Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2005? 2005
147?
417426
Original Article
FLOWERING PHENOLOGY and REPRODUCTIVE BIOLOGY OF
D. ANGLICA
G. L. MURZA and A. R. DAVIS
Botanical Journal of the Linnean Society, 2005, 147, 417–426. With 11 figures
Flowering phenology and reproductive biology of Drosera
anglica (Droseraceae)
GILLIAN L. MURZA and ARTHUR R. DAVIS*
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, Canada S7N 5E2
Received August 2004; accepted for publication October 2004
Prompted by the sparse knowledge of the reproductive biology of carnivorous plants, compared with studies of their
trapping habits, we investigated the flowering phenology and pollination biology of Drosera anglica Huds. in two fens
in mid-western Canada. Seed set and germination were used to compare the effectiveness of a series of pollination
treatments, including single insect visits to virgin flowers. Flowers opened during mid-morning but closed by early
afternoon, and exhibited pseudo-cleistogamic behaviour in cool, overcast weather. D. anglica was found to be selfcompatible, and able to self-pollinate and self-fertilize. Geitonogamy was an uncommon mode of self-reproduction
because plants typically possessed a lone inflorescence upon which a single, short-lived flower opened, a few days
before the next bud reached anthesis. Insect visits to the fragrance-lacking, nectarless flowers, chiefly by flies
(Diptera: Syrphidae), were infrequent (one visit per 1 h 40 min of observation), and the low frequency of seed set and
low numbers of seeds per fruit in pollination treatments involving insects, suggest the species does not rely on insects
to effect pollination. Self-pollination, with or without the aid of a vector (insects, wind) was as effective as natural
pollination; ultimately, autogamy is chiefly responsible for natural seed set. Thus, the species exhibits characteristics
of facultative autogamy. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005,
147, 417–426.
ADDITIONAL KEYWORDS: facultative autogamy – oblong-leaved sundew – pollination – seed germination
– seed set – single insect visits – Syrphidae.
INTRODUCTION
The plant–arthropod interactions of carnivorous
plants known as sundews (Droseraceae: Drosera) have
been exhaustively studied in terms of trap biology (see
Juniper, Robins & Joel, 1989 and references therein;
Thum, 1986, 1988, 1989; Gibson, 1991; Verbeek &
Boasson, 1993) and the importance of arthropod prey
for their growth and reproduction has long been
known (Darwin, 1878; Kellermann & von Raumer,
1878, cited in Thum, 1988). In contrast, only a single
known study has ascertained the importance of
insects in the pollination biology of a Drosera species,
D. tracyi (Wilson, 1995). Furthermore, there are few
recorded observations of flower visitors to other
Drosera species (D. cistiflora and D. pauciflora:
Goldblatt, Bernhardt & Manning, 1998; D. parvula
and D. macrantha ssp. macrantha: Lowrie, 2001;
*Corresponding author. E-mail: [email protected]
D. rotundifolia: Engelhardt, 1998; Scott Elliot, cited in
Knuth, 1908), and these were not rigorous studies
allowing determination of whether the observed visitors were indeed pollinators.
With respect to additional attributes of the reproductive biology of the genus, Knuth (1908) and Hansgirg (cited by Knuth) reported that most Drosera
flowers, including those of D. anglica, D. intermedia,
and D. rotundifolia, are cleistogamous (bud-like flowers that remain permanently closed and self-fertilize)
or ‘pseudo-cleistogamous’ (normally chasmogamous
flowers, which under circumstances of deficient light,
warmth, high water levels or strong currents, remain
closed yet fertilize). Although many Drosera species
are self-compatible and reportedly able to self-pollinate and self-fertilize without the aid of a vector (see
Pietropaolo & Pietropaolo, 1986), Chen, James &
Stace (1997) have reported that of 20 Western Australian Drosera species (19 clonal perennial, one annual),
17 are self-incompatible and only three are selfcompatible (two clonal, one annual). In their descrip-
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
417
418
G. L. MURZA and A. R. DAVIS
tion of sundews of the British Isles, Crowder et al.
(1990) stated that D. anglica, D. intermedia and
D. rotundifolia are able to reproduce by apomixis, but
no methodology or specific results were provided.
Drosera anglica Huds., commonly known as the
oblong-leaved or English sundew, is found in fens and
pond edges across the boreal forest throughout the
northern hemisphere (Johnson et al., 1995). Arising
from the centre of the perennial rosette of trap leaves
is an elongate, leafless stalk that bears a raceme of one
to several small (6–7 mm; Schnell, 1995), perfect
(bisexual), pentamerous, actinomorphic flowers possessing white petals (Murza & Davis, 2003).
Recognizing the paucity of investigations of the
reproductive biology of Drosera, the pollination biology of D. anglica was studied with the following
objectives: to determine (1) its flowering phenology; (2)
whether or not the species is self-compatible; (3)
whether a vector is required for pollination; and (4)
the role of various insects as pollinators.
MATERIAL AND METHODS
PLANT
MATERIAL
During July and August of 2000 and 2001, field-work
involving Drosera anglica Huds. was conducted in
two fens (site 1: 52∞57.556¢N, 106∞04.378¢W; site
2: 52∞57.914¢N, 106∞04.042¢W) within the Macdowall
Bog Protected Region located in the Nisbet Provincial
Forest of central Saskatchewan, Canada. Voucher
specimens are housed at the W. P. Fraser Herbarium
(SASK), University of Saskatchewan.
FLOWERING
PHENOLOGY
To determine attributes of floral phenology, a sample
of 25 plants at site 1 was observed daily throughout
the flowering period in July 2000. The sample was
restricted to those plants (the vast majority) that had
more than one flower per inflorescence, so that the
numbers of flowers open per day per plant and the
interval between flowering days per plant (to assess
the possibility of geitonogamy) could be ascertained.
POLLINATION
TREATMENTS
Six pollination treatments (see below) were applied to
flowers at random to investigate their pollination biology. Mature fruits (loculicidal capsules) from these
experimental flowers were harvested before dehiscence and seed set used to estimate fertilization success. Experiments were restricted to plants having
more than one flower per inflorescence due to potentially limiting maternal effects which may nonrandomly favour only a single flower, i.e. if resources for
seed set are shunted only into a single developing fruit,
rather than into several fruits, as is the case with multiple developing fruits on an inflorescence (Stephenson, 1981). The number of buds per plant used in the
experiment was recorded and compared to assess any
difference in bud production between year and site.
Since typically only one flower per inflorescence
opens per day, each flower was considered an experimental unit. Only one bud per plant was used in the
pollination study, selection of bud position being random. One day prior to anticipated anthesis, each inflorescence was covered with a fine mesh bag [openings
were approximately triangular in shape with
maximum dimensions of 0.25 mm (base) by 0.6 mm
(height)] to exclude any potential pollinators and
hence, introduced pollen. Bags were placed over entire
inflorescences rather than individual flowers due to
the small flower size and delicate nature of pedicels. A
series of small wooden stakes (medical swab sticks)
inserted into the substrate supported the weight of the
bagged inflorescences.
Pollination treatments were: (1) bagged; (2) bagged
and emasculated; (3) bagged and self-pollinated by
hand; (4) emasculated and open-pollinated; (5) openpollinated, and (6) bagged and emasculated, but the
bag being removed at anthesis to allow a single insect
visit (see next subheading).
The numbers of flowers utilized in each of the first
five treatments were: 2000 – site 1: 12–19, site 2: 8–14;
2001 – site 1: 18–26, site 2: 19–37. Note that emasculations were performed on the day of anthesis, but
prior to anther dehiscence. For treatment 3, bags were
removed at dehiscence and the flowers hand-pollinated by gently touching the anthers to stigmas (to
simulate autogamous pollination). In so doing, all
available pollen per flower was used in the hand selfpollinations. Inflorescences remained bagged for two
full days following anthesis of experimental flowers, to
ensure exclusion of visitors.
The rationale for the selected treatments is as follows. If flowers from treatment 1 set seed, then autogamy has occurred, and the species is able to selfpollinate and self-fertilize without the aid of a vector.
If flowers from treatment 2 set seed, then some pollen
may be getting through the bag via wind or transported by very small arthropods, or apomixis may be
occurring. If flowers from treatment 3 set seed, then
the species is self-compatible. If flowers from treatment 4 or 6 set seed, then the species may be xenogamous. The particular value of treatment 4 is that it
allows distinction between facultatively autogamous
and facultatively xenogamous plants, because autogamous flowers are visited infrequently by pollinators
and will rarely set fruit, whereas facultatively xenogamous flowers are visited more often by insects and
will likely set fruit (Kearns & Inouye, 1993). Treat-
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
FLOWERING PHENOLOGY AND REPRODUCTIVE BIOLOGY OF D. ANGLICA
ment 5 allowed estimates of natural seed set, either by
autogamous or xenogamous means.
The germinability of seeds resulting from the various treatments was tested. Once seed sets were quantified, seeds were stratified (recommended for all
Drosera that form winter buds: Pietropaolo & Pietropaolo, 1986) on damp unbleached cotton, in sealed,
plastic bags in the refrigerator at 4 ∞C, for 22–
25 weeks (2000) or 14–20 weeks (2001). The shorter
stratification period in 2001 was given due to a perceived loss of seed germinability resulting from prolonged stratification. Seeds were surface sterilized
using 0.6% solution of sodium hypochlorite for 10 minutes, before rinsing three times in sterilized distilled
water. Seeds of each capsule were plated onto sterile
0.7% agar media (pH 5.0) in their own sterile Petri
dish, which was double wrapped in Parafilm, and then
germinated in a growth chamber using a 14 h light/
10 h dark photoperiod (light intensity 228 mE m-2 s-1)
and 20/10 ∞C temperature regime. Here, seed germination refers to full emergence of the radicle from the
seed coat. Final percentage germination was recorded
on day 45.
SINGLE
INSECT VISIT STUDIES AND INSECT
IDENTIFICATION
In treatment 6, flowers were emasculated and bagged,
but the bag was removed at anthesis to permit one
insect visit, thereby allowing the relative contribution
of different insects to pollination to be determined
(Davis, 1997). During single visits, flower visitors were
watched closely to determine what reward, if any, was
being sought, and the duration of the visit was
recorded. Once a visit was complete, the flower was rebagged and attempts to capture the visitor made. Captured insects were transferred individually to a clean
glass vial to avoid any potential contamination with
D. anglica pollen from other visitors, frozen, and
pinned for future identification. Using the dissecting
microscope, they were inspected for the distinctive
yellow, pollenkitt-coated tetrads of echinate pollen
grains of D. anglica. The only other members
of Saskatchewan Droseraceae, D. linearis and
D. rotundifolia, produce pollen that is orange and
white, respectively (Wood, 1955). Scanning electron
microscopy of the bodies of a few visitors was utilized
to confirm the adherence of D. anglica tetrads. Insects
were mounted directly on aluminium stubs using double-sided tape before gold-coating (Edwards Sputter
Coater, S150B) and examination with a Philips 505
SEM at 30 kV. Photographs were taken with Polaroid
665 positive/negative film. Images scanned with a
CanoScan D660U (Canon Inc., Tokyo, Japan) were
enhanced using ArcSoft Photostudio (ArcSoft Inc,
Freemont, CA, USA).
419
Single visits were attempted at both sites in both
years. The total observation time devoted to them in
2000 was 327 min at site 1 (N = 7 flowers), and
213 min at site 2 (N = 7). In 2001, virgin flowers were
watched for 150 min at site 1 (N = 4), and for 509 min
at site 2 (N = 11). Flowers not visited during the observation periods were eventually treated as emasculated
and open-pollinated (4). The results for the single visit
treatment (6) are analysed separately from the other
five treatments because different flower visitors were
involved for each visit.
All captured flower visitors were identified to genus,
or further when possible, using keys of Robinson
& Vockeroth (1981), Shewell (1987) and Vockeroth
(1992). Representative specimens were then sent to
experts for verification or further identification.
Voucher specimens are housed in the Entomology
Museum of the Department of Biology, University of
Saskatchewan.
STATISTICAL
ANALYSES
Mean number of buds per plant and differences
between pollination treatments in terms of seed set
per fruit and seed germinability, were assessed using
an analysis of variance (ANOVA: General Linear
Model). The terms year, site and their interactions
were considered random effects and treatment was
considered a fixed effect in analyses, unless otherwise
stated. When factors and/or their interactions were
significant, Tukey multiple comparison tests were performed to determine where the significant differences
occurred. SAS (SAS Institute Inc., Cary, NC, USA) was
used to perform all analyses.
Due to heterogeneous variation in the seed set data,
a natural log transformation [ln (X +1)] was used to
equalize variation. The two emasculation treatments
(2, 4) had to be excluded from statistical tests because
the capsules contained no germinable seeds, except for
a few capsules that were atypical from the rest of the
data set. Although theoretically the terms year and
site should be considered random terms in this statistical model, they were treated as fixed, so that inconsistencies in the data sets could be addressed.
For the seed germination data, an arcsine conversion [ arcsine( proportion ) ] of the data was applied
before statistical comparisons were made, as recommended for percentage data by Sokal & Rohlf (1981).
RESULTS
FLOWERING
PHENOLOGY
At site 1 in 2000, the average number of buds per
plant was 2.84 ± 0.25 (mean ± SE, N = 25 plants),
and the mean interval between flowering days was
3.55 ± 0.35 days (for all buds per plant, vs. 3.66 ± 0.50
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
420
G. L. MURZA and A. R. DAVIS
for only buds that opened; see below). No plant in the
census produced more than one inflorescence. The
mean flowering period per plant was 5.62 ± 0.60 days.
Typically, only one flower per inflorescence opened per
day, but there was one two-flower plant, and one threeflower plant. When more than one flower was open
per plant, the most basal flower appeared normal,
whereas the remaining open flowers typically
appeared abnormal (stigmas and stamens stunted, little pollen produced). Thus, the possibility that geitonogamy might have occurred is unlikely, given that
only a single flower appeared reproductively normal
when more than one flower was open per plant. The
flowering period commenced 6 July and ceased 27 July
2000, with the phenology study beginning 10 July.
There were two peaks (15 and 22 July) of flowering
interrupted by five nonflowering days (16–20 July).
The lack of flowering during this time is closely
related to the cool temperatures (Fig. 1). Fourteen
buds on 11 plants never opened; ten remained closed
during the five nonflowering days, whereas the other
four remained closed on typical flowering days.
Flowers opened only on a single day for as much as
5 h, with the timing of phenological events varying
with the weather conditions. For example, on warm,
clear, sunny days, flowers began to open mid-morning
(09:05-10:40 h CST), with anther dehiscence occurring shortly after corollas began to expand (09:25–
10:10). Corollas were reflexed by late-morning (09:45–
11:00) and closed by early afternoon (14:23–14:40). On
sunny days, flowers became fully reflexed, but on cool
or overcast days, flowers only opened to 1/3–1/2 of
their maximum diameter, or never opened at all (see
above). On clear, sunny days that became suddenly
overcast, the flowers closed earlier (13:15) than on constantly clear days.
There was an effect of site on number of buds per
plant (F1,1 = 190.40, P = 0.05), the mean number per
inflorescence being significantly higher at site 2 than
at site 1 (Table 1). There was no effect of year
30
16
Open flowers/ da y
14
25
12
20
10
15
8
6
10
4
5
Open flowers per day (N)
Mean temperature (°C)
Mean daily temperature
2
(F1,1 = 2.05, P = 0.39) or of the site and year interaction
(F1,396 = 0.24, P = 0.62). Note that the number of buds
per plant for site 1 in 2000 includes the buds used in
the phenology study (N = 25). The flowering season
began earlier in 2001 (site 1: 1–21 July; site 2: 26 June
-19 July) than in 2000 (site 1: 6–28 July; site 2: 14
July -1 August), probably owing to the difference in
weather conditions. In 2001, the weather during the
growing season was hot and dry (ranges of -0.3 to
+2.3 ∞C of normal temperature and 17–103% of normal rainfall), whereas in 2000, the conditions were
comparatively cooler, with greater precipitation (-1.5
to +0.5 ∞C of normal temperature and 94–139% of normal rainfall) (Table 2).
POLLINATION
TREATMENTS
Comparison using seed set
Capsules were harvested immediately prior to dehiscence (2000 - site 1: 32.44 ± 0.65 days from anthesis to
capsule maturity, site 2: 31.24 ± 0.46; 2001 - site 1:
29.89 ± 0.32, site 2: 28.57 ± 0.38). At harvest, 11% (42/
366) of the total number of capsules were missing from
Table 1. Mean number of buds (> 1) per plant (N) of Drosera anglica at two sites censused over 2 years. Means
followed by different letters are significantly different at
the 0.05 level
Year
Site
N
Mean ± SE
2000
1
2
1
2
107
56
108
129
2.62 ± 0.11a
3.45 ± 0.20b
2.59 ± 0.07a
3.31 ± 0.09b
2001
Table 2. Comparison of mean monthly temperature and
total rainfall over the growing season of two consecutive
years (2000, 2001) at the Macdowall Bog Protected Region,
Nisbet Provincial Forest, SK, with long-term normals
(1971–2000). Records for 2000 and 2001 are for the Macdowall weather station. Records for normals are for the
Prince Albert weather station, located approximately
28 km north-east of Macdowall, SK
Mean temperature (∞C)
Year
Total rainfall (mm)
Year
Month
2000
2001
normal
2000
2001
normal
June
July
August
13.7
18.0
15.9
14.9
18.8
18.6
15.2
17.5
16.3
101.0
92.3
54.8
28.0
79.0
9.6
72.5
76.8
58.0
0
0
10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
July 2000 date
Figure 1. Daily mean temperature and number of Drosera
anglica flowers open per day from 25 plants censused over
the flowering period (10–27 July 2000) at site 1.
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
FLOWERING PHENOLOGY AND REPRODUCTIVE BIOLOGY OF D. ANGLICA
421
Table 3. ANOVA results for seed set per capsule [ln (X +1)] and per cent germination [ arcsine( proportion ) ] of Drosera
anglica for three pollination treatments conducted at two sites
Seed set per capsule
Source of variation
Year (Y)
Site (S)
Treatment (T)
Y¥S
Y¥T
S¥T
Y¥S¥T
Error
d.f.
1
1
2
1
2
2
2
153
F
11.96
0.13
10.59
1.41
4.65
2.44
3.98
experimental plants, due to senescence of the inflorescence prior to capsule maturation, and possibly to
herbivory. Thus, of the initial experimental fruits, 92
and 93% were harvested in 2000 at sites 1 and 2,
respectively, while in 2001, 85 and 87% were harvested at sites 1 and 2, respectively. Seventeen per
cent (56/324) of the remaining capsules were excluded
from seed set analyses for the following reasons: (1)
flowers never opened (2000); (2) pollen contacted stigmas during emasculations; (3) capsules were harvested after dehiscence began, resulting in potential
seed loss; and (4) stigmas and anthers appeared
abnormal. Accordingly, of the harvested capsules in
2000, 75% (54/72) were used in the seed set analyses
for site 1, and 80% (41/51) for site 2. In 2001, 88% (80/
91) of the capsules at site 1, and 85% (93/110) at site 2,
were included in seed set analyses. As a point of interest, those flowers that did not open were indeed capable of setting seed; 29% (N = 7) and 100% (N = 3) of
bagged and open-pollinated flowers, respectively, set
fruit.
The two emasculation treatments (2, 4) excluded
from statistical tests did result in seed set within a few
capsules, atypical from the rest of the data set (zero
seed set), as follows: bagged and emasculated treatment (2) [2000 – 2/13 capsules (site 1), 0/6 (site 2);
2001 – 2/14 (site 1), 1/14 (site 2)]; emasculated and
open-pollinated treatment (4) [2000 – 1/10 capsules
(site 1), 1/10 (site 2); 2001 – 4/17 (site 1), 3/19 (site 2)].
Statistical comparisons for the remaining treatments [bagged (1), bagged and self-pollinated by hand
(3), and open-pollinated (5)] revealed no effect of site
on seed set, but there was an effect of year and of
treatment (Table 3). There was no effect of the year
and site interaction, or of the site and treatment interaction. However, there were significant interactions
between year and treatment, and between year, site
and treatment.
To better understand the reasons behind the significance of certain effects and their interactions, a series
Per cent germination
P
d.f.
1
1
2
1
2
2
2
130
0.001
0.72
< 0.001
0.24
0.01
0.09
0.02
F
4.02
0.51
0.09
4.45
0.46
6.88
0.26
P
0.35
0.54
0.92
0.17
0.69
0.13
0.77
Table 4. Transformed means [ln (X + 1)] of seed set per
capsule (N) of Drosera anglica for three pollination treatments (T1, bagged; T3, bagged and self-pollinated; T5,
open-pollinated) conducted at the two sites. Means followed
by the same letter are not significantly different at the 0.05
level
Year
Site
Treatment
N
Mean ± SE
2000
1
T1
T3
T5
T1
T3
T5
T1
T3
T5
T1
T3
T5
7
10
14
9
8
8
15
14
20
21
14
25
3.32 ± 0.44abcd
1.76 ± 0.37a
3.79 ± 0.31cd
4.09 ± 0.39cd
1.96 ± 0.41ab
2.33 ± 0.41abc
3.51 ± 0.30bcd
3.18 ± 0.31abcd
3.51 ± 0.26bcd
3.73 ± 0.25cd
3.40 ± 0.31bcd
3.98 ± 0.23d
2
2001
1
2
of Tukey tests was conducted to compare the transformed means [ln (X +1)] of the three pollination treatments included in the model [bagged (1), bagged and
self-pollinated by hand (3), open pollinated (5)] at both
sites in both years (Table 4). At both sites, consistently
low seed set occurred in the bagged and self-pollinated
by hand treatment (3), compared to the bagged (1) and
open-pollinated (5) treatments in both 2000 (except
open-pollinated treatment (5) at site 2) and 2001. The
comparatively low seed set for the open-pollinated
treatment (5) at site 2 in 2000 would have been closer
to all other open-pollinated treatments (5), had it not
been for three of the eight capsules not setting any
seed.
In 2001, the quantities of seeds set in all three treatments at both sites were not significantly different
from each other, nor were they different from the open-
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
422
G. L. MURZA and A. R. DAVIS
2
4
3
5
7
9
6
8
10
11
Figures 2–11. Scanning electron and light micrographs of flower visitors (Diptera, Syrphidae) of Drosera anglica. Figs 2–
6. Toxomerus marginatus. Figs 7–11. Trichopsomyia sp. Fig. 2. Lateral view. Fig. 3. Dorsolateral view showing individual
pollen tetrads on the wing margin, calypter and scutellum (arrows). Fig. 4. Tetrad on sensilla of the wing margin, as in
Fig. 3. Fig. 5. Tetrad on sensilla along margin of calypter, as in Fig. 3. Fig. 6. Tetrad on dorsal surface of scutellum, as in
Fig. 3. Fig. 7. Lateral view. Figs 8, 9. Tetrad on the lateral surface of the thorax. Figs 10, 11. Tetrads on the ventral surface
of the abdomen. Scale bars: Figs 4–6, 9, 11 = 50 mm; Figs 2, 3, 7, 8, 10 = 1 mm.
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
FLOWERING PHENOLOGY AND REPRODUCTIVE BIOLOGY OF D. ANGLICA
pollinated (5 at site 1) or from the bagged treatments
(1) in 2000. If the results of the bagged and self-pollinated treatments in 2001 are taken into account, the
statistical comparisons generally suggest that seed
sets in the bagged, bagged and self-pollinated by hand,
and open-pollinated treatments are not significantly
different.
Comparison using seed germination
Results of the analysis of variance for three pollination treatments [bagged (1), bagged and self-pollinated by hand (3), open-pollinated (5)] indicate no
significant differences in seed germination between
year, site, treatment, or their interactions (Table 3).
Thus, the seed produced in all three treatments germinated equally, with a mean of 38.1 ± 3.0% (N = 142).
SINGLE
INSECT VISIT STUDIES
Attempts to study visits by insects to previouslyunvisited, emasculated receptive flowers were made
with varying success [2000 – 4/7 flowers visited (site
1), 1/7 (site 2); 2001 – 1/4 (site 1), 6/11 (site 2)], resulting in a total of 12 observed insect visits. All visitors
to virgin flowers were adult dipterans, with 6/12
being captured and identified as members of the
family Syrphidae [flower or hover flies; Neoascia
sp. (N = 1), Orthonevra pulchella (Will.) (N = 2), Toxomerus marginatus (Say) (N = 2), Trichopsomyia sp.
(N = 1)]. Of the six visitors not captured, four were
tentatively identified as members of the Calliphoridae [blow flies; Phormia regina (Meigen)
(N = 2)], Dolichopodidae [long-legged flies; Dolichopus
sp. (N = 1)], as well as an additional member of the
Syrphidae [Syrphus sp. (N = 1)], whereas two could
not be further identified. Visit duration by all flies
was short (3.7 ± 0.6 s), and behaviour varied from
briefly alighting on the flowers, to searching for
rewards (pollen present, nectar absent). These particular visitors never alighted on nearby flowers in the
area (with one exception, calliphorid) after completing their visits to the D. anglica flowers, making
capture difficult. Of the captured visitors, only two
individuals, both taken from site 2 in 2001, carried
the distinctive pollen tetrads of D. anglica (Orthonevra pulchella, on a mesothoracic leg; and Trichopsomyia sp., on prothoracic and metathoracic legs).
Other specimens of these syrphid taxa collected following visits to nonexperimental, nonemasculated
flowers were found to carry tetrads of pollen on the
thorax, wings, and/or abdomen (Figs 2–11).
Of the 12 capsules harvested following these insect
visits to virgin flowers, one was lost due to senescence
of the entire flower stalk. The only visit that apparently resulted in pollination, and subsequent seed set,
was that by an unidentified dipteran in 2000. How-
423
ever, when tested for germination along with the seeds
from all other pollination treatments, none of the ten
seeds from this capsule germinated.
DISCUSSION
FLOWERING
PHENOLOGY
The flowering phenology of Drosera anglica (i.e. a single flower opens per inflorescence every 3-4 days in
the mid-morning and closes by early afternoon) is similar to that of D. rotundifolia in California (Engelhardt, 1998: one flower per inflorescence opens every
second day between 10:30 and 12:30) and D. tracyi in
Florida (Wilson, 1995: one flower opens daily per inflorescence between 07:00 and 12:45). In these studies
there was only a single inflorescence per plant. These
observations also discount geitonogamy as a major
form of reproduction, if indeed it occurs at all. No evidence of true cleistogamy was found for D. anglica,
although observations in this study during a brief
period of cool (9.3–14.5 ∞C), overcast weather do support Knuth (1908) in that they offer evidence for
pseudo-cleistogamy (i.e. flowers that never opened setting fruit), which Crowder et al. (1990) had reported
frequently for D. anglica in cloudy or wet weather in
the British Isles.
POLLINATION
BIOLOGY
The low seed set of the bagged and self-pollinated treatment (3) in 2000 compared to 2001 (Table 4) is intriguing and may be due to differences in experimental
procedure. Hand pollinations for treatment 3 were performed at both sites each day in 2000, and were performed last, up to 3 h after the other treatments. In
2001, flowers were pollinated by hand only at a single
site each day, as soon as anther dehiscence occurred, to
ensure that any loss of stigma receptivity or pollen viability did not occur. Preliminary studies of pollen viability suggest that pollen is still germinable on stigmas
up to 5 h following dehiscence (Murza, 2002), basically
the entire duration of anthesis, but whether its viability remains constant has not been determined. Future
research on the precise period of peak pollen viability
and the duration of stigma receptivity is required if further studies are to be attempted. Interestingly, reduced
seed set resulting from hand-pollinations was also
encountered by Engelhardt (1998) on D. rotundifolia in
California, and by Ortega Olivencia, Carrasco Claver &
Devesa Alcaraz (1995) on Drosophyllum lusitanicum,
another droseracean species, in Spain.
Comparisons of the treatments in terms of seed set
and germination indicate that D. anglica is self-compatible [germinable seed was set in the bagged and
self-pollinated by hand treatment (3)] and able to selfpollinate and self-fertilize without the aid of a vector
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
424
G. L. MURZA and A. R. DAVIS
[germinable seed was formed in the bagged treatment
(1)] as reported by Crowder et al. (1990). Furthermore,
self-pollination, with or without the aid of a vector,
may be as effective as natural pollination [generally
no significant differences between seed set or germination of bagged (1), bagged and self-pollinated by
hand (3), and open-pollinated (5) treatments]. These
findings suggest that autogamy may be the predominant form of reproduction. The low frequency of seed
set in the emasculated and open-pollinated treatment
(4) offers additional support for this contention, since
emasculated and open-pollinated flowers rarely set
fruit in facultatively autogamous species due to
infrequent pollinator visitation (Kearns & Inouye,
1993). Similarly, Engelhardt (1998) reported that
D. rotundifolia has a facultatively autogamous breeding system and does not rely on a vector to effect pollination. Furthermore, D. anglica has a low pollen to
ovule ratio of 9.1 (Murza & Davis, 2003), between the
ranges reported for cleistogamy and obligate autogamy by Cruden (1977). Based on comparisons to ovule
numbers (mean of 115 ovules/capsule; Murza & Davis,
2003), it is evident that seed set (Table 4) was rarely
maximal, compared with 95% following hand pollinations in D. tracyi (Wilson, 1995).
Another possible mode of reproduction for D. anglica
is apomixis, since seed set did occur in the bagged and
emasculated treatment (2). Crowder et al. (1990)
reported that apomixis may occur infrequently for
D. anglica, D. intermedia and D. rotundifolia. However, there are other potential explanations for seed set
in this treatment. Seeds may have resulted from pollination by very small insects, possibly thrips, which
may have entered the bags surrounding inflorescences,
or from experimentor error that resulted in pollen contacting stigmas. It is conceivable, though unlikely, that
pollen could have entered the bag via wind, since the
pollen tetrads are echinate and covered with pollenkitt,
and thus display features normally associated with
animal rather than wind pollination (i.e. dry, smooth
pollen; Kevan, 1997). However, it has been suggested
that D. anglica and D. rotundifolia may be wind-pollinated (Crowder et al., 1990).
FLOWER
VISITORS
All insect visitors to virgin flowers of D. anglica
were dipterans. Of the flies identifiable beyond order
level (10/12 = 83%), syrphids were most frequent
(7/10 = 70%), followed by calliphorids (20%) and a dolichopodid (10%). Next to bees (Hymenoptera: Apoidea),
dipterans are the second most important order of
anthophilous (flower-visiting) and flower-pollinating
insects, with syrphids being perhaps the most significant anthophiles (Larson, Kevan & Inouye, 2001).
Adult syrphids may be pollenophagous or nectaroph-
agous (or both, in some instances). Calliphorids are
also well-known anthophiles and nectarophages,
while dolichopodids have been noted as nectarophages, although they are infrequent flower visitors
(Larson et al., 2001).
As to the role of insects in the pollination of
D. anglica, their normally brief and infrequent visits
(0.6 visits per h, or one visit per 1 h 40 min of observation), the general lack of pollination effected by
visitors involved in the single visit treatment (6) (one
dipteran from a total of 12 visits), the infrequency
with which they attended another flower upon departure from previously unvisited flowers, as well as the
extremely low frequency of seed set for the emasculated and open-pollinated treatment (4), suggest that
the species does not rely heavily on insects to effect
pollination. The scarcity of insect visits may partially
be explained by the lack of floral nectar production
(Murza & Davis, 2003) or fragrance. Although some
captured visitors did carry D. anglica pollen [2/6
= 33%. Syrphidae - Orthonevra pulchella (1), Trichopsomyia sp. (1)], this finding does not necessarily qualify all observed anthophiles as pollinators, since
visitors must effectively transfer pollen to stigmas
within the duration of pollen viability (see Larson
et al., 2001 and references therein).
Flower visitor guilds to other Drosera species differ
from each other, and from that reported here for
D. anglica. Visitors to Drosera flowers include birds
(D. macrantha ssp. macrantha: Lowrie, 2001), bees
(D. indica: Lowrie, 2001; Susandarini et al., 2002),
and monkey beetles and muscid flies (D. cistiflora and
D. pauciflora: Goldblatt et al., 1998). Although the
behaviour of these visitors suggests that they may
indeed be pollinators, no experiments were conducted
to ascertain their role (i.e. whether they both remove
pollen from anthers and deposit it on stigmas). The
role of insects as pollinators has been established for
D. tracyi, a species which, like D. anglica, is self-compatible yet has comparatively large flowers (22 mm
diameter) that require insects to move pollen (Wilson,
1995). The chief pollinators of D. tracyi were bees, followed by syrphid flies and meloid beetles. Similarly,
in our study, flies were not major pollinators of
D. anglica.
The role of insects in the pollination of carnivorous
plants is potentially problematic, since arthropods are
consumed as prey by the trap leaves. A forthcoming
paper (G. Murza, J. Heaver & A. Davis, submitted)
examines this potential conflict between the flower
visitors and prey of D. anglica.
ACKNOWLEDGEMENTS
We thank Mr Jack Keel, Saskatchewan Environment
and Resource Management, for permission to collect
© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 417–426
FLOWERING PHENOLOGY AND REPRODUCTIVE BIOLOGY OF D. ANGLICA
material from the Macdowall Bog Protected Region,
Joanne Heaver for help with pollination studies in the
field, Professor Emeritus Bob Baker for assistance
with statistics, Mr Don Ryback for supplying temperature and precipitation data, and the following individuals for insect verifications/further identifications:
Mr S. Brooks (Dolichopodidae), Mr B. Cooper (Calliphoridae) and Dr J. R. Vockeroth (Syrphidae). Funding
of this project to G. L. Murza from the following institutions is gratefully acknowledged: Natural Sciences
and Engineering Research Council (NSERC) of
Canada (Postgraduate Scholarship A); Department of
Biology, University of Saskatchewan (Graduate
Teaching Fellowship, Margaret MacKay Scholarship
in Biology, R. Jan F. Smith Memorial Scholarship) and
the Entomological Society of Saskatchewan (Brooks
Scholarship). This research was supported by a Discovery Grant from NSERC of Canada awarded to A. R.
Davis.
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