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Reproductive Biology |
Middlebury College, Biology Department, Middlebury, Vermont 05753 USA
Received for publication March 23, 2001. Accepted for publication October 2, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Autographa californica • Caryophyllaceae • Hadena variolata • Hyles gallii • Leucania multilinea • moth pollination • nocturnal pollination • Silene alba • Silene latifolia
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Pellmyr and Thompson, 1996
; Waser et al., 1996
). Two major factors determine the effectiveness of each species of pollinator: their relative abundance among the pollinator "pool" and the efficiency with which they remove and deposit pollen. When relative abundance and pollen transfer efficiency vary temporally, selection will favor generalization in the plant–pollinator mutualism. Only when the most abundant pollinator is also the most efficient will selection favor specialization (Waser et al., 1996
). Variation among visitors in pollination efficiency is therefore a precondition for the evolution of specialization (Schemske and Horvitz, 1984
).
Flowers open for >12 h are exposed to potential visitation by a variety of diurnal and nocturnal pollinators (Cruden, 1973
; Bertin and Willson, 1980
; Haber and Frankie, 1982
; Jennersten, 1988
; Jennersten and Morse, 1991
; Guitian, Guitan, and Navarro, 1993
; Shykoff and Bucheli, 1995
; Miyake and Yahara, 1998
; Arizaga et al., 2000
; Slauson, 2000
). These studies showed that diurnal bees, by virtue of their high abundance and visitation rate, contributed more to seed production than the rarer, but more efficient (on a per-visit basis) nocturnal moths (Table 1). Therefore, some "moth-pollinated" or "bat-pollinated" plants may also be pollinated by bees (Cruden, 1973
; Baum, 1995
; Fleming and Holland, 1998
; Miyake and Yahara, 1998
; Groman and Pellmyr, 1999
; Arizaga et al., 2000
; Slauson, 2000
) or hummingbirds (Willmott and Burquez, 1996
). At issue, then, is the relative role of different pollinators in plant reproductive success and whether pollination syndromes truly reflect the morphology, behavior, and dietary requirements of the most effective pollinator.
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). In fact, based solely on floral morphology and phenology, Witt et al. (1999)
state that S. alba is "a nocturnal species that strictly excludes day-active flower visitors" (p. 334). Yet, previous studies of insect visitors to Silene alba reveal that flowers are visited both at night and during the day (Real, Marschall, and Roche, 1992
; Roche, 1993
; Shykoff and Bucheli, 1995
; Altizer, Thrall, and Antonovics, 1998
). These studies were performed at the Mt. Lake Biological Station in Virginia, USA, and were concerned with the role of different insects in the spread of the smut fungus Microbotryum violacea (Pers.) Deml. & Oberw. (= Ustilago violcaea Pers.). As such, they did not examine the role of diurnal and nocturnal insects in plant reproductive success. What role does visitation by diurnal insects play in the pollination and reproductive biology of this species?
Pollination success can be measured by two factors: female reproductive success (number of pollen grains deposited on stigmas, ovule fertilization, seed production) and male reproductive success (pollen removal, pollen movement distances, success of pollen on the stigmas of conspecifics). These may be coupled such that pollinators deposit a high proportion of the pollen they remove (Conner, Davis, and Rush, 1995
), or they may be uncoupled resulting in visitors that remove large quantities of pollen but deposit very little pollen on conspecific stigmas (the Apis visiting jewelweed in Wilson and Thomson, 1991
). The fact that not all pollen removed is deposited on conspecific stigmas and that different pollinator taxa differ in the proportion of pollen they remove that they deposit on stigmas led Miyake and Yahara (1999)
to model how the timing of anthesis (flower opening) influences pollen removal and deposition. They used their data from Lonicera japonica (Miyake and Yahara, 1998
) to predict that nocturnal anthesis will be favored when the nocturnal pollinator removes less pollen, but is more efficient in the transfer of pollen than the diurnal pollinator. Thus, nocturnal anthesis may be favored, not because nocturnal pollinators are more efficient at fertilizing ovules, but because they waste less pollen in the transfer of pollen.
In this study, I sought to: (1) examine the relative effectiveness of diurnal (bees, flies, wasps) and nocturnal (moths) insects to female reproductive success of a species with flowers indicative of nocturnal pollination (S. alba); and (2) examine the distances that pollen is transported (through dye analogs) by diurnal and nocturnal pollinators.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). It has since spread westward and northward, to the midwest and western United States (Reed and Hughs, 1970
) and Canada (McNeill, 1977
). Its showy white flowers open in the evening. In Europe, it is pollinated by sphingid and noctuid moths (Brantjes, 1978
). One of the noctuids in The Netherlands, Hadena bicruris, oviposits in the ovaries as well as pollinates the flowers (Brantjes, 1978
). In Europe and southeastern North America, individuals are infected with a smut fungus [Microbotryum violacea (Pers) Deml. & Oberw. (= Ustilago violcaea Pers.)]. I saw no evidence of infection on any plants in Colorado, USA. The small seeds of S. alba are dispersed by gravity (and to a lesser extent wind; Baker, 1947
). The mature dry capsule splits open at the apex and seeds disperse when the plant is disturbed or when the capsule tips over as the plant senesces. I have measured seed dispersal distances in the field and found mean dispersal distance to be 40 cm. McCauley (1997)
found that gene flow via pollen was greater than gene flow via seeds.
Sexual dimorphism in flower size and open flower number of this species have been extensively and specifically covered in the literature (see Meagher, 1992
, and papers cited therein). The females flowers of S. alba are larger than the male flowers (Alexander and Maltby, 1990
; personal observation), but male plants have more flowers open at a given time than females (Shykoff and Bucheli, 1995
). The white flowers open in the early evening and remain open into the following day. Under cool and humid conditions, they will remain open for several days. In July in Colorado, the air is hot and dry, and flowers of both sexes tend to wilt by late morning but reopen in the evening. In Virginia, Shykoff, Bucheli, and Kaltz (1996)
found that male flowers are open for 1–2 d (mean ± 1 SE = 1.5 ± 0.05 d), and female flowers wilt soon after ovule fertilization (Roche, 1993
; Shykoff, Bucheli, and Kaltz, 1996
; personal observation). In the greenhouse, female flowers are open from 4 to 7 d (Primack, 1985
). It is important to recognize that flowers at this study site are open during the day for at least 5 h before they wilt in the midday sun and are thus potentially visited by diurnal insects.
This study was conducted in a mid-elevation (2367 m) meadow near Golden, Colorado (Jefferson County) (43'9'' N, 105'15'' W). Experiments were conducted in July and August of 1994 and 1995.
Pollinators
The nocturnal visitors of S. alba in Colorado are moths: Hyles gallii Rottenburg (galium sphinx moth, Sphingidae), Autographa californica Speyer (looper moth, Noctuidae), Leucania multilinea Walker (Noctuidae), and Hadena variolata Smith (Noctuidae). None of these species had been identified as visitors to Silene previously, although Autographa precationis and Hyles lineata pollinate S. alba in Virginia (Altizer, Thrall, and Antonovics, 1998
), and Hadena bicruris pollinates and oviposits on S. alba in Europe (Brantjes, 1978
). Autographa gamma pollinates Silene vulgaris (Pettersson, 1991a
) and three species of Hadena pollinate S. vulgaris on the Baltic Island of Oland off Sweden (Pettersson, 1991b
). The diurnal visitors to S. alba in Colorado are bees (Bombus spp., Apis mellifera, and small andrenids), flies (syrphids), and wasps.
Moths visit flowers of S. alba starting at dusk (
1915), with visible visitation peaking between 2040 and 2100. Moths continue to visit flowers after 2120 but can't be seen clearly to follow their movements. Moths were never seen during the morning hours (0500 to 0700) or before dusk. Conversely, bees, wasps, and flies were observed foraging at 0700 at the earliest and 1700 at the latest. Therefore, the temporal distribution of diurnal and nocturnal floral visitors was clearly disjunct.
Pollinator effectiveness
To test for the presence and effectiveness of diurnal and nocturnal pollinators, I bagged entire branches of female plants with netting made of bridal veil (seven holes per centimeter) in July 1994. Within each female plant (N = 17), there were four bagging treatments:
(1) To examine the effect of diurnal pollinators, I placed bags on branches every evening at dusk and removed them the next morning at dawn, repeating this process until all the flowers on those branches had completed flowering (N = 22 flowers).
(2) I performed the opposite bagging experiment to test for nocturnal pollination: bagging branches every morning and removing bags in the evening (N = 43 flowers).
(3) To determine if small insects (smaller than the holes in the netting) or wind were pollinating S. alba, I bagged some flowers both day and night (N = 10 flowers).
(4) Lastly, some flowers were never bagged to detect natural levels of seed production when flowers are exposed to both diurnal and nocturnal pollinators (N = 28 flowers).
One plant received only one bagging treatment, but the remaining 16 plants had at least two bagging treatments represented among their flowers. Bags were placed on branches and removed at dusk and dawn. Before manipulating bags, I made certain that the "wrong" pollinators were not active (at dusk, I waited until I saw no bees foraging before removing bags from the nocturnal treatment and placing bags on the diurnal treatment and vice versa at dawn).
Female flowers were marked individually (with numbered jeweler's tags on the pedicels), and floral longevity was measured as the number of hours between initial flower opening and flower senescence. Since I censused flowers at dawn (0600) and dusk (1900), floral longevity was grouped into classes of 12-h intervals. Flowers were deemed senescent when the petals wilted; since censusing occurred at dawn and dusk, when air temperatures were relatively low, flowers that had wilted petals at those times were considered senescent. Flowers thus classified never reopened.
Mature fruits were collected 30 d after pollination. All of the flowers in the pollinator effectiveness study set fruit, so I used seed set as an estimate of female reproductive success. Care was taken to collect the fruits before they opened, thereby preventing seed loss. Seeds were counted and weighed (en masse) for each fruit. Variation in seed number per fruit, seed mass per fruit, and floral longevity were partitioned into the plant effect (randomized block), the treatment effect (fixed block), and the interaction between plant and treatment.
Pollen dispersal
I delineated four sites on a hillside, ranging from 18 to 95 m apart (mean = 47 m). Beginning on 15 July 1995, I applied fluorescent dye (Radiant Color, Richmond, California, USA) to the anthers of three flowers on each of four male plants at each site, using a different color dye on each male. These male plants were in close proximity to one another (usually their nearest male neighbors) in the center of the population. Dye was applied using a toothpick and care was taken to dust only the anthers with dye. Dye was applied to anthers at dawn and dusk. I checked the donor flowers twice daily (dawn and dusk) from 15 to 31 July. As dyed flowers wilted (12–36 h after anthers were dusted), I dusted another flower on the same plant with the same color dye so that three flowers served as dye donors for each of four dye colors on each day and night.
Each day at dawn (to detect movement of dye caused by moths) and dusk (to detect movement of dyes caused by bees), female and male flowers were examined in each population for the presence of dye. A hand-held uv light was used to detect fluorescent dye on recipient flowers. When a dyed flower was found, the distance between it and the source plant of the same color dye was measured. Flowers were examined up to 10 m from the dyed plants. Many insects moved among flowers of the marked plants and these were included in the 0-cm movement class. Obviously, individuals of S. alba cannot self-fertilize (they are dioecious); pollen moving exclusively among the flowers of male plants is wasted.
To determine whether insects were moving to the nearest neighbor of each marked plant, I measured the distance to the nearest six plants of each of the four central plants and recorded their sex and the number of open flowers at three of the sites (Site 1 had ceased flowering when these measurements were made).
To detect whether pollinators were choosing flowers on the basis of corolla size, on two days I measured the corolla width of flowers receiving dye (both male and female; N = 45). Nearby, unvisited (receiving no fluorescent dye), but randomly chosen flowers of the same sex as the visited flowers were measured for comparison (N = 45). Therefore, the visited flower data set had the same sex ratio as the unvisited flower data set.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and they are small enough to enter the pollination bags. There was no significant difference in seed number of flowers always bagged and flowers bagged at night, suggesting that the larger diurnal visitors (bees, wasps, and flies) contribute little to seed production.
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; Shykoff, Bucheli, and Kaltz, 1996
; personal observation). These results suggest that flowers visited only by moths were saturated with pollen earlier than flowers visited only by bees.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Bertin and Willson, 1980
; Haber and Frankie, 1982
; Jennersten, 1988
; Jennersten and Morse, 1991
; Guitian, Guitian, and Navarro, 1993
; Miyake and Yahara, 1998
). An exception to this pattern is Manfreda virginica (Agavaceae) in which diurnal visitation is greater than nocturnal, but nocturnal visitation results in greater seed production (Groman and Pellmyr, 1999
). In this species, the per-visit effectiveness of the moths must be particularly high. At this point, I do not know the per-visit effectiveness or insect visitation rates in this system, but I have shown that overall pollinator effectiveness (seed set and pollen dispersal) is greater for nocturnal visitors than for diurnal visitors.
Data on the relative visitation frequencies of diurnal and nocturnal visitors to S. alba in Virginia are conflicting. Shykoff and Bucheli (1995)
, through the analysis of fluorescent dye movement, conclude that nocturnal visitation (by noctuid, sphingid, and geometrid moths) is much higher than diurnal (bumble and honey bees, syrphid flies and andrenid bees) visitation. In contrast, by videotaping visitors, Altizer, Thrall, and Antonovics (1998)
found that diurnal visitation was greater than nocturnal visitation. Both of these studies found that nocturnal pollinators showed a significant preference for male flowers.
One possible explanation for the lower seed set of flowers exposed to diurnal pollinators is a detrimental effect of stigma aging on pollen germination or pollen tube growth. Flowers of S. alba open in the evening, so they are at least 12-h old before diurnal insects visit them. Do 12-h-old stigmas inhibit pollen features that would lead to fertilization, relative to younger stigmas? A controlled greenhouse study on S. alba showed that stigma age at pollination (up to 120 h) did not affect seed production (Young and Gravitz, in press). So, the reduction in seed production caused by diurnal insects is a property of the quantity or quality of pollen they deposit, not the age of the stigma.
Shykoff and Bucheli (1995)
found that female flowers produced less concentrated nectar than males, but do not differ from males in nectar quantity; therefore females produce less sugar than males. They also found that nocturnal pollinators preferred male flowers. Brantjes (1978)
found that Hadena bicruris, a noctuid moth that both pollinates and oviposits in the flowers of S. alba in Europe, uses petal odor to distinguish between the sexes of the flowers, choosing female flowers to oviposit in. These same olfactory cues could be used by moths in Virginia to detect the male flowers for visitation to extract nectar. However, in my study, moths visited flowers randomly with respect to flower sex. This could be explained by the equal nectar production of male and female flowers (Shykoff and Bucheli, 1995
).
Overall, nocturnal moths are more effective pollinators than diurnal bees: visitation by moths results in greater seed production and greater pollen (dye) movement. Moths visit flowers randomly with respect to sex, facilitating greater transfer of pollen from male flowers to female flowers than bees, which visited only male flowers. All visits by diurnal insects were to collect nectar, not pollen (personal observation), so the male flower to male flower visitation pattern of these insects cannot be explained by their preferring male flowers because of their pollen. It is important to acknowledge that pollinator communities of a particular plant species and the relative importance of different members of those communities may vary both temporally and spatially (Herrera, 1988
; Fenster and Dudash, 2001
; Potts, Dafni, and Ne'eman, 2001
). In studying the relative effectiveness of diurnal and nocturnal pollinators of S. alba in only one year, it is not known to what extent their abundance and/or effectiveness vary either over time or among sites.
Pollen moves farther than seeds
Moths visiting S. alba carry fluorescent dye an average of 1.3 m between male and female flowers. This is twice the distance to the nearest female flower. Lepidoptera (butterflies and moths) can carry pollen for extensive periods of time (Courtney, Hill, and Westerman, 1982
) and great distances between consecutive flower visits (Schmitt, 1980
; Nilsson, Rabakonandrianina, and Pettersson, 1992
). Hawk moths carry large pollen loads (Kislev, Kraviz, and Lorch, 1972
), and they cover long distances rapidly (Haber and Frankie, 1982
).
The validity of estimating pollen movement using fluorescent dye has been examined extensively. Thomson et al. (1986)
found that fluorescent dye moved an average of 1.43 times farther than pollen in a system of bumble bee pollination. This is because particles of fluorescent dye are smaller than pollen grains and tend to be removed and deposited in greater numbers than pollen. In contrast, in a hummingbird-pollinated system (Ipomopsis aggregata), Campbell (1991)
compared fluorescent dye movement with actual paternity and found that dye movement resulted in a more restricted prediction of gene movement than actually occurred (mostly due to post-pollination effects such as abortion of fruits resulting from inbreeding). In addition, pollen flow measured by movement of dyes varied tremendously among populations of I. aggregata and among years (Campbell and Waser, 1989
). A similar analysis has not been done for moth-pollinated species, but the results of Thomson and Campbell would suggest that, on average, pollen movement in S. alba is between 85 (121 cm distance I observed divided by 1.43) and 121 cm. Both of these distances are substantially greater than the mean distance I observed seeds dispersing (40 cm; unpublished data). This supports McCauley's (1997)
finding, through the analysis of chloroplast DNA and nuclear DNA spatial patterns, that pollen dispersal is greater than seed dispersal in S. alba. In fact, he states that "the movement of pollinators results in effectively random mating among individuals separated by a few tens of meters" in S. alba (McCauley, 1997
, p. 261). When they isolated female plants of S. alba 10, 20, 40, 80, 160, 320, and 640 m from males, Richards, Church, and McCauley (1999)
found that 47% of the seeds produced were sired by males 20 m away and 6% from males 80 m away. Over 85% of pollinations occurred within the first 40 m from the pollen source. They suggest that this long-distance pollen flow is due to the strong flying of nocturnal sphingid moths. In a dense field of S. alba, this relatively long-distance pollen movement will result in very large genetic neighborhoods, despite the fact that seeds do not disperse far.
Pollen transfer
In studying Silene vulgaris, Pettersson (1991a)
found that only 10% of moths (noctuids and hawk moths) deposit enough pollen in one visit to set full seed (
150 pollen grains), indicating that full seed set usually results from multiple visits. This relative of S. alba has fewer ovules and seeds than S. alba: 165 ovules and setting 55 seeds (Pettersson, 1991a
). Fruits of S. alba have a maximum of 570 seeds (personal observation), suggesting that many more than 150 pollen grains are necessary for full seed set. Hawk moths in Jerusalem carry an average of slightly more than 400 pollen grains of either Silene longipetala or S. vulgaris on their probosci (Kislev, Kraviz, and Lorch, 1972
), with a range of 0–2500 pollen grains. I did not measure pollen deposition by moths in S. alba, but if I use the data from Pettersson (1991a)
, at least 3.8 moth visits are necessary, on average, to deposit enough pollen to fertilize all ovules (if all pollen deposited germinates and fertilizes ovules); an average of two visits would be required to set full seed if I use Kislev, Kraviz, and Lorch's data, with some moths carrying enough pollen to fertilize all ovules. All of the experimental flowers in my study set fruit, suggesting that many or all of these flowers were visited repeatedly, a process that would lead to multiple paternity within fruits. Multiple paternity was found to be common in S. alba in Spain (J. Wilcox Wright, University of California, Davis, personal communication), but rare in Virginia (D. McCauley, Vanderbilt University, personal communication).
Timing of anthesis and nectar production
Miyake and Yahara (1999)
suggest that moths are more efficient with the pollen they remove (a greater proportion is deposited on conspecific stigmas than the pollen that diurnal visitors, especially bees, remove). Indeed, they find that most of the pollen deposition on the stigmas of Lonicera japonica occurs at night by moths, yet most of the pollen removal from anthers occurs during the day by bees (Miyake and Yahara, 1998
). This is due, in part, to the behavior of some bees of collecting pollen and storing pollen in corbiculae on their hind legs, thereby removing that pollen from the system. Moths are visiting flowers solely for nectar; any pollen they pick up is incidental and a greater proportion remains "in the system." Under these conditions, selection will favor the nocturnal anthesis of flowers (Miyake and Yahara, 1999
). Cruden (1973)
found that the pollen : ovule ratio of Lychnis alba (= S. alba) is 600 : 1, a relatively low value relative to other insect-pollinated species. He suggests that the flowers close during the day to protect pollen from foraging bees. This supports Miyake and Yahara's (1999)
ideas about nocturnal anthesis: that it evolved in systems where diurnal visitors "waste" pollen (the "ugly" pollinators of Thomson and Thomson, 1992
).
The timing of nectar production in S. alba is what one would expect from a nocturnally pollinated plant: peak nectar production occurs in the evening for both male and female plants (Witt et al., 1999
). Although some nectar is produced at other times of the day (usually <0.5 µL), production increased between 1600 and 2200 (up to 2.5 µL) (Witt et al., 1999
). Therefore, S. alba appears to have evolved phenological and nectar production patterns that maximize visitation by its most effective pollinators, nocturnal moths.
General conclusion
When more than one taxa of pollinator visit the flowers of a plant species, selection may be acting on the morphological, chemical, or phenological features of the flowers that increase visitation by the most effective of the pollinators. This selection has been so strong and consistent for each pollinator taxa that pollinator syndromes exist: there is a discrete set of traits that characterize the flowers pollinated by a specific pollinator. It is misleading, however, to think that pollination "syndromes" are completely predictive as to who the visitors to the flower are (for instance, "bat flowers" may be visited by a variety of nocturnal and diurnal insects, Baum, 1995
; Slauson, 2000
) or who the most effective pollinators are. Documenting the effect of each visitor on the pollination success of a plant is important in revealing current selection pressures on the plant species, rather than relying on the syndrome characteristics that are reflective more of the selective forces in the past. This study has demonstrated that a relative newcomer to North America has maintained the pollination biology that it has in its native Europe. Silene alba is visited by a variety of diurnal insects, but they appear to play little role in the reproductive biology of this species.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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