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Post-Floral Perianth Functionality: Contribution of Persistent Sepals to Seed Development in Helleborus Foetidus (Ranunculaceae)1

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Post-Floral Perianth Functionality: Contribution of Persistent Sepals to Seed Development in Helleborus Foetidus (Ranunculaceae)1 American Journal of Botany 92(9): 1486±1491. 2005. POST-FLORAL PERIANTH FUNCTIONALITY: CONTRIBUTION OF PERSISTENT SEPALS TO SEED DEVELOPMENT IN HELLEBORUS FOETIDUS (RANUNCULACEAE)1 CARLOS M. HERRERA2 EstacioÂn BioloÂgica de DonÄana, Consejo Superior de Investigaciones Cientõ®cas, Avenida de MarõÂa Luisa s/n, E-41013 Sevilla, Spain The perianth persists after ¯owering in many plants, yet its post-¯oral functionality has been little investigated, and the few studies available provide ambiguous evidence. This paper tests the hypothesis that the green persistent sepals of the perennial herb, Helleborus foetidus, contribute to the plant's ®tness by enhancing seed number and/or size. Post-¯oral contribution of the calyx to fruit and seed development was evaluated by manipulating sepal number and measuring the effect on follicle size, seed set, seeds per follicle, and mean seed mass. The allometric relationship between calyx size and follicle mass was examined for ¯ower buds, open ¯owers, and immature fruits differing in follicle number. Calyx manipulation had no signi®cant effect on follicle size, seed set, or number of seeds per follicle, but it did have a signi®cant in¯uence on the size of individual seeds. Calyx size and mean seed mass were positively, linearly related. The calyx mass/seed number ratio declined with increasing number of follicles per fruit. The persistent sepals of Helleborus do contribute resources to the development of seeds, although there is not evidence of post-¯oral allometric adjustment of the calyx mass/follicle number ratio that could compensate for variations in seed number per fruit. Key words: allometry; calyx size; Helleborus foetidus; perianth persistence; Ranunculaceae; seed size; sepal photosynthesis. In many species of ¯owering plants, the calyx, the corolla, vides a protection from parasitoids to the caterpillars of the and/or some ¯oral ancillary structures (e.g., bracts) persist well Physalis-specialist herbivore Heliothis sub¯exa while they beyond completion of anthesis, often until fruit maturation and feed on the fruit enclosed within the calyx, a herbivore-pro- seed release. The protracted presence of structures whose gen- tective function that can hardly be interpreted as enhancing uine function is to contribute to the success of ¯owers (pollen plant ®tness (Sisterson and Gould, 1999). In cultivated persim- export and import) suggests that, after anthesis, they are co- mon fruits (Diospyros kaki), intense photosynthesis by the opted for new, different functions unrelated to the pollination large, persistent green calyx lobes does not contribute to fruit process. The nature of this post-¯oral function is fairly evident development (Nakano et al., 1997). Further investigations on in some cases, as in species where the ¯eshy ``fruits'' made a variety of species in diverse ecological scenarios are needed up of juicy bracts or hypanthia, or the spiny, plumose, or oth- to assess the functional signi®cance and possible adaptive val- erwise modi®ed calices, play an essential role in seed dispersal ue of perianth persistence, a widespread but poorly understood (Ridley, 1930; van der Pijl, 1982). In fact, the ``recycling'' of ¯oral feature. In addition, an improved understanding of the pre-existing ¯oral structures seems one of the main evolution- functionality of persistent perianth parts past ¯owering would ary avenues leading to the diversi®cation of seed dispersal allow one to address the more general issue of whether, be- mechanisms in higher plants (Stebbins, 1974). In other in- cause of contrasting selective pressures operating at the ¯oral stances, however, the post-¯oral function of persistent perianth and post-¯oral stages, multifunctionality of a given ¯oral parts is much less clear and can only be tentatively guessed. structure may contribute to the evolution of compromise ¯oral Consider, for example, the dry persistent corollas found in so attributes, an aspect that remains essentially unexplored. many plant families (Cronquist, 1981), the in¯ated calyx of This paper evaluates the hypothesis that the large, persistent Physalis (Sisterson and Gould, 1999), or the large accrescent green sepals of the perennial herb, Helleborus foetidus L. calices of species of Olacaceae, Hypericum,orHelleborus (Ranunculaceae), make some measurable contribution to the (among many others; Heywood, 1978; Mathew, 1989). plant's ®tness in terms of enhanced seed number or size. In Investigations on the post-¯oral functions of perianth parts the genus Helleborus the petals have become modi®ed into other than those related to seed dispersal are strikingly scarce nectaries, and sepals are enlarged and look like petals (Ma- (Sisterson and Gould, 1999; Salopek-Sondi et al., 2000, 2002), thew, 1989; Tamura, 1993). Depending on the species, they and these few studies do not always con®rm an immediate may be green or, less often, white, pink, or purple at anthesis, utility or presumable adaptive value of perianth persistence. In turning green afterwards and persisting through the fruiting Physalis angulata, for example, the large in¯ated calyx pro- stage. This observation has fueled the traditional view that Helleborus sepals ``assist in photosynthesis'' (Mathew, 1989, 1 Manuscript received 13 February 2005; revision accepted 16 May 2005. p. 40), ``helping the seed-pods to swell'' (Rice and Strangman, Thanks are due Jose L. Garrido, MoÂnica Medrano, and Pedro J. Rey for 1993, p. 8). Strong indirect support for this idea was recently comments and discussion on the manuscript, and the ConsejerõÂa de Medio provided by Salopek-Sondi et al. (2000, 2002) for Helleborus Ambiente, Junta de AndalucõÂa, for authorizing my research in Sierra de Ca- niger. In this species, fruit initiation triggers post-¯oral expan- zorla and providing invaluable facilities there. This research was funded by grants BOS2000-1122-C03-01 and BOS2003-03979-C02-01 from Ministerio sion of the white sepals and regreening through tranformation de Ciencia y TecnologõÂa. of leucoplasts into chloroplasts, which confers a photosyn- 2 E-mail: [email protected]. thetic capacity similar to those of young leaves. This ®nding 1486 September 2005] HERRERAÐSEPAL CONTRIBUTION TO SEED DEVELOPMENT 1487 Fig. 1. Flower (a) and developing ``fruit'' (b) of Helleborus foetidus. After ¯owering, the green sepals spread out and remain, subtending the apocarpous follicles until the follicles complete development, and fruit ripening and seed release take place. suggests that chlorophyll-containing sepals may be a source follicle(s) (Fig. 1b). Sepals remain green and persist until the follicles mature of assimilates for the developing seeds in this and other species in June±early July and seed dispersal takes place. For convenience, the com- of Helleborus, but this hypothesis has not been tested directly. posite structure made up of the developing follicle(s) plus the subtending The main objective of this study was to determine if, under sepals (Fig. 1b) will be termed here a ``fruit,'' and the set of sepals will be natural ®eld conditions, experimental modi®cation of calyx referred to as the ``calyx'' regardless of whether they are part of a ¯ower or size after ¯owering affected the size of the associated fruit and/ a developing fruit. The term ``follicle'' will be used to designate either the or the number and size of seeds produced, and if so, whether carpels of ¯owers or ¯ower buds, or the true follicles of developing fruits. calyx size and the response variable(s) were linked by a linear Further details on the reproductive ecology of H. foetidus in the Iberian Pen- relationship. If selection had enhanced the photosynthetic con- insula may be found in Garrido et al. (2002), Herrera et al. (2002), and GuitiaÂn tribution of the calyx to developing seeds, one would expect et al. (2003). calyx mass and total fruit mass to be linked by a proportion- ality relationship independent of variations in fruit size. A sec- Study area and methodsÐThis study was carried out during March±June ond objective of this study was to examine the allometric re- 2002 at a large, more or less continuous population of H. foetidus located at lationship between calyx and fruit size, speci®cally whether 950±1100 m elevation in wooded slopes around the small village of Vadillo- there is some post-¯oral adjustment of calyx size to variations Castril, in the Parque Natural Sierras de Cazorla-Segura-Las Villas, JaeÂn Prov- in the number of fruit follicles and developing seeds. ince, southeastern Spain. Plants were growing in the understory of pine (Pinus pinaster and P. nigra) and evergreen oak (Quercus ilex) mixed woodlands. MATERIALS AND METHODS Flower buds, open ¯owers, and immature fruits were collected to examine patterns of variation in calyx size from the ¯ower bud through the nearly Study plantÐHelleborus foetidus is a perennial herb widely distributed in mature fruit stages, and also to determine the allometric relationships between western and southwestern Europe (Werner and Ebel, 1994). In the Iberian calyx size and follicle size in ¯owers and fruits differing in follicle number. Peninsula, it typically occurs in clearings, forest edges, and the understory of Collections were done on ®ve different dates between 7 March and 25 May montane forests, mainly on limestone substrates. Flowering mainly takes place from a large number of ¯owering and/or fruiting plants scattered over the during January±March. Flowers are hermaphroditic and self-compatible, and study area. Only structures without signs of herbivore damage were collected. although some spontaneous autogamy occurs when pollinators are excluded The sample of fruits comprised all developmental stages from newly withered experimentally, successful reproduction requires insect pollination. Bumble ¯owers up to nearly mature fruits in roughly similar proportions. Efforts were bees and anthophorid bees are the main pollinators (Herrera et al., 2001). The made to sample the whole range of follicle number occurring in the population green, pendent, bell-shaped ¯owers (Fig. 1a) are 14±19 mm long and 12±17 (range 5 1±5), yet ¯owers and fruits with ®ve follicles were too scarce to mm wide.
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