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Reproductive Biology |
Laboratório de Genética Molecular Vegetal and Laboratório de Cultura de Tecidos e Transformação Genética de Plantas, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, CP15053, CEP 91501-970, Porto Alegre, RS, Brazil
Received for publication May 4, 2006. Accepted for publication February 26, 2007.
ABSTRACT
Plant fertility is a central subject of many questions in plant evolutionary and conservation biology. Pollen availability, abiotic resources, and flowering pattern can limit fruit and seed production. Open pollination and pollen supplementation studies are used to estimate any pollen limitation in natural populations. To study the impact of these factors on the reproductive success of Vriesea gigantea, an epiphytic bromeliad in the Atlantic Rainforest in Brazil, its fertility in four natural populations in Itapuã State Park was assessed by considering plant and inflorescence size, flower production, fruit and seed set, flower and fruit set pattern, and seed viability and germination rate. Supplemental pollination in adult plants was used to determine whether fruit production in V. gigantea is limited by reception of pollen. The results showed that V. gigantea has a high production of flowers, fruits, and seeds. Seeds are highly viable in all populations, presenting an average germination rate of 94% (SE ± 3.5). Plants of V. gigantea from Itapuã State Park are highly fertile. The high proportion of fruit and seed set after manual hand pollination indicates that the species is self-compatible. Pollination treatments showed evidence of pollinator limitation in the Itapuã State Park population.
Key Words: Bromeliaceae • flower production • fruit set • Itapuã • State Park • pollen limitation • seed viability • self-compatibility
Plant fertility and limits to fertility are issues of central importance to many questions in plant evolutionary biology and conservation biology. The degree of pollen limitation on fertility will affect the role of female mate choice in plants, the opportunity for selection on floral traits, or the possibility of changes in the mating system (Charlesworth et al., 1987
; Fenster and Ritland, 1994
; Dudash and Fenster, 1997
). From a conservation point of view, an important question is whether fertility in plants is limited primarily by pollen or resource availability (Willson and Burley, 1983
; Haig and Estoby, 1988; Huang and Guo, 2002
). The disruption of plant-pollinator mutualisms has the potential of affecting the viability of populations. This phenomenon may occur when habitat fragmentation directly affects the pollinator populations or when plant population drops below the critical size threshold needed to attract and sustain pollinators (Johnson et al., 2004
). Forest fragmentation and the resulting spatial isolation of plant species can modify the activity of pollinators and may have important implications for the reproductive success and reproductive systems in plants they pollinate (Byers, 1995
). Moreover, pollinator limitation in natural plant populations may account for low fruit and seed set and may have profound consequence for the evolutionary ecology of plants, including, for example, the evolution of selfing (Schemske and Lande, 1985
).
Several features associated with plant fertility have been used to determine population viability, such as plant size, flower production, fruit and seed set, pattern of fruit production, pollen limitation, and seed viability (Ishii and Kadono, 2002; McIntosh, 2002
; Burne et al., 2003
; Ortiz et al., 2003
; Buide, 2004
; Clark-Tapia and Molina-Freaner, 2004
; Johnson et al., 2004
; Kéry and Matthies, 2004
; Hampe, 2005
). The fruit and seed production in plants can be limited by the availability of pollen and abiotic resources. The decrease of seed production can be the result of insufficient pollinator visits or reduction in both pollen quantity and pollen quality deposited per visit (Huang and Guo, 2002
; Ashman et al., 2004
; Buide, 2004
). Abiotic resource limitations include inadequate soil nutrients, water, light, and climatic factors (Willson and Burley, 1983
; McIntosh, 2002
; Gaudeul and Till-Bottraud, 2004
). Although pollen limitation and abiotic resource limitation appear to be two alternative hypotheses for inadequate seed production in plants, some authors have suggested that in equilibrium, seed production in plants should be limited by both factors (Haig and Westoby, 1988
; Dogterom et al., 2000
).
The flowering pattern is another intrinsic feature that may limit the fruit and seed production. When fruit set is low, the distribution of fruits and seeds within an individual plant is not uniform, and fruit maturation has frequently been found to decrease from the base to the apex of individual inflorescences (Diggle, 1995
; Ortiz et al., 2003
). This could be a consequence of the opening sequence because flowers that open first have the opportunity to be pollinated and fertilized earlier (Diggle, 1995
).
The Bromeliaceae family has nearly 3000 species divided into three subfamilies: Pitcairnioideae, Bromelioideae, and Tillandsioideae (Smith and Downs, 1974
). Vriesea gigantea Gaud. (Tillandsioideae) an epiphytic, saxicolous, and terrestrial bromeliad that grows in the Atlantic Rainforest, Brazil, is greatly valued as an ornamental plant. Wild populations of V. gigantea have been reduced by anthropogenic disturbance of their habitat and by predatory collection practices, causing inclusion of V. gigantea in the list of endangered species of the state of Rio Grande do Sul. In spite of this, no publications are currently available about the fertility of V. gigantea. Here we aim to fill this gap to aid conservation plans for this ecologically and horticulturally important species and to initiate studies on the fundamental biology of this charismatic bromeliad genus.
The investigation of the relative importance of the factors described will help elucidate their impact on the overall reproductive success of V. gigantea. To evaluate the fertility of V. gigantea in four populations from southern Brazil, we aimed (1) to record production of flowers, fruits, and seeds, the pattern of fruiting in the inflorescence, and the heights of plants and inflorescences; (2) to evaluate whether populations differ in fertility; (3) to investigate whether fruit and seed set are limited by pollen or abiotic resources; and (4) to determine the levels of seed germination and viability.
MATERIALS AND METHODS
Study species
Vogel (1969)
and Sazima et al. (1999)
described Vriesea gigantea as an outcrossing bat-pollinated bromeliad species (Fig. 1A) growing from Espírito Santo (ES) to Rio Grande do Sul (RS) in the Atlantic rainforest in southeastern and southern Brazil, respectively. Furthermore, V. gigantea plays an important role in ecosystems, because its vegetative structure forms reservoirs that are able to hold many liters of water, providing a resource base for the associated biota (Benzing, 2000
). A typical inflorescence has a central axis with several branches on each side and one flower on each side of the lateral axis (Reitz, 1983
). The flowers (Fig. 1B) are tube-shaped with three petals that are colored in accord with a chiropterophilous syndrome (Vogel, 1969
). Flowers in the basal position of the inflorescence open first, whereas flowers in the center and apex position open later (Reitz, 1983
; Benzing, 2000
).
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); (4) number of seeds per fruit from five fruits randomly collected from 10 plants– (estimated by comparing the mass of 20 seeds with the mass of all seeds from each fruit); (5) flower and fruit set position (proportion of flowers and fruit set in the base, center, and apex of the inflorescence). The position of each flower and fruit was recorded for each inflorescence and was classified into three categories: apex (when found in the upper third of the inflorescence), center (in the middle third), or base (in the lower third).
Seed viability and germination rate
Seed viability and germination rate are among the less studied aspects of bromeliad fertility and reproductive biology (Benzing, 2000
). These aspects vary within Bromeliaceae because most species respond differently to light and temperature (Downs, 1963
; Benzing, 2000
). To analyze seed viability, five plants of V. gigantea were randomly sampled in each population (August 2004), totaling 20 plants. Two fruits (30 seeds/fruit) were used per plant. Seeds were disinfected and placed in petri dishes with a culture medium, containing 
MS salts (Murashige and Skoog, 1962
), B5 vitamins (Gamborg et al., 1968
), 3% sucrose, and 0.3% Phytagel (Sigma, Saint Louis, MO, USA), pH 6.4. The dishes were incubated in a climate-control chamber with relative humidity near 100% and photoperiod of 16 h light at 25°C and 8 h dark at 22°C. Germination was monitored daily for 30 d.
Pollen supplementation
Field studies were conducted during the plant reproductive cycle, from January to March and in August 2005. To determine whether fruit production in V. gigantea is limited by reception of pollen, we performed supplemental pollination in the four populations studied. The pollination treatments were accomplished as follows:
(1) Open-pollination (OP)—flowers, which opened during the day and were available to any visitor, were tagged; (2) manual self-pollination (MSP)—when flowers opened around midday and pollen was available, they were hand-pollinated by rubbing anthers with fresh pollen in the stigma from the same flower and then bagged. Two or three flowers from 16 plants distributed throughout the populations were pollinated, whereas three other single flowers on each plant were marked as control (OP treatment). The results (i.e., aborted or developing fruit) of the pollination treatments were recorded 6 months later, and the fruit set was calculated using the formula described earlier. Mature fruits were collected and the number of seeds per fruit estimated by the mass method. To evaluate whether pollen supplementation affected seed set, the number of seeds from hand-pollinated and naturally pollinated fruits were compared.
Statistical analyses
All statistical analyses were performed using the SAS software package (version 8, SAS Institute, Cary, North Carolina, USA). When necessary, data were transformed to stabilize variances and achieve approximate normality of residuals. The plant height parameter and pollen-supplementation per population data were analyzed by the nested Kruskal-Wallis test. The effect of pollen supplementation per treatment was analyzed by the Wilcoxon two-sample test. The inflorescence height (square-root transformed), flower production, fruit set, flower/fruit set position, and the number of seeds per fruit were analyzed by the nested ANOVA test followed by the Tukey test to determine if the differences among plants or populations were significant.
RESULTS
Reproductive success: flower production, fruit, and seed set
The overall means of plant and inflorescence height were 0.95 m (SE ± 0.045) and 1.51 m (SE ± 0.044), respectively, without significant differences among populations (Table 2). The mean of flowers per plant was 143.93 (SE ± 11.08), without significant differences among populations (Table 3). The fruit set per plant ranged from 9.88 to 69.92% with an overall mean of 42.71% (SE ± 8.24). Significant differences were detected among populations. Fruit set was higher in Pedra da Visão and lower in Trilha do Fenômeno and Praia do Araçá populations (Table 3). The number of seeds per fruit ranged from 0 to 839, with significant differences among plants (Fig. 3). Plants number 6, 8, and 10 had significantly lower production of seeds per fruit when compared with plant number 1; no seeds were obtained from plant 9. The architecture of the inflorescence did not affect the flower production pattern (Fig. 4). On the other hand, fruits were not homogeneously distributed on the inflorescence: the upper third (apex) presented significantly lower fruit set than the lower third (base) (Fig. 4).
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Pollen-supplementation
There was a significant effect of pollen supplementation on fruit and seed set (Table 4). On average, 47.92% (SE ± 9.61) of open-pollinated flowers developed fruits. The mean fruit set of manual self-pollinated plants was 85.42 % (SE ± 5.67). Manual self-pollinated flowers produced more than twice as many seeds as naturally pollinated flowers (544.25 vs. 245.71). Data on pollen-supplementation per population are in Table 5. The mean seeds per fruit in Morro da Grota was significantly higher than in the Pedra da Visão population after manual self-pollination. Nonetheless, fruit set did not differ significantly among populations. In the open treatment (control), although the differences among populations were not significant, Praia do Araçá population yielded only a mean of 102.89 (SE ± 69.16) seeds per fruit, around 3.8 times lower than the Morro da Grota population (Table 5).
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Reproductive success: flower production, fruit, and seed set
The adult individuals of V. gigantea presented a height general mean of 2.46 m, with inflorescences (Table 2). This is in agreement with Reitz (1983)
who reported an average height of 2.00 m for adult individuals of this species. The four analyzed populations of V. gigantea produced a high number of flowers, fruits, and seeds. Considering mean of flowers per plant (143.93 ± 11.08), the mean of seeds per fruit (303), and taking into account that 43% of flowers developed into fruit, it is possible to estimate that one plant can produce about 18.753 seeds in each reproductive cycle. Intriguingly, although differences among populations were detected only on fruit set, plants from Praia do Araçá presented lower values in all parameters evaluated (Tables 2 and 3). These results suggest lower plant fertility in this population. Several factors may have been responsible for this phenomenon. As the Praia do Araçá population is located 5 m from Guaíba Lake (Fig. 2), local growth conditions may be quite different from those of other populations. McIntosh (2002)
and Kéry and Matthies (2004)
reported that the reduction in plant size, flower size, number of seeds per plant or fruit, and flower number in small populations can be a consequence of lower habitat quality, reduced pollination, or inbreeding depression. The relative importance of each factor in limiting fruit set in the Praia do Araçá population is difficult to determine. Nevertheless, we assumed those abiotic resources, such as climatic variation and soil conditions, and other factors such as pollen limitation may have contributed to the reduced plant fertility in this population.
A decrease in fruit set was observed from the base to the apex of the inflorescence in V. gigantea (Fig. 4). A similar result was reported by Ortiz et al. (2003)
in Stryphnodendron adstringens. The reproductive success of flowering plants appears to be affected by a variety of factors, including the timing, frequency, duration of the flowering period, and flowering pattern (Rathcke and Lacey, 1985
; Diggle, 1995
; Ortiz et al., 2003
). According to Thomson (1989)
, in some species the reproductive potential differs from one flower to another, e.g., flowers that open later may have fewer ovules, and thus they are less likely to produce fruits (usually found in the apex of the inflorescence). This is consistent with the hypothesis that plants tend to direct fewer resources to the production of ovules that have little chance of being converted into seeds (Ortiz et al., 2003
).
Seed viability and germination rate
Seeds from all analyzed populations were highly viable, presenting a germination rate of 94%. Downs (1963)
reported similar results for other bromeliad species. Seed production, seed viability and germination rate and the longevity and mortality rate of plants may affect population dynamics (Kéry and Matthies, 2004
). As far as we know, the results described here are the first reported on seed viability and germination rate in V. gigantea. Further studies on plant longevity, mortality rate, and recruitment of new individuals will be essential to evaluate the V. gigantea populations dynamic.
Pollen supplementation
The mean fruit set from manual self-pollinated plants was 85.42%, indicating that V. gigantea is self-compatible as described for other members of this genus (Martinelli, 1994
). In natural conditions, 47.92% of open-pollinated flowers developed fruits (Table 4). Similar results were recorded by Canela and Sazima (2005)
for Bromelia antiacantha (Bert.), whose fruit set under natural conditions, occurred in 50% of the flowers. The differences among populations regarding seed production in the pollen-supplementation experiments may be associated with the lower level of genetic variability found in Pedra da Visão population (G. M. Paggi, C. Palma-Silva, L. C. T. Silveira, J. A. T. Sampaio, E. Kaltchuk-Santos, M. H. Bodanese-Zanetinni, F. Bered, Universidade Federal do Rio Grande do Sul, unpublished manuscript). Reduced genetic variability may result in inbreeding depression and a decrease in plant size and fruit/seed set (Huang and Guo, 2002
; Buide, 2004
; Kéry and Matthies, 2004
; Yang et al., 2005
).
Under open-pollination, plants from Praia do Araçá yielded 3.8-fold less seeds than those from Morro da Grota (Table 5). It could be hypothesized that the low seed production may be due to pollen-limitation in Praia do Araçá. Similarly, Clark-Tapia and Molina-Freaner (2004)
and Ishii and Kadono (2002) concluded that pollen-limitation may be the most important factor contributing to the low seed productivity for Stenocereus eruca and Poaceae species, respectively. Furthermore, in Ferocactus cylindraceus species, both extrinsic and intrinsic factors were considered important in limiting reproductive output (McIntosh, 2002
).
Pollen limitation is fairly common in plants and can be considered a natural phenomenon (DiFazio et al., 1998
; Thomson, 2001
; Ishii and Kadomo, 2002
). According to Buide (2004)
, evidence from pollination treatments and spatial variation in fruit set seem to indicate that pollinators limit female fecundity. As V. gigantea is a bat-pollinated species (Sazima et al., 1999
), observations on pollinator visits could provide important information to confirm our hypotheses of pollen limitation. The occurrence of glossophagines bats, such as Anoura caudifer and Glossophaga soricina, has been recorded throughout the Itapuã State Park (Fábian et al., 1999
; T. Freitas, Universidade Federal do Rio Grande do Sul, personal communication). Moreover, the largest bat population was observed in Morro da Grota (W. Silva, Secretaria do Meio Ambiente do Rio Grande do Sul, personal communication). The high abundance of bats in this population could explain the high number of seeds and fruit setting under open pollination (Table 5). However, our observation on pollinator visits are limited, and further field studies should be carried out to understand pollinator behavior and its effects on the breeding system of this species.
Evolutionary and conservation considerations
The pollen-supplementation results (Table 4) agree with the pollinator-limitation hypothesis, which suggests that observed fruit production is below some optimal level that would be achieved if pollinators were more abundant (Calvo and Horvitz, 1990
). Consequently, pollen limitation appears to be the case for V. gigantea. Genetic models of mutation and selection to analyze the joint evolution of inbreeding depression and self-fertilization in natural populations demonstrate that in many situations the two extremes (predominant outcrossing and predominant self-fertilization) represent alternative stable states of the mating system (Schemske and Lande, 1985
). Which of these two extremes will be the case depends largely on a species' history, e.g., species with a long history of occasional population bottlenecks and/or pollinator failure are expected to have relatively little inbreeding depression and to be selected for self-fertilization, whereas species with historically large, outcrossing populations are expected to have substantial inbreeding depression when forced to self and to be selected for mechanisms to prevent inbreeding. In addition to the lack of pollinators, there are several other selective factors thought to promote the evolution of selfing, such as cost of outcrossing, repeated colonization of new areas by single individuals (= the need for reproductive assurance), and selection for local adaptation (Lande and Schemske, 1985
; Charlesworth et al., 1987
). Although Vogel (1969)
has described V. gigantea as an outcrossing species, our results indicate that this species is self-compatible and has the potential to tolerate selfing (Table 4). We note that occasional selfing in monoecious or hermaphroditic outcrossers is often an incidental by-product of self-compatibility (Schemske and Lande, 1987). In the future, molecular marker-based assessment of inbreeding coefficients and outcrossing rates in natural populations and progeny arrays (Weir and Cockerham, 1984
; Ritland, 2002
) will help us shed light on the breeding system of V. gigantea.
In summary, this study demonstrates that the analyzed populations are viable. Plants produce large number of flowers, fruits, and highly viable seeds. A high proportion of fruits matured, and seeds in the manual self-pollination treatment indicate that species is self-compatible. Reduction in seed set of individuals from Praia do Araçá was probably due to pollinator limitation. If pollinator abundance is reduced, outcrossing will be suppressed, and genetic variability will also be reduced. Pollen limitation is most likely a consequence of habitat fragmentation, and, specifically, a disruption of the bat pollination mutualism. Hence, to ensure the continuous survival of populations and to maintain their evolutionary potential, large-scale conservation strategy is necessary to protect plants and pollinators.
FOOTNOTES
1 The authors thank the staff of Itapuã State Park for helping to collect samples; L. E. C. Schmit, J. Soares, R. Webber, C. E. M. Gomes, J. A. T. Sampaio, and S. N. C. Richter for collecting plant material and/or providing locality information; C. Lexer for valuable comments and English revision; N. Rufino de Albuquerque, J. César de Lima and B. Silva for English revision and suggestions. Research was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and PROPESQ/UFRGS (Pró-Reitoria de Pesquisa/Universidade Federal do Rio Grande do Sul). 
2 Author for correspondence (e-mail: fbered{at}portoweb.com.br
; phone: +55-51-33086742; fax: +55-51-33087311
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