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Fruit production frequency as an indication of self-pollination in Lepanthes eximia (Orchidaceae: Pleurothallidinae) in Monteverde, Costa Rica Kathryn A. Lulling Department of Biochemistry Arizona State University ABSTRACT Most orchids are capable of self-pollination, but outcrossing promotes the variation in flower structure and the specificity of pollination mechanisms prevalent in orchids. For this reason there are many elaborate pollination mechanisms involving specific pollinators. Highly specific mechanisms ensure efficient pollination, yet low fruit production is common in orchids and in the genus Lepanthes An exception to this trend is Lepanthes eximia which has a relatively high fruit set. This may indicate that L. eximia does not depend on rare pollination events, bu t self-pollinates, accepting low genetic variability in order to increase its number of offspring. Two groups of L. eximia one exposed to potential pollinators and one covered with mesh bonnets, were observed for differences in fruit production in the orchid garden of Dr. Karen Masters in Monteverde, Costa Rica to determine if L.eximia self-pollinates. Comparisons in morphological variation of L. eximia and L. pygmaea, both exposed to potential pollinators, were made to examine the differences in variance between inbred and outbred species. Lepanthes eximia was found to be capable of self-pollination, but no significant difference in the va riability of morphological traits of inbred and outbred species of Lepanthes exists. RESUMEN La mayora de las orqudeas son capaces de polinizarse a s mismas, pero la estructura floral y los mecanismos especficos de la polinizacin tiende a la polinizacin cruzada. Por eso, hay muchos mecanismos complicados de polinizaci n con polinizadores especficos. Los mecanismos muy especficos aseguran la polinizacin eficiente, si n embargo la baja produ ccin de frutas es comn en las orqudeas y en el gnero Lepanthes Una excepcin a esta tendencia es Lepanthes eximia que tiene un grupo alto de frutas. Esto indica que L. eximia no depende de los eventos raros de po linizacin, pero se poliniza a s misma, aceptando baja variabilidad gentica para aumentar el nmero de descende ncias. Dos grupos de L. eximia uno exponido a polinizadores potenciales y otro cubierto con gorras de malla, estuvieron siendo observados para ver las diferencias en la produccin de frutas en el jardn de Karen Masters en Monteverde, Costa Rica para determinar si L. eximia se poliniza a s misma. Las comparaci ones entre la variacin morfolgica de L. eximia y L. pygmaea, ambos exponidos a polinizadores poten ciales, han hecho para examinar las diferencias en variacin entre especies innata s y especies no innatas. Se encontr que L. eximia es capaz de polinizarse a s mismo, pero no hay diferencia si gnificativa en la variabilidad de caractersticas morfolgicas de especies innatas y no innatas de Lepanthes INTRODUCTION Orchidaceae is the largest family of angi osperms with recent estimates exceeding 20,000 species and 700 genera (Christenson 2004). Am ong the flowering pl ants, orchids claim the most species richness, with its peak in the American tropical cloud forest (Walter 1983; Dressler 1990). One of the most fascinatin g characteristics of orchids is the great variety of pollination mechanisms and the specificity of the relationship between an 1
orchid species and its pollinator (Christenson 2004). The variation in floral shapes, sizes and colors reflects the variet y and specificity of orchid pollinators (Dressler 1990). The diversity and complexity of orchid pollination mechanisms and relationships have been the subjects of many studies that attempt to understand the evolution of the most diverse flowering plant family on Earth. Pollination is a key mechanism in plant reproduction and may underpin the high levels of speciation in orchids (Esquiln and Tremblay 1999). There are two basic types of pollination. The first type, cross-pollinati on, increases heterozygosity and fitness by reducing inbreeding depression in offspring (Esquiln and Tremblay 1999; Jerskov and Johnson 2006). The second type, self-pollina tion, increases homozygosity, causing the loss of genetic variability. However, it has the short-term advantage of producing huge numbers of seeds without depending on the ofte n rare and erratic pollinator visitation that is characteristic for orchids (Dressler 1990; Esquiln and Tremblay 1999; Walter 1983). Most orchids are capable of se lf-pollination, but outcrossing is more prevalent, increasing variation in flower structur e and specificity of pollination mechanisms in future populations (Dressler 1990; Walter 1983). Sele ctive pressures encouraging pollination with a conspecific has promoted the evoluti on of highly specific pollination relationships (Dressler 1990). Orchids are adapted for rare and specifi c pollination events (Christenson 2004). Pollination mechanisms may be simple with orchids offering rewards to their pollinators such as nectar, oil, or wax in exchan ge for pollen dispersal (Walter 1983). Other mechanisms are more elaborate than others One mechanism is buzz pollination, where the pollinator has to buzz at a specific fre quency in order to have access to the reward. Another pollination mechanism may require th e elongated proboscis of a sphingid moth. Not all orchid species offer rewards. Instead, they use deception mechanisms that include floral structures mimicking male intruders or female mates of the pollinator species to provoke attack or copulating behavior in a potential pollinator. Orchids also mimic nectar-producing flowers and give off fragrances that attract pollinators but do not actually reward the pollinator with nectar (Walter 1983). The pollination of orchids is highly efficient due to these pollinator specifi c mechanisms and they ensure that pollinia will be transferred to an individual of the same species. Even though orchids have various species-specific pollination mechanisms, fruiting failure and low fruit production are common in orchids (Blanco and Barboza 2005; Calvo 1990; Janzen 1998; Tremblay 1997), indicating low pollination success and pollinator-limitation (Janzen 1998). Alt hough outcrossing is favored promoting specialized relationships with pollinators, autogamy (self-pollination within one flower on an individual plant) and cleistogamy (selfpollination because the flower never opens) are known among some orchids, possibly to ma intain populations that would otherwise never be pollinated (Endress 1994). As with most orchids, many species of the epiphytic genus Lepanthes (Pleurothallidinae) experience infrequent pollinator visitation and commonly have low fruit sets (Blanco and Barboza 2005). Pollinators for Lepanthes are still largely unknown, but a few studies indicate that sexual deception to induce pseudocopulatory pollination by small Diptera is a possibility (Blanco and Barboza 2005; Tremblay 1997; Tremblay et al. 1998). Although Lepanthes species lack any detectable floral rewards for potential 2
pollinators, the majority of the species share the same basic floral structures that may attract male Diptera (B lanco and Barboza 2005). One exception to the low fr uit production trend in Lepanthes orchids is the species L. eximia No pollinator has been observed for this species and contrary to the trend for congeners, L. eximia has a very high fruit set (K.L. Masters, pers. comm. 2006). The flowers and flowering patterns of this spec ies have been described in the cloud forest by Hammel et al. (2003). The purpose of this study is to investigate how L. eximia is able to produce a high fruit set despite pollinatorlimitation in the genus. I hypothesize that L. eximia is self-pollinated and is therefore able to produce a high fruit set because it does not depend on rare pollination events. I predict that fruit production of L. eximia will not differ significantly between groups where outbreeding is prevented and groups where it is allowed. I further predict that L. eximia will vary little morphologically because of low genetic variation and inbreeding in comparison to an outbred congener, L. pygmaea (K.L. Masters, pers. comm. 2006). MATERIALS AND METHODS This study was conducted in November of 200 6 in the orchid garden of Dr. Karen Masters located southwest of La Estacin Bi olgica de Monteverde in Monteverde, Costa Rica. The orchid garden consists of various orchid species living on frames covered in moss. The site is surrounded by Lower Montan e Wet Forest at 1530 m. I first observed Lepanthes eximia in order to define its developmen tal stages for my study. The stages included the following succession: a new flow er bud develops into a mature bud, the mature bud opens to a flower, the flower closes, then the pedicel may swell and produce a fruit. New and mature flower buds were dis tinguished from each other in this study by their size. A new flower bud m easures a few millimeters in length with a width equal to or smaller than the width of the pedicel and has a red tip. The mature bud is larger than the pedicel and is ready to open as a flower. The pedicel is located just below the flower bud and as soon as it showed any swelling or a capsule-like appearan ce I called it a fruit. Two groups of L. eximia individuals were previously separated in the garden. These two groups represented the experimental and control groups when testing for selfpollination. The experimental group consisted of 26 individuals enclosed in green mesh bonnets shaped with malleable wire to prevent access by potential pollinators. The control group consisted of 23 individuals w ithout mesh bonnets and was easily accessible to potential pollinators. Before beginning my observations to test for self-pollination, I counted the number of mature buds and fru its that were produced previous to my observations (Figure 1). The pr eviously produced mature buds and fruits remained on the plants for the duration of the study. On the first day of the study and on ten days (not always consecutive) thereafter, I counted the number of leaves, new and matu re flower buds, new fruits, and open flowers on each individual of the exposed and capped L. eximia (Figure 1). Leaves were not counted if they had not completely unfurle d. New and mature flower buds and new fruits were identified by the characteristics previ ously described. Open flowers were noted as remaining open for a period of 24 hours. Not all new mature buds were observe d to open and close, and the exact developmental stage of the mature buds obser ved previous to the experiment was not 3
known. Before the pedicel swells, which occurs between five and six days after a flower closes in the observed L. eximia a flower that has opened and closed looks like a mature bud. Therefore a closed flower may have b een counted as a mature bud even though it had already passed this developmental stage. It is unlikely that double counting of mature buds occurred because of close observation, but that possibility exists. There was also the possibility that some previously produced mature buds were not identified as such and were actually closed flowers. To test the variation in morphological tr aits between an inbred and an outbred species, I compared 23 individuals of L. eximia (inbred) and 17 individuals of L. pygmaea (outbred). L. pygmaea is similarly a tiny, epiphytic orchid and as in L. eximia, these individuals had been collected in 2005 and positioned along frames in the garden. The lengths of 94 leaves of L. eximia and 117 leaves of L. pygmaea were measured (in millimeters) using a caliper. The Equality of Variances F-test was used to compare the variance of leaf length between L. eximia population and the L. pygmaea population. I then tested the variation in average leaf lengths between i ndividuals in each population. Bartletts test was used to compare the varia tion of average leaf lengths of 17 individuals within the L. pygmaea population and within subsets of 23 L. eximia individuals. RESULTS Over the course of two weeks, four new ma ture buds, zero open flowers, and three new fruits were observed in 23 individuals of the L. eximia population exposed to pollinators (Figure 1). Although there were three new fruits, only one fruit was produced by a new mature bud observed in all stages of deve lopment. Nine new mature buds, four open flowers, and twelve new fruits were observed in the 26 capped individuals of L. eximia (Figure 1). Although there were twelve new fruits, only thre e fruits were produced by new mature buds observed in all stages of development. Four flowers were observed open in the capped L. eximia and remained open for about a 24-hour period. Three of these flowers produced fruits within the tim e frame of the study. No pollinators were observed at any time during the study. 0 5 10 15 20 25 30PPM Bu ds P P F ruit s Obse rv ati o n s B e gin Mature Bud s Flowers FruitsDevelopmental stage Exposed Capped 0 5 10 15 20 25 30 35 4-4.95-5.96-6.97-7.98-8.99-9.91010.9 1111.9 Leaf Length (mm) L. pygmaea L. eximia 4
______________________________ ______________________________ FIGURE 1. Observed number of previously FIGURE 2. The frequency of leaf lengths producedmature buds (PPM Buds) and fruits (mm) in 94 leaves of L. eximia an inbred (PP Fruits), mature buds, open flowers, and species, and 117 leaves of L. pygmaea an fruits in the exposed and capped group of outbred species. Lepanthes eximia for the duration of 2 weeks _____________________________________ in Monteverde, Costa Rica. ______________________________________ There was significant difference in the am ount of variability between the inbred population of L. eximia and the outbred population of L. pygmaea with L. eximia demonstrating greater variability in morphol ogical traits (F-test, F = 1.908, P = 0.0012, df = 93, n = 94, n = 117) (Figure 2). The frequency of leaf lengths in L. eximia expands across a wider range of intervals (4 mm-12 mm) than L. pygmaea (4 mm-10 mm). The frequencies of each leaf length ar e also more variable in the L. eximia population across its range as opposed to the mo re continuous frequencies in L. pygmaea (Figure 2). A 0 1 2 3 4 5 6 7 8 5-5.96-6.97-7.98-8.99-9.91010.9 Leaf Length (mm) Observed NormalB 0 1 2 3 4 5 6 7 8 9 4-4.95-5.96-6.97-7.98-8.9 Leaf Length (mm) Observed Normal ______________________________________________________________________________________ FIGURE 3. Observed and normal frequency distribution of average leaf lengths (mm) for A) subsets of 23 individuals of Lepanthes eximia and B)17 individuals of Lepanthes pygmaea in Monteverde, Costa Rica. ______________________________________________________________________________________ When comparing the average l eaf lengths of individuals of L. eximia and L. pygmaea, the frequency distribution of aver age leaf length per individual of 23 individuals of L. eximia appeared nonnormal and to have two or three modes (Figure 3A). The modes demonstrate subsets in L. eximia with leaf lengths between 5 mm and 7.9 mm, 8 mm and 9.9 mm, and 10 mm and 10.9 mm (Figure 3A). Th e frequency distribution of average leaf length per indivi dual of 17 individuals of L. pygmaea was normal (Figure 3B)(Bartletts test, F-ratio = 2.47, df = 3, p = 0.0598). DISCUSSION The purpose of this study was to determine whether L. eximia is self-pollinated and to examine the morphological variance in an inbred species compared to an outbred species. Few pollinators have been described or observed for Lepanthes and low fruit production indicates that the genus is pollinator-limited. In two studies performed by Tremblay 5
(1997) and Tremblay et al. (1998) over the course of two years on populations of L. caritensis zero fruits were observed even though adult plants flowered continuously during the period of observa tion. In another study on L. glicensteinii in the Monteverde Orchid Garden, frequent pollination visits by Bradysia floribunda, a fungus gnat, yielded no fruits (Blanco and Barboza 2005). Contrary to this trend of low fruit production that was considered to be characteristic of all Lepanthes species, L. eximia displays a high fruit set despite having no observed pollinators. The columns in Figure 1 demonstrate that a total of 23 new and previously produced fr uits were found on the 26 individuals of the capped L. eximia and seven new and previously produced fruits were found on the 23 individuals of the exposed group. When comparing the observed fruits of L. eximia with those of L. caritensis and L. glicensteinii in previous studies, L. eximia demonstrates high fruit production. Initially, Figure 1 appears to show a high number of plant parts in each developmental stage in the capped L. eximia but the ratio of the sum of the number of new mature buds and previously produced buds to the number of new fruits was 10 buds to 3 fruits for the exposed L. eximia and 33 buds to 12 fruits for the capped L. eximia (Figure 1). About the same percentages, 33% and 36%, of new fruits produced were produced from a combination of new and prev iously produced mature buds in both the exposed and capped groups. Although somewhat crude, this assessment indicates that the exposed group did not produce any more fr uits than the capped group. Therefore, although the exposed group could have been bot h pollinated and self-pollinated and in so doing produce even more fruits, this did not seem to happen. Similar ratios for new mature buds that were observed producing new fruits suggest the same conclusion. One new fruit was produced from four new mature buds for the exposed group and three new fruits were produced from nine new mature buds for the capped group (Figure 1). These results are consistent with the results of a study by Esquiln and Tremblay (1999), which found no quantitative differences in fruit pr oduction when comparing self-pollinated and cross-pollinated populations of L. woodburyana. This supports my prediction that fruit production in the L. eximia group exposed to potentia l pollinators will not vary significantly from fruit production in the capped L. eximia In addition to these observations and comparisons, I observed four flowers open in L. eximia unexposed to potential pollinators, three of which produced fruits within the time frame of the study. This is a clear indication that L. eximia is capable of selfpollination and implies that it is self-compatible. Self-compatibility implies that the seeds in the produced fruits are viable and will gene rate offspring. The viability of the seeds of these populations of L. eximia was not tested in this study, but may be a subject for further research. After determining that L. eximia is self-pollinated, two comparisons of the variation in morphological traits were made. In the first comp arison, the variation in leaf length between all leaves in the exposed group of L. eximia (n = 94) and in the group of L. pygmaea (n = 117) was tested to compare the variation of morphol ogical features for an inbred and an outbred species (Figure 2). It was expected that both populations would display a unimodal normal curv e, but that the curve of L. eximia would have a narrower range of leaf lengths (Figure 4A and 4B). Lepanthes pygmaea did display a normal curve, but L. eximia displayed a wider range of leaf lengths than L. pygmaea The inbred population of L. eximia demonstrated greater variation in morphological traits when 6
compared to the outbred population of L. pygmaea (Figure 2). One possible explanation for this unexpected result could be that each leaf was examined and tested as if it were an individual, when each leaf is actually connected closely to an other leaf on the same plant. The scale of the comparison may have been wrong; therefore a s econd comparison on a different scale was performed. The second comparison examined the va riation in averag e leaf length of individuals within L. eximia (n = 23) and the variation in average leaf length of individuals within L. pygmaea (n = 17). It was expected that both populations of individuals would display norma l curves. The individuals in L. pygmaea would display a unimodal curve, but the curve of the L. eximia individuals would either be unimodal with a narrow range of average leaf lengths or multimodal with more variance overall (Figure 4A and 4C). Lepanthes pygmaea did display a unimodal normal curve, but L. eximia displayed multiple modes. There appeared to be three separate modes in L. eximia in terms of average leaf length (Figure 3A). Because it is possi ble to have high variation if the population consists of highl y distinct subpopulations or lineages, the three modes may represent three different lineages (A, B, and C) of inbreeding (Figure 3A). It was expected that individuals shar ing a gene pool and a similar environment would also have similar phenotypes, or physical characteris tics, so the three separate lineages of L. eximia observed was unexpected (Tremblay 1997) (Figur e 3A). These results did not fit the normal curve, which indicates high genetic variability across subpopulations and low levels of inbreeding in the population despite self-pollination (Fi gure 3A). The observed leaf lengths of L. pygmaea were similar to the expected leaf lengths of a homogeneous population (Figure 3B). When comparing the variance of average leaf lengths of individuals between Lineages A, B, and C of L. eximia and individuals of L. pygmaea it cannot be concluded that inbred populatio ns are more homogeneous than outbred populations because Lineage A, an inbred population, was more variable in average leaf length per individual than L. pygmaea, an outbred population. Frequency Frequency Frequency A B C Quantitative trait Quantitative trait Quantitative trait FIGURE 4. The expected curves for the quantitative traits in A) an outbreeding population, B) an inbreeding population, and C) a population with multiple subpopulations. 7
In a study examining morphological varia tion in tropical orchids, Tremblay (1997) found that morphological varia tion within and among populations in Lepanthes is large. He also found that gene flow among Lepanthes is low and that the majority of genetically distinct populations consisted of less than 20 indi viduals (Tremblay 1997). This is significant because it provides a possibl e explanation for the separate lineages in L. eximia. Tremblays (1997) study supports that intraspecific morphological variation, between Lineage A, B, and C of L. eximia of my study, causes ge netic substructuring within one population. The concept of substructuring as a result of morphological variance within a population is also supported by Walter (1983) who states that sympatric species of orchids can become reproductively isolated through mor phologic adaptations. The substructuring of L. eximia could also be due to environmental differences in the microhabitats in which the individual plants spent most of their lives. The plants in the garden were collected from different lo cations in the cloud forest, and populations that are physically farther apart from each other are not as phenotypically or genotypically similar as those in closer pr oximity (Tremblay 1997). Another explanation could be that the age of the L. eximia individuals was not consid ered and may have been more varied causing differences in leaf le ngth; one individual may have had more young leaves or more mature leaves. In order to further explore substruc turing, a future study could examine the variation in floral characteristics of L. eximia as opposed to leaf traits, which are more likely to be more influenced by the environment. Although most morphological structures of orchids in Lepanthes favor crosspollination, this study indicates that L. eximia utilizes self-pollination. With selfpollination as its reproductive mechanism, inbreeding and low genetic variability are expected to be expressed in the morphol ogy of individuals in the population, but the results of this study do not support this pr ediction. It cannot be concluded that L. eximia demonstrates little morphological variation because of inbreeding, whereas an outbred species, L. pygmaea, demonstrates more variabi lity. Additional studies on the physiological and ethological caus es of substructuring within L eximia may be enlightening as to why high morphological va riance is present in a self-pollinating population. ACKNOWLEDGEMENTS I thank Dr. Karen Masters, Camryn Pennington, and Tom McFarland for assistance in the field and statistical analysis. I thank them and my peers for moral support and encouragement during the research and write-up of this project. I thank La Estacin de Biolgia in Monteverde, Costa Rica for their hospitality and for allowing admittance to the cloud forest reserve. I thank Karen Masters for allowing me to study Lepanthes eximia and Lepanthes pygmaea in her beautiful orchid garden adjacent to La Estacin de Biolgia. I thank Stephanie Siemek and Lili Prahl for peer-editing my first draft and for their support. Lastly, but most importantly I thank God and evolution for the magnificent biodiversity that we all enjoy. LITERATURE CITED Blanco, M.A. and G. Barboza. 20 05. Pseudocopulatory pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by fungus gnats. Annals of Botany 95: 763-772. 8
9Calvo, R.N. 1990. Inflorescence size and fruit distribution among individuals in three orchid species. Amer. J. Bot. 77: 1378-1381. Christenson, E. 2004. Or chidaceae (Orchid Family). In N. Smith, S.A. Mori, A. Henderson, D.W. Stevenson and S.V. Heald (Eds.). Flowering Plants of the Neotropics, pp. 465-468. Princeton University Press, Princeton, New Jersey. Dressler, R.L. 1990. The Orchids: Natural Histor y and Classification. Harvard University Press, Cambridge, Massachusetts. Endress, P.K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge, Great Britain. Esquiln, E. and R.L. Tremblay. 1999. Reproductive biology of the orchid Lepanthes woodburyana Stimson. Plant Species Biology 14:179. Hammel, B.E., M.H. Grayum, C. Herrera, and N. Zamora (Eds.). 2003. Manual de Plantas de Costa Rica: Volumen III. Missouri Botanical Garden Press, St. Louis, Missouri. Janzen, D.H. 1998. Selfand cross-pollination of Encyclia cordigera (Orchidaceae) in Santa Rosa National Park, Costa Rica. Biotropica 12: 72-74. Jerskov, J. and S.D. Johnson. 2006. Lack of flor al nectar reduces self-po llination in a fly-pollinated orchid. Oecologia 147: 60-68. Tremblay, R.L. 1997. Lepanthes caritensis an endangered orchid: No sex, no future? Selbyana 18: 160166. Tremblay, R.L. 1997. Morphological variance among populations of three tropical orchids with restricted gene flow. Plant Species Biology 12: 85-96. Tremblay, R.L., J.K. Zimmerman, L. Lebrn, P. Bayman I. Sastre, F. Axelrod and J. Alers-Garca. 1998. Host specificity and low reproductive success in the rare endemic Puerto Rican orchid Lepanthes caritensis Biological Conservation 85: 298-304. Walter, K.S. 1983. Orchid aceae (Orqudeas, Orchids). In D.H. Janzen (Eds.). Costa Rican Natural History, pp. 282-292. The University of Chicago Press, Chicago, Illinois.
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Lulling, Kathryn A.
Frecuencia de produccin de fruto como una indicacin de la auto-polinizacin en Lepanthes eximia (Orchidaceae: Pleurothallidinae) en Monteverde, Costa Rica
Fruit production frequency as an indication of self-pollination in Lepanthes eximia (Orchidaceae: Pleurothallidinae) in Monteverde, Costa Rica
Most orchids are capable of self-pollination, but outcrossing promotes the variation in flower structure and the specificity of pollination mechanisms prevalent in orchids. For this reason there are many elaborate pollination mechanisms involving specific pollinators. Highly specific mechanisms ensure efficient pollination, yet low fruit production is common in orchids and in the genus Lepanthes. An exception to this trend is Lepanthes eximia, which has a relatively high fruit set. This may indicate that L. eximia does not depend on rare pollination events, but self-pollinates, accepting low genetic variability in order to increase its number of offspring. Two groups of L. eximia, one exposed to potential pollinators and one covered with mesh bonnets, were observed for differences in fruit production in the orchid garden of Dr. Karen Masters in Monteverde, Costa Rica to determine if L.eximia self-pollinates. Comparisons in morphological variation of L. eximia and L. pygmaea, both exposed to potential pollinators, were made to examine the differences in variance between inbred and outbred species. Lepanthes eximia was found to be capable of self-pollination, but no significant difference in the variability of morphological traits of inbred and outbred species of Lepanthes exists.
La mayora de las orqudeas son capaces de auto-polinizarse, pero la estructura floral y los mecanismos especficos de la polinizacin tienden a la polinizacin cruzada. Por eso, hay muchos mecanismos complicados de polinizacin con polinizadores especficos. Los mecanismos muy especficos aseguran la polinizacin eficiente, sin embargo la baja produccin de frutas es comn en las orqudeas y en el genero Lepanthes. Una excepcin a esta tendencia es Lepanthes eximia, que tiene un grupo alto de frutas. Esto indica que L. eximia no depende de los eventos raros de la polinizacin, pero se auto poliniza, aceptando la baja variabilidad gentica para aumentar el nmero de descendencias. Se observaron a dos grupos de L. eximia, uno expuesto a los polinizadores potenciales y el otro cubierto con gorras de malla, para ver las diferencias en la produccin de frutas en el jardn de orqudeas de la Dra. Karen Masters en Monteverde, Costa Rica para determinar si L. eximia se auto poliniza.
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Tropical Ecology 2006
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