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.

Insights into the evolutionary dynamics of Neotropical biomes from the phylogeography and paleodistribution modeling of Bromelia balansae.

PREMISE OF THE STUDY: Historical abiotic and biotic factors have strongly affected species diversification and speciation. Although pre-Pleistocene events have been linked to the divergence of several Neotropical organisms, studies have highlighted a more prominent role of Pleistocene climatic oscillations in shaping current patterns of genetic variation of plants. METHODS: We performed phylogeographic analyses based on plastidial markers and modeled the current distribution and paleodistribution of Bromelia balansae (Bromeliaceae), an herbaceous species with a wide geographical distribution in South America, to infer the processes underlying its evolutionary history. KEY RESULTS: Combined molecular and paleodistributional modeling analyses indicated retraction during the Last Glacial Maximum followed by interglacial expansion. Populations occurring in the semideciduous Atlantic Forest and the Cerrado formed two distinct genetic clusters, which have been historically or ecologically isolated since late Pliocene to early Pleistocene. Populations located in the transition zone had higher levels of genetic diversity, as expected by the long-term climatic stability in the region detected in our ecological niche models. CONCLUSIONS: Our study adds important information on how herbaceous species have been affected by past climate in Central and Southeast Brazil, helping to disentangle the complex processes that have triggered the evolution of Neotropical biota.

Trade-off between soluble protein production and nutritional storage in Bromeliaceae.

BACKGROUND AND AIMS: Bromeliads are able to occupy some of the most nutrient-poor environments especially because they possess absorptive leaf trichomes, leaves organized in rosettes, distinct photosynthetic pathways [C3, Crassulacean acid metabolism (CAM) or facultative C3-CAM], and may present an epiphytic habit. The more derived features related to these traits are described for the Tillandsioideae subfamily. In this context, the aims of this study were to evaluate how terrestrial predators contribute to the nutrition and performance of bromeliad species, subfamilies and ecophysiological types, whether these species differ in their ecophysiological traits and whether the physiological outcomes are consistent among subfamilies and types (e.g. presence/absence of tank, soil/tank/atmosphere source of nutrients, trichomes/roots access to nutrients). METHODS: Isotopic (15N-enriched predator faeces) and physiological methods (analyses of plant protein, amino acids, growth, leaf mass per area and total N incorporated) in greenhouse experiments were used to investigate the ecophysiological contrasts between Tillandsioideae and Bromelioideae, and among ecophysiological types when a predatory anuran contributes to their nutrition. KEY RESULTS: It was observed that Bromelioideae had higher concentrations of soluble protein and only one species grew more (Ananas bracteatus), while Tillandsioideae showed higher concentrations of total amino acids, asparagine and did not grow. The ecophysiological types that showed similar protein contents also had similar growth. Additionally, an ordination analysis showed that the subfamilies and ecophysiological types were discrepant considering the results of the total nitrogen incorporated from predators, soluble protein and asparagine concentrations, relative growth rate and leaf mass per area. CONCLUSIONS: Bromeliad subfamilies showed a trade-off between two strategies: Tillandsioideae stored nitrogen into amino acids possibly for transamination reactions during nutritional stress and did not grow, whereas Bromelioideae used nitrogen for soluble protein production for immediate utilization, possibly for fast growth. These results highlight that Bromeliaceae evolution may be directly associated with the ability to stock nutrients.

Breeding Guild Determines Frog Distributions in Response to Edge Effects and Habitat Conversion in the Brazil's Atlantic Forest.

Understanding the response of species with differing life-history traits to habitat edges and habitat conversion helps predict their likelihood of persistence across changing landscape. In Brazil's Atlantic Forest, we evaluated frog richness and abundance by breeding guild at four distances from the edge of a reserve: i) 200 m inside the forest, ii) 50 m inside the forest, iii) at the forest edge, and iv) 50 m inside three different converted habitats (coffee plantation, non-native Eucalyptus plantation, and abandoned pastures, hereafter matrix types). By sampling a dry and a wet season, we recorded 622 individual frogs representing 29 species, of which three were undescribed. Breeding guild (i.e. bromeliad, leaf-litter, and water-body breeders) was the most important variable explaining frog distributions in relation to edge effects and matrix types. Leaf-litter and bromeliad breeders decreased in richness and abundance from the forest interior toward the matrix habitats. Water-body breeders increased in richness toward the matrix and remained relatively stable in abundance across distances. Number of large trees (i.e. DBH > 15 cm) and bromeliads best explained frog richness and abundance across distances. Twenty species found in the interior of the forest were not found in any matrix habitat. Richness and abundance across breeding guilds were higher in the rainy season but frog distributions were similar across the four distances in the two seasons. Across matrix types, leaf-litter species primarily used Eucalyptus plantations, whereas water-body species primarily used coffee plantations. Bromeliad breeders were not found inside any matrix habitat. Our study highlights the importance of primary forest for bromeliad and leaf-litter breeders. We propose that water-body breeders use edge and matrix habitats to reach breeding habitats along the valleys. Including life-history characteristics, such as breeding guild, can improve predictions of frog distributions in response to edge effect and matrix types, and can guide more effective management and conservation actions.

Species-Specific Effects of Ant Inhabitants on Bromeliad Nutrition.

Predator activities may lead to the accumulation of nutrients in specific areas of terrestrial habitats where they dispose of prey carcasses. In their feeding sites, predators may increase nutrient availability in the soil and favor plant nutrition and growth. However, the translocation of nutrients from one habitat to another may depend on predator identity and diet, as well as on the amount of prey intake. Here we used isotopic (15N) and physiological methods in greenhouse experiments to evaluate the effects of the identity of predatory ants (i.e., the consumption of prey and nest sites) on the nutrition and growth of the bromeliad Quesnelia arvensis. We showed that predatory ants with protein-based nutrition (i.e., Odontomachus hastatus, Gnamptogenys moelleri) improved the performance of their host bromeliads (i.e., increased foliar N, production of soluble proteins and growth). On the other hand, the contribution of Camponotus crassus for the nutritional status of bromeliads did not differ from bromeliads without ants, possibly because this ant does not have arthropod prey as a preferred food source. Our results show, for the first time, that predatory ants can translocate nutrients from one habitat to another within forests, accumulating nutrients in their feeding sites that become available to bromeliads. Additionally, we highlight that ant contribution to plant nutrition may depend on predator identity and its dietary requirements. Nest debris may be especially important for epiphytic and terrestrial bromeliads in nutrient-poor environments.

Food-web structure in relation to environmental gradients and predator-prey ratios in tank-bromeliad ecosystems.

Little is known of how linkage patterns between species change along environmental gradients. The small, spatially discrete food webs inhabiting tank-bromeliads provide an excellent opportunity to analyse patterns of community diversity and food-web topology (connectance, linkage density, nestedness) in relation to key environmental variables (habitat size, detrital resource, incident radiation) and predators:prey ratios. We sampled 365 bromeliads in a wide range of understorey environments in French Guiana and used gut contents of invertebrates to draw the corresponding 365 connectance webs. At the bromeliad scale, habitat size (water volume) determined the number of species that constitute food-web nodes, the proportion of predators, and food-web topology. The number of species as well as the proportion of predators within bromeliads declined from open to forested habitats, where the volume of water collected by bromeliads was generally lower because of rainfall interception by the canopy. A core group of microorganisms and generalist detritivores remained relatively constant across environments. This suggests that (i) a highly-connected core ensures food-web stability and key ecosystem functions across environments, and (ii) larger deviations in food-web structures can be expected following disturbance if detritivores share traits that determine responses to environmental changes. While linkage density and nestedness were lower in bromeliads in the forest than in open areas, experiments are needed to confirm a trend for lower food-web stability in the understorey of primary forests.

Are sun- and shade-type anatomy required for the acclimation of Neoregelia cruenta?

Sun and shade plants are often discriminated by a number of sun- and shade-type anatomies. Nonetheless, we propose that among tank-bromeliads, changes in rosette architecture satisfy the requirements for coping with contrasting light levels. The tank-bromeliad Neoregelia cruenta naturally colonises sub-habitats ranging from full exposure to direct sunlight, to shaded environments in sand ridge plains. We quantified anatomical and morphological traits of leaves and rosettes of N. cruenta grown under sun and shade conditions. Cells with undulated lateral walls within the water parenchyma are for the first time described for the family. Under high light, leaf blades were wider, shorter, and yellowish. The rosette diameter of sun plants was less than half that of shade plants. Sun leaves overlapped with neighbouring leaves for most of their length, forming a cylindrical rosette where water accumulates. Shade leaves only overlapped in the centre of the rosette. Most anatomical traits were similar under both growth conditions. Stomata were absent from the base of sun leaves, which is probably explained by limited gas exchange at the base of the tight sun-type rosette. Data suggest that the ability of N. cruenta to acclimate to sun and shade is better explained by changes in rosette architecture than by leaf anatomy.

Are algae relevant to the detritus-based food web in tank-bromeliads?

We assessed the occurrence of algae in five species of tank-bromeliads found in contrasting environmental sites in a Neotropical, primary rainforest around the Nouragues Research Station, French Guiana. The distributions of both algal abundance and biomass were examined based on physical parameters, the morphological characteristics of bromeliad species and with regard to the structure of other aquatic microbial communities held in the tanks. Algae were retrieved in all of the bromeliad species with mean densities ranging from ∼10(2) to 10(4) cells/mL. Their biomass was positively correlated to light exposure and bacterial biomass. Algae represented a tiny component of the detrital food web in shaded bromeliads but accounted for up to 30 percent of the living microbial carbon in the tanks of Catopsis berteroniana, located in a highly exposed area. Thus, while nutrient supplies are believed to originate from wind-borne particles and trapped insects (i.e., allochtonous organic matter), our results indicate that primary producers (i.e., autochtonous organic matter) are present in this insectivorous bromeliad. Using a 24-h incubation of size-fractionated and manipulated samples from this plant, we evaluated the impact of mosquito foraging on algae, other microorganisms and rotifers. The prey assemblages were greatly altered by the predation of mosquito larvae. Grazing losses indicated that the dominant algal taxon, Bumilleriopsis sp., like protozoa and rotifers, is a significant part of the diet of mosquito larvae. We conclude that algae are a relevant functional community of the aquatic food web in C. berteroniana and might form the basis of a complementary non-detrital food web.

Spider-fed bromeliads: seasonal and interspecific variation in plant performance.

BACKGROUND AND AIMS: Several animals that live on bromeliads can contribute to plant nutrition through nitrogen provisioning (digestive mutualism). The bromeliad-living spider Psecas chapoda (Salticidae) inhabits and breeds on Bromelia balansae in regions of South America, but in specific regions can also appear on Ananas comosus (pineapple) plantations and Aechmea distichantha. METHODS: Using isotopic and physiological methods in greenhouse experiments, the role of labelled ((15)N) spider faeces and Drosophila melanogaster flies in the nutrition and growth of each host plant was evaluated, as well as seasonal variation in the importance of this digestive mutualism. KEY RESULTS: Spiders contributed 0·6 ± 0·2 % (mean ± s.e.; dry season) to 2·7 ± 1 % (wet season) to the total nitrogen in B. balansae, 2·4 ± 0·4 % (dry) to 4·1 ± 0·3 % (wet) in An. comosus and 3·8 ± 0·4 % (dry) to 5 ± 1 % (wet) in Ae. distichantha. In contrast, flies did not contribute to the nutrition of these bromeliads. Chlorophylls and carotenoid concentrations did not differ among treatments. Plants that received faeces had higher soluble protein concentrations and leaf growth (RGR) only during the wet season. CONCLUSIONS: These results indicate that the mutualism between spiders and bromeliads is seasonally restricted, generating a conditional outcome. There was interspecific variation in nutrient uptake, probably related to each species' performance and photosynthetic pathways. Whereas B. balansae seems to use nitrogen for growth, Ae. distichantha apparently stores nitrogen for stressful nutritional conditions. Bromeliads absorbed more nitrogen coming from spider faeces than from flies, reinforcing the beneficial role played by predators in these digestive mutualisms.

The pollination of Bromelia antiacantha (Bromeliaceae) in southeastern Brazil: ornithophilous versus melittophilous features.

Bromelia antiacantha flowered from December to February and during this period the central leaves and bracts displayed a bright red colour. The inflorescence bears 150-350 flowers, with 10-35 flowers opening per day over 4-5 days. The flowers are dark magenta coloured with white margins, tubular-shaped with a wide opening, and their stigma is situated below the anthers. Anthesis began around 4:00 h and flowers lasted approximately 15 h. The highest nectar volume and sugar concentration occurred between 4:00-6:00 h; after this period, both decreased throughout the day. B. antiacantha is partially self-incompatible, non-autogamous, and therefore, pollinator dependent. The hummingbirds Thalurania glaucopis, Amazilia fimbriata, and Ramphodon naevius were its most frequent pollinators (55% of the visits), visiting flowers mainly in the afternoon. The scattered distribution of B. antiacantha promoted trap-lining behaviour of the hummingbirds, which favoured fruit set through xenogamy. Corolla colour, wide flower opening, sweet odour and concentrated nectar early in the day favoured bee visitation. Of the 38 % of bee visits, 96% were made by Bombus morio, mainly in the morning and their behaviour promoted self-pollination. The bee Trigona spinipes frequently acted as a pollen and nectar thief early in the morning, excluding most of the hummingbirds. Bromelia antiacantha has ornithophilous and melittophilous features, and despite being pollinated by two kinds of agents, its reproductive success depends on a given set of circumstances.

Aechmea pectinata: a hummingbird-dependent bromeliad with inconspicuous flowers from the rainforest in south-eastern Brazil.

The pollination biology of Aechmea pectinata (Bromeliaceae) was studied in a submontane rainforest in south-eastern Brazil. This species has a mainly clumped distribution and its aggregated individuals are likely to be clones. From October to January, during the flowering period, the distal third of its leaves becomes red. The inflorescence produces 1-15 flowers per day over a period of 20-25 d. The flowers are inconspicuous, greenish-white coloured, tubular shaped with a narrow opening, and the stigma is situated just above the anthers. Anthesis begins at 0400 h and flowers last for about 13 h. The highest nectar volume and sugar concentration occur between 0600 and 1000 h, and decrease throughout the day. Aechmea pectinata is self-incompatible and therefore pollinator-dependent. Hummingbirds are its main pollinators (about 90 % of the visits), visiting flowers mainly in the morning. There is a positive correlation between the number of hummingbird visits per inflorescence and the production of nectar, suggesting that the availability of this resource is important in attracting and maintaining visitors. The arrangement of the floral structures favours pollen deposition on the bill of the hummingbirds. Flowers in clumps promote hummingbird territoriality, and a consequence is self-pollination in a broader sense (geitonogamy) as individuals in assemblages are genetically close. However, trap-lining and intruding hummingbirds promote cross-pollination. These observations suggest that successful fruit set of A. pectinata depends on both the spatial distribution of its individuals and the interactions among hummingbirds.