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(American Journal of Botany. 2008;95:1652-1659.) doi: 10.3732/ajb.0800118 © 2008 Botanical Society of America, Inc. |
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Brief Communication |
2 San Francisco State University, 1600 Holloway Avenue, San Francisco, California 94132 USA 3 University of South Carolina, Coker Life Sciences Building, Columbia, South Carolina 29205 USA
Received for publication 18 July 2007. Accepted for publication 8 August 2008.
ABSTRACT
Floral reproductive morphology and scent are of primary importance to pollinators in guiding foraging decisions. We compared the floral scent and reproductive morphology between two subspecies of Linanthus dichotomus (Polemoniaceae) that are taxonomically distinguished by geography and flowering time: the vespertine L. dichotomus subsp. dichotomus and the diurnal L. dichotomus subsp. meridianus. Disparity in flowering time between the two subspecies is accompanied by differences in flower visitors. We collected floral volatiles using dynamic headspace methods and analyzed them using gas chromatography and mass spectroscopy. Together, the subspecies produced a total of 39 floral scent compounds. Subspecies differ in the quantitative pattern of volatiles that attract noctuid moths (e.g., lilac aldehydes) vs. a more general suite of visitors (e.g., phenylacetaldehyde), but not in overall scent emission rates. A discriminant function analysis correctly distinguished between the two subspecies based on scent samples 86% of the time. We measured seven reproductive morphological traits; a discriminant function analysis distinguished between the two subspecies based on morphological samples 81% of the time. We found significant differences between subspecies in scent but not in individual morphological traits. The evidence presented here is most consistent with a hypothesis of pollinator-mediated selection.
Key Words: floral odor • generalized pollination • lilac compounds • Linanthus dichotomus • noctuid moths • Polemoniaceae • principal component analysis
The diurnal pattern of flower petal closure has been proposed to influence pollinator visitation, water balance, and florivory (Stebbins, 1970
; Stone et al., 1998; Galen et al., 1999; McCall and Irwin, 2006). While much research has focused on the mechanics of flower petal movement, less is known about the ecological consequences of this aspect of floral anthesis. If the timing of flower closure restricts or "filters" the pollinator community, there is the potential for pollinator foraging preferences to drive the divergence of other floral traits (Armbruster and McCormick, 1990). Verne Grant (1949) was among the first to formally suggest that pollinator-mediated selection, as a result of its effects on reproductive characters, ultimately could lead to diversification and speciation through reproductive isolation. The potential for pollinator-mediated selection has almost exclusively been investigated with respect to visual or architectural aspects of floral phenotype (i.e., color, depth, or shape). However, flower morphology is only part of the story because pollinator attraction and visitation behavior often are driven, at least in part, by dynamic patterns in floral scent emission (Raguso, 2004). To date, relatively few studies of pollinator-mediated selection have included chemical analyses of potential variation in floral scent (Salzmann et al., 2007).
Floral scent is an important attractant for many insect and mammal pollinators (Dobson, 2006). Olfactory cues are especially important in plants with crepuscular or nocturnal flowering because the lack of daylight causes pollinators to rely more heavily on nonvisual cues, either as primary attractants or as synergists for visual stimuli (Baker, 1961; Raguso and Willis, 2002). The strong, sweet fragrances of moth-pollinated flowers are characterized by specific classes of volatile compounds commonly used in perfumery (Knudsen and Tollsten, 1993). Acyclic terpene alcohols and their corresponding hydrocarbons, esters formed from aromatic alcohols, salicylic and benzoic acid, and nitrogenous aldoximes and indole are common to moth-pollinated flowers (Kaiser, 1993; Raguso et al., 2003a, b). Hence, some scent compounds are correlated with particular suites of pollinators, suggesting that the latter have served as selective agents in the evolution of floral scent composition (Dobson, 2006; Knudsen et al., 2006).
Linanthus dichotomus Benth. (Polemoniaceae) presents an excellent opportunity to study the effects of variation in floral anthesis on the potential for pollinator-mediated selection on floral traits, including scent. Alice Eastwood (1945) distinguished the two subspecies of L. dichotomus by flowering time and geographic distribution. The flowers open and close daily; although the subspecies differ in their times of anthesis, flowers of both subspecies close at dawn. Linanthus dichotomus subsp. meridianus (Eastw.) H. Mason has flowers that open during the day and remain open throughout the night, whereas L. dichotomus subsp. dichotomus has flowers that open at sunset and remain open through the night. The vespertine anthesis (evening flowering) of L. dichotomus subsp. dichotomus flowers is typical of moth-pollinated plants and should effectively restrict floral visitation to nocturnal insects. In contrast, the flowers of L. dichotomus subsp. meridianus should be available to a broader spectrum of insect visitors because they are open during parts of the day. In the parlance of community ecologists studying pollinator networks (e.g., Jordano et al., 2006), flower closure constitutes a mechanical barrier or "floral filter" resulting in more specialized flower-pollinator webs. The temporal disparity of flower closure in L. dichotomus and the resulting filter on visitors provides an exceptional system in which to study local adaptation.
To investigate the effect of variation in floral anthesis on the floral biology of two subspecies of Linanthus dichotomus, we analyzed floral reproductive characters including scent composition and reproductive morphology, and we observed the insect communities that visit each subspecies. We found clear differences in floral scent chemistry and reproductive morphology between the two subspecies of Linanthus dichotomus, suggesting the potential for pollinator-mediated selection across the geographic distribution of this species.
MATERIALS AND METHODS
Study species
Linanthus dichotomus (Polemoniaceae) Benth. occupies open, dry areas in Arizona, Nevada, and California below 1700 m a.s.l. Linanthus dichotomus flowers have radial symmetry, with all floral parts of each tissue type being isomorphic (e.g., all anthers are equal in length). This annual herb flowers from March through May and sets seed from May through July. The stigma is always inferior to the anthers, and both are enclosed within the corolla tube. Located north of the San Francisco Bay, the flowers of L. dichotomus subsp. meridianus open during the day, typically by noon, and close the next morning. In contrast, L. dichotomus subsp. dichotomus is vespertine in flowering habit: flowers open in the evening and close the next morning. Individual flowers can persist for more than 30 d (Chess, 2005), but flower opening and closure occur each day. Several lines of evidence suggest that the diurnal condition is derived. First, Linanthus dichotomus is derived in its section (Bell and Patterson, 2000), and L. dichotomus subsp. meridianus is the only taxon in Linanthus sect. Linanthus known to bloom diurnally (Patterson, 1996). Furthermore, Linanthus dichotomus is the only taxon known to occur outside the mountains of the southwestern United States and northern Mexico. Also, the narrow range of L. dichotomus subsp. meridianus (a subset of counties in northern California) compared to the much wider distribution of L. dichotomus subsp. dichotomus (in parts of three states in the USA) is consistent with the hypothesis that this subspecies and its diurnal anthesis represent a derived condition in the genus Linanthus.
Study sites
We located 10 populations of Linanthus dichotomus around the San Francisco Bay area: five populations of subspecies meridianus to the north and five populations of subspecies dichotomus to the south (Fig. 1). We collected seed from 30 to 40 plants from nine of the 10 populations in May 2002, and bulk seed from the 10th population (Jolon) in July 2001. We grew plants in a mix of 50% Ultra Potting Mix, 25% Fine Sand (American Soil Products, Richmond, California, USA), and 25% Turface MVP (Profile Products, Buffalo Grove, Illinois, USA) in the San Francisco State University greenhouse.
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). Therefore, it was not possible to assess insect visitation using quantitative methods common to other pollination studies. However, the sexual organs of L. dichotomus are contained almost entirely within the plant’s narrow floral tubes, making it likely that insects with a long proboscis will transfer some pollen (Haber, 1984). Some visitors were identified on the wing; we netted unfamiliar insects for later identification. An infrared spotlight-equipped Digital Handycam (Model DCR-TRV330, Sony, Tokyo, Japan) was used to document visitation after dark. All observations and recordings were made during April-May 2003.
Floral scent sampling and chemical analysis
To determine if there are differences in scent between the two subspecies, we collected samples from intact flowers from six to 10 plants from each of the 10 populations grown in the greenhouse. Each sample plant represented a different maternal line. This common greenhouse design was intended to standardize the environmental influences on population-specific floral traits. To standardize for the effects of flower age on scent production, we sampled only flowers that were 1 day old; analysis of preliminary scent collections showed this to be the peak time of scent production. Preliminary sampling also showed that both subspecies maximize scent production at night (indeed, L. dichotomus subsp. dichotomus only produces scent at night, when its flowers are open). To make a direct comparison of the floral scent of the two subspecies, we collected scent samples for three hour intervals between 6 pm and midnight. We also collected scent samples during the day in three L. dichotomus subsp. meridianus populations: Robert Louis Stevenson, Middletown, and Detert. Details on volatile collections and chemical analysis methods can be found in Appendix S1 (see Supplemental Data with the online version of this article).
Analysis of scent variation
We used principal component analysis (PCA) to explore quantitative variation in the emissions (in ng) of various scent compounds released by flowers of the 10 study populations. To reduce scent profiles to the smallest number of independent variables, we performed PCA with varimax rotation on 35 of the identified scent compounds; four compounds were omitted from the PCA because they were absent from more than half of the populations. In these cases, the four omitted compounds were present in less than 10% of samples; some of these four compounds were present in both subspecies, and some in only one. To include these rare compounds might result in more obvious differences in the ordination of L. dichotomus subspecies, but would violate the assumptions of the PCA model (Tabachnick and Fidell, 2001). A discriminant function analysis (DFA) was performed on the resulting factors to determine if there were differences in the nocturnal floral scent between L. dichotomus subsp. meridianus and L. dichotomus subsp. dichotomus. Only factors with eigenvalues greater than unity were retained.
We also considered the alternative hypothesis that total scent emission rates, rather than composition of specific volatile compounds, might differ between subspecies and/or populations. Standardized emission rates (ng scent•g flower-1•h-1) of log-transformed (y = ln(x +1)) floral scent data were compared between populations using one-way ANOVA and between subspecies using an unpaired t test on pooled data. These analyses provided two-tailed tests of the null hypothesis of no significant differences in odor strength between populations or between subspecies of L. dichotomus, respectively. All statistical analyses were done with the program SPSS 12.0 (SPSS, Chicago, Illinois, USA).
Reproductive morphology
We took morphological measurements from the first flower on each of 8–15 plants from each of the 10 populations of Linanthus dichotomus grown in a common greenhouse environment at San Francisco State University. Each sample plant represented a different maternal line. We measured (in mm) (a) corolla depth, the distance between the base of the receptacle and the corolla tube aperture; (b) functional corolla depth, the distance from the corolla tube aperture to the top of a nectary; (c) stigma–anther separation; (d) corolla lobe length, the distance between the corolla tube aperture and the outer edge of a corolla lobe; (e) width of the corolla tube aperture; (f) corolla tube aperture depth, the distance from the corolla aperture to the tops of the anthers in the corolla tube; (g) nectary pad height (Fig. 2). A discriminant function analysis (DFA) of these seven traits determined whether the reproductive morphology of the two subspecies differed.
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Insect visitors
During 37 h of direct observation, Apis mellifera L. (honeybee), Bombus melanopygus Nylander (bumblebee), an assortment of hoverflies (Syrphidae: Euphodes sp., Scaeva pyrastri L., and Syrphus opinator Osten Sacken), Bombylius major L. (beefly), Proserpinus clarkiae Boisduval (Clark’s sphinx moth), and Coenonympha tullia Mueller (common ringlet butterfly) visited flowers of L. dichotomus subsp. meridianus during the day (Table 1). The diversity of visitors was balanced by the infrequency of their visits. For example, as seen in Table 1, no visitors were observed during 6 h of daytime monitoring at the Middletown population. As expected, only moths were observed to visit flowers of L. dichotomus subsp. dichotomus (Table 1). Thirty-nine hours of night videotaping revealed floral visitation by unidentified noctuid moths to both subspecies of L. dichotomus.
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). The scent blends are dominated by the monoterpene trans-β-ocimene, the aromatic aldehydes benzaldehyde and phenylacetaldehyde, the aromatic ester benzyl acetate, and lilac aldehydes derived from S-linalool (Kreck et al., 2003; Dötterl et al., 2006b). We also found small quantities of other compounds in the same chemical classes as well as aromatic alcohols, nitrogenous compounds, irregular terpenoids, one sesquiterpene hydrocarbon, and several methoxy-substituted aromatic compounds (e.g., 1,2-dimethoxybenzene and 2-methoxyphenol) and structurally related phenolic compounds (e.g., m-cresol). We also analyzed odors produced during the day in three L. dichotomus subsp. meridianus populations. The daytime scent compounds identified included most of the scents produced during the night (except for aromatic ethers and nitrogenous compounds), but emission rates were substantially reduced compared to nocturnal floral scent (online Appendix S2). There are several differences in the nighttime and daytime floral scent samples taken from Linanthus dichotomus subsp. meridianus flowers. Trans-β-ocimene comprises 8–24% of nighttime samples but never comprises even 4% of daytime samples. However, the other monoterpenes found in L. dichotomus subsp. meridianus account for up to 41% of scent emissions in daytime samples but never even 1% in nighttime samples. Benzaldehyde and phenylacetaldehyde are much more prevalent in nighttime samples (12–20% and 12–16%, respectively) than in daytime samples (less than 4% and less than 1%, respectively). Emission rates for nighttime samples of Linanthus dichotomus subsp. meridianus flowers range from 375 to 506 ng scent•g flower-1•h-1, while daytime emission rates range from 9 to 116 ng scent•g flower-1•h-1.
Subspecific variation in floral scent
The PCA reduced the 35 consistently present compounds to nine factors, accounting for 79% of the variance among populations (see Table 2; Appendix S3; see Supplemental Data with online version of this article). The DFA identified three factors for distinguishing between the subspecies based on scent (Table 3). Factor 1 consists primarily of lilac aldehydes and unknown compound 1. Factor 2 is dominated by biosynthetically related aromatic compounds, such as 2-phenylethanol, phenylacetaldehyde, benzyl alcohol, and 2-phenylethyl acetate. Factor 5 is comprised of trans-β-ocimene and the structurally related β-myrcene. Using these factors, the DFA correctly assigned 95.1% of 41 L. dichotomus subsp. meridianus samples and 76.3% of 38 L. dichotomus subsp. dichotomus samples to their respective subspecies.
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DISCUSSION
Our study confirms that the two subspecies of Linanthus dichotomus are distinguishable by floral scent composition and reproductive morphology. Our results also indicate that floral visitors to both subspecies are rare and would require many more observer hours at each population to survey thoroughly. Furthermore, the paucity of observed visits (Grant and Grant, 1965) suggests that experiments with captive insects would be necessary to rigorously evaluate the effectiveness of different visitors as pollinators, as well as the impact of poor nectar rewards on their behavior. Nevertheless, our data confirm that diurnal anthesis in L. dichotomus subsp. meridianus promotes floral visitation by bees, flies, and butterflies that are, de facto, denied entry to flowers of L. dichotomus subsp. dichotomus, which remain closed during the daytime. Assuming that nocturnal visitors to both subspecies are comparable in abundance and pollinator effectiveness, we discuss the potential for the addition of copollinators (see Aigner, 2001) to modify floral phenotype in L. dichotomus.
Subspecific variation in floral scent
In broad terms, the pollination syndrome concept suggests that flowers with particular combinations of floral traits will be pollinated by certain suites or functional classes of visitors (Faegri and van der Pijl, 1979; Fenster et al., 2004). In theory, such traits should include the chemical composition of floral scent chemistry and/or its patterns of emission, which constitute the olfactory components of floral phenotype. In this study, evolutionary shifts in visitor spectrum between subspecies of Linanthus dichotomus are associated with floral scent composition, but not with overall emission rates. The results of our DFA on floral scent are consistent with the putative expansion in insect fauna from nocturnal moths observed to visit Linanthus dichotomus subsp. dichotomus to a more generalized system including bees, flies, and butterflies for Linanthus dichotomus subsp. meridianus. Three factors distinguished the two subspecies of L. dichotomus based on floral scent chemistry (Appendix S3, see Supplemental Data with the online version of this article). Factor 1 comprises compounds generally associated with noctuid moth pollination (Knudsen and Tollsten, 1993; Jürgens et al., 2002); it loads positively for night-blooming L. dichotomus subsp. dichotomus and negatively for the day- and night-blooming L. dichotomus subsp. meridianus. Factor 1 is made up of lilac compounds, methyl salicylate, an epoxide of 4-oxo-isophorone, and one unidentified compound. Methyl salicylate is a common component of the scent bouquets of flowers pollinated by different moth families (Raguso and Pichersky, 1995; Raguso et al., 2003a). The lilac compounds are unusual in floral scents, but when present, are most often found in flowers pollinated by noctuid moths (Knudsen and Tollsten, 1993; Jürgens et al., 2002; Dobson, 2006) for which they are potent attractants (Plepys et al., 2002; Dötterl et al., 2006a, b). Although L. dichotomus subsp. meridianus has retained moths as visitors, there is a decrease in the amount of moth-specific attractants emitted. Coincident with the reduction of moth-specific attractants is an increase in scent compounds such as phenylacetaldehyde (PAA, factor 2; see Tables 2 and 3) that are known to attract honeybees and other generalized pollinators (Roy and Raguso, 1997; Theis, 2006).
Waelti et al. (2008) used similar methods in a study of closely related species of Silene (Caryophyllaceae) in Switzerland. Remarkably, they identified interspecific differences in floral scent that were largely explained by the abundance of lilac aldehydes in noctuid moth-pollinated S. latifolia and the dominance of PAA in S. dioica, pollinated by a suite of bumble bees, butterflies, and hoverflies (Waelti et al., 2008). The experimental augmentation of each species with phenylacetaldehyde in mixed arrays resulted in greater amounts of heterospecific pollen transfer from S. dioica to S. latifolia, suggesting that diurnal insects visited S. latifolia flowers more frequently when they emitted more PAA. This is precisely the pattern that we have documented for L. dichotomus subsp. meridianus.
The available evidence suggests that lilac aldehydes are important attractants of the crepuscular and nocturnal moths observed to visit L. dichotomus subsp. dichotomus. Coupled electrophysiological and behavioral studies have shown that a synthetic mixture of stereoisomers of lilac aldehydes is as attractive to Autographa gamma, a noctuid moth that pollinates European Platanthera and Silene species, as a complex mixture of scent compounds (Plepys et al., 2002). In wind tunnel bioassays with another noctuid pollinator, Hadena bicruris, Dötterl et al. (2006a) found that lilac aldehyde isomers were as attractive as the scent of a single Silene latifolia flower; 90% of tested moths were attracted to the single flower and to lilac aldehyde isomers. No other tested compound yielded comparable results in either study, providing compelling evidence that lilac aldehydes alone are potent attractants for noctuid moth pollinators.
Reproductive morphology
Our DFA of reproductive morphology in L. dichotomus correctly classified over 81% of samples, revealing morphometric differences between the subspecies. However, differences between subspecies on any individual measurement were not statistically significant. The PC loadings for these four characters had the same sign (Table 3) and differed in more subtle and less predictable ways between subspecies than did floral scent characters. Linanthus dichotomus subsp. meridianus had a greater corolla lobe length, functional corolla depth, and aperture depth, whereas L. dichotomus subsp. dichotomus had greater overall corolla depth. Corolla lobe length is one measure of floral display. Larger floral display could easily be justified for either subspecies because it might increase the attraction of primarily visually oriented diurnal visitors, or it could increase the visibility of flowers to moths under nocturnal conditions (e.g., Schemske, 1980). Alternatively, slightly greater floral diameter in L. dichotomus subsp. meridianus might reflect reduced water stress (e.g., Schemske and Bierzychudek, 2001) in cooler, mesic northern California populations.
The Robert Louis Stevenson population is the farthest south of the L. dichotomus subsp. meridianus populations in this study, placing it closest to populations of Linanthus dichotomus subsp. dichotomus. Perhaps the inability of the DFA to correctly assign to subspecies the samples from Robert Louis Stevenson reflects gene flow from an unknown or now extinct population of L. dichotomus subsp. dichotomus or the vestiges of a more continuous, clinal geographic distribution of floral anthesis and morphology. In the absence of population genetic data on the relatedness between individual populations, we have no explanation for why the Snell samples were not classified more accurately.
Evolutionary considerations and synthesis
Surveys of geographic variation in floral scent rarely measure visual/morphological traits at the same time, and observed differences among populations are as likely to reflect sampling error due to low replication or phenotypic plasticity due to abiotic influences as they are to indicate genetic differences between sites. Our sampling scheme, though modest by population genetic standards, is more robust than all but two published studies of intraspecific scent variation (Mant et al., 2005; Svensson et al., 2005) and is the only one to use a common garden design. These attributes lend greater confidence to our identification of subspecies-level differences in reproductive morphology and floral scent in Linanthus dichotomus, in addition to the differences in flower opening and closure rhythms that inspired the original description of the two subspecies.
Discriminant function analyses correctly classified to subspecies over 81% of reproductive morphological samples and over 86% of floral scent samples. Our observations suggest that this pattern may reflect differences in insect visitors between the two subspecies, but further observations and population genetic data will be required to distinguish between this and alternative hypotheses (e.g., genetic drift). The divergence of the two subspecies of L. dichotomus in floral morphology and scent chemistry cannot be due to site-specific environmental factors (e.g., soil or humidity) because we analyzed plants grown in a common greenhouse setting. In the absence of additional ecological or genetic data, the evidence presented here suggests the potential for pollinator-mediated selection.
One possible direction of evolution in this taxon is that L. dichotomus extended its ancestral range from the deserts of southern California, Nevada, and Arizona into the grassland and chaparral of northern California. It is possible that the dependability of nocturnal moths may decrease along a latitudinal gradient, due to cooler evenings at higher latitudes (Baker, 1961; Cruden et al., 1976; Miller, 1981). At the same time, the extended anthesis time of L. dichotomus subsp. meridianus into the heat of the day, as well as increased corolla size, is likely to be less detrimental in northern California than it would be in the deserts of southern California, where water stress is correlated with variation in flower pigment in other Linanthus species (Schemske and Bierzychudek, 2001, 2007).
Variations in flower morphology, combined with geographical separation, suggest that these subspecies are good candidates for incipient speciation. Despite continued interfertility (G. LeBuhn, unpublished data), their geographical isolation prevents interbreeding and allopatric speciation may occur as drift and environmental selection cause different genetic changes to accumulate in the separate gene pools (Grant, 1993). If vespertine anthesis is ancestral in this system, then there has been a shift from a specialized pollination system to a more generalized one. According to Stebbins (1970), this reversal from a specialized to a more generalized reproductive strategy is likely to be a frequent occurrence, but one that may be difficult to recognize. More recent investigations identify such a pattern in a clade of Dalechampia that putatively dispersed to Madagascar from continental Africa (Armbruster and Baldwin, 1998). Generalization is thought to be beneficial when the most abundant and/or effective pollinators are unreliable over time (Waser et al., 1996); specialization should occur when the most abundant and/or effective pollinators are consistent over time (Stebbins, 1970; Johnson and Steiner, 2000). Our study suggests that the shift to diurnal floral anthesis in Linanthus dichotomus subsp. meridianus, combined with subtle but significant shifts in floral morphology and scent chemistry, may have facilitated a transition to a more generalized pollination system.
FOOTNOTES
1 This study was supported in part by the ARCS Foundation, the California Native Plant Society, and the East Bay chapter of the California Native Plant Society. This work was performed in part at the University of California Natural Reserve System’s Donald and Sylvia McLaughlin Reserve. Scent analysis in the Raguso laboratory was supported by US National Science Foundation Grant DEB-0317217. Thanks to S. Dötterl for determination of the lilac compounds, Q. McFrederick for determination of the Bombus species, N. Evanhuis for determination of Bombylius major, and F. C. Thompson for determination of the Syrphidae. 
4 Present address: Cornell University, Corson-Mudd Building, Ithaca, New York 14853-2702 USA
5 Author for correspondence (e-mail: sallychess{at}gmail.com
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  Compiled by, F. Tooke, T. Chiurugwi, and N. Battey Flowering Newsletter bibliography for 2008 J. Exp. Bot., June 23, 2009; (2009) erp154v1. [Full Text] [PDF]
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