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2 Laboratoire de Biologie des Populations d'Altitude CNRS-UMR 5553, Université Joseph Fourier, B.P. 53, F-38041 Grenoble Cedex 09, France; and 3 Laboratoire d'Ecologie Terrestre CNRS-UMR 5552, Université Paul Sabatier, Zoologie Ecologie, Bât. 4R3, 118, route de Narbonne, F-31062 Toulouse Cedex 04, France
Received for publication August 3, 1999. Accepted for publication April 11, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Ericaceae • pollination system • reproductive assurance • Rhododendron ferrugineum • stamen development • stamen size
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Arroyo, Primack, and Armesto, 1982
; Kudo, 1993
; Totland, 1994
; Jacquemart and Thompson, 1995
). However, some animal-pollinated plants growing in severe environmental conditions have a mixed-mating system and can produce spontaneous selfed seeds. Outcrossing will usually occur when reproductive fitness is not limited by a paucity of animal visits. Where such limitations exist, features that maximize within-flower selfing (autogamy) may be favored (Richards, 1997
). Although autogamy is frequent, it is rarely predominant, probably because most plants growing in harsh conditions are long-lived perennials for which constraints on reproductive fitness by seed are low (Richards, 1997
). In Rhododendron parviflorum and R. redowskianum (in Siberia) spontaneous autogamy occurs in the absence of pollinators (Tikhmenev, 1985
), however in some Vaccinium in the Belgian Ardennes (V. myrtillus, V. uliginosum, V. vitis-idaea; Jacquemart and Thompson, 1995
), insect-mediated self-pollination accounts for the majority of seeds produced by selfing. In other species, like Rhododendron aureum (in Japanese mountains), spontaneous selfing does not occur and insect pollination is necessary for seed set (Kudo, 1993
). One character that plays a key role in promoting reproductive assurance in self-compatible species is the reduction of stigma-anther separation (Piper, Charlesworth, and Charlesworth, 1986
).
The species studied here, Rhododendron ferrugineum L. (Ericaceae), is an evergreen shrub with a mean height of 70 cm that grows at the subalpine level from 
1600 to 2200 m. It reproduces both vegetatively (by layering) and sexually. Asexual propagation occurs in closed and mature populations (Pornon et al., 1997
) and preferentially down hill (Escaravage et al., 1998
). Rhododendron ferrugineum produces an inflorescence of 5–22 bright-red nectariferous flowers. The flowers are protandrous (anthers mature before the stigma) and are initiated the year before they mature (Escaravage et al., 1997
). Rhododendron ferrugineum is a self-compatible species, mainly pollinated by bees, bumble bees, and diptera. Spontaneous selfing occurs in the absence of pollinators (Escaravage et al., 1997
). A study of the floral morphology revealed herkogamy (spatial separation between anther and stigma) with different stamen lengths: short-level stamens below or at the same height as the style and long-level ones above the style (Escaravage et al., 1997
). The term stamen dimorphism will be used subsequently. Stamens are mediafixed (filament links to the back of the anther) and are located on two whorls (five stamens per whorl) with long- and short-level stamens on the inner and outer whorls, respectively (E. Flubacker, personal observation). This has not been described in other Rhododendron species and the question that arises is: what are the mechanisms that promote this spatial separation? Are developmental processes involved? Floral developmental studies have been performed on heterostylous taxa (Cheung and Sattler, 1967
; Ganders, 1979
) and more recently Richards and Barrett (1984, 1987)
examined floral developmental differentiation among morphs in tristylous species. In these species, the variability caused by timing and position of stamen origin probably accounts for variation in stamen length within flowers of heterostylous species that have two whorls of stamens (Richards and Barrett, 1992
). In some arctic Primula species, homostyly has replaced heterostyly (Kelso, 1992
). It is suggested that both restrictions of pollination efficiency and developmental constraints (imposed by the need for reciprocity in organ position and to limit stigma-anther separation) are involved in this evolutionary process (Richards and Barrett, 1992
).
In this study, we focused on stamen dimorphism and its possible consequences on the breeding system of Rhododendron ferrugineum. The aims of this paper are (1) to describe the development of the stamens in Rhododendron ferrugineum (from the bud stage to full bloom) to determine at what phenological stage stamen dimorphism can first be detected, and (2) to determine the role of long- and short-level stamens in the pollination of the species.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Experimental design
Stamen development
To study patterns of stamen development, we randomly selected ten individuals in each population. On each individual we conducted the following experiments: we collected three inflorescences per individual at five successive phenological stages [inflorescence buds (t0), young inflorescences (t0 + 2 d), medium-aged inflorescences (t0 + 4 d), advance-aged inflorescences (t0 + 6 d), and inflorescences with flowers in full bloom (t0 + 8 d)]. One flower per inflorescence was dissected and measured under a dissecting microscope, together with the filaments, anthers, and style.
Effects of population, individual, flower, whorl, and position of stamens on anther and filament length in mature flowers were statistically tested by performing five-way mixed analysis of variance using PROC GLM (SAS, 1990
). Population, whorl, and position of stamens were treated as fixed effects; individual and flower were random effects. Population, individual, and flower, and position and whorl were nested (see Table 2).
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). Data were ln transformed for normality. All these tests were performed for each developmental stage. The mean daily growth rate, computed as the length of each stamen at the end of the last phenological stage (full bloom) divided by the number of days elapsed between bud breaking and full bloom (8 d), was compared by performing a Tukey HSD multiple-range test using SPSS for Windows, release 9.0.0.
Effects of partial emasculation
To determine whether the presence of long-level stamens (inner whorl) limits the development of short-level stamens (outer whorl), we selected three other inflorescences on the same ten individuals in which we partially emasculated three flowers at the bud stage. Anthers of long-level stamens (inner whorl) were removed (but their filaments remained) and short-level stamens (outer whorl) were left intact. It would have been interesting to remove the stamens of the outer whorl to compare the results, but unfortunately this experiment was difficult to perform without damaging the flower. The other flowers of the inflorescence were unmanipulated. When flowers reached their mature size, we collected all the treated inflorescences. We dissected the partially emasculated flowers under a dissecting scope and measured the style, anther, and filament lengths of the intact stamens of outer whorl, and the filament length of emasculated stamens (inner whorl). We dissected and performed the same measurements on one unemasculated flower of each inflorescence as a control. In both experiments, stamens were numbered according to their position in the flower. Stigma-anther separation was calculated as filament length minus style length.
In this experiment, the effects of population, individual, flower, treatment (flower partially emasculated or not), and position of stamens on filament length of each stamen (emasculated or not) were tested by five-way mixed analysis of variance (SAS, 1990
) with population, emasculation, and whorl of stamens as fixed effects, individual and flower as random effects, and population, individual, and flower nested. The treatment effect tested for an effect of partial emasculation on the whole, whereas the effect of emasculation on the longer filaments was tested by the treatment x whorl interaction. For each site and treatment (partial emasculation or not) the whorl effect on filament length and stigma-anther separation was tested by one-way analysis of variance (SAS, 1990
).
At the end of the flowering period (mid-July), floral primordia for the next flowering season are initiated. To determine when meiosis of pollen grains occurred, we collected two flowers (from different inflorescences) per individual, on ten individuals in each population every week from mid-July to mid-August. We dissected the flowers and crushed the anthers on a slide in a drop of Alexander's stain (Alexander, 1969
), and observed the slide under a microscope. As pollen is released in tetrads in the Ericaceae, observation of single cells indicates that meiosis had not yet occurred.
Pollination trials
To study the respective roles of short- and long-level stamens in sexual reproduction, we (1) quantified the number of pollen grains per anther in the two whorls and (2) performed a series of pollination treatments. To quantify pollen production we collected one inflorescence bud on each of ten individuals and preserved it in 70% ethanol in May 1997. One flower from each bud was dissected under a dissecting scope. Each stamen was measured according to its position (Fig. 1) and pollen grains were quantified after acid extraction from the anther using a hemacytometer according to Escaravage et al. (1997)
. Pollen production was analyzed by performing five-way mixed analysis of variance as described in the stamen development analysis (see above). The association between the number of pollen grains and stamen length was tested by a correlation analysis (SAS, 1990
). We performed seven pollination treatments (summarized in Table 1) on ten other randomly selected individuals in each population. Each individual received all seven treatments, and each treatment was performed on two inflorescences, on at least five flowers per inflorescence. We thus studied a total of 140 inflorescences and 700 flowers at each site.
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2 d after the inflorescence bud opened. At this stage, inflorescences were very small and the flowers were still closed. Five flowers per inflorescence (except for T1 and T2) received one of the seven treatments. All other flowers (between one to five flowers) were removed. This manipulation did not disturb the development of the remaining flowers (Escaravage et al., 1997
). Fruits were collected shortly before dehiscence (early September) and the seeds counted.
To detect the effects of individual, inflorescence, and treatment on the number of seeds per fruit, we performed three-way mixed analysis of variance using PROC GLM (SAS, 1990
) for each population. Treatment was a fixed effect while inflorescence and individual were treated as random effects. Inflorescence was nested within individual. Mean comparisons between specific treatments were also carried out by using a Scheffé multiple-range test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In unmanipulated flowers, short- and long-level stamens are located on the outer and inner whorls, respectively. Filaments and anthers from the inner whorl are significantly longer than those of the outer whorl (P < 0.001; Table 2). The position within the whorl significantly affects filament length but not anther height. Stamen number 6 was always the smallest at each site and each phenological stage; the longest stamens were number 1, 3, and 9. This conferred slight zygomorphy following a plane of symmetry passing through stamens 1 and 6 (Fig. 1). Although filament length is significantly affected by population (P < 0.05; Table 2), stamen dimorphism is preserved among populations as indicated by the non significant interactions of population by whorl and population by position nested in whorl (Table 2). The mean stigma-anther separation at Chamrousse was: 0.83 mm (±0.11 SD) for the outer, short-level whorl and 1.63 mm (±0.14 SD) for the inner, long-level whorl. At Collet d'Allevard the mean stigma–anther separation was 0.42 mm (±0.12 SD) and 1.30 mm (±0.14 SD) for the inner, short-level and outer, long-level whorls, respectively. The slopes in Fig. 2 represent the growth rate of anthers (a) or filaments (b) of the long-level stamens relative to those of the short-level stamens for each developmental stage. A positive correlation exists between anther height of long- and short-level stamens from the bud (A) to medium (C) stages (P < 0.001; Fig. 2a) suggesting that during these stages anther growth still occurs. However, in later phenological stages, the growth rates, are similar until anthers have reached their final size. In contrast, stamen elongation occurs throughout the development of the flower (Fig. 2b). For each stamen, the daily mean growth rate is shown in Fig. 3. Stamen 6 (the shortest stamen) has the slowest growth rate, whereas stamens 1, 3 and 9 (the longest stamens) have the fastest.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and Eichhornia (Richards and Barrett, 1984
) and in distylous species of Primula (Stirling, 1932
), stamen dimorphism in R. ferrugineum appears in premeiotic stamens and is maintained throughout phenological stages.
Early in flower development, anthers occupy most of the volume in the flower while the corolla, style, and filaments are poorly developed. Thus, arrangement in staggered rows seems to be the most appropriate means to limit the size of young flowers in the buds. Overwintering of floral primordia has been described in many alpine and tundra plants species (Bliss, 1971
; Bell and Bliss, 1980
; Diggle, 1997
; Aydelotte and Diggle, 1997
) and allows the flower to bloom early in the spring (Bliss, 1971
; Diggle, 1997
). However, it does not seem to be a specificity of plants growing in harsh environments (Diggle, 1997
), since it occurs in plants that flower very early in the year (Alnus glutinosa, Coryllus avellana; N. Escaravage, personal observation). In alpine environments, early anther formation and spermatogenesis could be a strategy to allow the flower to become functional rapidly and could be an adaptation to the short optimal reproductive period, allowing the plant to flower as soon as the temperature increases. The formation of pollen grains in the season preceding flowering is risky since a severe winter could occur and freeze the buds. However, this risk is reduced because flowers are protected in bud scales and plants of R. ferrugineum usually spend the winter under thick snow cover that buffers temperature effects (Larcher and Siegwolf, 1985
).
Two main categories of causes can explain stamen dimorphism: (1) "proximate" and (2) "ultimate" causes that refer to developmental and selective aspects, respectively. Under the first category filament expansion can be regulated, through anthers, by growth hormones such as cytokinin (Hess and Morré, 1978
), gibberellins (Greyson and Tepfer, 1967
), or auxin (Koning, 1983
). Greyson and Tepfer (1967)
argued that inhibition of filament growth following emasculation in Nigella hispanica could be accompanied by inhibition of both cell elongation and cell division in the epidermis. In R. ferrugineum, emasculation of the inner whorl results in extra growth of the outer whorl, yet emasculation does not affect the growth of the inner whorl. This suggests that, if hormonal control is involved it is only in the one direction. Testing for hormonal control can be challenging because it is often difficult to distinguish between hormonal control and homeostatic responses.
Monopolization of space by anthers of long stamens could represent a sufficient barrier to the development of the short stamens to create a mechanical resistance to filament cell division. Thus, the different sizes should disappear when the spatial constraint imposed by the long stamen is removed. However the size difference between long- and short-level stamens lies primarily in filament length and filament growth occurs when flowers open and space is not as limiting. Daily stamen growth rate is similar across all stamens except for the shortest, stamen 6, and the longest ones, stamens 1, 3, and 9 (Fig. 3). We detected no difference in stamen growth rate between inner and outer whorls (data not shown). This is different from several heterostylous species (Richards and Barrett, 1984, 1987
) in which differences in stamen length among morphs arise through differences in the relative growth rate and the duration of growth. However, some species of Pontederiaceae, Lythraceae, and Oxalidaceae initiate two temporally separated stamen sizes. The difference in time of origin establishes a size differential between stamen series that is maintained throughout development. This mechanism could account for the two stamen levels in R. ferrugineum.
Short stamens might benefit from resources normally allocated to the development of long stamens (inner whorl). However, this suggestion seems unlikely since differences in nutrient availability between populations, individuals, inflorescences, and flowers would induce variation in stamen size within the two whorls. On the contrary, stamen hierarchy in relation to their position in whorls appears to be similar in both populations.
In the second category, ultimate causes, the two stamen levels may have different functions in pollination in R. ferrugineum. Our results indicate that long-level stamens do not participate autonomously in self-pollination in the absence of pollinators since no seeds were produced when short stamens are removed (T6; Fig. 5). Because unemasculated flowers could self in the absence of pollinators, spontaneous self-pollination is likely due to short-level stamens. However, our experiments provided no formal proof. The treatment in which long-level stamens were removed also produced no seeds in the absence of pollinators (T7; Fig. 5), but, when short-level stamens were in the corolla alone, they grew to the height of long-level stamens. Thus they function similarly to long-level stamens and are inefficient in autonomous selfing. Spatial separation between the stigma and the anther of the longest stamen is on average 1.50 mm. This distance seems to be sufficient to avoid self-pollination (Webb and Lloyd, 1986
), especially in R. ferrugineum where pollen is sticky and dehiscence poricidal.
The distance between stigmas and anthers of short-level stamens is smaller at Collet d'Allevard than at Chamrousse. This may explain why plants at Collet d'Allevard produced more seeds in treatment T5. The pollination mechanism in open-pollinated treatment T1 is less obvious, and we do not know the proportion of seeds sired by self- and cross-pollination, or which stamen level is involved. However in this species the autofertility index is high (0.92; Escaravage et al., 1997
), suggesting that autogamy could account for the majority of seeds produced.
In a previous study on the genotypic structure of a R. ferrugineum population, Escaravage et al. (1998)
showed that genotypes were closely related. These authors hypothesized that autogamy and geitonogamy (fertilization between different flowers on the same plant) may be responsible for such a relatively homogeneous genetic structure. However, we have yet to estimate the proportion of outcrossed or selfed seeds. Both fertilization modes can occur synchronously at each generation and at all reproductive stages. In alpine environments, snow and frost often occur during periods of growth and reproduction and result in a scarcity of pollinators (Arroyo, Primack, and Armesto, 1982
; Escaravage, 1997
). In such a context, self-pollination can compensate for the insufficient pollinator activity and act as reproductive assurance (Arrroyo, 1974
; Wyatt, 1983
; Holsinger, 1992
; Harder and Barrett, 1995
). Therefore, in R. ferrugineum, pollination by short-level stamens could act as reproductive assurance in the absence of pollinators that would prevent outcrossing. Reproductive assurance is promoted in numerous plants growing in severe environments. In arctic Primula species, it is common to see a shift in breeding system from distyly to homostyly and at least facultative autogamy (Kelso, 1992
; Mazer and Hultgard, 1993
; Miller et al., 1994
). Armeria maritima has also lost distyly in the tundra portion of its range (Vekemans et al., 1990
).
Anther position can affect pollen removal through its influence on the timing of anther dehiscence (Harder and Barrett, 1993
). However, all anthers of R. ferrugineum flowers dehisce before the flower opens (as in R. ponticum; Percival, 1955
), whereas stigmas become receptive when the flower opens (Escaravage et al., 1997
). No difference in the timing of anther dehiscence among whorls has been observed (N. Escaravage, personal observation). Anther position can also determine the placement of pollen on a pollinator's body, which influences the likelihood of pollen loss through grooming (Faegri and van der Pijl, 1979
). It seems that the advantages of a particular anther position depend on the morphological and behavioral characteristics of a plant's dominant pollinators (Harder and Barrett, 1993
). For bee-pollinated species with tubular flowers, anther placement in the opening of the perianth mouth seems to be the best position for pollen removal. King and Buchmann (1995)
suggested that Rhododendron spp. are seldom buzz-pollinated because the flowers are too large. However, R. ferrugineum has relatively small flowers and stamens are short and located in the perianth mouth, where bees and bumble bees can be in contact with all of the anthers. So far, this pollination aspect has not been addressed in R. ferrugineum and should be studied in future investigations.
Rhododendron ferrugineum seems to fit well with the usual theories concerning plants that grow in drastic environments: (1) this species spreads vegetatively and (2) has a high sexual reproduction potential (0.4–2.5 million seeds/m2 of heathland; Pornon et al., 1997
). Thus, even if seedling establishment occurs rarely, episodic recruitment is sufficient to maintain a high level of genotypic diversity in the populations (Escaravage et al., 1998
); Also, (3) all floral organs are formed in the year previous to flowering allowing the species to flower as soon as conditions become favorable and (4) R. ferrugineum reproduces both through self- and cross-pollination (Escaravage et al., 1997
) with one level of stamens (the short ones) devoted to self-pollination when pollinators are scarce.
The stamen dimorphism in flowers of R. ferrugineum has been studied under both developmental and selective aspects. According to Gould and Lewontin (1979)
, evolutionary biologists focus exclusively on immediate adaptation to local conditions and tend to ignore developmental constraints. In this study we showed that stamen dimorphism in R. ferrugineum flowers may originate from developmental constraints. However, it also becomes adaptive by favoring reproductive assurance.
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FOOTNOTES |
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3 Author for reprint requests (e-mail: pornon{at}cict.fr
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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