Reproductive biology of six species of Tillandsia L. (Bromeliaceae) in Mexico.
Bromeliaceae is the largest family endemic to the Neotropics, with 56 genera and ca. 3,086 species (Luther 2006). Mexico has 18 genera and 342 species of Bromeliaceae (Espejo-Serna, Lopez-Ferrari et al. 2004), with Tillandsia as the most diverse genus in the country with ca. 192 spp.
Despite the key importance of the family mainly in the epiphytic guild in Neo-tropical communities, the reproductive biology of bromeliads is still poorly known. Breeding systems and pollination biology play an important role in the conservation biology of the species. Data from these studies combined with population demography, abundance, pollinator behavior, population genetics and dynamics, supply the biological bases to propose conservation strategies in plant populations. The epiphytic guild in particular has specific nutritional and water restrictions that imply a different scenario as compared to terrestrial plants, i.e., the high nutritional restrictions imposed a set of different life strategies, such as the fact that they have to grow, reproduce, and perpetuate with limited resources, attached to and tied to the phorophyte life cycle.
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Bromeliaceae is a clade composed mainly of hermaphroditic species and with wide morphological, floral, ecological variation, and different life histories that suggest different breeding systems. Different flower sexes and breeding systems have been reported for Bromeliaceae (Table 1) ranging from bisexual flowers to unisexual flowers and from xenogamy to cleistogmy.
In this study, the main questions were: how variable are breeding systems in the genus Tillandsia? How much floral morphology and biology predict breeding systems? How could this information help us in proposing conservation strategies about bromeliads?
Study Site: We studied the pollination biology and evaluated the breeding systems of the sympatric species Tillandsia brachycaulos (Figure 1), T. elongata var. subimbricata (Figure 2) and T. balbisiana (Figure 3) in low caducifolius forest at the Dzibilchaltun National Park (figure 4), ca. 17 km N of the city of Merida (21[degrees]5'N, 89[degrees]35'W), while studies on T. utriculata (Figure 5) were carried out in mangrove forest at the Zona Arqueologica de Xcambo (Figure 6), N of the village of Dzemul, Yucatan (21[degrees]20'N, 89[degrees]20'W) on the coast of Yucatan. Studies of T. dasyliirfolia populations were performed at the coastal shrublands near San Benito, N of Dzemul, Yucatan (21[degrees]19'N, 89[degrees]25'W), while those of T.streptophylla were performed in mangrove vegetation at Celestun, Yucatan. All locations are less than 50 m above sea level (see Figure 7).
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The studies were conducted during the flowering seasons of the species (see Figure 5). The Mexican portion of the Yucatan Peninsula comprises the states of Yucatan, Campeche, and Quintana Roo, surrounded by the Mexican Gulf, and the Caribbean sea, while to the south it shares boundaries with the Mexican state of Tabasco, Belize, and the Guatemalan Peten. Yucatan as here defined is a diverse region; the climate varies from hot and dry in the northwest to humid in the southwith average annual temperature 24 to 26[degrees]C.
Study group: We selected six Tillandsia species native although not endemic to the Mexican portion of the Yucatan Peninsula. Selected species vary in floral morphology and biology, i.e., inflorescence architecture, corolla shape and color, sexual organs (anthers and/or stigma exerted or inserted in corolla tube) anthesis hours and fruit setting (see Table 2 for a detailed comparison). All species belong in subgenus Tillandsia sensu Smith & Downs except Tillandsia elongata var. subimbricata that has been placed in subgenus Allardtia (Smith and Downs 1977).
Methodology: To evaluate the breeding systems we performed a series of manipulated crosses following the methodology of Ramirez & Seres (1994)and summarized in Ramirez-Morillo, Carnevali et al. (2004). With the use of this methodology we try to assess whether the plant sets fruit or not, if produce seeds without fertilization (agamospermy, or also called apomixis) or only produce fruits by cross pollination. Also, we studied possible mechanisms that have evolved in order to avoid selfing in those species that are self compatible.
Results: Results of manipulated crosses in the six species of Tillandsia are shown on Table III. All species except Tillandsia streptophylla are self compatible (no fruits produced in manual or unassisted selfing). All species display high fruit set by cross pollination except T. elongata avar. subimbricata. In the field, all species produced fruits with T. balbisiana having the lowest fruit production (34%). T. dasyliriifolia is the species with the highest fruit set in all experimental crosses, it is self compatible and also produced fruits by cross pollination.
Discussion and conclusions: These preliminary results suggest that mating systems are variable even among species with similar floral morphology and biology, i.e. tubular flowers, exerted sexual organs and diurnal anthesis, probably all pollinated by hummingbirds. We suggest mechanisms such as herkogamy (separation of sexual organs) and dicogamy (differential maturation of sexual organs) prevent self pollination in self-compatible species. Self incompatibility is reported for the first time in a tillandsia species: Tillandsia streptophylla only produces fruits by cross pollination while, unlike most tillandsia species, its fruit production in the field is very low, suggesting pollinator limitation. Tillandsia balbisiana is a xenogamous species based on results of cross pollination but its fruit setting is relatively low, probably another case of pollinator limitant. Tillandsia brachycaulos seems to produce fruits in all crosses, suggesting self compatibility although it has relatively low fruit setting that is balanced by the strategy of high production of offsets. Tillandsia elongata var. subimbricata has the sexual organs inserted in the corolla tube and late afternoon anthesis, and also shows highest fruit setting by selfing. This species usually grows as solitary rosettes that bloom and produce many fruits with seeds that germinate close to the mother plant forming a large colony of seedlings. Finally, T. dasyliriifolia and T. utriculata seem to be the best adapted species since they produce fruit by unassisted pollination, self and cross pollination and present the highest fruit setting in the field. Tillandsia dasyliriifolia also produced "keikis" in the inflorescence (see Ramirez and Carnevali 2004).
Mating systems and pollination ecology suggest strong bases to explain distributional patterns and abundance of several species of Tillandsia in the natural habitat. More studies evaluating the mating systems based on seed amount, viability and germination, are needed to evaluate the effects of the different breeding systems in this species that produced fruits by several strategies. Also, density, biology, dynamics of the populations as well as pollinator behavior will provide important data to understand the different scenarios regarding the capacity of the populations to maintain and grow and the effect of natural phenomena such as hurricanes in this epiphytic species.
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Finally, self compatible species with unassisted pollination and clonal growth will have better chances to perpetuate (i.e., Tillandsia dasyliriifolia and T. utriculata) compared to those self incompatible and pollinator dependant species (i.e. T. streptophylla).
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Acknowledgments: To the Bromeliad Society Inc. and Dr. Sue Sill for the invitation to the First International Tillandsia Symposium where the first author presented these results. The first author thanks the Elizabeth Bascom Scholarship from the Missouri Botanical Garden and the Kew Latin America Research Fellowships Programme (Klarf) for scholarships granted to study their Mexican Bromeliaceae herbarium collections. Authors thanks to the authorities of Dzibilcahtun National Park and Celestun Reserve for granting permission to carry out field studies in the park. Thanks to Herbarium CICY, Centro de Investigacion Cientifica de Yucatan, A. C. The second author thanks CONACYT for the scholarship to pursue part of this study as a thesis research.
Benzing, D. H. (2000). Reproductive Structure. Bromeliaceae: profile of adaptive radiation. D. H. Benzing. London, Cambridge University Press: 79-106.
Espejo-Serna, A., A. R. Lopez-Ferrari, et al. (2004). "Checklist of Mexican Bromeliaceae with notes on species distribution by state and municipality, and levels of endemism." Selbyana 25: 33-86.
Gardner, C. S. (1986). "Preliminary classification of Tillandsia based on floral characters." Selbyana 9: 130-146.
Gilmartin, A. J. and G. K. Brown (1985). "Cleistogamy in Tillandsia capillaris." Biotropica 17(3): 256-259.
Lenz, L. W. (1995). "A new species of Hechtia (Bromeliaceae, Pitcairnioideae) from the Cape Region, Baja California Sur, Mexico." Aliso 14(1): 59-61.
Luther, H. (2006). An alphabetical list of bromeliad binomials 10th edition. Sarasota, FL, Bromeliad Society International.
Ramirez-Morillo, I. (1996). Systematics, phylogeny, and chromosome number evolution of Cryptanthus (Bromeliaceae). St. Louis, University of Missouri-St. Louis. PhD: p. 268.
Ramirez-Morillo, I., F. Chi-May, et al. (2000). "Portraits of Bromeliaceae from the Mexican Yucatan Peninsula-I: Hechtia schottii Baker ex Hemsley (Pitcairnioideae)." J. Bromeliad Soc. 50(1): 20-24.
Ramirez-Morillo, I. M., G. Carnevali, et al. (2004). "Portraits of Bromeliaceae from the Mexican Yucatan Peninsula-1V:Tillandsia dasyliriifolia Baker: Taxonomy and Reproductive Biology." Journal of the Bromeliad Society 54(3): 112--121.
Ramirez, N. and A. Seres (1994). "Plant reproductive biology of herbaceous monocots in a Venezuelan tropical cloud forest." Plant Syst Evol 190: 129-142.
Smith, L. B. and R. J. Downs (1977). Flora Neotropica Monograph No. 14, Part 2: Tillandsioideae (Bromeliaceae). New York, Hafner Press.
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Corresponding author: firstname.lastname@example.org
Centro de Investigacion Cientifica de Yucatan, A. C. (CICY) Calle 43 # 130, Colonia Chuburna de Hidalgo, Merida, Yucatan 97200, Mexico
Table I. Different floral sex and breeding systems reported in Bromeliaceae. Genus Floral sex/Breeding system References Tillandsia Hermaphrodite/ Xenogamy, Gilmartin & Brown, Cleistogamy 1985; Gardner, 1986 Hechtia, Dyckia, Unisexual, bisexual/ Benzing, 2000; Cottendorfia, Polygamomonoecy, monoecy, Lenz, 1995; Lindmania xenogamy Ramirez et al., 2000 Cryptanthus Hermaphrodite, unisexual/ Ramirez, 1996 andromonoecy, xenogamy Pitcarinia Hermaphodite/self Wendt et al., 2001 compatibility, autogamy, xenogamy Table II. Comparison of different life history characters among Tillandsia species in this study. Species Inflorescence scape Corolla shape T. balbisiana Long scape, panicle Tubular 1-divided Rarely simple T. brachycaulos Non scape, nidular, Tubular panicule 2- 1-divided, condensed branches T. dasyliriifolia Long scape, panicle Tubular 2-divided T. elongata var. Inflorescence with Basally tubular, subimbricta long scape, panicle then petals 1-divided spreading T. streptophylla Inflorescence with Tubular long scape, panicle 1-divided Species Corolla color Sexual organs T. balbisiana Purple, tubular Exerted from corolla tube T. brachycaulos Purple, actinomorphic Exerted from corolla tube T. dasyliriifolia Whitish, actinomorphic Exerted from corolla tube T. elongata var. White basally, light Inserted subimbricta purple apically, in corolla tube actinomorphic T. streptophylla Light purple, Exerted from actinomorphic corolla tube Species Anthesis hours New recruitment of individuals T. balbisiana Diurnal By seeds and less (morning) frequently offsets T. brachycaulos Diurnal By offsets and less (morning) frequently by seeds T. dasyliriifolia Diurnal By seeds, offsets, (morning) and "keikis" on the inflorescence T. elongata var. Diurnal (late Mostly new subimbricta afternoon) individuals from seeds T. streptophylla Diurnal By seeds, rarely by (morning) offsets Species Fruit setting Vegetation type in the field T. balbisiana Below 50% Mainly low caducifolius forests, medium statured forests and mangroves T. brachycaulos Ca. 100% Mainly low caducifolious forests, also medium statured caducifolious forest T. dasyliriifolia Ca. 100% Coastal scrubland, low inundated forest, tall evergreen forest T. elongata var. Ca. 100% Low caducifolious subimbricta forest T. streptophylla Below 50% Mangroves and low inundated forests Species Phorophyte position Geographical distribution T. balbisiana Mostly exposed places N South America to Florida T. brachycaulos In shaded and less South Mexico to frequently exposed Panama Venezuela places T. dasyliriifolia Mostly exposed places Mexico and Belize T. elongata var. Isolated individuals Florida Mexico to subimbricta on exposed places N South America T. streptophylla Isolated individuals N Mexico to Honduras on exposed places, Costa Rica rarely clumps of 2-3 rosettes Table III. Results on manipulated crossings in six Tillandsia species in Mexico. Numbers represent percentage of fruit setting. Numbers with same letters do not differ statistically for the same species. An Xi2 test was performed to test for differences among crosses and all are significantly different. Unassisted Manual Cross Species selfing selfing pollination T. balbisiana 0.6D 60B 82A T. brachycaulos 24B 19B 43A T. dasyliriifolia 93A 93A 91A Species Natural pollination Xi2 T. balbisiana 34C 148.75 (p<0.05**) T. brachycaulos 50A 124.37 (p<0.05*) T. dasyliriifolia 88A 462.35 (p<0.01**)
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|Author:||Ramirez, Ivon M.; Gonzalez, Jose U.; Chi, Francisco; Carnevali, German; May, Filogonio|
|Publication:||Journal of the Bromeliad Society|
|Date:||Jul 1, 2008|
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