| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Reproductive Biology |
Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo. 1095, 41080-Sevilla, Spain
Received for publication July 4, 2005. Accepted for publication January 24, 2006.
ABSTRACT
Pollen limitation, resource limitation, fruit abortion, and predation have all been proposed as factors explaining low fruit set in hermaphroditic plants. We conducted a 5-year study combining field observations and pollination experiments to determine the causes of the low fruit set in Aristolochia paucinervis, a Mediterranean species with a specialized pollination system in two populations in SW Spain. Fruit initiation was markedly low, and between 28.6 and 75.0% of the flowering stems did not initiate any fruit. In most flowers, the number of germinated pollen grains was less than the number of ovules, and supplemental pollination significantly increased fruiting, indicating deficient pollination. In A. paucinervis, autonomous self-pollination seems to be a decisive factor in fruit production because the number of germinated pollen and the fruit set from flowers bagged before anthesis were similar to those in free-pollinated flowers. Only in 2005 did flowers that were successfully pollinated outnumber ripened fruits, suggesting that other factors limit fruiting. We found a significant positive correlation between tuber mass and fruit set. Deficient pollination and lack of resources could explain the low fruit set, but the relative consequences seem to vary spatially and temporarily.
Key Words: Aristolochia paucinervis • Aristolochiaceae • autonomous self-pollination • fruit set • multi-year study • pollen limitation • resource limitation • Spain
Among hermaphroditic plants, a low fruit-to-flower ratio is a common phenomenon that has been widely reported (Stephenson, 1981
; Sutherland, 1986
; Ehrlén, 1991
; Ramirez, 1993
; Guitián et al., 1996
; Arista et al., 1999
; Holland et al., 2004
). Various non-exclusive factors have been put forward to explain low fruit set in plant species, such as predation, lack of pollination, or lack of resources (Bierzychudek, 1981
; Lee and Bazzaz, 1982
; Bookman, 1984
; Campbell, 1985
; Johnston, 1991
; Vesprini and Galetto, 2000
). The fact that fruit set is limited by one or others of these factors is relevant to diverse aspects of reproductive biology, including the evolution of breeding systems and floral displays (Knight et al., 2005
and references therein).
Pollination can be the first factor limiting fruit production (Schemske, 1980
; Howell and Roth, 1981
; Arista et al., 1999
). Flower surplus may be a strategy to increase pollinator visits, because the plants would be more attractive visually and offer a greater reward (Willson and Rathcke, 1974
; Podolosky, 1992
; Bartareau, 1995
). Resource availability is another important factor limiting fruit production (Stephenson, 1981
; Bawa and Webb, 1984
; Torres and Galetto, 1999
). Provided that pollination is efficient and more fruits are initiated than the ones that can ripen, the production of surplus flowers allows the selective abortion of lowest quality fruits (Lloyd, 1980
; Stephenson, 1981
; Bookman, 1984
; Sutherland and Delph, 1984
; Sutherland, 1986
, 1987
; Guitián et al., 1996
; Torres et al., 2002
).
Factors affecting fruiting can vary within years and within populations and may alter patterns of selection for plant traits (Stebbins, 1970
; Aigner, 2001
). Pollen limitation varies among years (Campbell, 1987
; Vaughton, 1991
) and can occur in conjunction with resource limitation (Zimmerman and Pyke, 1988; Ehrlén, 1992
). Differences among populations in factors affecting fruit set are commonly reported in the literature (e.g., Arista et al., 1999
; Larson and Barrett, 1999
). However long-term studies on fruiting patterns of a species and factors affecting it are rarely reported (Vaughton, 1991
), but they are essential for understanding biotic and abiotic controls on fruit production. These kinds of studies are specially relevant in ecosystems with unpredictable environmental conditions such as those in the Mediterranean region (Cowling et al., 1996
; Rodó and Comín, 2001
) where both resource and pollinator availability markedly change over years (Herrera, 1989
; Thomson, 2001
; Valladares et al., 2002
).
Although one can expect that plants with more specialized flowers may have less pollen limitation (Neal et al., 1998
; Knight et al., 2005
), a greater variance in fruit set over years can occur in taxa for which floral traits preclude pollination by the majority of floral visitors, because abundance of a few specialized pollinators may fluctuate more than that of many generalized pollinators (Waser et al., 1996
; Larson and Barrett, 1999
; Knight et al., 2005
). Aristolochia species have a highly specialized pollination system, trapping insects in their modified tubular perianths and imprisoning them for a time. Their protogynous flowers attract flies when they open, and the insects are trapped inside the perianth; when the anthers dehisce some time later, the flies are released with their pollen loads. The pollination mechanism in Aristolochia species is regarded as deceptive and, because pollinators belong to saprophagous groups, they are not likely to depend on floral nectar and pollen of Aristolochia (Wolda and Sabrosky, 1986
; Sakai, 2002
). Exceptionally, in some species of Aristolochia, the pollinators oviposit and their brood develops in the flowers (Hime and Costa, 1985
; Sakai, 2002
; Burgess et al., 2004
). Some Aristolochia species are adapted for capturing certain size classes and families of flies and also may trap species that are not effective pollinators (Brantjes, 1980
; Sakai, 2002
; Burgess et al., 2004
). Thus, in A. bracteolata only 10.5% of the floral visitors carried pollen grains on their bodies (Razzak et al., 1992
). There is little information about reproductive success of Aristolochia species, although low fruit set was reported in two species, and the lack of compatible pollen was suggested as factor determining fruit set (Sakai, 2002
). The importance of other factors affecting fruit set, such as predation or resource availability, is practically unknown.
Aristolochia paucinervis Pomel has remarkably low fruit set in natural populations in SW Spain. We show here the fruiting pattern of Aristolochia paucinervis and factors affecting it and discuss the importance of flower color, pollination, predation, and reserves stored in the underground organs for fruit production. Due to the unpredictability of both environmental conditions and pollinator availability in Mediterranean ecosystems, our study was done over five consecutive years and combined pollination experiments and field observations to achieve a more meaningful interpretation of the data.
MATERIALS AND METHODS
Study area and study species
The study was carried out on two populations: Membrillo and Cuadrejón, situated in Hinojos, Huelva, SW Spain (UTM 29S 072 413, 37°16–18' N latitude and 6°23–26' W longitude). The Membrillo population is placed on sandy soils in a valley near a stream. Vegetation consists of a dense forest of Quercus suber L. (Fagaceae) with scattered individuals of Pinus pinea L. (Pinaceae); the shrub layer is mainly Cistus salviifolius L. (Cistaceae), Myrtus communis L. (Myrtaceae), and Rubus ulmifolius Schott (Rosaceae). The Cuadrejón population is placed on clayey soils on a hill. Vegetation consists of scattered individuals of P. pinea with some trees of Q. suber, and the shrub layer is mainly C. ladanifer L. (Cistaceae), C. salviifolius and M. communis. In the two populations, Aristolochia paucinervis is abundant, but in the Membrillo Aristolochia plants are in the shade of the canopy forest, and in the Cuadrejón, the trees are sparser so that Aristolochia individuals are mostly in sunny conditions.
Climatic conditions were similar in both populations. During the study period, annual mean temperatures ranged from 16.6°C to 17.6°C. Annual precipitation was 893 mm in 2000–2001 (September–August), 910.5 mm in 2001–2002, 661.5 mm in 2002–2003 and 970.3 mm in 2003–2004, whereas in 2004–2005 total precipitation was markedly lower, only 226 mm.
Aristolochia paucinervis is a perennial herb frequent in the undergrowth of the western Mediterranean region. It has a tuber for storage of reserves and loses its aerial part in summer, producing new stems each year. Its protogynous flower has a straight tubular perianth, formed by a modified calyx. The base of the perianth forms a chamber (the utricle) around the fused styles, stigmata, and anthers, forming a gynostemium.
Two floral phenotypes are found: plants with yellowish-white flowers, and others with brownish-purple flowers (R. Berjano, personal observation). Flowers of A. paucinervis produce a mean of 2100 pollen grains and 42 ovules. The pollination mechanism of Aristolochia paucinervis involves the trapping of small Diptera during the female phase and their liberation during the male phase. After flowering, the stigmata fall, together with the perianths, while the ovaries remain on the plant. Aristolochia paucinervis has capsular fruits, up to 3 cm in length, that take up to 3 months to ripen. Each capsule contains a mean of 11 large seeds with abundant reserves.
Sampling methods
In Aristolochia paucinervis, it is difficult to distinguish individuals, because the seeds often germinate so close together that the stems intermingle. In both populations, the fruit set in 46 uprooted whole plants was compared with that of individual stems of each plant chosen at random; no significant differences were found between them (Mann–Whitney U test: U = 471.00, Z = –0.92, P = 0.356 for the Membrillo population and U = 1122.50, Z = –0.55, P = 0.579 for the Cuadrejón population). Thus, in this study, one stem per plant was chosen at random because it gives a good estimate of the fruit set of the whole plant.
For a detailed study of the factors affecting fruiting, from 2001 to 2005, between 30 and 56 stems separated from each other by at least 1 m were tagged randomly each year in the populations of A. paucinervis. During flowering, these stems were visited every 7–15 days. At each visit, flowers with signs of predation were noted, and any ovaries beginning to grow were considered as initiated fruits and were tagged. These ovaries were monitored for predation, abortion, and maturation on subsequent visits. In addition, at the end of each flowering period, all floral pedicels on each tagged stem were counted. Detected predators were collected for identification. To check if flower color affected the fruiting of A. paucinervis, during 2001 and 2002 the tagged stems were separated in two subsamples according to their floral phenotypes and their production of flowers and fruits were analyzed. Given that these stems were randomly tagged, the sizes of the subsamples would reflect the proportions of each floral phenotype in the field.
Pollination as a limiting factor for fruiting
To elucidate whether pollination is a limiting factor for fruiting in A. paucinervis, randomly chosen flowers were tagged both in Membrillo (N = 38 in 2004, N = 134 in 2005) and Cuadrejón (N = 48 in 2004, N = 140 in 2005). Given that after flowering, the stigma and the perianth fall jointly while the ovary remains on the plant, in each tagged flower the perianth was taped to the pedicel to avoid the loss of stigmata. These flowers were left to pollinate freely, and their stigmata were collected after flowering, fixed in FAA (formalin-ethyl alcohol 70%-acetic acid, 5:90:5), stained with aniline blue (0.01%), and observed using fluorescence microscopy (Martin, 1959
). Germinated pollen grains on each stigma were counted. In the field, the development of these ovaries was recorded, noting whether fruit ripened. In addition, ovules were counted in randomly chosen flowers in the two populations (N = 20 in Cuadrejón, N = 23 in Membrillo).
To check if pollination could significantly increase fruit set, in 2003 manual pollinations were made in the Membrillo population, both with pollen from plants separated by at least 5 m (N = 84, xenogamy) and with pollen from the same stem (N = 100, geitonogamy). Some flowers (N = 98) were bagged prior to anthesis to check for autonomous self-pollination. Control flowers were allowed to pollinate freely (N = 99).
To quantify pollen deposition in autonomously self-pollinated flowers of A. paucinervis, during 2004 in each population, between 26 and 39 randomly chosen flowers were bagged before anthesis, impeding the access of pollinators. After anthesis, the stigmata of these flowers were collected, to count the germinated pollen grains on each; in the field, the ovaries were monitored for fruit development.
Tuber size as a determinant of fruiting
To examine whether underground reserves affect the production of aerial biomass and/or fruits, in 2004, 45 whole plants in the Membrillo population were uprooted at the end of fruiting. The stems, flowers, and fruits produced by each of these plants were counted, and the tubers were dried at 60°C for 48 h, and weighed.
Statistical analyses
The numbers of flowers, initiated fruits, ripe fruits, and the fruit set, were compared between stems with different flower color within each population by the nonparametric Mann–Whitney U test (Hollander and Wolfe, 1999
), because the data could not be normalized by any of the usual transformations. Independently of floral phenotype, we used a Kruskal–Wallis ANOVA (Hollander and Wolfe, 1999
) to compare the number of flowers, the number of initiated, aborted, predated, and ripe fruits, and the fruit set between years within each population. The comparisons between populations within the same year were made with Mann–Whitney U tests. In each population, the number of germinated pollen grains on the stigmata in relation to the fate of the flowers (fruit ripening or not) was also compared with a U test, because again the data could not be normalized. For each plant, Pearson parametric correlations were established between tuber mass and production of stems, flowers, and fruits.
RESULTS
Differences depending on flower color
Both in the Membrillo and the Cuadrejón populations and in the two studied years, flower production of stems with yellowish-white flowers was statistically similar to that of stems with brownish-purple flowers (Table 1; U = 131.50, Z = 0.02, P = 0.987 for Membrillo 2001; U = 163.00, Z = 0.68, P = 0.497 for Membrillo 2002; U = 296.00, Z = 0.06, P = 0.952 for Cuadrejón 2001; U = 268.00, Z = 0.57, P = 0.568 for Cuadrejón 2002). In both populations and for the two years, the number of initiated fruits, the number of ripe fruits, and the fruit set had medians of zero for the two floral colors (Table 1), nor did these variables differ significantly between the two flower colors (Mann–Whitney U test, P > 0.05). Given that flower color had no effect on fruiting, for the rest of the study this factor was not taken into account.
|
|
The abortion of developing fruits was, in general, infrequent and irregularly distributed. Only during 2001 in Membrillo and during 2005 in both populations was the percentage of aborted fruits per stem high, with a median of 75.0% in Membrillo during 2001, and 71.43% and 100% in Membrillo and Cuadrejón, respectively, during 2005 (Table 3). The median of the percentage of aborted fruits per stem was zero in all other cases. Differences between years within each population were significant (Membrillo: H = 16.71, df = 4, P = 0.002; Cuadrejón: H = 15.35, df = 4, P = 0.004). Differences between populations were significant only for the year 2001 (U = 71.00, Z = 2.31, P = 0.021).
|
The number of ripe fruits produced per stem was low in relation to the number of flowers and varied among years. In both populations, between 48.6% and 92.3% of stems with flowers did not produce any ripe fruit (Fig. 1). The number of fruits per stem had a median of zero in the two populations during the 5 years, except for Membrillo in 2003 and Cuadrejón in 2004, where the median was one. In the Membrillo population, only one stem (in 2003) achieved seven fruits, and the rest did not exceed four fruits. In the Cuadrejón population, only three stems (in 2004) achieved five fruits (Fig. 1).
|
Predation of developing fruits was by Zerynthia rumina and wood mice, Apodemus sylvaticus L. (Muridae) and generally low. Most stems were not affected, although in some stems every fruit initiated was had signs of predation (Table 3). In both populations during the 5 years, the median percentage of predator-affected fruits per stem was zero. Neither differences between years within each population nor differences between populations within the same year were significant.
Pollination as limiting factor of fruiting
All pollen grains observed on the stigmata of the flowers had germinated. In the Membrillo population the freely pollinated flowers had a median of 12 germinated pollen grains on their stigmata (N = 38) in 2004, and of 28.5 (N = 134) in 2005. In the Cuadrejón population these flowers had a median of 3.5 germinated pollen grains (N = 48) in 2004 and 6 (N = 140) in 2005. In the Membrillo population, only 10.5% in 2004 and 6.1% in 2005 of these flowers developed ripe fruits. Similarly, in the Cuadrejón population, only 8.3% in 2004 and 2.1% in 2005 of these flowers had ripe fruits. The number of germinated pollen grains on the stigmata of the flowers that yielded ripened fruit was markedly higher than in those that did not yield ripen fruit (Fig. 2; Membrillo 2004: U = 0.00, Z = –3.23, P = 0.001; Membrillo 2005: U = 56.00, Z = –4.20, P < 0.001; Cuadrejón 2004: U = 2.00, Z = –3.21, P = 0.001; Cuadrejón 2005: U = 50.00, Z = –2.24, P = 0.025). At least 50 germinated pollen grains were found on the stigmata of any flower that developed fruit.
|
2, Membrillo: p = 0.496; Cuadrejón: p = 0.221). Nevertheless, in 2005, the percentage of flowers with sufficient pollen doses was significantly higher than the fruit set of these flowers: 41.0% vs. 6.1% in Membrillo and 13.6% vs. 2.1% in Cuadrejón (2: p < 0.001).
|
2: p < 0.01). Fruit set after geitonogamous and xenogamous pollination were not statistically different (2: p = 0.768), indicating that this species does not have self-incompatibility system. In A. paucinervis autonomous self-pollination occurs, and the fruit set in flowers bagged prior anthesis was statistically similar to that of free-pollinated flowers (7.1% vs. 12.1%; 2: p = 0.235).
The stigmata of bagged flowers supported between 0 and 70 germinated pollen grains, with a median of 14 (N = 26) for the Membrillo population, and between 0 and 144 germinated pollen grains, with a median of 13 (N = 39) for Cuadrejón. In Membrillo only one flower produced fruit (3.85% fruit set), and its stigma supported 70 germinated pollen grains. In Cuadrejón also, only one flower set fruit (2.56% fruit set) and it had 144 germinated pollen grains. In 2004 in both populations, the number of pollen grains on stigmata in autonomous self-pollinated flowers was statistically similar to that in freely pollinated flowers (Membrillo: U = 479.50, Z = 0.20, P = 0.843; Cuadrejón: U = 913.50, Z = –0.20, P = 0.848). Similarly, fruit set in autonomous self-pollinated flowers was statistically similar to that in freely pollinated flowers (2: p > 0.05).
Tuber size as determinant of fruiting
In A. paucinervis, the plants with heaviest tubers produced more stems, flowers, and fruits. A significant positive correlation was found between the tuber mass and the number of stems (r = 0.844; P < 0.001, N = 45), the number of flowers (r = 0.886, P < 0.001; N = 45), the number of initiated fruits (r = 0.554, P < 0.001, N = 40) and the number of ripe fruits (r = 0.582, P < 0.001, N = 40). No plants with a tuber mass under 24 g had ripened fruits. A significant positive correlation between the tuber mass and the fruit set was also found (r = 0.398, P = 0.011, N = 40).
DISCUSSION
Low fruit set seems to be a general phenomenon in Aristolochia paucinervis because it was markedly low in the two populations during this 5-year study, indicating the existence of flower surplus, as in many other plant species (Stephenson, 1981
; Sutherland, 1986
; Guitián et al., 1996
; Arista et al., 1999
). In A. paucinervis, there is no pollinator discrimination with regard to flower color. A similar situation has been reported in A. pilosa (Wolda and Sabrosky, 1986
). The role of perianth color in attracting pollinators has been suggested in some Aristolochia species, but the strong scent of the flowers appears to be the attractant in most species (Brantjes, 1980
; Vogel, 1990
; Burgess et al., 2004
). Although A. paucinervis has no obvious fragrance, a compound attractive to insects but not perceptible by humans could be an attractant as in other trap species (Wolda and Sabrosky, 1986
; Hall and Brown, 1993
).
In A. paucinervis a minimum of 50 germinated pollen grains is required to obtain a fruit. Given that this species has an average of 43 ovules per flower, 50 germinated pollen grains represents 1.2 times the number of ovules per flower. Because the fruits of A. paucinervis presented an average of 11 seeds, at least 4.5 germinated pollen grains seem to be required to produce a seed. Although species such as Passiflora vitifolia have a pollen to seed ratio of 1:1 (Snow, 1982
), more than one pollen grain is usually required to produce a seed. Thus, the ratio found in A. paucinervis is similar to those found in other species (Snow, 1986
; Winsor et al., 2000
).
The results show the scant importance of predation as a limiting factor of fruit initiation. Lack of resources or insufficient pollination could be the main causes of the sparse fruit initiation in A. paucinervis. Tuber mass is an indicator of the amount of stored reserves available for sexual reproduction (Herrera, 1988
). During the 5 years of study a high proportion of plants of both populations did flower but did not initiate any fruit. Plants with small tubers did not fruit, and the correlation between tuber mass and fruit set is evidence that fruiting in small plants is limited by available resources. However, fruiting was markedly low even in biggest plants.
Insufficient pollination can be the consequence of inviable pollen or of scarce or inefficient pollinators. The pollen grains found on the stigmata of A. paucinervis had germinated, ruling out pollen inviability as the cause of low fruit initiation. Aristolochia paucinervis flowers are visited by small Diptera, which are trapped inside the perianth and are liberated later; however, few insects were found inside the flowers, and they were often dead (R. Berjano, unpublished data). This lack suggests insufficient pollination and is supported by the scarce pollen found on the stigmata of the freely pollinated flowers, the lack of fruit production from most flowers, and the presence of fewer germinated pollen grains than ovules on most stigmata of freely pollinated flowers. In addition, manual pollinations significantly increased fruit set.
Persistent pollen limitation has evolutionary consequences. Most notably, pollen limitation may favor the evolution of self-compatibility and/or increased selfing when selfing offers reproductive assurance (Knight et al., 2005
). Results indicate that A. paucinervis is a self-compatible species, and autonomous selfing occurs despite its protogyny. Nevertheless, the existence of autonomous self-pollination in Aristolochia has already been proven in other species (Razzak et al., 1992
; Sakai, 2002
). In A. paucinervis, pollen deposition in bagged flowers and fruit set by autonomous self-pollination were similar to those of free pollinated flowers. The fact that in A. paucinervis insufficient pollination was a recurrent situation during the 5-year study could indicate that the trap mechanism is inefficient, and thus autonomous self-pollination would be crucial for fruit production. Consistently, the low pollen to ovule ratio of A. paucinervis (50) would indicate that this is a species with high selfing (Cruden, 1977
). In another Aristolochia species the importance of autonomous self-pollination for fruiting has been reported (Razzak et al., 1992
). Similarly, in Tacca chantrieri, another species with a trap mechanism, fruiting is a consequence of autonomous self-pollination (Zhang et al., 2005
). Thus, in flowers with trap mechanism an important role of autonomous self-pollination in fruiting seems common, at least in self-compatible species, probably as a consequence of persistent pollen limitation.
Although pollen limitation is persistent in A. paucinervis, during 2005, fruit set was significantly lower than the percentage of flowers with sufficient pollen doses, and the abortion rate was high in both populations. The extreme drought in 2005, less than 34% rainfall than in previous years, was a resource limitation and made abortion an important limitation to fruiting. Thus, in A. paucinervis the role of the different factors limiting fruiting varied among years, as reported in others multiyear studies (Dudash and Fenster, 1997
; Zimmerman and Pyke, 1998
).
In conclusion, the low fruit production in A. paucinervis is a consequence mainly of insufficient pollination and secondarily of resource limitation, with the relative importance of these factors varying over time. Insufficient pollination was a recurrent situation during the 5 years of study, and generally this insufficiency was high enough to avoid resource limitation. Only in stressful environmental conditions such as those of the year 2005, did resource limitation operate. Pollination by insects was inefficient, and autonomous self-pollination seems to be decisive to produce fruit.
FOOTNOTES
1 This work was supported by a Ph.D. grant from the Ministerio de Educación, Cultura y Deporte to R.B. and by two projects of the Spanish CICYT (REN2002-04354-C02-02/GLO and REN2002-04634-C05-03) and by grant from Junta de Andalucía (RNM 204). The authors thank L. Berjano for linguistic advice and two anonymous reviewers for providing critical and constructive review of the manuscript. 
2 Author for correspondence (regina{at}us.es
)
LITERATURE CITED
Aigner P. A.. 2001. Optimality modeling and fitness trade-offs: when should plants become pollinator specialists?. Oikos 95: 177-184.[CrossRef][ISI]
Arista M. Ortiz P. L. Talavera S.. 1999. Apical pattern of fruit production in the racemes of Ceratonia siliqua (Leguminosae: Caesalpinoideae): role of pollinators. American Journal of Botany 86: 1708-1716.
Bartareau T.. 1995. Pollination limitation, costs of capsule production and the capsule-to-flower ratio in Dendrobium monophyllum F. Muell. (Orchidaceae). Australian Journal of Ecology 20: 257-265.
Bawa K. S. Webb C. J.. 1984. Flower, fruit and seed abortion in tropical forest tree: implications for the evolution of paternal and maternal reproductive patterns. American Journal of Botany 71: 736-751.[CrossRef][ISI]
Bierzychudek P.. 1981. Pollinator limitation of plant reproductive effort. American Naturalist 117: 838-840.[CrossRef][ISI]
Bookman S. S.. 1984. Evidence for selective fruit production in Asclepias. Evolution 38: 72-86.[CrossRef][ISI]
Brantjes B. M.. 1980. Flower morphology of Aristolochia species and the consequences for pollination. Acta Botanica Neerlandica 29: 212-213.
Burgess K. S. Singfield J. Melendez V. Kevan P. G.. 2004. Pollination biology of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico. Annals of the Missouri Botanical Garden 91: 346-356.[ISI]
Campbell D. R.. 1985. Pollinator sharing and seed set of Stellaria pubera: competition for pollination. Ecology 66: 544-553.[CrossRef][ISI]
Campbell D. R.. 1987. Interpopulation variation in fruit production: the role of pollinator limitation in the Olympic mountains. American Journal of Botany 74: 269-273.[CrossRef][ISI]
Cowling R. M. Rundel P. W. Lamont B. B. Arroyo M. K. Arianoutsou M.. 1996. Plant diversity in the Mediterranean-climate regions. Trends in Ecology and Evolution 11: 352-360.
Cruden R. W.. 1977. Pollen–ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31: 32-46.
Dudash M. R. Fenster C. B.. 1997. Multiyear study of pollen limitation and cost of reproduction in the iteroparous Silene virginica. Ecology 78: 484-493.[CrossRef][ISI]
Ehrlén J.. 1991. Why do plants produce surplus flowers? A reserve-ovary model. American Naturalist 138: 918-933.[CrossRef][ISI]
Ehrlén J.. 1992. Proximate limits to seed production in a herbaceous perennial legume, Lathyrus vernus. Ecology 73: 1820-1831.[CrossRef][ISI]
Guitián J. Guitián P. Navarro L.. 1996. Fruit set, fruit reduction and fruiting strategy in Cornus sanguinea (Cornaceae). American Journal of Botany 83: 744-748.[CrossRef][ISI]
Hall D. W. Brown B. V.. 1993. Pollination of Aristolochia littoralis (Aristolochiales: Aristolochiaceae) by males of Megaselia spp. (Diptera: Phoridae). Annals of the Entomological Society of America 86: 609-613.
Hime da C. de L. Costa E.. 1985. Sobre Megaselia (M.) aristolochiea n. sp. (Diptera, Phoridea) cujas larvas se criam nas flores de Aristolochia labiata Willd. (Aristolochiaceae). Revista Brasileira de Biologia 45: 621-625.
Herrera C. M.. 1989. Pollinator abundance, morphology, and flower visitation rate: analysis of the "quantity" component in a plant-pollinator system. Oecologia 80: 241-248.[ISI]
Herrera J.. 1988. Reproducción sexual y multiplicación vegetativa en Arisarum simorrhinum Durieu (Araceae). Lagascalia 15: 25-41.
Holland J. N. Bronstein J.L. DeAngelis D. L.. 2004. Testing hypotheses for excess flower production and low fruit-to-flower ratios in a pollinating seed-consuming mutualism. Oikos 105: 633-640.[CrossRef][ISI]
Hollander M. Wolfe D. A.. 1999. Non-parametric statistical methods, 2nd ed Wiley, New York, New York, USA.
Howell D. Roth B.. 1981. Sexual reproduction in agaves: the benefits of bats, the cost of semelparous advertising. Ecology 62: 1-7.[CrossRef][ISI]
Johnston M. O.. 1991. Pollen limitation of female reproduction in Lobelia cardinalis and L. siphilitica. Ecology 72: 1500-1503.[CrossRef][ISI]
Knight T. M. Steets J. A. Vamosi J. C. Mazer S. J. Burd M. Campbell D. R. Dudash M. R. Johnston M. O. Mitchell R. J. Ashman T. L.. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics 36: 467-497.
Larson B. M. H. Barrett S. C. H.. 1999. The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). Journal of Ecology 87: 371-381.[CrossRef]
Lee T. D. Bazzaz F. A.. 1982. Regulation of fruit and seed production in an annual legume, Cassia fasciculata. Ecology 63: 1363-1373.[CrossRef][ISI]
Lloyd D. G.. 1980. Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive season. New Phytologist 86: 69-79.[CrossRef][ISI]
Martin F. N.. 1959. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34: 125-128.[ISI][Medline]
Neal P. R. Dafni A. Giurfa M.. 1998. Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annual Review of Ecology and Systematics 29: 345-373.[CrossRef][ISI]
Podolosky R. D.. 1992. Strange floral attractors: pollination attraction and the evolution of plant sexual systems. Science 258: 791-793.
Ramirez N.. 1993. Production and cost of fruits and seeds among life forms. Biotropica 25: 46-60.[CrossRef][ISI]
Razzak M. A. Ali T. Ali S. I.. 1992. The pollination biology of Aristolochia bracteolata Lamk. (Aristolochiaceae). Pakistan Journal of Botany 24: 79-87.[ISI]
Rodó X. Comín F.. 2001. Fluctuaciones del clima mediterráneo. Conexiones globales y consecuencias regionales. In R. Zamora, F. I. Pugnaire [eds.] Ecosistemas mediterráneos, análisis funcional 1-35 CSIC, Madrid, Spain.
Sakai S.. 2002. Aristolochia spp. (Aristolochiaceae) pollinated by flies breeding on decomposing flowers in Panama. American Journal of Botany 89: 527-534.
Schemske D. W.. 1980. Evolution of floral display in the orchid Brassavola nodosa. Evolution 34: 489-493.[CrossRef][ISI]
Snow A. A.. 1982. Pollination intensity and seed set in Passiflora vitifolia. Oecologia 55: 231-216.[CrossRef][ISI]
Snow A. A.. 1986. Pollination dynamics in Epilobium canum (Onagraceae): consequences for gametophytic selection. American Journal of Botany 73: 139-151.[CrossRef][ISI]
Stebbins G. L.. 1970. Adaptive radiation of reproductive characteristics in angiosperms. I. Pollination mechanisms. Annual Review of Ecology and Systematics 1: 307-326.
Stephenson A. G.. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12: 253-279.
Sutherland S.. 1986. Patterns of fruit set: what controls fruit-flower ratios in plants?. Evolution 40: 177-128.
Sutherland S.. 1987. Why hermaphroditic plants produce many more flowers than fruits: experimental test with Agave mckelveyana. Evolution 41: 750-759.[CrossRef][ISI]
Sutherland S. Delph L. F.. 1984. On the importance of male fitness in plants: patterns of fruit-set. Ecology 65: 1093-1104.[CrossRef][ISI]
Thomson J. D.. 2001. How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system. Oecologia 126: 386-394.[CrossRef][ISI]
Torres C. Eynard M. C. Aizen M. A. Galetto L.. 2002. Selective fruit maturation and seedling performance in Acacia caven (Fabaceae). International Journal of Plant Sciences 163: 809-813.[CrossRef]
Torres C. Galetto L.. 1999. Factors constraining fruit set in Mandevilla pentlandiana (Apocynaceae). Biological Journal of the Linnean Society 29: 187-205.
Valladares F. Balaguer L. Martínez-Ferri E. Pérez-Corona E. Manrique E.. 2002. Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems?. New Phytologist 156: 457-467.[CrossRef][ISI]
Vaughton G.. 1991. Variation between years in pollen and nutrient limitation of fruit-set in Banksia spinulosa. Journal of Ecology 79: 389-400.[CrossRef]
Vesprini J. L. Galetto L.. 2000. The reproductive biology of Jaborosa integrifolia (Solanaceae): why are its fruits so rare?. Plant Systematics and Evolution 225: 15-28.[CrossRef][ISI]
Vogel S.. 1990. The role of scent glands in pollination. On the structure and function of osmophores Smithsonian Institution Libraries and the National Science Foundation, Washington, D.C., USA.
Waser N. M. Chittka L. Price M. V. Williams N. M. Ollerton J.. 1996. Generalization in pollination systems, and why it matters. Ecology 77: 1043-160.[CrossRef]
Willson M. F. Rathcke B. J.. 1974. Adaptive design of the floral display in Asclepias syriaca L. American Midland Naturalist 92: 47-57.[CrossRef][ISI]
Winsor J. A. Peretz S. Stephenson A. G.. 2000. Pollen competition in a natural population of Cucurbita foetidissima (Cucurbitaceae). American Journal of Botany 87: 527-532.
Wolda H. Sabrosky C. W.. 1986. Insect visitors to two forms of Aristolochia pilosa in Las Cumbres, Panama. Biotropica 18: 295-299.[CrossRef][ISI]
Zhang L. Barrett S. C. H. Gao J. Chen J. Cole W.W. Liu Y. Bai Z. Li Q.. 2005. Predicting mating patterns from pollination syndromes: the case of "sapromyophily" in Tacca chantrieri (Taccaceae). American Journal of Botany 92: 517-524.
Zimmerman M. Pyke G. H.. 1998. Reproduction in Polemonium: assessing the factors limiting seed set. American Naturalist 131: 723-738.[CrossRef]
This article has been cited by other articles:
|
|
 |
|
  A. V. Etcheverry, M. M. Aleman, and T. F. Fleming Flower Morphology, Pollination Biology and Mating System of the Complex Flower of Vigna caracalla (Fabaceae: Papilionoideae) Ann. Bot., June 28, 2008; (2008) mcn106v1. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
