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Spatial aspects of seed dispersal and seedling recruitment in orchids

2007; Wiley; Volume: 176; Issue: 2 Linguagem: Inglês

10.1111/j.1469-8137.2007.02223.x

1469-8137

Jana Jersáková, Tamara Malinová,

Plant Parasitism and Resistance

Growing interest in spatial plant ecology is resulting in new approaches to the study of seed dispersal and seedling recruitment; two important processes determining population dynamics, genetic structure within and among plant populations and the colonization of new areas (Vekemans & Hardy, 2004). In general, seed dispersion patterns are determined by the spatial pattern of reproductive adults, their seed outputs and their seed shadows, while seedling recruitment mainly depends on the probability of seed arrival and the availability of a suitable microsite (Nathan & Muller-Landau, 2000). In the orchid family, successful germination and seedling establishment are crucial life history stages, as orchid seeds are unusual in being among the smallest seeds of all flowering plants, with an undifferentiated embryo that contains minimal reserves. Therefore, at germination, orchids are fully dependent on an interaction with a mycorrhizal fungus, which colonizes the seeds and provides all nutrients essential for seedling development. In the past decade, there have been several attempts to investigate the process of orchid seed germination in a spatial context (Perkins & McGee, 1995; McKendrick et al., 2000; Batty et al., 2001; Feuerherdt et al., 2005; Diez, 2007); however, these studies have told us little about the extent to which seed dispersal and germination are associated with the spatial distribution of recruits. In this issue of New Phytologist(pp. 448–459), Jacquemyn et al. provide more insights into the within-population spatial genetic structure and recruitment potential of an orchid species, for which little is known regarding seed dispersal patterns and the successful establishment of mycorrhiza-dependent seedlings. 'Such a fine-scale population genetic structure may have serious consequences for the seed quality resulting from pollen transport between neighbouring plants in outcrossing species' Orchid seeds are very small, extremely light and produced in great numbers. The embryo occupies only a very small part of the space inside the seed coat, the remainder of which is filled with air. As a result, orchid seeds can remain airborne for long periods and travel thousands of kilometres. Long-distance dispersal events are well demonstrated by the colonization of volcanic islands, where orchids were among the first plants to grow after island formation (Arditti & Ghani, 2000). Although orchids have fine dust-like seeds, most studies investigating spatial genetic structure within terrestrial orchid populations have found a significant pattern, which in most cases was explained by limited seed dispersal (Machon et al., 2003). Similarly, the parentage analysis in the study of Jacquemyn et al. suggests that seed dispersal with subsequent recruitment within two Orchis purpurea populations was limited to median distances of 4 and 7 m. The typical seed rain density in terrestrial orchids thus decreases as a function of distance from the parent plant (Fig. 1), where the long tail represents only a small proportion of seeds, which is, however, sufficient for colonizing new areas. Proportion of seeds captured by sticky Petri dishes, which were positioned at six distance classes, in six directions, from adult plants of Pseudorchis albida, Anacamptis morio and Dactylorhiza majalis (in low and high vegetation). The value for each distance class is based on the sum for three directions. Data were fitted by Gaussian curves (J. Jersáková, unpublished data). Such a fine-scale population genetic structure may have serious consequences for the seed quality resulting from pollen transport between neighbouring plants in outcrossing species, as is the case for most orchids. For example, in Dactylorhiza praetermissa, a nonrewarding orchid species in terms of nectar production, pollination between plants growing less than 10 m apart yielded seeds with a lower proportion of embryos and decreased germination rates compared with pollination between plants growing more than 20 m apart (Ferdy et al., 2001). This effect may be even more pronounced in orchids producing rewards, as pollinators tend to fly shorter distances in rewarding patches, which leads to increased inbreeding depression in progeny if neighbouring plants are closely related (Vekemans & Hardy, 2004). The orchid family is renowned for an unusually high occurrence of nonrewarding flowers compared with other plant families (Jersákováet al., 2006). The limited seed dispersal thus could indirectly favour the evolution and stability of deceptive pollination systems in orchids, where pollen dispersal distances are greater than in rewarding plants, to compensate for the homogamy that would arise from recruitment in the extreme vicinity (Jersákováet al., 2006). The concept of a 'safe site' describes the specific conditions that allow a seedling of a particular species to emerge successfully from the soil and to develop into an adult, reproductive plant (Harper et al., 1965). For orchid seedlings, which are fully dependent on nutrients supplied by a mycorrhizal fungus until they reach the autotrophic stage, recruitment success will be strongly influenced by the availability of a suitable fungal strain. Our knowledge of spatial aspects of seed germination was greatly improved when Rasmussen & Whigham (1993) developed an inexpensive and simple method for in situ seed germination (Fig. 2a). This method enables seed cultivation under nearly natural conditions and colonization by fungal hyphae from the surrounding soil (Fig. 2b). Not only do the seed packets retrieved allow assessment of germination, but the mycorrhizal seedlings obtained can be used in further molecular analyses and in vitro cultivation of fungal symbionts. To date, orchids have been found to associate with several groups of fungi, and differences in the ecology and nutritional demands of these fungi may strongly impact seed germination patterns. (a) The in situ seed germination technique employs a plastic slide and nylon mesh with enclosed seeds. (b) Developmental stages of Epipactis helleborine seedlings after 23 months in the soil. Orchids of open habitats typically associate with saprotrophic basidiomycetes of several lineages, collectively named Rhizoctonia after their asexual stage (Rasmussen, 2002). When not in association with orchid roots, these soil-borne fungi are considered to be saprophytic or parasitic on plants, but little is known about their spatial distribution in the environment, their nutrient demands, and their fine-scale propagation. The above-mentioned studies, which focused on the spatial aspects of orchid seed germination, suggest that mycorrhizal fungi have an aggregated distribution within the habitats. Although in ordinary circumstances the mycorrhizal fungi are likely to be distributed independently of the orchids (Feuerherdt et al., 2005), higher abundances of fungal symbionts are typically found close to adult plants (Batty et al., 2001; Diez, 2007). For example, Perkins & McGee (1995) found Rhizoctonia solani within 50 cm of adult plants of the orchid Pterostylis acuminate. These 'safe sites' probably provide suitable environmental conditions for both fungus and orchid growth, as the seed germination rate was found to be correlated with specific edaphic factors, such as soil organic matter content, potassium content, soil acidity and moisture (Batty et al., 2001; Diez, 2007), which probably play important roles in the growth and density of saprophytic fungi (Ettema & Wardle, 2002). Conversely, constraints on fungus availability might be more pronounced in the germination of nonphotosynthetic myco-heterotrophic orchids and some green forest orchids, which were found to associate with ectomycorrhizal basidiomycetes and ascomycetes (Julou et al., 2005). In such cases, the fungus belongs to a tripartite symbiosis, in which the orchid indirectly recovers carbohydrates from surrounding trees via a shared mycorrhizal fungus. As the ectomycorrhizal root tips of host trees are usually found in the close vicinity of the root system of mycotrophic plants (Selosse et al., 2002), the successful germination of orchids may not simply depend on the presence of adult plants, but may be largely determined by the occurrence of ectomycorrhizal root tips. This view is supported by a nonsignificant effect of the presence of adult Corallorhiza trifida plants on the percentage of germinating seeds (McKendrick et al., 2000). Making a significant step forward, Jacquemyn et al. show that the probability of seed germination and further establishment of protocorms is closely associated with the spatial distribution of recruits. The authors investigated the spatial patterns of seedling recruitment within two populations of O. purpurea, an orchid that is likely to associate with Rhizoctonia-like fungi from the Tulasnellales fungal subgroup (GenBank accession number AJ549121). The germination rates were found to differ markedly between the two populations of O. purpurea. At the first site, seed germination was confined to particular microsites, where both adults and seedlings were found to be clustered. At the second site, seed germination was not found to be restricted, and hence not all seedlings overlapped with adult clusters. The authors could, however, only speculate on whether the restricted germination at the first site was caused by a lack of appropriate fungus or by a lack of suitable soil substrate. Future studies might focus on establishing the presence or absence of the fungal symbiont in the soil using molecular methods such as those employing specific PCR primers or terminal restriction fragment length polymorphism, which provide fingerprints of whole fungal communities (Dickie et al., 2002). Orchids produce an enormous quantity of seeds, but the probability of one seed appearing above the ground as a seedling is extremely low. Seedling recruitment is a fundamental component in population dynamics models, but its value is very difficult to determine for orchids, for which little is known about the time elapsing between the heterotrophic and autotrophic stages and the persistence of the orchid seed bank. Seed baiting techniques can, however, help us to estimate this value more precisely, as seed germination and seedling recruitment rates seem to be highly correlated (Diez, 2007). Existing studies suggest that a relatively high proportion of orchid seeds start to germinate (ranging from 30 to 89% in suitable microsites; Rasmussen & Whigham, 1993; McKendrick et al., 2000), but only a small proportion of protocorms will reach the advanced stages of plant development (less than 1%; Batty et al., 2001). The insufficient development and subsequent death of seedlings in the later stages of development could stem from the fact that initial mycotrophic germination can be induced by a broader spectrum of mycobionts than is required for the further growth of a mycotroph, as reviewed by Bidartondo (2005) for Ericaceae seeds without food reserves. Convincing evidence, however, is still lacking for orchids. One attempt to calculate seedling recruitment was presented by Batty et al. (2001), who used a seed sowing technique with Caladenia arenicola. Batty et al. found that, of the approximately 34 500 seeds examined, less than 1% reached a stage at which they were able to survive summer dormancy. These data, combined with the mean number of seeds produced per plant per year (1200 seeds), the probability of reaching the seed bank (50%), the probability of finding a 'safe site' (10%), and the duration of the seed bank (< 1 yr), were used to estimate the overall success of C. arenicola recruitment as approximately 0.4 seedlings per parent plant per year. Several relevant long-term studies of orchid population ecology have now been published in which annual seedling recruitment was recorded. However, these studies neglected seed germination and protocorm survival, which are the main steps towards adulthood. Many of these studies are still running; in these and the new studies that are being undertaken, it would be valuable if demographic monitoring of the plants could be combined with seed packet experiments, which can be used as an efficient tool to determine how germination rates translate to population-level recruitment rates.