Jan 23, 2017

Pollination Biology and Breeding System of European Fritillaria meleagris L. (Liliaceae)

ABSTRACT
Fritillaria L. is a relatively large genus of the family Liliaceae, comprising 100–130 bulbiferous, mostly spring-flowering perennial plant species distributed in the Northern Hemisphere. Although most of Fritillaria species are of conservation concern, surprisingly little is known about the reproductive biology of these plants. For example, it would appear that, to date, the pollination biology of only two species has been studied extensively, and details of the breeding system are known only for a further small number of taxa. The present chapter explores the reproductive biology of the type species, F. meleagris, one of the most widely distributed representatives of the genus, red-listed or rare for all European countries of its range. Recent findings show that, contrary to earlier studies, this plant is not dichogamous nor obligatorily outcrossed. Fritillaria meleagris is a self-compatible plant, the P/O ratio indicates outcrossing species, and selfing (rarely occurring in natural populations) results in fully developed seeds. Throughout the species range its flowers are visited by almost 30 insect species, mostly social and solitary bees. The main reward for pollinators is pollen and nectar. The latter is produced by six perigonal nectaries and presented to pollinators throughout the flowering period of an individual flower. The maximum nectar secretion overlaps with that of maximum pollen presentation and stigmatic receptivity, and the nectar is resorbed at the final stages of flowering. The nectar composition is composed of sucrose, glucose and fructose in approximately equal quantities and this composition does not change significantly during subsequent stages of flowering. In the natural populations F. meleagris is not pollen limited. Although the largest recorded pollen loads are transferred by small pollen-collecting solitary bees, there are no significant differences in pollen deposition and removal among the key floral visitors. However, due to their abundance on flowers, seasonal and floral constancy and tolerance of bad weather conditions, the key pollinators of F. meleagris are bumblebees (mostly of the most common species Bombus terrestris and B. lapidarius). All available literature suggests that the current decline of F. meleagris seems not to be caused by the species’ pollination or breeding systems but by the plant’s habitat loss. However, ex situ experiments suggest that smaller populations may be prone to pollen-limitation and, in such cases, the plant species’ dependence on generally rare pollinators and largely out-crossed breeding system may prompt local extinctions of the species.

Introduction
Fritillaria L. (type species F. meleagris L.) is a genus of the family Liliaceae, comprising 100–130 species distributed in the Northern Hemisphere (Tamura 1998; Rønsted et al. 2005; Mabberley 2008), with a large representation in the Mediterranean region (Zaharof 1986; Teksen and Aytac 2011) and California (Rønsted et al. 2005). These species are bulbiferous, mostly spring-flowering perennials, with an erect flowering stem usually producing a single flower, but occasionally, a multi-flowered raceme. Although Fritillaria is a relatively large genus, and most of its species are of conservation concern, little is known about the reproductive biology of these plants. For example, it would appear that, to date, the pollination biology of only two species, namely, F. imperialis L. and F. meleagris, has been studied extensively, and details of the breeding system are known only for a further small number of taxa. Flowers of Fritillaria species are usually nodding, actinomorphic and have a typical tulip-like, trimerous, campanulate perianth (Tamura 1998). The perianth parts are usually white, greenish, yellow or purplish to reddish and the sepals of many species (e.g., the widely distributed European F. meleagris) have a characteristic checkerboard pattern, hence the name of the genus (Latin fritillus, a dice-box). The plants generally produce bisexual flowers, but some cases of andromonoecy, androdioecy or gender disphasy are also known (Knuth 1899; Shimizu et al. 1998; Mancuso and Peruzzi 2010; Peruzzi 2012; Peruzzi et al. 2012). Some species (e.g., F. imperialis, F. meleagris, and F. koidzumiana Ohwi) are considered to be dichogamous-protogynous (Knuth 1899; Hedström 1983; Burquez 1989; Kawano et al. 2008). This suggestion, however, may not necessarily reflect the true protogyny of the plants but may, in some cases, be based on the characteristically protruding, trifid stigma with its well-developed papilla, which is already present at the bud stage of the flower (Knuth 1899). This structure is mainly found in representatives of the subgenus Fritillaria (Rønsted et al. 2005), and is thought to indicate that stigma receptivity may precede the pollen presentation phase. Recently, Zych and Stpiczyńska (2012) have demonstrated experimentally that this is not true, at least for F. meleagris, and that stigmas in this species become receptive concomitantly with anthesis. This was also supported by pollen germination tests and the fact that flowers showed no receptivity prior to anther dehiscence.

Published data show that the breeding systems of Fritillaria species range from self-incompatible (Burquez 1989; Yashima et al. 1997) to self-compatible, demonstrating various degrees of out-crossing, including facultative autogamous species (Hedström 1983; Kawano et al. 2008; Mancuso and Peruzzi 2010; Zhang et al. 2010; Zych and Stpiczyńska 2012). Knuth (1899) suspected that some F. meleagris plants with cylindrical and closed corollas, as found in German populations of the species, may even be cleistogamous, but this is not true of cultivated plants or for another European population studied by Zych and Stpiczyńska (2012). Cases of nearly-sterile species of hybrid origin have also been reported (U.S. Fish and Wildlife Service 2003).

Based on nectar characteristics, Rix and Rast (1975) concluded that most Fritillaria species are probably pollinated by bees and wasps. These authors, however, studied only European and Asiatic taxa. Indeed, floral visitors to Fritillaria flowers often include, as well as Hymenoptera (mostly various species of bees and wasps), other insects, such as Diptera, Lepidoptera and Coleoptera (Hedström 1983; Bernhardt 1999; Kawano et al. 2008; Zych and Stpiczyńska 2012; Zych et al. 2013), an even birds, as in the case of Asiatic F. imperialis and some North American species, such as F. gentneri Gilkey and F. recurva Benth. (Burquez 1989; Peters et al. 1995; Bernhardt 1999; U.S. Fish and Wildlife Service 2003). This, however, does not necessarily reflect the whole spectrum of pollinator vectors for this genus, since a detailed assessment of the effectiveness of animals as pollinators has so far been undertaken only for F. imperialis (Burquez 1989) and F. meleagris (Zych and Stpiczyńska 2012; Zych et al. 2013).


One of the most widely distributed representatives of the genus is F. meleagris (Fig. 1), the type species. Recently, the reproductive biology of this taxon has been extensively studied (Hedström 1983; Stpiczyńska et al. 2012; Zych and Stpiczyńska 2012; Zych et al. 2013). Since it possesses many of the characteristic features of the genus, it is considered a good reference species for comparison with other representatives of both genus and family.

Fritillaria meleagris L.
Fritillaria meleagris L. is distributed from Western to Central Europe, growing on wet, eutrophic meadows (usually flood-plains) and in open woodlands. In the Alps, it is found in alpine pastures (Rix 1968), and British and Scandinavian populations of the species are regarded to have anthropogenic origins (Zhang and Hytteborn 1985; Harvey 1996). The plant is red-listed or rare for all European countries of its range, and considered vulnerable (VU) for the whole of Central Europe (Schnittler and Günther 1999). Fritillaria meleagris is a long-lived perennial (life span approx. 30 years; Horsthuis et al. 1994), that flowers in spring (April-May). During the flowering period (6–7 d; Zych and Stpiczyńska 2012), the plant grows to a height of approximately 15–60 cm and produces on the upper part of the stem 4–5 narrow, linear leaves and usually a single, large, pendulous, broadly campanulate terminal flower, or very rarely 2–3 flowers. These measure approximately 20 mm in diameter, consist of six purplish-pink (rarely white or whitish) tepals, some 30–45 mm long, marked with a characteristic tessellate pattern resembling that of a chess-board, six stamens whose fi laments measure 10–13 mm in length, and a single tricarpellary, superior ovary bearing a style terminating in a trifid stigma (Knuth 1899; Rix 1968; Piórecki 2001).

The ratio of white-flowering to purple-flowering individuals varies between populations. In the large, natural population found in Krówniki in SE Poland (>>1,000,000 flowering individuals) and studied by Zych and Stpiczyńska (2012), most flowers were purple (the authors encountered only 10–30 white individuals per annum), whereas in the smaller population at Stubno (approx. 15 km NE from Krówniki), only purple-flowered individuals were found. Richards (1997, p. 195) states that all British populations contain both white- and purple-flowered individuals. The Scandinavian populations described by Hedström (1983), however, contained 3.6–5.8% white-flowered plants, depending on the year. By contrast, the now extinct population at Sławno, near Koszalin, a coastal region of Poland, contained only approximately 5% purple-flowered plants. This population was, however, regarded to be anthropogenic in origin (Stecki et al. 1961). According to Hedström (1983), the white-colored form reflects more UV light than does the purple one, but in the Swedish population (Uppsala region) studied by that author, flower visitors (mostly bumblebees and honeybees) did not distinguish between differently colored flowers. We obtained similar results for an ex situ population created at the University of Warsaw Botanic Garden (described by Zych and Stpiczyńska 2012). The proportion of the white-flowered form in this population was quite high (approx. 0.25), and our observations, conducted over 3 d in 2011, during the peak flowering period, failed to demonstrate a preference by pollinators for either of the two color forms (Spearman r = 0.033, P = 0.94), and deposited similar numbers of pollen grains on the stigmas of both purple and white flowers (ANOVA on log-transformed data F1, 45 = 3.18, P = 0.08; Fig. 2).

Breeding System
An individual flower of F. meleagris produces, on average, 148 ± 26 ovules (Zych et al. 2013), and has a P/O ratio (the ratio of pollen grains to ovules) of 1825 and an OCI index (outcrossing index) of 4 (corolla > 6 mm wide, flowers herkogamous), indicating, according to Cruden (1977), that this is a xenogamous (outcrossing) species. This was confirmed experimentally for a Swedish population by Hedström (1983), who showed that self-pollinated plants did not set fruit. A similar experiment was also performed by Zych and Stpiczyńska (2012) for the largest Polish population of this species, and also on commercially available, cultivated plants. These authors showed that although autonomous self-pollination, probably due to floral herkogamy, indeed resulted in very low seed production (on average 0–6 seeds in bagged flowers vs. 86–118 seeds in open pollinated, wild plants), induced self-pollination (self-pollen actively transferred to the stigma) yielded much higher seed set (on average 8–69 seeds per annum; Fig. 2), indicating some potential for selfing (estimated by these authors as 3–34% seed production per annum).

Nectaries and Nectar
In F. meleagris, the main reward offered to pollinators is nectar. It is produced by specialized secretory structures, the floral nectaries. These are of the perigonal type and are positioned adaxially on each of six perianth segments, in a groove located 2–4 mm above the base of the tepal (Knuth 1899; Hedström 1983). All the nectaries, regardless of whether they are located on the inner or outer tepals, are of similar size and, at anthesis, are equally accessible to potential pollinators (Stpiczyńska et al. 2012). The nectar is presented on a relatively exposed, glabrous surface, unlike the subgenus Rhinopetalum, where the nectary surface is bordered by lobes or hairy ridges (Bakhshi Khaniki and Persson 1997) that may restrict nectar feeding by insects with relatively long proboscises. Moreover, the nodding flowers of F. meleagris also limit reward access to a relatively small group of visitors, predominantly large Hymenoptera (Zych and Stpiczyńska 2012).

Stpiczyńska et al. (2012) described in detail the floral nectar secretion in F. meleagris. These authors showed that nectar was presented to pollinators for approximately 5–6 d. The light green nectaries contrasted markedly with the white- and dark-purple-patterned tepals. SEM observations also revealed that the secretory surface was clearly different from that of the non-secretory region, since the cuticle of the former had distinct blisters that usually coincided with the position of the middle lamella between adjoining epidermal cells. Often, perforations were visible on these cuticular blisters, together with nectar residues. In terms of structure, the nectaries consisted of a single-layered epidermis lacking stomata and 3–4 layers of sub-epidermal, nectariferous parenchyma. The nectary was supplied by a single, main vascular bundle and several smaller vascular bundles that ended in the subepidermal secretory layer. These bundles contained xylem and phloem elements. The nectary secretory cells of F. meleagris shared many features with those of other plant species, in that they were small with large nuclei and contained small vacuoles and dense, intensely staining cytoplasm. TEM revealed abundant arrays of endoplasmic reticulum, dictyosomes and secretory vesicles. However, unlike the nectaries of the majority of investigated plant species, where amyloplasts or chloro-amyloplasts were present, at least during the pre-secretory stage, starch was not detected in the nectary cells of F. meleagris. In the absence of starch, sugars secreted in the nectar are probably delivered by the phloem sap.

Stpiczyńska et al. (2012) also reported the presence of transfer cells with prominent labyrinthine wall ingrowths in the nectariferous cells of F. meleagris. These outgrowths develop in the cells of many organs in plants, as well as in nectaries. They were also noted in fungi. Generally, cells with wall ingrowths are termed transfer cells, since wall ingrowths increase the surface area of the plasma-lemma and thus improve transport capacity (for a review see Offler et al. 2002). In F. meleagris, cell wall ingrowths are particularly prominent on the tangential walls of epidermal and nectariferous parenchyma cells during the stage of maximum secretory activity. The presence of wall ingrowths frequently polarizes the direction of solute flow, and it is possible that cell wall protuberances in F. meleagris facilitate the transport of nectar within the nectary, as well as nectar secretion and nectar resorption during the final stage of anthesis, since these structures persist unchanged in both nectariferous epidermal cells and subepidermal parenchyma (Stpiczyńska et al. 2012). These authors also showed that nectaries commence secretory activity, and small droplets of nectar appear on the surface of the nectary, just as the floral buds are opening (Stpiczyńska et al. 2012). The availability of secreted nectar increases concomitantly with anthesis, and the whole nectary groove becomes filled with nectar. Nectar remains on the nectary surface until the final stage of anthesis, but then disappears. This coincides with the tepals losing their turgor, and the flower reassuming a bud-like form. The period of maximum nectar secretion overlaps with that of maximum pollen presentation and stigmatic receptivity. Accumulation of rewards (nectar and pollen) at a given time may enhance the attractiveness of the flower to pollinators, and allow maximum benefit to be gained from just a single visit. This is particularly important since the frequency of pollinator visits to the flowers of F. meleagris is relatively low (0.2 visits per flower per h; Zych and Stpiczyńska 2012).

Stpiczyńska et al. (2012) also demonstrated that a single tepalar whorl, on average, secreted 5.4 ± 6.6 mg of nectar, whereas a single flower secreted 10.9 ± 13.0 mg of nectar. These authors also observed differences in nectar production from year to year. When perianth whorls were considered separately, the inner three tepals (inner whorl) produced approximately 20% more nectar than the outer whorl. In F. meleagris, the nectar concentration varied between 3–75%, and had an average sugar concentration that exceeded 50% (means calculated across years and floral stages). However, both nectar production and concentration depended on the floral stage being sampled (Fig. 3), with the highest scores, on average, being obtained for flowers displaying full anthesis (21.7 ± 16.8 mg; 70.5% mass and concentration, respectively) and the lowest obtained towards the end of anthesis (1.3 ± 2.69 mg; 16.9% mass and concentration, respectively). Intermediate results were obtained for flowers at the commencement of anthesis (9.8 ± 5.81 mg, 44% mass and concentration, respectively). A significant decline in the mass of nectar and nectar concentration during the final stage of anthesis indicated that nectar resorption occurs in the flowers of F. meleagris. Nectar resorption is a long-known phenomenon, but has rarely been addressed in studies based on nectar secretion (Nepi and Stpiczyńska 2008), and has generally been demonstrated (as in Fritillaria) only for the final stage of anthesis, as a post-pollination phenomenon, or following the completion of sexual stages in dichogamous flowers. It was generally considered to be a resource-recovery strategy resulting at least partially in the recycling of metabolites invested in nectar production. Moreover, it was thought that the modulation of two contrasting processes (nectar secretion and nectar resorption) resulted in homeostasis and maintained nectar composition within a narrow range appropriate for pollinators (Nepi et al. 2007). Reclamation of nectar components in Fritillary is facilitated by the presence of micro-channels or pores in the cuticle of the secretory epidermis (Stpiczyńska et al. 2012). Moreover, the efficiency of nectar resorption (and also secretion) may be further improved in this species by the persistence of wall ingrowths in nectariferous epidermal and parenchymatous cells, even during the final stages of anthesis, when nectar resorption occurs.

The nectar of F. meleagris is composed of sucrose, glucose and fructose (Rix and Rast 1975; Stpiczyńska et al. 2012). Detailed analysis, provided by the latter authors, showed that these sugars appear in approximately equal quantities, with the amount of fructose slightly exceeding that of glucose and sucrose in the nectar profile for all stages investigated (33:28:39; sucrose: glucose: fructose ratio expressed as the relative percentage of total sugars; means calculated across all flowering stages). No other sugars were detected in the nectar. Furthermore, nectar composition did not change significantly during subsequent stages of flowering. As shown by these authors, all nectar sugar constituents in Fritillaria nectar were resorbed to a similar degree, since the proportion of individual sugars at the final stage of anthesis remained almost unchanged.

Floral Scents
An overview of F. meleagris floral odors was given by Hedström (1983), who analyzed floral scent by means of GC/MS and found it to contain terpene, ketone and alcohol components. Methyl vinyloketone, α-pinene, β-pinene, myrcene, linalool oxide, decanal, linalool, α-farnesene, and possibly 4-methyl-2-pentanol, were identified for the scent profile, as well as other compounds.

Floral Visitors and Pollinators
Ever since the study by Knuth (1899), F. meleagris has been regarded a bumblebee-pollinated species. However, published records show that throughout its geographical range, flowers of this species are visited by almost 30 insect taxa, mostly Hymenopterans (Table 1). The most exhaustive data relating to insect visits to flowers of F. meleagris were recorded by Hedström (1983) and Zych and Stpiczyńska (2012). The latter authors made observations based on four flowering seasons for the largest Polish population of this species. In both cases, the most frequent visitors were bumblebees (Bombus spp.), and some years, these represented 100% of floral visitors to the Polish population (Zych and Stpiczyńska 2012). Visits by non-bee insects were reported to be extremely rare. This is in accordance with the observations of Knuth (1899), who, for a German population of F. meleagris, reported that flowers were visited only by B. terrestris (his observations, however, lasted for just one day). In contrast to other insects, e.g., honeybees (Apis mellifera) or solitary bees that appear on Fritillary flowers only during sunny and warm days, bumblebees visited flowers even during adverse weather conditions (Hedström 1983; Zych and Stpiczyńska 2012).

Regarding the quality component of pollination (Herrera 1987; Olsen 1997), some floral visitors, especially flies and beetles, proved to be ineffective pollinators, because they did not come into contact with the sexual parts of the flower or carried very little or no pollen (Hedström 1983; Zych and Stpiczyńska 2012). As shown by Zych et al. (2013), bumblebees and other large-bodied solitary bees (e.g., Anthophora plumipes) visit flowers of F. meleagris for nectar, whereas small solitary bees (e.g., Andrena spp.) visit for pollen. The large bees usually cling to sepals and, during their passage into the flower, they receive pollen on their thorax and wings, which is unlikely to be deposited in the same flower on exit, since these insects tend only to touch the outer part of the stigma, which is not receptive (Knuth 1899; Hedström 1983).

Small Andrena bees usually wander over the androecium and leave flowers with pollen grains that completely cover all their body surfaces. Their visits are generally longer than those of both bumblebees and honeybees (Zych and Stpiczyńska 2012; Zych et al. 2013). This behavior is probably caused by problems encountered by some pollinators while foraging on pendulous flowers (Makino and Thomson 2012) and this orientation of the flower may, in turn, provide an effective strategy for reducing the number of visits to a flower by inferior pollinators (Thomson 2003). Makino and Thomson (2012) demonstrated that generally, bumblebees prefer upwardly-facing flowers, as these are easier to handle and probably reflect the innate preferences of insects. Nevertheless, under field conditions, these insects may concentrate their visits on pendulous flowers, especially if the latter, as is probably the case for F. meleagris, offer a particularly attractive food source. This probably also explains the relatively larger average Fritillaria body pollen loads found by Zych and Stpiczyńska (2012) on small solitary bees, suggesting that, at least in terms of quality, they are perhaps superior pollinators. However, the above authors also showed that these insects simultaneously carry significantly more heterogenous pollen loads that contains a large proportion (>80%) of non-Fritillaria pollen grains, indicating that they readily switch to other floral resources, whereas bumblebees and honeybees appear to be more faithful floral visitors (>90% of Fritillary pollen in an average body pollen load). However, body pollen load is just one criterion used to estimate the effectiveness of a pollinator, and is not necessarily the best (Adler and Irwin 2006; Zych et al. 2013). In order to determine more precisely the effectiveness of an insect pollinator, direct methods are preferable, e.g., pollen deposition on a stigma by a given pollinator species, seed set following visits by insects or the exclusion of particular pollen vectors (Johnson and Steiner 2000; Pellmyr 2002; Willmer 2011). The results of such a survey were presented by Zych et al. (2013) for an ex situ population of F. meleagris located at the University of Warsaw Botanic Garden (Warsaw, Poland). In a small garden compartment, these authors established a regular 10 × 5 grid of test tubes containing water, where they provided virgin flowers, each at the stage of pollen presentation. As the experiment was located at the very center of the city, a small beehive and a commercially available colony of Bombus terrestris were placed in the vicinity of experimental plants in order to saturate the local pollinator community. Following a single visit by a bee to an experimental flower, the flower was collected and its stigma and anthers removed for further examination of stigmatic pollen load (pollen deposition) and pollen removal, respectively. These authors showed that flowers of this ex situ population, like those growing under natural field conditions, were serviced by overwintered, wild bumblebee queens and solitary bees. However, they did not observe any visits by individuals from the introduced honeybee or bumblebee colonies.

Pollen deposition did not differ significantly between the three functional groups that visited the flowers (Bombus spp., Anthophora plumipes males and Andrena spp.), and a single visit resulted, on average, in the deposition of 5715 ± 5954 Fritillaria pollen grains per stigma (mean ± SD)—sufficient to fertilize all ovules. At the same time, pollinators removed from each flower 18–37% of available pollen grains, but this varied greatly according to taxon, and consequently, the authors were not able to detect significant differences between visitor guilds. The estimated pollinator efficiency of pollen transfer was 5.8–7.6%, and approximately 1.3–2.2% of pollen produced by an individual Fritillary flower reached a conspecific stigma during a single visit. Given the dominance of Bombus visitors in all published records of F. meleagris pollination (Knuth 1899; Hedström 1983; Zych and Stpiczyńska 2012; Zych et al. 2013), the above results confirm that they are the most effective pollinators of this species throughout its geographical range in terms of both quality and quantity.

Concluding Remarks
Fritillaria meleagris is a threatened plant species throughout its geographical range (Schnittler and Günther 1999), and its populations are generally in decline (Zhang and Hytteborn 1985; Horsthuis et al. 1994; Iljanić et al. 1998; Čačko 2005; Cheffings and Farrell 2005; Piórecki 2005; Tomović et al. 2007; Andrienko and Tchorney 2009). The plant is zoogamous and mostly outcrossing, and is pollinated by bumblebees, insects that generally show a reduction both in population size and species diversity (Kosior et al. 2007; Goulson et al. 2008), indicating that pollination and subsequent seed production is a “demographically sensitive life history stage” (sensu Schemske et al. 1994). However, the pollination biology and breeding system characteristics of the species do not explain its decline, at least in Poland (Zych and Stpiczyńska 2012; Zych et al. 2013). All reported cases (Knuth 1899, Hedström 1983; Zych and Stpiczyńska 2012; Zych et al. 2013) show that Fritillary flowers are serviced mainly by B. lapidarius, B. ruderarius and B. terrestris, bumblebee species that are generally common (Pawlikowski 1996; Goulson 2003), and in some cases have even extended their range (MacDonald 2001; Dafni et al. 2010). Zych et al. (2013) also showed that this plant can be successfully pollinated by other floral visitors, even when present in relatively small populations. These authors, however, reported that a small population may be less attractive to honeybees or bumblebee workers, suggesting that there may be a “threshold” population size below which it no longer remains an attractive food source for certain pollinators. This well-known phenomenon of insect foraging, namely, floral constancy (for a general reference see, e.g., Goulson 2003; Willmer 2011), is generally correlated with the quality of food plant resources, as perceived by pollinators. When floral resources explored by pollinators become scarce, pollinators switch to other food sources, even when the original plant offers a larger reward per-flower. There is currently no data available on this phenomenon for F. meleagris, and breeding system experiments showed no pollen limitation for the large, natural population studied by Zych and Stpiczyńska (2012). Nevertheless, in the smaller ex situ population created by these authors at the botanic garden, seed production by pollen-supplemented flowers was greater than in control, open pollinated plants. Although these differences were not statistically significant, and could, as suggested by the authors, be caused by the close genetic proximity of experimental plants, it is possible that they also indicate a decline in plant fertility associated with the reduction in size of the population (the so-called Allee effect; Stephens et al. 1999). If a population reaches a critical density or size, a severe pollen limitation may occur resulting in diminished seed production. Such an effect has been observed for many plant species growing in a range of different habitats (e.g., Lamont et al. 1993; Brys et al. 2004; Cheptou and Avendaño 2006; Elam et al. 2007; Dauber et al. 2010), and is most likely to occur in small populations of Fritillary. Such a situation is probable if habitat fragmentation continues, and the present decline in this species coincides with the Europe-wide loss of traditionally used, extensive wet meadows (Grootjans et al. 1996) and habitat destruction, both the result of the intensification of, or changes to agricultural practices (Piórecki 2005). Smaller populations, which are usually more prone to herbivore attacks (see, e.g., Kolb 2008), can become unattractive to pollinators and suffer from a shortage of pollination events which, in turn, leads to local extinctions. Thus, any attempt to conserve this endangered plant should consider both the conservation of its habitat and its biology, in particular its pollination and breeding strategies.

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