliads, originally studied in 1993–1997, were resampled along an elevational gradient in tabonuco, palo colorado, and dwarf or cloud forest in Puerto Rico in 2010. These Puerto Rican montane rain forests were impacted strongly by hurricanes in 1989 and 1998, so the surveys in the 1990s represented 4–8 yr of post‐hurricane recovery, whereas our recent survey represents 12 yr of post‐hurricane recovery. At most elevations, species diversity, both within individual bromeliads and at the forest scale, declined between the 1990s and 2010. This decline in diversity between decades is associated with reductions in bromeliad density as the canopy progressively closed during recovery from hurricane damage. The observed decline in alpha and gamma diversity appears to have involved the loss of rarer species, as might be expected from standard metapopulation theory. By contrast, the most common species were remarkably stable in abundance, composition, and frequency of occurrence over the two decades. In the lowermost tabonuco forest, two endemic bromeliad specialists, restricted to bromeliads for their entire life cycle, were not found on resampling. This study also demonstrates that, at least in Puerto Rico, sets of ten plants from each forest were sufficient to monitor bromeliad invertebrate populations and their diversity over time.     

Macroinvertebrates associated with submerged macrophytes: sample size and power to detect effects

When planning and conducting ecological experiments, it is important to consider how many samples are necessary to detect differences among treatments with acceptably high statistical power. An analysis of statistical power is especially important when studying epiphytic macroinvertebrate colonization of submerged plants because they exhibit large plant-to-plant variability. Despite this variability, many studies have suggested that epiphytic macroinvertebrates preferentially colonize plants based on plant architecture type (broad versus dissected leaves). In this study, we calculated the power and number of samples necessary to detect differences in epiphytic macroinvertebrate abundance (numbers and biomass) among five species and two architecture types of macrophytes in a lake in MI, U.S.A. Using power analysis, we found that we had very high power to detect the differences present between macroinvertebrate abundance by architecture type and by macrophyte species (power = 1.000 and 0.994; effect sizes = 0.872 and 0.646, respectively. However, to detect very small differences between the two architecture types and the five plant species, we determined that many more samples were necessary to achieve similar statistical power (effect size = 0.1–0.3, number of samples = 60–527 and 36–310, respectively; power = 0.9). Our results suggest that macroinvertebrate abundance does in fact vary predictably with plant architecture. Dissected-leaf plants harbored higher abundances of macroinvertebrates than broad-leaf plants (ANOVA, density p = 0.001, biomass p < 0.001). This knowledge should allow us to better design future studies of epiphytic macroinvertebrates.     

Effects of Seasonality and Dispersal on the Ciliate Community Inhabiting Bromeliad Phytotelmata in Riparian Vegetation of a Large Tropical River

This study evaluated the influence of rainfall amount on the abundance, species richness, and species occurrence and abundance distribution of the ciliate community associated with the bromeliad Aechmea distichantha. The plants were collected from a rock wall of about 10‐km long at the left bank of Paraná River. We assessed the effects of both spatial and temporal variables on the community attributes, as well as whether plants geographically closer have a similar abundance distribution and species composition. The ciliate community was substantially distinct between both hydrological periods, with greater values of species richness and abundance in the rainy period. No spatial structuring (differences in the species occurrence and abundance distribution among strata) or geographical similarity (similarity in ciliate species composition among the plants) was found. Multiple regression analysis showed a positive relationship only between the ciliate abundances and water volumes for both periods. Although few of the formulated predictions were confirmed, our study provides valuable information on the ecological aspects of the ciliate community inhabiting bromeliad phytotelmata.     

Nitrogen deposition drives lichen community changes through differential species responses

Nitrogen (N) deposition has increased globally over the last 150 years and further increases are predicted. Epiphytic lichens decline in abundance and diversity in areas with high N loads, and the abundance of lichens decreases along gradients of increased deposition. Thus, although N is an essential nutrient for lichens, excessive loads may be detrimental for them. However, these gradients include many correlated pollutants and the mechanisms behind the decline are thus poorly known. The aim of this study was to assess effects of N deposition, alone, on the epiphytic lichen community composition in a naturally N‐poor boreal forest. For this purpose, whole spruce trees were fertilized daily with N at five levels, equivalent to 0.6, 6, 12.5, 25, and 50 kg N ha^?1 yr^?1, during four consecutive growing seasons (2006–2009), and changes in the abundance of lichens were monitored each autumn from the preceding year (2005). The studied lichen communities were highly dynamic and responded strongly to the environmental perturbation. N deposition detectably altered the direction of succession and reduced the species richness of the epiphytic lichen communities, even at the lowest fertilization application (6 kg N ha^?1 yr^?1). The simulated N deposition caused significant changes in the abundance of Alectoria sarmentosa, Bryoria spp., and Hypogymnia physodes, which all increased at low N loads and decreased at high loads, but with species‐specific optima. The rapid decline of A. sarmentosa may have been caused by the added nitrogen reducing the stability of the lichen thalli, possibly due to increases in the photobiont: mycobiont ratio or parasitic fungal attacks. We conclude that increases in nitrogen availability, per se, could be responsible for the reductions in lichen abundance and diversity observed along deposition gradients, and those community responses may be due to physiological responses of the individual species rather than changes in competitive interactions.     

Wasp florivory decreases reproductive success in an epiphytic bromeliad

Flower predation or florivory may alter the sexual expression, floral display, and reduce the reproductive success in plants. In this article, we estimated the effect of florivory on the reproductive success of the epiphytic bromeliad Werauhia gladioliflora during 2001–2003 in a premontane area in Costa Rica. Floral buds of W. gladioliflora are attacked by the wasp Eurytoma werauhia (Eurytomidae), which inhibits flower anthesis. Nearly, a quarter of the sampled population flowers were lost due to wasp infection and it accounted for nearly 70% of the reduction in fruit set. Flowers located on the inflorescence upper segment had a higher attack incidence. In the studied population, florivory has a major role in the reproductive success of W. gladioliflora. Florivory on epiphytic plants is scarcely reported in the literature, but evidence suggests that this phenomenon is more spread in the epiphytic community. Whether florivory in W. gladioliflora is a selective pressure influencing the reproductive success or a localized factor operating at the studied population is a subject requiring additional data.     

Nitrogen fluxes from treefrogs to tank epiphytic bromeliads: an isotopic and physiological approach

Diverse invertebrate and vertebrate species live in association with plants of the large Neotropical family Bromeliaceae. Although previous studies have assumed that debris of associated organisms improves plant nutrition, so far little evidence supports this assumption. In this study we used isotopic (¹⁵N) and physiological methods to investigate if the treefrog Scinax hayii, which uses the tank epiphytic bromeliad Vriesea bituminosa as a diurnal shelter, contributes to host plant nutrition. In the field, bromeliads with frogs had higher stable N isotopic composition (δ¹⁵N) values than those without frogs. Similar results were obtained from a controlled greenhouse experiment. Linear mixing models showed that frog feces and dead termites used to simulate insects that eventually fall inside the bromeliad tank contributed, respectively, 27.7% (±0.07 SE) and 49.6% (±0.50 SE) of the total N of V. bituminosa. Net photosynthetic rate was higher in plants that received feces and termites than in controls; however, this effect was only detected in the rainy, but not in the dry season. These results demonstrate for the first time that vertebrates contribute to bromeliad nutrition, and that this benefit is seasonally restricted. Since amphibian–bromeliad associations occur in diverse habitats in South and Central America, this mechanism for deriving nutrients may be important in bromeliad systems throughout the Neotropics.     

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.     

A simulation study on the importance of size-related changes in leaf morphology and physiology for carbon gain in an epiphytic bromeliad

This study addresses the question of how size-related changes in leaf morphology and physiology influence light absorption and carbon gain of the epiphytic bromeliad Vriesea sanguinolenta. A geometrically based computer model, Y-plant, was used for the three-dimensional reconstruction of entire plants and for calculation of whole plant light interception and carbon gain. Plants of different sizes were reconstructed, and morphological and physiological attributes of young and old leaves, and small and large plants were combined to examine the individual effects of each factor on light absorption and carbon gain of the plant. The influence of phyllotaxis on light absorption was also explored. Departure of measured divergence angles between successive leaves from the ideal 137.5 degrees slightly decreased light absorption. The only morphological parameter that consistently changed with plant size was leaf shape: larger plants produced more slender foliage, which substantially reduced self-shading. Nevertheless, self-shading increased with plant size. While the maximum rate of net CO(2) uptake of leaves increased linearly with plant size by a factor of two from the smallest to the largest individual, the potential plant carbon gain (based on total foliage area) showed a curvilinear relationship, but with similar numerical variation. We conclude that leaf physiology has a greater impact on plant carbon gain than leaf and plant morphology in this epiphytic bromeliad.     

Survival, Growth, and Ecosystem Dynamics of Displaced Bromeliads in a Montane Tropical Forest1

Epiphytes generally occupy arboreal perches, which are inherently unstable environments due to periodic windstorms, branch falls, and treefalls. During high wind events, arboreal bromeliads are often knocked from the canopy and deposited on the forest floor. In this study, we used a common epiphytic tank bromeliad, Guzmania berteroniana (R. & S.) Mez, to determine if fallen bromeliads can survive, grow, and reproduce on the forest floor and evaluate the potential impact of adult dispersal on plant and soil nutrient pools. Bromeliads were transplanted to and from tree stems and the forest floor and monitored intensively for six months; survival, growth, and impacts on ecosystem nutrient pools were followed on a subset of plants for 16 months. Six months after transplanting, bromeliad mortality was low (3%), and 19 percent of study individuals had flowered and produced new juvenile shoots. Mortality on the subset of plants followed for 16 months was 14–30 percent. Although survival rates were relatively high in all habitats, bromeliads transplanted to trees grew significantly more root length (x?± SE: 189 ± 43 cm) than those moved to the forest floor (53 ±15 cm) and experienced lower rates of leaf area loss. All transplanted bromeliads rapidly altered the substrate they occupied. Individuals transplanted to and among trees rapidly decreased base cation concentrations but significantly increased P concentrations of their underlying substrate. On the ground, bromeliads increased C, N, and P concentrations within nine months of placement. Our results suggest that in this montane tropical forest, bromeliads respond rapidly to displacement, locally modify their substrates, and can access the resources needed for survival regardless of habitat.     

Ammonium and urea as nitrogen sources for bromeliads

Epiphytic bromeliads have no contact with the pedosphere, so they need to draw their nutrients from the atmosphere as well as from the host tree and animal debris. Terrestrial bromeliads, like Ananas comosus, generally depend on the soil as their main nutrient source. The aim of this study was to investigate and compare some aspects of the nitrogen metabolism of two bromeliads with different growth habits: Ananas comosus, a terrestrial bromeliad, and Vriesea gigantea, an epiphytic tank bromeliad. Nitrogen-starved plants were grown in vitro for 3, 7, 15, 30, and 60 days, either with 5 mmol L⁻¹ ammonium [(NH₄)₂SO₄] or urea as the sole nitrogen source. When NH₄⁺ was supplied to the plants, it stimulated a faster increase of chlorophyll content in A. comosus than in V. gigantea. In the presence of urea, after 15 days of the plants in culture, there was a significant increase in tissue free-NH₄⁺ and total amino acids for V. gigantea only. V. gigantea presented a higher level of total free amino acids than A. comosus when nitrogen was supplied to the plants. Asparagine was the main amino acid accumulated in both bromeliads when plants were transferred to the medium with nitrogen. When the ratio of the main individual free amino acids between the bromeliads grown in NH₄⁺ and urea was compared, values such as 7.2 for asparagine, 5.3 for glutamate, and 1.8 for aspartate in A. comosus, and values such as 2.3 for asparagine, 1.1 for glutamate and 0.7 for aspartate in V. gigantea were observed, demonstrating that the last is more efficient in assimilating urea. The results prompted us to support the idea that V. gigantea, an epiphytic tank bromeliad, is better adapted to absorb and assimilate organic nitrogen, such as urea, while A. comosus, a terrestrial plant, is better adapted to inorganic nitrogen forms, such as ammonium. The natural exposure of tank bromeliads to urea is discussed in the paper.     

Establishment of Epiphytic Bromeliads in Successional Tropical Premontane Forests in Costa Rica

Plant community composition is the combined result of species-specific competitive abilities and the availability of propagules. For epiphytic plants, current hypotheses consider that dispersal-related factors are most important. By controlling seed dispersal constraints, we experimentally examined whether the community composition of epiphytic bromeliads in a tropical premontane area is determined during early phases of seedling recruitment. Also, we tested whether establishment success was related to eco-physiological traits of the species. A total of 7200 seeds were artificially affixed on several host trees in two secondary forest patches and in a mature forest stand. Four bromeliad species with differing physiological characteristics (CAM, C₃-CAM, and C₃) and habitat preference (secondary vs. primary forest) were selected. We found that differences in seed germination probability among habitats and species were not likely to influence community assembly. After 2 yr, seedling survival and plant development were relatively higher in the early-successional forest. Seedling establishment success was not associated with specific physiological and morphological adaptations or habitat preference of the studied species. Our results were not consistent with the described community composition and rates of population recruitment of the studied species in the same successional habitats. The results support the hypothesis that chance and historic events related to seed dispersal have an important influence on community assembly of epiphytic plants. In addition, differences in growth rates and reproductive turnover among species are expected to influence the relative abundance and recruitment rates in a particular habitat.     

Mutualism influences species distribution predictions for a bromeliad‐breeding anuran under climate change

Ecological niche models, or species distribution models, have been widely used to identify potentially suitable areas for species in future climate change scenarios. However, there are inherent errors to these models due to their inability to evaluate species occurrence influenced by non‐climatic factors. With the intuit to improve the modelling predictions for a bromeliad‐breeding treefrog (Phyllodytes melanomystax, Hylidae), we investigate how the climatic suitability of bromeliads influences the distribution model for the treefrog in the context of baseline and 2050 climate change scenarios. We used point occurrence data on the frog and the bromeliad (Vriesea procera, Bromeliaceae) to generate their predicted distributions based on baseline and 2050 climates. Using a consensus of five algorithms, we compared the accuracy of the models and the geographic predictions for the frog generated from two modelling procedures: (i) a climate‐only model for P. melanomystax and V. procera; and (ii) a climate‐biotic model for P. melanomystax, in which the climatic suitability of the bromeliad was jointly considered with the climatic variables. Both modelling approaches generated strong and similar predictive power for P. melanomystax, yet climate‐biotic modelling generated more concise predictions, particularly for the year 2050. Specifically, because the predicted area of the bromeliad overlaps with the predictions for the treefrog in the baseline climate, both modelling approaches produce reasonable similar predicted areas for the anuran. Alternatively, due to the predicted loss of northern climatically suitable areas for the bromeliad by 2050, only the climate‐biotic models provide evidence that northern populations of P. melanomystax will likely be negatively affected by 2050.     

Light microhabitats,growth and photosynthesis of an epiphytic bromeliad in a tropical dry forest

In the tropical dry forest of Dzibilchaltún, Yucatan, Mexico, light microhabitats, tissue acidity changes, chlorophyll fluorescence and growth were investigated for the epiphytic bromeliad Tillandsia brachycaulos Schltdl. Most individuals occurred in sites between 20 and 60% of the height of the tree, and directly on the main trunk or branches closed to the main trunk. During the dry season, individuals received about nine times more photon flux density (PFD) than during the rainy season. Individuals that occurred under 30–59% of the daily ambient PFD showed greater leaf length increase and monthly leaf production, and produced more flowers than individuals in the brighter (>60% of ambient PFD) and the darker (11–29% of ambient PFD) light microhabitats. Well-watered plants acclimated to deep shade (6% of ambient PFD) showed values of tissue acidity similar to plants under higher light treatments. Well-watered plants under 60% of daily ambient PFD showed low values of maximum quantum efficiency at midday during most of the year but showed similar values of tissue acidity than plants under 6 and 30% of ambient PFD. Leaf temperatures of plants in low sites within the canopy and on the forest floor were significantly higher than the air during about 1 h, indicating that those plants could not dissipate the excess of heat. Individuals located in the most shaded microhabitats could also receive less amount of water from rainfall and dew. Therefore, it would be less damaging for this epiphytic bromeliad to occur in the most exposed microhabitats than in the most shaded microhabitats in this tropical dry forest.     

Do cloud forest tree species differ in their suitability as a substrate for epiphytic bromeliads?

There is evidence for the existence of varying degrees of host preference in vascular epiphytes; certain tree species can be positively, neutrally, or negatively associated with epiphytes. The objective of this study was to evaluate whether tree species of the cloud forest differ in their suitability as a substrate for epiphytic bromeliads. To evaluate the association between epiphytic bromeliad cover and host tree species, we sampled 62 plots (each of 200 m²) in four cloud forest fragments in Veracruz, Mexico. For all trees ≥10 cm in diameter at breast height (DBH), we recorded species name, DBH, and percentage cover of bromeliads in categories of tree coverage. In total, 587 trees belonging to 52 species were recorded. All of the 10 tree species used to assess differences in epiphyte cover (each with a minimum of nine individuals) supported bromeliads, but mean bromeliad cover differed significantly among the tree species. The tree species that concentrated the highest bromeliad cover were Quercus sartorii (29.86%) and Liquidambar styraciflua (21.72%). Our results indicate that, while none of the tree species analyzed was a limiting host for epiphytic bromeliads in general, varying levels of bromeliad cover occur depending on the host species in tropical montane cloud forest fragments suggesting that certain tree species are better hosts than others. The implications for conservation efforts of differential tree species suitability as epiphyte hosts are discussed.     

Phyllosphere Bacteria Improve Animal Contribution to Plant Nutrition

Many plant species have evolved special adaptations for acquiring nitrogen in nutrient‐poor soils. In Brazilian savannas, the bromeliad Bromelia balansae (Bromeliaceae) is inhabited by mutualistic spiders (Psecas chapoda, Salticidae), which provide nutrients to the plant through their debris (feces, prey carcasses). In this study, we tested if bacteria present on the B. balansae phyllosphere improves plant nutrition and growth by mineralizing complex organic N compounds from spider debris that accumulate on the phyllosphere into simple compounds that may be absorbed easily by leaves. We conducted a greenhouse experiment by manipulating bacteria abundance on the bromeliad phyllosphere using antibiotics. Using isotopic mixed model equations, we demonstrated that debris from spiders contributed 10.7 ± 1.9 percent (mean ± standard error) of the N in bromeliads that had their bacterial abundance reduced. In contrast, spider feces contributed 27.1 ± 4.4 percent of bromeliad N in the presence of the entire bacterial assemblage. These bromeliads accumulated 57 percent more soluble protein and grew 13 percent more than bromeliads that were grown under reduced bacterial density. These results highlight the importance of mineralizing bacteria on phyllosphere as a mechanism of N uptake by bromeliads.     

The contribution of microorganisms and metazoans to mineral nutrition in bromeliads

Aims One critical challenge for plants is to maintain an adequate nutrient supply under fluctuating environmental conditions. This is particularly true for epiphytic species that have limited or no access to the pedosphere and often live in harsh climates. Bromeliads have evolved key innovations such as epiphytism, water-absorbing leaf trichomes, tank habit and Crassulacean acid metabolism (CAM) photosynthesis that enable them to survive under various environmental conditions. Bromeliads encompass diverse ecological types that live on different substrates (they can be terrestrial, epilithic or epiphytic) and vary in their ability to retain water (they can be tank-forming or tankless) and photosynthetic pathway (i.e. C₃ or CAM). In this review, we outline the nutritional modes and specializations that enable bromeliads to thrive in a wide range of nutrient-poor (mostly nitrogen-depleted) environments.Important findings Bromeliads have evolved a great diversity of morphologies and functional adaptations leading to the existence of numerous nutritional modes. Focusing on species that have absorptive foliar trichomes, we review evidence that bromeliads have evolved multi-faceted nutritional strategies to respond to fluctuations in the supply of natural nitrogen (N). These plants have developed mutualistic associations with many different and functionally diverse terrestrial and aquatic microorganisms and metazoans that contribute substantially to their mineral nutrition and, thus, their fitness and survival. Bacterial and fungal microbiota-assisted N provisioning, protocarnivory, digestive mutualisms and myrmecotrophic pathways are the main strategies used by bromeliads to acquire nitrogen. The combination of different nutritional pathways in bromeliads represents an important adaptation enabling them to exploit nutrient-poor habitats. Nonetheless, as has been shown for several other vascular plants, multiple partners are involved in nutrient acquisition indicating that there have been convergent adaptations to nutrient scarcity. Finally, we point out some gaps in the current knowledge of bromeliad nutrition that offer fascinating research opportunities.