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Reproductive Biology |
2Swedish Museum of Natural History, Research Division, Directorate, Box 50007, SE–104 05 Stockholm, Sweden; 3Department of Botany, University of Stockholm, SE–106 91 Stockholm, Sweden; 4Swedish Museum of Natural History, Department of Cryptogamic Botany, Box 50007, SE–104 05 Stockholm, Sweden
Received for publication October 20, 2005. Accepted for publication June 16, 2006.
ABSTRACT
A fundamental assumption in life-history theory is that reproduction is costly. Higher reproductive investment for fruits than for flowers may result in larger costs of reproduction in females than in males, which is often used to explain male-skewed sex ratios in unisexual seed plants. In contrast, bryophytes have predominantly female-biased sex ratios, suggested to be a product of a higher average cost of sexual reproduction in males. Empirical evidence to support this notion is largely lacking. We investigated sex-specific reproductive effort and costs in the unisexual moss Pseudocalliergon trifarium that has a female-dominated expressed sex ratio and rarely produces sporophytes. Annual vegetative segment mass did not differ among male, female, and non-expressing individuals, indicating that there was no threshold-size for sex expression. Mean and annual mass of sexual branches were higher in females than in males, but branch number per segment did not differ between sexes. Prefertilization reproductive effort for females was significantly greater (11.2%) than for males (8.6%). No cost for sexual branch production in terms of reduced relative vegetative growth or decreased investment in reproductive structures in consecutive years was detected. A higher realized reproductive cost in males cannot explain the unbalanced sex ratio in the study species.
Key Words: Amblystegiaceae • bryophyte • prefertilization reproductive effort and costs • resource allocation • sex ratio • sexual branches • Sweden
In plants with separate sexes (dioecy), progeny sex ratio is theoretically expected to be close to unity at the end of parental investment (Fischer, 1930
; Meagher, 1981
). Sex ratio studies in plants have concentrated on phanerogams, for which unbalanced ratios are often recorded (e.g., Sutherland, 1986
; Richards, 1997
; Delph, 1999
; de Jong and Klinkenhamer, 2002
). Also in many unisexual species of the bryophyte lineages, rarity or absence of one sex is recurrently observed, both at the level of the species and at the local or regional population scale (e. g., Shaw and Gaughan, 1993
; Bisang and Hedenäs, 2005
). Skewed sex ratios can be the result of mechanisms acting at several different ontogenetic stages (e. g., Putwain and Harper, 1972
; Freeman et al., 1976
; Allen and Antos, 1993
; McLetchie, 2001
; Hardy, 2002
; Fuselier and McLetchie, 2004
; Stehlik and Barrett, 2005
). For adult individuals, a higher reproductive allocation in one sex has been suggested to result in larger costs of reproduction in terms of lower future survival, growth or reproduction, and eventually in greater rarity, of that sex (for references, see Obeso, 2002
; Ortiz et al., 2002
). Higher demands for reproductive investment in one sex may also lead to a gender-specific sex expression threshold size (e.g., Allen and Antos, 1993
; Delph, 1999
). This will result in a prevalence of the sex with the lower shoot size threshold for sex expression, provided there is no general size difference between genders.
Comparatively little interest has been placed on searching to explain sex expression patterns in haploid-dominant bryophytes, in which dioecy is more common than among seed plants (e.g., Richards, 1997
; Charlesworth, 2002
). One must note, however, that dioecy in heterosporous seed plants (sporophytic dioecy) differs from dioicy in homosporous bryophytes (gametophytic dioicy) (e.g., Wyatt, 1985
). Dioecious seed plant sporophytes give rise to either male or female gametophytes. A bryophyte sporophyte produces spores that yield female plus male or bisexual gametophytes. Nevertheless, dioecy and dioicy are functionally comparable in many respects, including those addressed in this paper, and we will henceforth use dioecy for both organism groups. More than half of all moss taxa and roughly two thirds of the liverworts worldwide have a dioecious breeding system (unisexual individuals) (Wyatt, 1982
).
Among seed plants, even and male-biased sex ratios appear to be most common (Webb and Lloyd, 1980
; Sutherland, 1986
; Rottenberg, 1998
; Delph, 1999
), while bryophytes often exhibit a female bias in expressed sex ratios (e.g., Longton and Schuster, 1983
; Bisang and Hedenäs, 2005
). In dioecious seed plants, secondary male-dominated sex ratios have been explained by females usually spending more resources on reproduction and suffering a higher demographic cost of reproduction than males (e.g., Meagher, 1981
; Allen and Antos, 1993
; Silvertown and Lovett Doust, 1993
; Obeso, 2002
). In bryophytes, significant costs for sporophyte production, such as reduced growth, lower branching frequency, and decreased sex induction have been demonstrated (Ehrlén et al., 2000
; Bisang and Ehrlén, 2002
; Rydgren and Økland, 2003
). The overall importance of such costs may, however, be small in the many species that never or only rarely produce sporophytes (Longton, 1992
; Laaka-Lindberg et al., 2000
; Rydgren and Økland, 2002
). Dependence on external water for fertilization via motile spermatozoids, gamete dispersal distances of a few decimeters (Bisang et al., 2004
), and spatial segregation of sexes may account for this rarity of sporophytes. Without successful fertilization, the cost incurred by the female function is restricted to production of sexual branches comprising archegonia. Based on this line of reasoning, Stark et al. (2000
, p. 1600) proposed that "female-dominated sex ratios in dioecious mosses may be a product of a higher average realized cost of sexual reproduction in males." Other explanations of unbalanced adult bryophyte sex ratios include sex-specific life-history characteristics and habitat specialization (Stark et al., 2000
; Fuselier and McLetchie, 2004
). However, the empirical evidence in support of these hypotheses is very limited and equivocal. At higher levels, phylogenetic history may explain differences among lineages in the degree of male and/or female sex expression (Bisang and Hedenäs, 2005
) or the general phenomenon of female dominance among dioecious bryophytes. The latter could possibly be due to genetically based differences in habitat requirements between non-expressing male and female individuals, thus to habitat specialization (Stark et al., 2000
; Fuselier and McLetchie, 2004
). The intriguing pattern of male rarity among unisexual bryophytes therefore remains still largely unexplained.
We investigated if differences in allocation to reproduction could explain a female-skewed expressed sex ratio in the moss Pseudocalliergon trifarium (Web. & Mohr) Loeske, that rarely produces sporophytes. We addressed the following questions: (1) Is there a threshold size for sex expression, and does size of sex expressing individuals differ between sexes? (2) Does allocation to reproduction prior to fertilization differ between the sexes? (3) Is there a prefertilization cost of reproduction in terms of a reduced future growth and reproduction in the two sexes?
MATERIALS AND METHODS
In most cases, sex in bryophytes is assessed on the basis of gametangia production and the formation of associated structures (but see Newton, 1971
; McLetchie and Collins, 2002
). Although non-expressing plants sometimes occur frequently, it is not clear how accurately phenotypic sex ratios reflect genetic ratios (e.g., Shaw, 2000
). In this study, we refer to females and males as individuals expressing either sex if not otherwise specified.
The study species and collection site
Pseudocalliergon trifarium is a pleurocarpous moss of the order Hypnales and occurs in Europe, Asia, North America, and in the mountains of South America (Hedenäs, 1992
, 2003
). It is relatively common in the boreal zone and occurs mainly in deep fens or in sloping fens with moving water, in mineral-rich areas with a pH between 5.6 and 7.6 (values from central and northern Europe), and often together with Scorpidium scorpioides (Hedw.) Limpr. (Hedenäs et al., 2003
). Creeping or ascending, not or sparsely branched, yellow to brownish yellow shoots of the species grow interspersed among other wetland mosses, or more rarely form dense mats (Fig. 1). In the seasonal climate of its main distribution area, the leaves formed in the beginning of the growing period are smaller and more densely arranged than toward the end of the season, giving the early season shoot portions a narrow threadlike appearance, which results in distinctly perceivable shoot sections corresponding to one annual growth interval. Pseudocalliergon trifarium is dioecious, and the expressed sex ratio is skewed toward the female gender (F : M = 1.8, Bisang and Hedenäs, 2005
). Both female (perichaetia) (Fig. 2) and male sexual branches (perigonia) (Fig. 3) are produced in lateral positions along the main stem, as is characteristic for pleurocarpous mosses. Sex expression is uncommon (31.2%), and sporophyte development is rare (5.7%, N = 157) (Hedenäs et al., 2003
; Bisang and Hedenäs, 2005
). In northern and central Scandinavia, gametangia mature between ca. 15 August and 15 September (Arnell, 1875
).
|
; Bisang and Ehrlén, 2002
). We collected the material for the present study in a wet rich fen in central Sweden (Jämtland, Åre, north of the stone quarry 1 km ESE of Handöl, 63°15' N/12°28' E, 580 m a.s.l.) at the end of the local growing season (5 September 2003). At this time, annual growth is about terminated, and sexual branches are expected to be fully developed and to include mature gametangia. Female and male individuals of P. trifarium occurred together with non-expressing plants, partly mixed with Scorpidium scorpioides, in extensive patches in two discrete but homogeneous portions of the mire ca 200 m from each other. A narrow bog string separated the two portions.
Data collection
We gathered clusters of the study species, including female, male, and non-expressing plants from the two fen portions, using a random design. We separated single shoots, careful to include as many annual increments as possible and placed them on pieces of cardboard. The collected material was air-dried and stored at room temperature until further examination. In the laboratory, we picked individual, typically unbranched plants that contained at least 3 years of growth intervals (G0, current year's increment; G1, previous year's increment; G2, pre-previous year's increment) and that expressed female sex in at least G0, or male sex in at least G0, or were non-expressing (one male shoot consisted of G0 only). Branched shoots were only included if branches could unambiguously be ascribed to one of the considered years of growth (G0, G1, G2) (N = 6). Except for annual segment number, shoot size was not considered in the selection of the study individuals. Total annual segment mass did not differ between shoots from the study site and shoots collected at other localities in northern Sweden (analyses of variance, P
0.411; values for G0, study vs. other sites, mean [95% confidence interval, C.I.; N] = 1.44 [1.33–1.56; 141] vs. 1.46 [1.36–1.56; 68] mg). Using a dissecting microscope, forceps and razor blade, we dissected the study plants into annual segments at the positions with the smallest diameter. The sexual branches per annual growth interval were counted. We then carefully removed the entire structures (i.e., including all reproductive leaves differentiated from ordinary stem leaves). Accordingly, we used a functional approach for the assessment of reproductive investment and included all tissue associated with the archegonia and antheridia. For each shoot, we measured the length of the annual segments to the nearest mm and placed individual segments into small paper bags. For each annual segment, we collected all sexual branches in a small paper bag. After drying to constant mass at 70°C, the vegetative portions of the annual segments were weighed with a Mettler Toledo (Greifensee, Switzerland) AG245 balance with an accuracy of 0.01 mg. The sexual branches from individual annual segments were weighed to the nearest 0.1 µg with a Cahn (Cerritos, California, USA) C-31 microbalance, and mean mass per perichaetium or perigonium was estimated by dividing the measured mass by sexual branch number.
The estimation of reproductive effort is inherently difficult, and different ways to attain reliable estimates have been proposed. All of them have advantages and disadvantages, which have been repeatedly debated. This holds also true for the functional approach applied in this investigation, which suggests that all tissue in support of reproduction should be included in reproductive effort estimates. The advantage is that all structures that are needed for satisfactory functioning of reproduction are considered. A potential shortcoming is that some of these structures may have overlapping functions. The functional method has been applied previously and was recommended (e.g., Thompson and Stewert, 1981
; Reekie and Bazzaz, 1987a
, b
).
Data analyses
Shoot biomass was significantly related to shoot length (females, R2 = 0.463, P = 0.001, slope = 2.031, N = 21; males, R2 = 0.363, P = 0.003, slope = 2.218, N = 22) and was used as a measure for shoot size in subsequent analyses.
We investigated if there was a threshold size for current year (G0) sex expression by logistic regression analyses. Among sex-expressing shoots, we tested whether vegetative biomass of the current and previous years' increments (G0, G1) differed between perichaetia bearing and perigonia bearing plants by analysis of variance (ANOVA).
We calculated prefertilization reproductive effort [%] for formation of G0-sexual branches, i.e., the relative allocation to sexual branches in the current year as
dry mass of G0-sexual branches x [dry mass of vegetative G0-segment + dry mass of G0-sexual branches]–1 x 100
No sporophytes occurred at the study site. To get an idea of the effort for completed sexual reproduction (i.e., sporophyte development), we compared the biomass of sporophytes plus perichaetia with associated total annual shoot mass in some herbarium collections. This is a rough estimate because we had access to only a small sample size and because we had to use some capsules that were either not completely mature or dehisced.
The effects of sex (male, female) and shoot size (vegetative G0 mass) on investment in current year sexual branches (in terms of total annual investment, mean sexual branch mass, and number of sexual branches in G0) were examined by ANCOVA. The correction for vegetative segment mass allows us to test whether relative allocation to G0-sexual branches (i.e., prefertilization reproductive effort for formation of G0-sexual branches) differed between genders. There were no effects of the factor x covariate interactions (P = 0.82–0.99), and we therefore present only models without interactions.
We tested for potential costs of current year's sexual branch development in two ways. First, we used a general linear model with sex and relative annual biomass allocation to G0-sexual branches (i.e., as a proportion of the G0-segment mass) as predictors and the ratio of vegetative mass of G0 to G1 as response variable to test for costs in terms of reduced somatic growth. Second, we applied general linear models with sex and annual mass or number of G1-sexual branches as predictors, and annual mass or number of G0-sexual branches as response variables, to test for costs in terms of lower frequency of, or reduced investment in fertile branches. Interaction effects between predictors were nonsignificant (P = 0.102–0.462), and excluded from the presented models.
Values for G0-segment length and G1-segment total mass were log-transformed before statistical analyses to improve normality. The analyses were performed using the STATISTICA statistical packages (StatSoft, 1999
, 2003
).
RESULTS
Shoot size and sex expression
The probability to induce sex organs in the current year was not associated with vegetative shoot mass (Table 1A; non-expressing vs. expressing plants, mean [95% C.I.; N] = 1.40 [1.20–1.60; 25] vs. 1.35 [1.25–1.46; 43] mg). This holds also true if female and male plants were considered separately (non-expressing vs. perichaetia-bearing plants [N = 21], P = 0.837; non–expressing vs. perigonia-bearing plants [N = 22], P = 0.336). Vegetative shoot mass did not differ between female and male individuals with sexual branches in either the current (Table 1B; females vs. males, mean [95% C.I.; N] = 1.43 [1.28–1.57; 21] vs. 1.28 [1.12–1.45; 22] mg) or previous year (1.71 [1.30–2.12; 13] vs. 1.47 [1.22–1.72; 13] mg).
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In this study, we examine for the first time the hypothesis that female-skewed sex ratios in unisexual mosses may be a product of sex-specific realized cost of sexual reproduction in terms of shoot growth and future sex expression. This hypothesis was articulated based on higher prefertilization allocation to female than to male sexual organs in an acrocarpous desert moss (Stark et al., 2000
), but effects of such reproductive investment on performance had not been considered to date. We found no evidence of a cost for fertile branch formation in terms of decreased vegetative growth or reduced investments in sexual structures in consecutive years in either gender in the pleurocarpous P. trifarium with a documented female-biased sex expression. Pre-fertilized females invested more in sexual branches than males, both in absolute terms and in relation to concurrent vegetative growth. There was no evidence of a threshold size for sex expression, and among sex expressing individuals, annual vegetative shoot mass did not differ between females and males.
Shoot size and sex expression
If the formation of reproductive organs depends on a certain shoot size that differs between genders, this may result in one gender expressing sex more frequently than the other and eventually in a prevalence of sex expression in that gender. The nonsignificant effect of vegetative segment mass on sex induction in the current year's increment (G0) in either sex implies that there is no threshold size for sexual branch formation in this species. This, and the fact that G0- and G1-segment masses did not differ irrespective of whether they were carrying perichaetia or perigonia, suggests that fertile branch initiation and formation are not primarily governed by the overall resource level of the individual. In accordance, no threshold size for archegonia production was observed in Pogonatum dentatum (Bird.) Bird. (Hassel et al., 2005
), and Ehrlén et al. (2000)
found perichaetium induction to be independent of the resource status of the shoot in Dicranum polysetum Sw. Rydgren and Økland (2001)
and Rydgren et al. (1998)
provided evidence that enhanced radiation induced fertile branches in Hylocomium splendens (Hedw.) Schimp. For other species, a minimum size for sex expression was reported (Stark et al., 2001
; Pohjamo and Laaka-Lindberg, 2004
), which differed between females and males in the case of Anastrophyllum hellerianum (Lindenb.) R. M. Schust. (Pohjamo and Laaka-Lindberg, 2004
).
Annual segment mass did not differ between female and male plants in P. trifarium. Both evidence of and lack of sex-related dimorphism in a number of investigated traits are reported for bryophytes (for references, see Stark et al., 2001
). In agreement with our results, no size differences between male and female shoots were detected in Pleurozium schreberi (Brid.) Mitt., P. dentatum, and Syntrichia caninervis Mitt.; yet, females had a higher growth rate than males in P. dentatum (Longton and Greene, 1969
; Stark et al., 2001
; Hassel et al., 2005
). In contrast, female plants were longer than male and gemmiparous ones in A. hellerianum, a hepatic with a female-biased sex ratio (Pohjamo and Laaka-Lindberg, 2004
). In Lophozia silvicola H. Buch with male dominance, female individuals were shorter than male and gemmiparous ones (Laaka-Lindberg, 2001
). In Ceratodon purpureus (Hedw.) Brid., with variable population-wide overall sex ratios, female and male gametophytes were dimorphic in size, growth, maturation rates, and reproductive output in cultivation experiments (Shaw and Gaughan, 1993
; Shaw and Beer, 1999
).
Allocation to sexual branches
Investment into sexual reproduction is not larger in the rarer male gender than in females prior to fertilization in P. trifarium. Annual and mean masses of G0-sexual branches and prefertilization reproductive effort for G0-reproductive organs were higher in females than in males, while the fertile branch numbers on the G0-segment did not differ between the genders. Prefertilization biomass allocation to sexual structures has hardly been investigated in bryophytes, and comparisons are therefore limited. In the acrocarpous (i.e., producing one perichaetium per growing season in sex expressing individuals) desert moss S. caninervis with a strong prevalence of females and rare sporophyte production, the number of sexual branches per individual per three growing cycles did not differ between genders. Antheridia had approximately six-fold more biomass than archegonia (Stark et al., 2000
, 2001
). However, the mass of the surrounding gametangial leaves, which formed the sexual branches, was not assessed; thus a direct comparison with our findings is not feasible. The acrocarpous moss D. polysetum, commonly with sporophytes, assigned on the average 4.9% of the annual growth increment preceding sex induction to an unfertilized perichaetium (Bisang and Ehrlén, 2002
). The corresponding value in our study species is more than twice as large (11.2%). The estimated effort for completed reproduction (21.4–42.9%) was roughly two- to four-fold that of the female pre-zygotic reproductive effort, compared to approximately ten times in D. polysetum (44.5 vs. 4.9%) (Bisang and Ehrlén, 2002
). Pleurocarpous mosses have the potential to produce multiple lateral perichaetia on shoots that do not have growth terminated in the process. Because of this, pleurocarpy can be viewed as a pre-adaptation for a potential for greater reproductive output under favorable conditions. More sexual branches probably enhance the chance of successful fertilization, but it may also imply higher reproductive costs if fertilization is achieved. However, mechanisms that seem to limit excessive sporophyte formation have been reported (Stark, 1983
). Further investigations of female pre-zygotic reproductive effort in more species and its spatial and temporal variation will be needed to assess if it is indeed associated with growth form or if other factors related to sporophyte frequency, sex ratio, or environmental factors are more important.
It can be argued that leaves and stems of sexual branches are not part of the reproductive effort, but contribute to resource acquisition (e.g., Convey and Lewis Smith, 1993
; González-Mancebo and During, 1997
), that sexual branches are thus largely self-supporting, and that their formation is not expected to result in reproductive costs. It is true that including all structures that are necessary for proper function of the sexual reproductive process (functional approach, e.g., Thompson and Stewert, 1981
; Reekie and Bazzaz, 1987a
) may overestimate the proportion of resources allocated to reproduction and that leaves on fertile branches may have overlapping sexual and vegetative functions. Hence, our estimates of reproductive effort, which comprise sexual organs and the cluster of specialized surrounding leaves, should be regarded as a measure of the resources actually devoted to structures required for reproduction rather than as a measure of the "physiological cost" of reproduction (Bazzaz et al., 2000
). It is also true that sexual branches may be basically self-supporting and that they may not draw upon resources from other plant parts. However, this does not necessarily imply that a cost of reproduction, in terms of a negative correlation between current reproduction and future performance, cannot occur (see next section). This is because an alternative use of the resources allocated to sexual branches, i.e. for vegetative growth, may have resulted in increased reproduction in the future. The latter could happen if fertile branches were efficient enough to cover the demands of reproductive organs but less efficient than vegetative shoots with respect to carbon gain per unit investment.
Cost for production of sexual branches
According to the "realized cost of sexual reproduction hypothesis," one would expect the rarer sex (males in our study species) to exhibit a higher prefertilization reproductive cost. However, in P. trifarium increasing allocation to reproductive structures did not result in reduced growth capacity, which suggests no detectable costs for fertile branch formation. Investment in G0-sexual branches as a proportion of G0-segment mass was not related to vegetative G0-mass relative to G1. In agreement, neither female nor male shoots of P. dentatum grew slower after producing gametangia (Hassel et al., 2005
). Shoot mortality was higher among female than among male individuals in A. hellerianum, a liverwort with a female-dominated sex ratio, which was interpreted as an effect of higher reproductive cost in the former (Pohjamo and Laaka-Lindberg, 2003
). However, an unknown proportion of sporophytic shoots was included in the study sample, thus the observed costs may be related to sporophyte production rather than to prefertilization costs. In female Marchantia inflexa Nees & Mont., early sex-expressing individuals produced fewer gemmae cups than late expressing plants, indicating a trade-off between sex expression and asexual reproduction in females; but data for males were too limited for analysis (Fuselier and McLetchie, 2002
).
A trade-off between sex-expression in consecutive years could also be expected in case sexual branch development drains the shoot from resources necessary for future sex formation. However, formation of perichaetia or perigonia in the previous year (G1) did not negatively affect frequency or biomass of sexual branches in the current year in our study species.
While the developing sporophyte provides only a fraction of the photosynthetic products necessary for its development in almost all bryophyte species (Proctor, 1977
) and incurs a significant somatic cost (Ehrlén et al., 2000
; Rydgren and Økland, 2003
), sexual branches in bryophytes may indeed be self-supporting, as indicated by the present results for P. trifarium. Lack of or low reproductive costs were suggested for most algae because these have chlorophyllose sporangia (De Wrede and Klinger, 1988
). Accordingly, there is little empirical evidence in support of a (sex-specific) prefertilization reproductive cost in dioecious bryophytes.
Costs of reproduction may be difficult to detect for several reasons. One potential problem with assessing costs of reproduction from descriptive data is that differences in the allocation of resources to reproduction vs. vegetative growth are obscured by large differences in resource acquisition among individuals (van Noordwijk and de Jong, 1986
). Differences in resource acquisition that result in differences in aboveground size can often relatively easily be incorporated into assessments of reproductive costs. However, other differences in resource state, such as belowground storage, may be more difficult to estimate. As a result, studies of natural variation in reproduction in vascular plants have revealed negative as well as positive correlations between current reproduction and future performance (Obeso, 2002
). Our assessment of costs of reproduction in P. trifarium was based on descriptive data and is therefore subject to the suggested problems to detect costs. However, due to their growth form and lack of specific storage organs, bryophytes have a more limited capacity to stock up resources than vascular plants. We therefore expect that the problem to detect costs of reproduction in our study, accounting for size differences, should be smaller than in similar studies with vascular plants.
In conclusion, our data do not support the idea that a higher realized cost of sexual reproduction can generally explain rarity of male plants in unisexual bryophytes (Stark et al., 2000
). A recent meta-analysis of reproductive costs in seed plants showed that observed sexual dimorphism is apparently not fully explained by the "cost of reproduction hypothesis" in dioecious phanerogams either (Obeso, 2002
). Therefore, we may need to turn to alternative explanations, such as genetic mechanisms or the effects of habitat and stress levels, to achieve a more comprehensive understanding of skewed sex-ratios in bryophytes, as well as in plants in general.
FOOTNOTES
1 The authors thank the Department of Isotope Geology at the Swedish Museum of Natural History in Stockholm for the use of their balances. 
5 Author for correspondence (irene.bisang{at}nrm.se
)
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