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Relationship between Floral Advertisement and Pollinia Removal in Oerstedella exasperata (Orchidaceae). Mary Snayd Department of Biology, Northeastern University ABSTRACT The purpose of this study was to examine how the floral displays and morphology of Oerstedella exasperata affect reproductive success. This species of orchid is typified by extreme variability in both inflorescence and floral characteristics. In particular there is a wide distribution regarding the degree of symmetry observed in the labellum. The degrees of sy mmetry are characterized by variations within the fringe symmetry and bilateral symmetry. Furthermore, the surface area of the labellum varies greatly within a population. These remarkably diverse phenotypic morphologies and the summation of the floral traits can enhance or reduce the reproductive success of particular species. To test the relationship between floral advertisement and reproductive success, each flow er was examined and grouped according to pollinia presence or removal. Results indicated that pollinia removal was not affected by the degree of bilateral or fringe symmetry or by the size of the labellum. Furthermore, within the 100 individuals examined, the asymmetrical trends were considered directional for bilateral symmetry but nondirectional for fringe symmetry. RESUMEN El objetivo de este estudio fue examinar como los patr ones de asimetra en los ra sgos morfolgicos florales de Oerstedella exasperata afecta el xito reproductivo de esta especie. Esta especie de orqudea se caracteriza por la extrema variabilidad en las caractersticas de la flor y de la inflorescencia. El grado de simetra se caracteriza por variaciones en tre la simetra radial y la simetra bilateral. En otras palabras, el rea superficial del labio vara ampliamente dentro de una misma poblacin. Esta remarcable diversidad en la morfologa fenotipica adicionado a los rasgos florales puede incrementar o reducir el xito reproductivo de esa especie. Para determinar la relacin entre las ca ractersticas florales y el x ito reproductivo, cada flor fue examinada y agrupada de acuerdo a la presencia o ausencia de los tubos polnicos. Los resultados indican que la remocin de los tubos polnicos no se vio afectada por el grado de simetra bilateral o la radial, o por el tamao del labellum. Dentro de los 100 individuos examinados, de rasgos asimtricos fueron considerados direccionales para la simetra bilate ral y no direccionales para la simetra INTRODUCTION The Orchidaceae family is an extremely dive rse group of angiosperms that consist of over 20,000 species. Among these species and within individual species, various advertisement mechanisms are used to promot e successful pollinia removal. Pollinia are coherent waxy masses of pollen grains and th eir removal is an indirect measure of reproductive success (Nilsson & Fritz 1996). In order to ensure removal, pollination ecology and the advertisement strategies of or chids have been co-evolving for millions of years. Orchid species have evolved fine-tuned suites of advertisement strategies to further capture the attention of pollinators. The advertisement strategies of flowers rely on intense displays of color, symmetry, size, shape and inflorescence size (number and 1
arrangement of stalks, buds a nd open flowers). One of the predominant cues that orchids use to lure their pollinators is the attractiven ess and exploitation of their labellum, which is a modified median petal that is often critical in attracting, trapping, or providing a landing pad for pollinators. The labellum is further characterized by fleshy lumps, ridges, keels, fringes and lace (Dressler 1981). In addition to these ph enotypic traits, the production of nectar, scents and oils act as rewards to entice and create consistent pollinators. These individual characteristics a nd the summation of the displays provide various stimuli that promote pollinia removal and reproductive success (Murren & Ellison 1996). The majority of orchids are dependent on specific types of pollinators to ensure pollinia removal and reproductive success. However, due to the sheer number of orchid species, there is limited knowledge regarding each pollinator. There is an array of taxa that pollinate orchids; however bees are the most common. Bees are attracted to orchids that have a sweet honey smell, nectar guide s and lack a pure red coloration (van der Cingel 1996). Within this bee pollination syndrom e, there is a tendency for bees to visit preferentially different forms of flowers, ev en among intraspecies forms (Kiester et al. 1984). A general pollination syndrome has been applied to many understudied orchid species as a result. The tropical montane orchid, Oerstedella exasperata, is one of many understudied orchid species. Based on its morphological ch aracteristics and its tendency to follow the bee pollination syndrome it is assumed to be pollinated by bees. The morphological tendencies of O.exasperata show extreme variability in both inflorescence and floral characteristics. These remarkably dive rse phenotypic morphologies may affect pollination success. The flower is characterized by three brown valvate sepals with a pale yellow outline along the edge. The two petals te nd to have a pale green base which fades into a white/yellow color. The labellum is a predominately ornamental median petal that is white with distinct purple markings Based on morphological observations of the various labella within O. exasperata there are apparent differences amongst the coloration patterns, coloration intensity and surface area. Furthermore, there is obvious asymmetry in terms of the number and size of the labella fringes. Degrees of symmetry are based on differences between the right and left side of the labella. These quantitative measurements reveal that th e labella contained within O.exasperata populations have varying degrees of symmetry. Prior studies indicate that morphologi cal variation among intraspecies flowers directly affects their repr oductive success and ability to attract pollinators. The morphological variation observed in te rms of the symmetry and area of the O.exasperata labellum, raises the question of whether thes e variations also increase or decrease the reproductive success of the individual. In relation to the fluctuating asymmetric tendencies of the labella, studies have show n that in many species of flowers there is assortative pollination, in which the pollinator s preferentially vis it symmetrical flowers (Mller 1995). This relationship was further ex amined using artificial flower models and bumblebees; the results also indicated that bumblebees preferred to visit the larger, symmetrical flowers (Mller & Sorci 1997). Co rrelations between morphological flower variations and reproductive succ ess have also been analyzed in terms of surface area of floral structures It has been shown that butte rflies, honeybees and bumblebees preferentially visit and pollinate flowers with longer outlines (Dafni 1992). Based on 2
these previous studies, morphological character istics on the flower level play a key role in advertisement and reproductive success The morphological character istics and advertisements such as color intensity, symmetrical arrangements, inflorescence si ze and labellum size have most likely developed evolutionarily in conjunction with their corresponding pollinator. The morphological variations within O. exasperata should directly affect the percentage of pollinia removal. The specimens with the more attractive morphological variations should represent the specimens that have a greater percentage of pollinia removal. Therefore flowers with larger, more symmetri cal labella should have a higher percentage of pollinia removal. The intras pecies variability within the O. exasperata population gives an unusual opportunity to test pred ictions regarding the effects of flower morphology on pollinator behavior. MATERIALS AND METHODS Oerstedella exasperata is a predominantly terrestrial or chid that flowers between October and March from Costa Rica to Panama at an elevation of 1000-2,200 meters (Zuchowski 2005). This investigation was conducted be tween October 23, 2007 and November 18, 2007. The study site was located near the Mont everde Cloud Forest of Costa Rica at an elevation of approximately 1800 meters. All O. exasperata examined were found on the banks of Cerro Amigos heading toward s the Monteverde radio tower. Analysis focused on the labellum mor phology; however additional observations were made regarding inflorescence struct ure and size. The sample size included 100 recently senesced flowers which were taken from 19 individual plants. These older flowers were chosen in order to ensure that all flowers had an equal opportunity of being pollinated. The older flowers are characterized by a pale yellow coloration within the lip, rather than the white li p of the younger flowers. Each of the 100 flowers were marked, a ssigned a number and labeled with a letter indicating the parent plant. The number of stalks and the nu mber of flowers in bloom per plant were counted. For each labellum, the num ber of fringes on the right and left side were quantified. The difference in the number of fringes observed on the right and left side of the labellum was used as a parameter to determine the degree of symmetry. The absolute value of the difference between the number of fringes on the right and left side was considered the degree of fringe asym metry. The second parameter for measuring degree of symmetry was based on bilateral symme try in terms of the length of each side. The length of the right and left side of the lip was measured in millimeters using calipers. The absolute value of the difference between the two sides was considered the degree of bilateral asymmetry. Width measurements were also recoded; these measures were taken at the widest region of the labellum. Pollinia removal (PR) was determined by probing the inner column; if the flower had not been pollinated then four pollinia were present (PP) in the column. The last observation was made by removing the labellum from the column and measuring the area (cm2) using the Leaf Area Meter. This device will not take accurate area measurements if the sample is too translucent, th erefore prior to taking measurements it was necessary to color even ly the labellum with a permanent marker. The morphological characteristics of the labellum were analyzed separately and in relation to pollinia removal. Frequency distributions were performed in order to determine the degrees of asymmetry among the sampled individuals. Shapiro-Wilk 3
Normality tests were run on these distributions to adjust the distribu tion. A Sign test was conducted using the absolute values of the tw o degrees of asymmetry to determine if the trends in asymmetry were di rectional or non-directional. A simple regression analysis was run in order to determine if the two m easures of symmetry were correlated. Simple regressions were also conducted in order to determine if significant correlations existed between labellum size (width or area) and symmetry. Width and area were run individually against three measures of sy mmetry. The first two symmetry measures used were the previously calculated degree of fringe symmetry and degree of bilateral symmetry. The third measure was consider ed the index of asymmetry and it was calculated for each flower by multiplying the absolute value of the fringe symmetry to the absolute value of the bilateral symmetry. Finally six t-tests were performed to establish if individual morphological traits (symmetry, area and width) affected pollinia removal. RESULTS The results here indicate that there is a great degree of asymmetry in the population studied, in terms of both fringe and bilateral symmetry (Figs. 1 and 2). In the case of fringe symmetry, it is nondirecti onal, i.e., it fluctuates betw een having greater numbers of fringes on the left and right equally resulting in an average symmetry of nearly zero. The nondirectional symmetry was further supported by the results of a Sign te st. In the case of the length of the two sides of the lip, however, the symmetry is directional: there is a tendency for the lip to be slightly longer on the left side. A Sign test reinforced these results of directional symmetry seen in Figur e 2. There is no trend re lating the degree of bilateral or fringe symmetry (Fi gure 3), or between the area (cm2) of the lip or any measure of symmetry (Figure 4). Furtherm ore, there was not significant regression between the width of the labellum and the degree of symmetry (bilateral or fringe; Figure 5). Out of the 100 senesced flowers sample d, 55 had their pollinia removed (PR) while the remaining 45 had pollinia present (PP). Ho wever, there was no significant difference in the morphological features of the flowers with pollinia re moved versus those with it still present in terms of their symmet ry, lip width, or area (Figs. 6-8). DISCUSSION This study is the first to document th e amount of labella asymmetry found among O. exasperata individuals in the Monteverde population. A gradient of bilateral asymmetry was not only observed within the number of la bella fringes but, also in terms of the length of the right and le ft side. On each flower O. exasperata has lip fringes that number from two to six, often in unequal numbers, resulting in high asymmetry. The degree of fringe symmetry fluctuates randomly, such that the overall mean for the population is near zero. Fluctuating asymmetry is thought to be a result of either genetic or environmental factors (Neal et al. 1998). Studi es indicate that indi viduals with a higher level of fluctuating asymmetry tend to be le ss fit in terms of reproductive success because they are discriminated against by pollinators (Neal et al. 1998). Based on preliminary studies with O. exasperata, results did not coincide with the above findings, indicating that asymmetry does not nece ssarily result in reduced fitness for this species. 4
Regarding the second measure of asym metry, results indicated high bilateral asymmetry, but in this case, it is directional (with the left side usually larger). This may be due to how the flower twists while developing in the bud. O. exasperata has a resupinate labellum (on the bottom) and theref ore only twists once, just prior to opening (Dressler 1981). This process of twisting ma y be directional, a nd if so, during this process the left side may tend to elongate. Asymmetry tends to reflect developmental instability, i.e., a mismatch in the growth stages that the two sides of a bila terally symmetrical organism experiences in early development. Sometimes it arises among highly homozygous individuals, or otherwise genetically impaired individuals. Furthermore, the environment can have an impact on whether development proceeds as it should. According to N eal et al. (1998) the factors that trigger asymmetry may result in overall reduced fitness. This infers that one developmental obstacle can resu lt in subsequent reductions of other attractive traits. If this were true for O. exasperata then one would expect a corr elation to exist between the measures of all asymmetry. However, resu lts indicated that there was no correlation between the degree of bilateral asymmetry a nd the degree of fringe asymmetry (Figure 3). Perhaps the asymmetry in the two traits arises due to developmental problems that occur at different stages or under the influence of differentia l environmental factors. If the traits are genetically decoupled or under environmental influences then it is understandable that a correlation does not exis t between the two degrees of symmetry. In a recent study, Strauss (1997) indicated that fitness is also based on other morphological characteristics ( e.g. surface area) that attract pollinators. If asymmetry truly affected the fitness of O. exasperata then one could expect other morphological characteristics such as the area and width of th e labellum to be affected as well. However, the asymmetrical tendencies observed within th e individual labella di d not correlate to the corresponding widths or area. These findings counter past studies performed by both Mller (1995) and Neal et al. (1998) who indicated asymmetry results in an overall decrease of fitness. Despite the non-significant correlations observed between asymmetry and surface area, future studies may want to consider the relationship between asymmetry and other more attractive traits not examined in this study, fo r example, lip color, nectar concentration, or floral scent. Both symmetry and surface area as floral displays are considered signals of phenotypic and genotypic quality (Mlle r 1995). According to Mller (1995), bumblebees preferentially visited and pollin ated flowers that were either large or symmetrical. Based on these findings it was r easonable to study the effects of labellum symmetry and labellum area on pollinia removal. However, results were not consistent with previous findings. Results indicated that flowers that had pollinia removed were no more symmetrical, nor did they have larger or wider lips, than the flowers whose pollinia were removed. The contradictory results may be due to the quantity and quality of O. exasperata nectar production. The studies that have shown that insect pollinators preferentially pollinate symmetrical or large flowers had indicated that nectar production was greater for these individuals (Mller 1995). In terms of sy mmetry alone, this signal and the high quality reward has exerted selec tive pressures on those flowers that are not as symmetrical (Giurfa et al. 1999; Mller & Sorci 1997) Due to the fact that O. exasperata is extremely understudied it is no t known whether nectar production correlates with symmetry or any other mor phological trait. If mo rphological signals are not signaling greater rewards, than there is no reason why the degree of symmetry or 5
degree of one morphological trait would be uniform throughout the population. On another note, pollinia removal may not have been dependent on symmetry or flower size due to the possibility that the pollinators of O. exasperata are simply more enticed by overall plant and inflorescence size rath er than the parameters examined. A greater understanding of the reproductive success of O. exasperata is dependent on future studies taking into account other morphological parameters. These parameters must include plant location, plan t density, inflorescence size, and flower density seeing as these attributes are more than likely responsible for initially attracting pollinators. Studies have indicated that reproductive success is not only affected by morphological variations on a flower level but it is also influenced by the morphology on a plant level (Lehtila & Strauss 1997; Larson & Larson 1990; Bierzy chudek 1981; Flores-Palados & GarciaFranco 2000; Todzia 1983). Pollinator behavior and the reproductive success of flowers have also been linked to chem ical attractants (Galen et al 1987) and environmental factors (Johnson & Bond 1992), therefore these two dynamics are worthy of investigation as well. Furthermore, in order to obtain a better grasp on the morphological trends and reproductive success within the population of O. exasperata, studies must focus on determining who in fact pollinates this species. Assumptions will hinder further understanding between floral displays and reproductive success because the sensory capabilities may be very different between bees, flie s and butterflies. In terms of reproductive success and po llinia removal the parameters tested proved to be an oversimplification of po llination ecology. Although this study explored floral characteristics that have been deemed important in other species; the lack of such importance here implies that future O. exasperata studies will require a multifactorial approach. This multi-dimensional approach along with the acknowledgement that many cues operate simultaneously on the pollin ator will enhance our understanding of pollination systems, floral mor phology and reproductive success. ACKNOWLEDGEMENTS I would like to extend my gratitude to Dr. Karen Masters for all of her support and guidance throughout the project. This study would not have been the same had she not provided the initial inspiration for exploring this understudied species of orchids. I am also gr eatly appreciative to both Taegan McMahon and Pablo Allen for their continued help with the statistics. Furthermore, I am grateful for Nicole Williams companionship up on the clay hill and those people who offered continued encouragement when crunch time arrived. LITERATURE CITED Bierzychudek, P. 1981. Asclepia, Lantana, and Epidendrum: a floral mimicry complex? Reproductive Botany 11: 54-58. Dafni, A. 1992. Pollination ecology. Oxford University Press Inc. New York. 92-102. Dressler, R L. 1981. The orchids; natural history and classification. Harvard University Press. Cambridge, Massachusetts. 43 Flores-Palacios A., J.G. Garcia Franco. 2000. Eff ects of floral display and plant abundance on fruit production on Ryncholaelia glauca (Orchidaceae), Rev. Biol. Trop 51(1): 71-78. Galen, C., K.A Zimmer, AND M.E. Newport. 1987. Pollination in floral scent morphs of Polemonium viscosum a mechanism for disruptive selection on flower size. Evolution 41: 599-606. Giurfa, M., A. Dafni, AND P. Neal. 1999. Floral symmetry and its role in plant-pollinator systems. International Journal of Plant Sciences 160(6): S41-S50. 6
Johnson S.D., AND W.J Bond 1992. Habitat dependent pollination success in a cape orchid. Oecologia 91: 455-457. Kiester, R.A., R. Lande AND D.W. Schemske. 1984. Models of coevolution and speciation in plants and their pollinators. The American Naturalist 124(2): 221. Larson, K.S. AND R.J. Larson. 1990. Lure the locks: showiest ladies-tresses orchids, Spiranthes romanzoffiana affect bumblebee, Bombus spp ., foraging behavior. Can. Nat. 104: 519-525. Lehtila, K., AND S.Y. Strauss. 1997. Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphaniastrum. Oecologia 111: 396-403. Mller, A.P. 1995. Bumblebee prefer ence for symmetrical flowers. Pr oceedings of the National Academy of Sciences of the United Stat es of America 92: 2288-2292. Mller, A. P., AND M. Ericsson. 1995. Pollinator preference for symmetrical flowers and sexual selection in plants. Oikos, 73(1): 15-22. Mller, A.P., AND G. Sorci. 1997. Insect pref erence for symmetrical artificial flowers. Oecologia 114: 3742. Murren, C.J., AND E.M. Ellison. 1996. Effects of habitat, plant size, and floral display on male and female reproductive success of the morphological orchid Brassavola nodosa Biotropica 28(1): 30-41. Neal, P.R., A. Dafni, AND M. Giurfa. 1998. Floral symmetry and its role in plant pollinator systems: Terminolgy, distribution, and hypotheses. Annual Review of Ecology and Systematics 29: 345373. Nilsson, A., AND A. Fritz. 1996. Reproductive su ccess and gender variation in deceit-pollinated orchids. In: Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants, D. G. Lloyd, AND S.C. Barrett. Chapman & Hall, New York, NY. 340-342. Strauss, S.Y. 1997. Floral charact ers link herbivores, pollinators, and plant fitness. Ecology 78(6): 16401645. Todzia, C A. 1983. Epidendrum radicans (Bandera Espaola, Gallito). In: Costa Rican Natural History, D.H. Janzen, ed. The University of Chicago, Chicago, IL. 241-242. van der Cingel, N.A. 2001. An atlas of orchid pollin ation: America, Africa, As ia and Australia. Belkema Publishers, Rotterdam Netherlands. 16-25. Zuchowski, W. 2005. A Guide to tropical plants of Costa Rica. Distribuidores Zona Tropical, Miami, FL. 420. 7
-3-2-1012 0 5 10 15 20 25 30 35 40Frequency of Flowers Fre q uenc y of Flowers Degree of Fringe Asymmetry Figure 1: Frequency distribution of the degr ee of fringe asymmetry on the labellum of Oerstedella exasperata in Monteverde. Degree of fringe asymmetry = (# of fringes on right of the labellum)-(#of fringes on left of the labellum). Shapiro-Wilk Test of Normality; SW-W = 0.92, P < .0001, n = 100 recently senesced flowers. -1.4-1.2-1.0-0.8-0.6-0.4-0.20.00.20.40.60.81.01.2 0 2 4 6 8 10 12 14 16 18 20 22 24 26 qy Fre q uenc y of Flowers Degree of Bilateral Asymmetry Figure 2: Frequency distribution of the degr ee of bilateral asymmetry on the labellum of Oerstedella exasperata in Monteverde. Degree of bilatera l asymmetry = (length of right)(length on left). Shapiro-Wilk Test of Normality; SW-W = 0.97, P = 0.01, n = 100 recently senesced flowers. (NOTE: here we have a case of directional asymmetry: the left si de tends to be longer than the right. This is evident by the p valu e, and the high frequency of negative values.) 8
0 0.2 0.4 0.6 0.8 1 0123 Absolute Value of the Degree of Fringe AsymmetryAbsolute Value of the Degre1.2 4 e of Bilateral Asymmetry Figure 3: Relationship between the degree of bilateral symmetry and fringe symmetry. R2 = 0.00, P = 0.92, n = 100 recently senesced flowers. 9
0 0.2 0.4 0.6 0.8 0123 Degree of Fringe Asymmetry Area of Labellum (cm21 1.2 4)a. 0 0.2 0.4 0.6 0.8 1 1.2 00.20.40.60.811.2 Degree of Bilateral Asymmetry Area of Labellum (cm2)b. 0 0.2 0.4 0.6 0.8 1 1.2 00 511 5 Index of Asymmetry Area of Labellum (cm2)c. 2 Figure 4: Simple Regressions illustrating a. relationships between lip area and degree of fringe symmetry R2 = 0.00, P = 0.78. b. relationship between lip area and degree of bilateral symmetry R2 = 0.02, P = 0.14. c. relationship between lip area and index of asymmetry (abs fringe asymmetry x abs bilateral asymmetry) R2 = 0.01 P = 0.24. For all, n = 100 recently senesced flowers. 10
0 0.5 1 1.5 2 2.5 3 3.5 4 0204060801 Degree of Fringe AsymmetryWidth of Labellum(mm4.5 00 ) 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 0 0.5 1 1.5 2 A s y mmetr y Inde x Width of Labellum(mm ) c. a. 0 0.2 0.4 0.6 0.8 1 1.2 0204060801 Degree of Bilateral AsymmetryWidth of Labellum(mm00 ) b. Figure 5: Simple Regressions illustrating a. relationships between width and degree of fringe symmetry R2 = 0.01, P = 0.49. b. relationship between width and degree of bilateral symmetry R2 = 0.03, P = 0.05. c. relationship between width and index of asymmetry (abs fringe asymmetry x abs bilateral asymmetry) R2 = 0.02, P = 0.19. For all, n = 100 recently senesced flowers. 11
0 0.2 0.4 0.6 0.8 1 1.2PR PPAverage Fringe Asymmetr y a. 0 0.2 0.4 0.6 0.8 1 1.2PR PPAverage Bilateral Asymmetr y b. 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2 PR PPAverage Index of Asymmetr y c. Figure 6: Relationship between pollinia re moval (PR) pollinia presence (PP) and symmetry. a. relationship between pollinia removal and degree of fringe asymmetry, t = 0.17, P = 0.87. b. relationship between pollinia re moval and average bilateral asymmetry, t = 0.16, P = 0.88. c. pollinia removal and index of asymmetry, t = -0.33, P = 0.75. For all, n = 100 recently senesced flowers. 12
0.56 0.58 0.6 0.62 0.64 0.66 0.68 0.7 PR PPAverage Area of Labellum (cm2 ) Figure 7: Relationship between pollinia remova l (PR) pollinia presence (PP) and lip area, t = 0.48, P = 0.63, n =100. 2.25 2.3 2.35 2.4 2.45 2.5 2.55 2.6 PR PPAverage Lip Width (mm) Figure 8: Relationship between pollinia removal (PR) pollinia presence (PP) and lip width, t = 0.12, P = 0.91, n = 100. 13
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La relacin entre la publicidad floral y la eliminacin de las polinias en Oerstedella exasperata (Orchidaceae).
Relationship between floral advertisement and Pollinia removal in Oerstedella exasperata (Orchidaceae).
The purpose of this study was to examine how the floral displays and morphology of Oerstedella exasperata affect reproductive success. This species of orchid is typified by extreme variability in both inflorescence and floral characteristics. In particular there is a wide distribution regarding the degree of symmetry observed in the labellum. The degrees of symmetry are characterized by variations within the fringe symmetry and bilateral symmetry. Furthermore, the surface area of the labellum varies greatly within a population. These remarkably diverse phenotypic morphologies and the summation of the floral traits can enhance or reduce the reproductive success of particular species. To test the relationship between floral advertisement and reproductive success, each flower was examined and grouped according to pollinia presence or removal. Results indicated that pollinia removal was not affected by the degree of bilateral or fringe symmetry or by the size of the labellum. Furthermore, within the 100 individuals examined, the asymmetrical trends were considered directional for bilateral symmetry but nondirectional for fringe symmetry.
El propsito de este estudio era examinar cmo los patrones de asimetra en los rasgos morfolgicos florales de Oerstedella exasperata afecta el xito reproductivo de esta especie.
Text in English.
Tropical Ecology 2007
Ecologa Tropical 2007
Eliminacin de pollinia
t Monteverde Institute : Tropical Ecology