First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae)

Background and Aims

Bromeliaceae is a species-rich neotropical plant family that uses a variety of pollinators, principally vertebrates. Tillandsia is the most diverse genus, and includes more than one-third of all bromeliad species. Within this genus, the majority of species rely on diurnal pollination by hummingbirds; however, the flowers of some Tillandsia species show some characteristics typical for pollination by nocturnal animals, particularly bats and moths. In this study an examination is made of the floral and reproductive biology of the epiphytic bromeliad Tillandsia macropetala in a fragment of humid montane forest in central Veracruz, Mexico.

Methods

The reproductive system of the species, duration of anthesis, production of nectar and floral scent, as well as diurnal and nocturnal floral visitors and their effectiveness in pollination were determined.

Key Results

Tillandsia macropetala is a self-compatible species that achieves a higher fruit production through outcrossing. Nectar production is restricted to the night, and only nocturnal visits result in the development of fruits. The most frequent visitor (75 % of visits) and the only pollinator of this bromeliad (in 96 % of visits) was the nectarivorous bat Anoura geoffroyi (Phyllostomidae: Glossophaginae).

Conclusions

This is the first report of chiropterophily within the genus Tillandsia. The results on the pollination biology of this bromeliad suggest an ongoing evolutionary switch from pollination by birds or moths to bats.     

Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae)

We examined the relationships between H2O and CO2 gas exchange parameters and leaf trichome cover in 12 species of Tillandsia that exhibit a wide range in trichome size and trichome cover. Previous investigations have hypothesized that trichomes function to enhance boundary layers around Tillandsioid leaves thereby buffering the evaporative demand of the atmosphere and retarding transpirational water loss. Data presented herein suggest that trichome-enhanced boundary layers have negligible effects on Tillandsia gas exchange, as indicated by the lack of statistically significant relationships in regression analyses of gas exchange parameters and trichome cover. We calculated trichome and leaf boundary layer components, and their associated effects on H2O and CO2 gas exchange. The results further indicate trichome-enhanced boundary layers do not significantly reduce transpirational water loss. We conclude that although the trichomes undoubtedly increase the thickness of the boundary layer, the increase due to Tillandsioid trichomes is inconsequential in terms of whole leaf boundary layers, and any associated reduction in transpirational water loss is also negligible within the whole plant gas exchange pathway.     

Systematics of Tillandsia subgenus Pseudalcantarea (Bromeliaceae)

Tillandsia subg.Pseudalcantarea (Bromeliaceae) includes four species as currently delimited. The phylogenetic relationships of the species in this group are investigated by a cladistic analysis using 16 morphological characters, withVriesea subg.Alcantarea employed as the outgroup.Tillandsia subg.Pseudalcantarea is found to be paraphyletic.Tillandsia grandis andT. paniculata are transferred toTillandsia subg.Tillandsia because they are hypothesized to share a more recent common ancestor withT. utriculata, the type of the genus, than they do with the other two species placed in subg.Pseudalcantarea, i.e.,T. baliophylla andT. viridiflora. These latter two species possibly constitute a basal clade withinTillandsia and are provisionally retained within subg.Pseudalcantarea.     

The influence of air pollution on the phyllosphere microflora composition of Tillandsia leaves (Bromeliaceae)

The effect of air pollution on total phyllospheric microflora from two species of the epiphytic neotropical genus Tillandsia (Bromeliaceae) was studied by comparing unpolluted plants living in a forest (Escazú, San José) with polluted ones from an urban site of Costa Rica (San José city). Dilutions of homogenized leaf samples were plated on media suitable for each microbial group. For each microorganism group, total counts were performed and purified strains of randomly chosen colonies were identified. There was a global reduction in the number of living microorganisms due to pollution effects, especially yeasts and bacteria, while nitrogen-fixing microorganisms and fungi were less affected. Our results showed that the phyllosphere microflora of Tillandsia plants living in a tropical urban environment changes in terms of number and species composition of yeasts and bacteria with respect to plants living in unpolluted environment.     

Effects of Irradiance on Crassulacean Acid Metabolism in the Epiphyte Tillandsia usneoides L. (Bromeliaceae)

Spanish moss (Tillandsia usneoides L.) was collected in South Carolina, maintained in a greenhouse, then exposed to five levels of photosynthetic photon flux density (PPFD) for 3 weeks. Following this treatment, plants were sampled for chlorophyll concentrations, nocturnal acid accumulations, and photosynthetic responses to subsequent exposure at a range of PPFD. No acclimation to PPFD was observed; all plants exhibited similar patterns of nocturnal CO₂ uptake and acid accumulation regardless of initial PPFD treatment. These patterns revealed that at a PPFD level of approximately 200 micromoles per square meter per second (daytime integrated PPFD of 10 moles per square meter per day), CAM saturated or, in low-PPFD plants, was optimal. The results of this study indicate that adaptation to high PPFD is not necessarily a requirement of CAM.     

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.     

Population dynamics of the epiphytic bromeliad Tillandsia butzii in cloud forest

Epiphytes are a major component of tropical montane cloud forests. Over-exploitation and forest loss and degradation affect remnant populations. In this study, we analysed the population dynamics of the epiphytic bromeliad Tillandsia butzii over a 2-y period in a tropical montane cloud forest fragment in southern Mexico. Matrix analysis revealed that the T. butzii population is likely to be stable at the study site. On average the λ value did not differ significantly from unity: λ (95% confidence interval) = 0.978 (0.936–1.001). λ was highly influenced by stasis, to a lesser extent by growth and only slightly by fecundity. Overall, adult plant stasis and phalanx growth habit played a fundamental role in population maintenance. T. butzii tolerance to xeric conditions may contribute to population stability in the studied region.     

Formation and function of a new pollen aperture pattern in angiosperms: The proximal sulcus of Tillandsia leiboldiana (Bromeliaceae)

Pollen grains are generally surrounded by an extremely resistant wall interrupted in places by apertures that play a key role in reproduction; pollen tube growth is initiated at these sites. The shift from a proximal to distal aperture location is a striking innovation in seed plant reproduction. Reversals to proximal aperture position have only very rarely been described in angiosperms. The genus Tillandsia belongs to the Bromeliaceae family, and its aperture pattern has been described as distal monosulcate, the most widespread aperture patterns recorded in monocots and basal angiosperms. Here we report developmental and functional elements to demonstrate that the sulcate aperture in Tillandsia leiboldiana is not distal as previously described but proximal. Postmeitotic tetrad observation indicates unambiguously the proximal position of the sulcus, and in vitro germination of pollen grains confirms that the aperture is functional. This is the first report of a sulcate proximal aperture with proximal germination. The observation of microsporogenesis reveals specific features in the patterns of callose thickenings in postmeiotic tetrads.     

A new genus of water mites (Acari,Hydrachnidia, Wettinidae) from bromeliad phytotelmata in the Brazilian Atlantic rainforest

Adults of Bromeliacaruscardosogen. n., sp. n. are described from phytotelmata of Quesneliaarvensis (Vellozo) Mez. (Bromeliaceae) in the subtropical area of the Atlantic rainforest, São Paulo State, Brazil. The new genus Bromeliacarus is proposed and diagnosed, based primarily on the autapomorphic presence of 7–9 pairs of acetabula flanking the gonopore. A possible relationship between Bromeliacarus and other Wettinidae are discussed.     

Responses of photosynthetic O2 evolution to PPFD in the CAM epiphyte Tillandsia usneoides L. (Bromeliaceae)

Past studies of the effects of varying levels of photosynthetic photon flux density (PPFD) on the morphology and physiology of the epiphytic Crassulacean acid metabolism (CAM) plant Tillandsia usneoides L. (Bromeliaceae) have resulted in two important findings: (1) CAM, measured as integrated nocturnal CO₂ uptake or as nocturnal increases in tissue acidity, saturates at relatively low PPFD, and (2) this plant does not acclimate to different PPFD levels, these findings require substantiation using photosynthetic responses immediately attributable to different PPFD levels, e.g., O₂ evolution, as opposed to the delayed, nocturnal responses (CO₂ uptake and acid accumulation). In the present study, instantaneous responses of O₂ evolution to PPFD level were measured using plants grown eight weeks at three PPFD (20–45, 200–350, and 750–800 mol m^-2s^-1) in a growth chamber, and using shoots taken from the exposed upper portions (maximum PPFD of 800 mol m^-2s^-1) and shaded lower portions (maximum PPFD of 140 mol m^-2s^-1) of plants grown ten years in a greenhouse. In addition, nocturnal increases in acidity were measured in the growth chamber plants. Regardless of the PPFD levels during growth, O₂ evolution rates saturated around 500 mol m^-2s^-1. Furthermore, nocturnal increases in tissue acidity saturated at much lower PPFD. Thus, previous results were confirmed: photosynthesis saturated at low PPFD, and this epiphyte does not acclimate to different levels of PPFD.Abbreviations ANOVA analysis of variance - CAM Crassulacean acid metabolism - DW dry weight - PPFD photosynthetic photon flux density - SNK Student-Newman-Keuls (to whom all correspondence should be sent-present address and reprint requests);     

Classical macroautophagy in Lobivia rauschii (Cactaceae) and possible plastidial autophagy in Tillandsia albida (Bromeliaceae) tapetum cells

The tapetum in anthers is a tissue that undergoes programmed cell death (PCD) during the production of pollen. We observed two types of autophagy prior to cell death. In Lobivia rauschii (Cactaceae), tapetum cells showed plant-type autophagosomes–autolysosomes, which have been found previously exclusively in root meristem cells. The autophagic structures were formed by a network of tubules which apparently merged laterally, thereby sequestering a portion of the cytoplasm. The organelles observed in the sequestered material included multilamellar bodies, which have not been reported earlier in these organelles. By contrast, Tillandsia albida (Bromeliaceae) tapetum cells contained no such organelles but showed plastids that might possibly carry out autophagy, as they contained portions of the cytoplasm similar to the phenomenon reported earlier in Phaseolus and Dendrobium. However, the ultrastructure of the T. albida plastids was different from that in the previous reports. It is concluded that in L. rauschii classical plant macroautophagy was involved in degradation of the cytoplasm, while in T. albida such classical macroautophagy was not observed. Instead, the data in T. albida suggested the hypothesis that plastids are able to carry out degradation of the cytoplasm.     

A new species and two new combinations of Ecuadorian Bromeliaceae (Tillandsioideae)

A new species of Guzmania, G. henniae , from southeastern Ecuador is described and illustrated. Two new combinations in the newly erected, segregate genus Racinaea (formerly Tillandsia subgenus Pseudocatopsis), R. dielsii and R. undulifolia are presented and discussed.     

Miscellaneous new taxa of Bromeliaceae (XVI)

Four new taxa of Bromeliaceae are described:Billbergia acreana from Brazil;Pitcairnia chocoensis from Colombia; andGuzmania diazii andPitcairnia filifera from Peru. Also included is the new nameWerauhia moralesii from Costa Rica. Miscellaneous new taxa of Bromeliaceae (XV) appeared in Selbyana 21: 125–131. 2000.     

Physiological responses of the CAM epiphyte Tillandsia usneoides L. (Bromeliaceae) to variations in light and water supply

In an effort to understand the mechanisms that sustain rootless atmospheric plants, the modulation of Crassulacean acid metabolism (CAM) in response to variations in irradiance and water supply was investigated in the epiphyte Tillandsia usneoides. Plants were acclimated to three light regimes, i.e. high, intermediate and low, with integrated photon flux densities (PFD) of 14.40, 8.64 and 4.32 mol m-2 d-1 equivalent to an instantaneous PFD of 200, 100, and 50 mumol m-2 s-1, respectively. Daily watering was then withdrawn from half of the plants at each PFD for 7 d prior to sampling. In response to the three PFD treatments, chlorophyll content increased in plants acclimated to lower irradiances. Light response curves using non-invasive measurements of chlorophyll fluorescence demonstrated that photosystem II efficiency (phi PSII) was maintained in high PFD acclimated plants, as they exhibited a larger capacity for non-photochemical dissipation (NPQ) of excess light energy than low PFD acclimated plants. Net CO2 uptake increased in response to higher PFD, reflecting enhanced carboxylation capacity in terms of phosphoenolpyruvate carboxylase (PEPc) and ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activities. After water was withdrawn, nocturnal net CO2 uptake and accumulated levels of acidity declined in all PFD treatments, concomitant with increased respiratory recycling of malate. Examining the strategies employed by epiphytes such as T. usneodies to tolerate extreme light and water regimes has demonstrated the importance of physiological mechanisms that allow flexible carboxylation capacity and continued carbon cycling to maintain photosynthetic integrity.     

A new ontogenetic classification of stomatal types

A new ontogenetic classification of stomatal types is proposed which replaces the three ontogenetic types of Pant (1965) with seven new ones. The new classification clearly differentiates between the developmental involvement of the subsidiary cells and the purely structural relationship of the neighbouring cells. All known, and hypothetical, ontogenetic pathways of stomatal development can he incorporated into the new classification.
An, hitherto unknown, ontogenetic type which incorporates neighbouring, mesogene subsidiary, and perigene subsidiary cell elements into the stomatal complex is described from the fern, Polypodium vulgare L.     

A new genus of the Verrucalvaceae (Oomycetes)

DICK. M. W., CROFT, B. J., MAGARF.Y, R. C, de COCK, A. W. A. M. & CLARK, G., 1989. A new genus of the Verrucalvaceae (Oomycetes) . A fungus, isolated from sugar cane in Queensland, Australia and causing the Poor Root Syndrome disease, is described and shown to be related to Verrucalvus and possesses verrucate oogonia containing plerotic oospores; it is placed in the Verrucalvaceae (Sclerosporales). On the basis of morphological and DNA studies the Verrucalvaceae has to be placed in the Saprolegniomycetidae. It follows that the order Sclerosporales (and also the Leptomitales) must be removed from the Peronosporomycetidae and placed in the Saprolegniomycetidae.     

Crassulacean acid metabolism,CO2-recycling,and tissue desiccation in the Mexican epiphyte Tillandsia schiedeana Steud (Bromeliaceae)

After 23 days without water in a greenhouse, rates of nocturnal CO₂ uptake in Tillandsia schiedeana decreased substantially and maximum rates occurred later in the dark period eventually coinciding with the onset of illumination. Nocturnal CO₂ uptake accounted for less than half the total nighttime increase in acidity measured in well-watered plants. With increased tissue desiccation, only 11–12% of measured acid accumulation was attributable to atmospheric CO₂ uptake. Plants desiccated for 30 days regained initial levels of nocturnal acid accumulation and CO₂ uptake after rehydration for 10h. These results stress the importance of CO₂ recycling via CAM in this epiphytic bromeliad, especially during droughts.Partially supported by Biomedical Sciences Support Grant RR07037.