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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