Effects of lianas on forest biogeochemistry during their lives and afterlives.

Climate change and other anthropogenic disturbances are increasing liana abundance and biomass in many tropical and subtropical forests. While the effects of living lianas on species diversity, ecosystem carbon, and nutrient dynamics are receiving increasing attention, the role of dead lianas in forest ecosystems has been little studied and is poorly understood. Trees and lianas coexist as the major woody components of forests worldwide, but they have very different ecological strategies, with lianas relying on trees for mechanical support. Consequently, trees and lianas have evolved highly divergent stem, leaf, and root traits. Here we show that this trait divergence is likely to persist after death, into the afterlives of these organs, leading to divergent effects on forest biogeochemistry. We introduce a conceptual framework combining horizontal, vertical, and time dimensions for the effects of liana proliferation and liana tissue decomposition on ecosystem carbon and nutrient cycling. We propose a series of empirical studies comparing traits between lianas and trees to answer questions concerning the influence of trait afterlives on the decomposability of liana and tree organs. Such studies will increase our understanding of the contribution of lianas to terrestrial biogeochemical cycling, and help predict the effects of their increasing abundance.

Modelling the carbon balance in bryophytes and lichens: Presentation of PoiCarb 1.0, a new model for explaining distribution patterns and predicting climate-change effects.

PREMISE: Bryophytes and lichens have important functional roles in many ecosystems. Insight into their CO2 -exchange responses to climatic conditions is essential for understanding current and predicting future productivity and biomass patterns, but responses are hard to quantify at time scales beyond instantaneous measurements. We present PoiCarb 1.0, a model to study how CO2 -exchange rates of these poikilohydric organisms change through time as a function of weather conditions. METHODS: PoiCarb simulates diel fluctuations of CO2 exchange and estimates long-term carbon balances, identifying optimal and limiting climatic patterns. Modelled processes were net photosynthesis, dark respiration, evaporation and water uptake. Measured CO2 -exchange responses to light, temperature, atmospheric CO2 concentration, and thallus water content (calculated in a separate module) were used to parameterize the model's carbon module. We validated the model by comparing modelled diel courses of net CO2 exchange to such courses from field measurements on the tropical lichen Crocodia aurata. To demonstrate the model's usefulness, we simulated potential climate-change effects. RESULTS: Diel patterns were reproduced well, and the modelled and observed diel carbon balances were strongly positively correlated. Simulated warming effects via changes in metabolic rates were consistently negative, while effects via faster drying were variable, depending on the timing of hydration. CONCLUSIONS: Reproducing weather-dependent variation in diel carbon balances is a clear improvement compared to simply extrapolating short-term measurements or potential photosynthetic rates. Apart from predicting climate-change effects, future uses of PoiCarb include testing hypotheses about distribution patterns of poikilohydric organisms and guiding conservation strategies for species.

A new approach to an old problem: how to categorize the habit of ferns and lycophytes.

BACKGROUND AND AIMS: Substrate preferences are often treated as species traits and are used to distinguish different habits, i.e. an epiphytic, lithophytic or terrestrial habit. Such a categorization, however, ignores substantial intraspecific variation. An approach that takes biological variability within a species into account is needed. METHODS: We focused on four large genera of ferns and lycophytes and found relevant information in >500 sources, such as online databases, checklists, floras and species descriptions. Translating textual information into a quantitative index, we quantified the propensity to grow on either substrate as a continuous trait for 1475 species. KEY RESULTS: Only a minority of species exhibited strict substrate fidelity, but a majority of them showed clear habitat preferences. The relative frequencies of intermediates between strict lithophytes, epiphytes and terrestrials does not support the frequent notion of ecological similarity of the lithophytic and epiphytic habitat. CONCLUSIONS: The compiled data are useful immediately for ecological and evolutionary studies with the focal taxa. More importantly, we propose the replacement of the concept of distinct habits with one of gradual differences. This should have a profound impact on any such study with plants in general.

Phylogenetic diversity and the structure of host-epiphyte interactions across the Neotropics.

Understanding the mechanisms driving community assembly has been a major focus of ecological research for nearly a century, yet little is known about these mechanisms in commensal communities, particularly with respect to their historical/evolutionary components. Here, we use a large-scale dataset of 4,440 vascular plant species to explore the relationship between the evolutionary distinctiveness (ED) (as measured by the 'species evolutionary history' (SEH)) of host species and the phylogenetic diversity (PD) of their associated epiphyte species. Although there was considerable variation across hosts and their associated epiphyte species, they were largely unrelated to host SEH. Our results mostly support the idea that the determinants of epiphyte colonization success might involve host characteristics that are unrelated to host SEH (e.g., architectural differences between hosts). While determinants of PD of epiphyte assemblages are poorly known, they do not appear to be related to the evolutionary history of host species. Instead, they might be better explained by neutral processes of colonization and extinction. However, the high level of phylogenetic signal in epiphyte PD (independent of SEH) suggests it might still be influenced by yet unrecognized evolutionary determinants. This study highlights how little is still known about the phylogenetic determinants of epiphyte communities.

Does A Velamen Radicum Effectively Protect Epiphyte Roots against Excessive Infrared Radiation?

Velamen radicum, a dead tissue at maturity, characterizes the roots of many epiphytes. Apart from a role in water and nutrient uptake, protection against excessive radiation in the upper forest canopy has also been suggested, but this function has never been critically assessed. To test this notion, we studied the roots of 18 species of Orchidaceae and Araceae. We defined thermal insulation traits of velamina by monitoring the temperature on the velamen surface and just below the velamen while exposing it to infrared radiation. We investigated velamen's functionality-correlating morphological and thermal insulation traits. In addition, we investigated the viability of the living root tissue after heat exposure. The maximal surface temperatures ranged from 37-51 °C, while the temperature difference between the upper and lower velamen surface (i.e., ∆Tmax) ranged from 0.6-3.2 °C. We found a relationship of velamen thickness with ∆Tmax. Tissue viability was strongly affected by temperatures >42 °C, and no significant recovery after heat exposure was found. Thus, there is only limited support for an insulating function of velamen, but the data suggest considerable species-specific differences in heat tolerance. The latter could be a crucial determinant of the vertical distribution of epiphytes.

Smoothing out the misconceptions of the role of bark roughness in vascular epiphyte attachment.

Vascular epiphytes represent c. 10% of all vascular plant species. In epiphytes, attachment is essential for survival throughout consecutive ontogenetic stages of their life, starting with: (1) initial propagule attachment to the host; followed by (2) the development of first root-substrate connections; and (3) maintenance of this attachment despite increased size and mechanical disturbances by rain, wind, or crossing animals. Although structural dependence on a host is a defining characteristic of an epiphyte, the fundamental mechanism(s) of how these plants initially attach and remain attached to their hosts remain poorly understood. Bark characteristics such as stability and roughness have been highlighted as keys to an understanding of this connection. Here, we stress that the understanding of how an epiphyte attaches itself to the substrate is central for a meaningful quantification and interpretation of bark roughness. Without explicit information on the attachment mechanism or the relative sizes of the attaching structures, simply linking a haphazardly chosen index of bark roughness to epiphyte establishment is flawed. This review introduces a conceptual framework to explain the mechanistic link between epiphytes and host in different ontogenetic stages and should guide future work designed to improve our understanding of this vital part of epiphyte ecology.

Exo- and endophytic fungi enable rapid transfer of nutrients from ant waste to orchid tissue.

The epiphytic orchid Caularthron bilamellatum sacrifices its water storage tissue for nutrients from the waste of ants lodging inside its hollow pseudobulb. Here, we investigate whether fungi are involved in the rapid translocation of nutrients. Uptake was analysed with a 15 N labelling experiment, subsequent isotope ratio mass spectrometry (IRMS) and secondary ion mass spectrometry (ToF-SIMS and NanoSIMS). We encountered two hyphae types: a thick melanized type assigned to 'black fungi' (Chaetothyriales, Cladosporiales, and Mycosphaerellales) in ant waste, and a thin endophytic type belonging to Hypocreales. In few cell layers, both hyphae types co-occurred. 15 N accumulation in both hyphae types was conspicuous, while for translocation to the vessels only Hypocreales were involved. There is evidence that the occurrence of the two hyphae types results in a synergism in terms of nutrient uptake. Our study provides the first evidence that a pseudobulb (=stem)-born endophytic network of Hypocreales is involved in the rapid translocation of nitrogen from insect-derived waste to the vegetative and reproductive tissue of the host orchid. For C. bilamellatum that has no contact with the soil, ant waste in the hollow pseudobulbs serves as equivalent to soil in terms of nutrient sources.

CAM plants: their importance in epiphyte communities and prospects with global change.

BACKGROUND AND SCOPE: The epiphytic life form characterizes almost 10 % of all vascular plants. Defined by structural dependence throughout their life and their non-parasitic relationship with the host, the term epiphyte describes a heterogeneous and taxonomically diverse group of plants. This article reviews the importance of crassulacean acid metabolism (CAM) among epiphytes in current climatic conditions and explores the prospects under global change. RESULTS AND CONCLUSIONS: We question the view of a disproportionate importance of CAM among epiphytes and its role as a 'key innovation' for epiphytism but do identify ecological conditions in which epiphytic existence seems to be contingent on the presence of this photosynthetic pathway. Possibly divergent responses of CAM and C3 epiphytes to future changes in climate and land use are discussed with the help of experimental evidence, current distributional patterns and the results of several long-term descriptive community studies. The results and their interpretation aim to stimulate a fruitful discussion on the role of CAM in epiphytes in current climatic conditions and in altered climatic conditions in the future.

New Proposal of Epiphytic Bromeliaceae Functional Groups to Include Nebulophytes and Shallow Tanks.

The Bromeliaceae family has been used as a model to study adaptive radiation due to its terrestrial, epilithic, and epiphytic habits with wide morpho-physiological variation. Functional groups described by Pittendrigh in 1948 have been an integral part of ecophysiological studies. In the current study, we revisited the functional groups of epiphytic bromeliads using a 204 species trait database sampled throughout the Americas. Our objective was to define epiphytic functional groups within bromeliads based on unsupervised classification, including species from the dry to the wet end of the Neotropics. We performed a hierarchical cluster analysis with 16 functional traits and a discriminant analysis, to test for the separation between these groups. Herbarium records were used to map species distributions and to analyze the climate and ecosystems inhabited. The clustering supported five groups, C3 tank and CAM tank bromeliads with deep tanks, while the atmospheric group (according to Pittendrigh) was divided into nebulophytes, bromeliads with shallow tanks, and bromeliads with pseudobulbs. The two former groups showed distinct traits related to resource (water) acquisition, such as fog (nebulophytes) and dew (shallow tanks). We discuss how the functional traits relate to the ecosystems inhabited and the relevance of acknowledging the new functional groups.

The relationship between chlorophyllous spores and mycorrhizal associations in ferns: evidence from an evolutionary approach.

PREMISE: Approximately 14% of all fern species have physiologically active chlorophyllous spores that are much more short-lived than the more common and dormant achlorophyllous spores. Most chlorophyllous-spored species (70%) are epiphytes and account for almost 37% of all epiphytic ferns. Chlorophyllous-spored ferns are also overrepresented among fern species in habitats with waterlogged soils, of which nearly 60% have chlorophyllous spores. Ferns in these disparate habitat types also have a low incidence of mycorrhizal associations. We therefore hypothesized that autotrophic chlorophyllous spores represent an adaptation of ferns to habitats with scarce mycorrhizal associations. METHODS: We evaluated the coevolution of chlorophyllous spores and mycorrhizal associations in ferns and their relation to habitat type using phylogenetic comparative methods. RESULTS: Although we did not find support for the coevolution of spore type and mycorrhizal associations, we did find that chlorophyllous spores and the absence of mycorrhizal associations have coevolved with epiphytic and waterlogged habitats. Transition rates to epiphytic and waterlogged habitats were significantly higher in species with chlorophyllous spores compared to achlorophyllous lineages. CONCLUSIONS: Spore type and mycorrhizal associations appear to play important roles in the radiation of ferns into different habitat types. Future work should focus on clarifying the functional significance of these associations.

Diversity and putative metabolic function of prokaryotic communities in tank bromeliads along an elevation gradient in tropical Mexico.

Tank bromeliads are unique canopy microhabitats that offer freshwater and organic nutrient-rich substrates in the Neotropics. In them it is possible to thoroughly characterize environmental factors and species composition of terrestrial and aquatic biota. Therefore, these plants have been used as natural models to study how communities are distributed and assembled. Here we used amplicon sequencing of the 16S rRNA gene and their functional annotations to study the diversity and metabolic potential of prokaryotic communities in tank bromeliads in five different forests along an elevation gradient in tropical Mexico. Furthermore, we analyzed the effects of vegetation type and environmental factors inside the tanks on prokaryotic composition. We found a high prokaryotic diversity in tank bromeliads along the elevation gradient. Prokaryotes commonly observed in acidic environments rich in organic carbon, and the potential pathogen Pasteurella multocida, were present in all samples, but few amplicon sequence variants were shared between forests. The prokaryotic composition was affected by forest type, and comparisons against null models suggest that it was shaped by non-neutral processes. Furthermore, prokaryotic community changes significantly covaried with tank water temperature, pH, and inorganic carbon. We found a high diversity of putative metabolic groups dominated by chemoheterotrophs and fermenters, but taxonomic groups involved in nitrogen and sulfur cycling were also present in all samples. These results suggest that tank bromeliads promote taxonomic and metabolic diversity of the prokaryotic community at a local and regional scale and play an important role in the biogeochemistry of forest canopies in the Neotropics.

Cellular Growth in Aerial Roots Differs From That in Typical Substrate Roots.

Background and Aims: In the roots of most vascular plants, the growth zone is small, the meristem and the elongation zone are sharply separated, and only meristematic cells divide. This statement is based almost entirely on studies with soil-rooted plants. Whether aerial roots of structurally dependent (=epiphytic/hemiepiphytic) species differ is virtually unexplored. Methods: Growth of aerial roots in 20 structurally dependent plant species from eight families was studied ex situ. In 12 species, we studied the anatomical structure and distribution of cortex cell lengths and rhizoderm in the growth zone. Key Results: All the studied aerial roots had an open apical meristem, and mitoses were not restricted to the meristem. In contrast to belowground roots, relative growth rate did not strongly increase upon transition to the elongation zone, while elongating growth was often prolonged. Still, the relative growth rate was lower than in belowground roots in soil, and in different species, it did not change considerably compared to each other. Conclusions: A distinct elongation zone with rapid cell growth was missing in the studied aerial roots. Rather, there was a growth zone in which division, growth, and differentiation co-occurred. We observed a generally low relative growth rate in aerial roots and a surprisingly similar initial growth pattern in spite of the diversity in taxonomy and ecology, which resembled initial cellular growth in leaves, stems, and fleshy dicotyledonous fruit.

Holding on or falling off: The attachment mechanism of epiphytic Anthurium obtusum changes with substrate roughness.

PREMISE: For vascular epiphytes, secure attachment to their hosts is vital for survival. Yet studies detailing the adhesion mechanism of epiphytes to their substrate are scarce. Examination of the root hair-substrate interface is essential to understand the attachment mechanism of epiphytes to their substrate. This study also investigated how substrate microroughness relates to the root-substrate attachment strength and the underlying mechanism(s). METHODS: Seeds of Anthurium obtusum were germinated, and seedlings were transferred onto substrates made of epoxy resin with different defined roughness. After 2 months of growth, roots that adhered to the resin tiles were subjected to anchorage tests, and root hair morphology at different roughness levels was analyzed using light and cryo scanning electron microscopy. RESULTS: The highest maximum peeling force was recorded on the smooth surface (glass replica, 0 µm). Maximum peeling force was significantly higher on fine roughness (0, 0.3, 12 µm) than on coarse (162 µm). Root hair morphology varied according to the roughness of the substrate. On smoother surfaces, root hairs were flattened to achieve large surface contact with the substrate. Attachment was mainly by adhesion with the presence of a glue-like substance. On coarser surfaces, root hairs were tubular and conformed to spaces between the asperities on the surface. Attachment was mainly via mechanical interlocking of root hairs and substrate. CONCLUSIONS: This study demonstrates for the first time that the attachment mechanism of epiphytes varies depending on substrate microtopography, which is important for understanding epiphyte attachment on natural substrates varying in roughness.

Heterogeneity within and among co-occurring foundation species increases biodiversity.

Habitat heterogeneity is considered a primary causal driver underpinning patterns of diversity, yet the universal role of heterogeneity in structuring biodiversity is unclear due to a lack of coordinated experiments testing its effects across geographic scales and habitat types. Furthermore, key species interactions that can enhance heterogeneity, such as facilitation cascades of foundation species, have been largely overlooked in general biodiversity models. Here, we performed 22 geographically distributed experiments in different ecosystems and biogeographical regions to assess the extent to which variation in biodiversity is explained by three axes of habitat heterogeneity: the amount of habitat, its morphological complexity, and capacity to provide ecological resources (e.g. food) within and between co-occurring foundation species. We show that positive and additive effects across the three axes of heterogeneity are common, providing a compelling mechanistic insight into the universal importance of habitat heterogeneity in promoting biodiversity via cascades of facilitative interactions. Because many aspects of habitat heterogeneity can be controlled through restoration and management interventions, our findings are directly relevant to biodiversity conservation.

Simulating climate change in situ in a tropical rainforest understorey using active air warming and CO2 addition.

Future climate-change effects on plant growth are most effectively studied using microclimate-manipulation experiments, the design of which has seen much advance in recent years. For tropical forests, however, such experiments are particularly hard to install and have hence not been widely used. We present a system of active heating and CO2 fertilization for use in tropical forest understoreys, where passive heating is not possible. The system was run for 2 years to study climate-change effects on epiphytic bryophytes, but is also deemed suitable to study other understorey plants. Warm air and CO2 addition were applied in 1.6-m-tall, 1.2-m-diameter hexagonal open-top chambers and the microclimate in the chambers compared to outside air. Warming was regulated with a feedback system while CO2 addition was fixed. The setup successfully heated the air by 2.8 K and increased CO2 by 250 ppm on average, with +3 K and +300 ppm as the targets. Variation was high, especially due to technical breakdowns, but not biased to times of the day or year. In the warming treatment, absolute humidity slightly increased but relative humidity dropped by between 6% and 15% (and the vapor pressure deficit increased) compared to ambient, depending on the level of warming achieved in each chamber. Compared to other heating systems, the chambers provide a realistic warming and CO2 treatment, but moistening the incoming air would be needed to avoid drying as a confounding factor. The method is preferable over infrared heating in the radiation-poor forest understorey, particularly when combined with CO2 fertilization. It is suitable for plant-level studies, but ecosystem-level studies in forests may require chamber-less approaches like infrared heating and free-air CO2 enrichment. By presenting the advantages and limitations of our approach, we aim to facilitate further climate-change experiments in tropical forests, which are urgently needed to understand the processes determining future element fluxes and biodiversity changes in these ecosystems.

Biovera-Epi: A new database on species diversity, community composition and leaf functional traits of vascular epiphytes along gradients of elevation and forest-use intensity in Mexico.

BACKGROUND: This data paper describes a new, comprehensive database (BIOVERA-Epi) on species distributions and leaf functional traits of vascular epiphytes, a poorly studied plant group, along gradients of elevation and forest-use intensity in the central part of Veracruz State, Mexico. The distribution data include frequencies of 271 vascular epiphyte species belonging to 92 genera and 23 families across 120 20 m × 20 m forest plots at eight study sites along an elevational gradient from sea level to 3500 m a.s.l. In addition, BIOVERA-Epi provides information on 1595 measurements of nine morphological and chemical leaf traits from 474 individuals and 102 species. For morphological leaf traits, we provide data on each sampled leaf. For chemical leaf traits, we provide data at the species level per site and land-use type. We also provide complementary information for each of the sampled plots and host trees. BIOVERA-Epi contributes to an emerging body of synthetic epiphytes studies combining functional traits and community composition. NEW INFORMATION: BIOVERA-Epi includes data on species frequency and leaf traits from 120 forest plots distributed along an elevational gradient, including six different forest types and three levels of forest-use intensity. It will expand the breadth of studies on epiphyte diversity, conservation and functional plant ecology in the Neotropics and will contribute to future synthetic studies on the ecology and diversity of tropical epiphyte assemblages.

Go with the flow: The extent of drag reduction as epiphytic bromeliads reorient in wind.

Vascular epiphytes represent almost 10% of all terrestrial plant diversity. Being structurally dependent on trees, epiphytes live at the interface of vegetation and atmosphere, making them susceptible to atmospheric changes. Despite the extensive research on vascular epiphytes, little is known about wind disturbance on these plants. Therefore, this study investigated the wind-epiphyte mechanical interactions by quantifying the drag forces on epiphytic bromeliads when subjected to increasing wind speeds (5-22 m s-1) in a wind tunnel. Drag coefficients (Cd) and Vogel exponents (B) were calculated to quantify the streamlining ability of different bromeliad species. Bromeliads' reconfiguration occurred first via bending and aligning leaves in the flow direction. Then leaves clustered and reduced the overall plant frontal area. This reconfiguration caused drag forces to increase at a slower rate as wind velocity increased. In the extreme case, drag force was reduced by 50% in a large Guzmania monostachia individual at a wind velocity of 22 m s-1, compared to a stiff model. This species had one of the smallest Cd (0.58) at the highest wind velocity, and the largest negative mean B (-0.98), representing the largest reconfiguration capacity amongst the tested bromeliads. The streamlining ability of bromeliads was mainly restricted by the rigidity of the lower part of the plant where the leaves are already densely clustered. Wind speeds used in this study were generally low as compared to storm force winds. At these low wind speeds, reconfiguration was an effective mechanism for drag reduction in bromeliads. This mechanism is likely to lose its effectiveness at higher wind speeds when continuous vigorous fluttering results in leaf damage and aspects such as root-attachment strength and substrate stability become more relevant. This study is a first step towards an understanding of the mechanical bottleneck in the epiphyte-tree-system under wind stress.

Agent-based modeling of the effects of forest dynamics, selective logging, and fragment size on epiphyte communities.

Forest canopies play a crucial role in structuring communities of vascular epiphytes by providing substrate for colonization, by locally varying microclimate, and by causing epiphyte mortality due to branch or tree fall. However, as field studies in the three-dimensional habitat of epiphytes are generally challenging, our understanding of how forest structure and dynamics influence the structure and dynamics of epiphyte communities is scarce.Mechanistic models can improve our understanding of epiphyte community dynamics. We present such a model that couples dispersal, growth, and mortality of individual epiphytes with substrate dynamics, obtained from a three-dimensional functional-structural forest model, allowing the study of forest-epiphyte interactions. After validating the epiphyte model with independent field data, we performed several theoretical simulation experiments to assess how (a) differences in natural forest dynamics, (b) selective logging, and (c) forest fragmentation could influence the long-term dynamics of epiphyte communities.The proportion of arboreal substrate occupied by epiphytes (i.e., saturation level) was tightly linked with forest dynamics and increased with decreasing forest turnover rates. While species richness was, in general, negatively correlated with forest turnover rates, low species numbers in forests with very-low-turnover rates were due to competitive exclusion when epiphyte communities became saturated. Logging had a negative impact on epiphyte communities, potentially leading to a near-complete extirpation of epiphytes when the simulated target diameters fell below a threshold. Fragment size had no effect on epiphyte abundance and saturation level but correlated positively with species numbers.Synthesis: The presented model is a first step toward studying the dynamic forest-epiphyte interactions in an agent-based modeling framework. Our study suggests forest dynamics as key factor in controlling epiphyte communities. Thus, both natural and human-induced changes in forest dynamics, for example, increased mortality rates or the loss of large trees, pose challenges for epiphyte conservation.