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Austral Ecology (2012) ••, ••–••
The relative importance of solitary bees and syrphid flies
as pollinators of two outcrossing plant species in the
New Zealand alpine
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MASCHA BISCHOFF,1,2* DIANE R. CAMPBELL,1 JANICE M. LORD2
AND ALASTAIR W. ROBERTSON3
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Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
(Email: [email protected]), 2Department of Botany, Otago University, Dunedin, New
Zealand, and 3Institute of Natural Resources, Massey University, Palmerston North, New Zealand
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Abstract Pollinators vary in their relative contribution to the conspecific pollen deposited onto receptive stigmas,
because of variation in both visitation rate and effectiveness of pollen transfer. Syrphid flies and short-tongued
solitary bees are common flower visitors in alpine New Zealand, yet their relative importance as pollinators is
unknown. We measured pollinator performance of the New Zealand alpine endemics Hylaeus matamoko
(Hymenoptera: Colletidae) and Allograpta spp. (Diptera: Syrphidae) on two New Zealand alpine herbs, Ourisia
glandulosa (Plantaginaceae) and Wahlenbergia albomarginata (Campanulaceae). Ourisia glandulosa received visits by
solitary bees and syrphid flies at equal frequencies, whereas W. albomarginata was mostly visited by H. matamoko.
Based on single-visit pollen deposition to virgin stigmas, H. matamoko was a much more effective pollinator than
Allograpta spp., delivering 10 times as much pollen per visit to O. glandulosa stigmas and 3 times as much to
W. albomarginata stigmas. By multiplying visitation frequency by single-visit pollen deposition, we estimated that
H. matamoko performed 90% and 95% of the pollination of O. glandulosa and W. albomarginata, respectively.
Although H. matamoko bees are short-tongued and small in size, they are critically important to plant reproductive
success in the New Zealand alpine. These bees contributed most of the pollination, even to a species that received
just as many visits by flies, underscoring the need to consider per-visit effectiveness as well as visitation rate in
assessing the importance of different pollinators.
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Key words: alpine plant, Hylaeus matamoko, New Zealand, pollinator effectiveness, syrphid fly.
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INTRODUCTION
Pollinators provide an essential service to terrestrial
ecosystems (Kearns et al. 1998), with approximately
87% of angiosperm species on a worldwide basis pollinated at least in part by animals (Ollerton et al. 2011).
Different species of pollinators can, however, vary considerably in relative importance (e.g. Sahli & Conner
2007). For about four decades, evolutionary biologists,
ecologists, conservation biologists and agronomists
have attempted to compare the importance of different
pollinator species to various plant species (Primack &
Silander 1975; recent review by Ne’eman et al. 2010).
From an evolutionary point of view, more important
pollinators are likely to be stronger agents of natural
selection on floral traits (Stebbins 1970). From an
ecological point of view, plant–pollinator interactions
are increasingly threatened by habitat loss, climate
change and the introduction of alien species (Rathcke &
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*Corresponding author.
Accepted for publication March 2012.
© 2012 The Authors
Journal compilation © 2012 Ecological Society of Australia
Jules 1993; Allen–Wardell et al. 1998; Debinsky & Holt
2000). For this reason, it is especially timely for conservation biologists to understand the relative roles of
different native pollinators, and particularly so in areas,
such as the New Zealand alpine, that have received
scant attention to date.
Pollination systems in New Zealand have traditionally been characterized as having low rates of selfincompatibility and a lack of specialized pollination, as
well as little dependence on animal pollination (Newstrom & Robertson 2005). Flowers are often small in
size and simple in architecture, with an overall lack of
bright colours (Lloyd 1985). The alpine flora of New
Zealand is particularly unusual, as over 70% of plant
species in that particular New Zealand habitat have
flowers that appear white or near-white to humans,
which is one of the highest percentages of white
flowers in the alpine anywhere in the world (Wardle
1978). A strong trend towards autogamy in this habitat
has been assumed (Raven 1973; Wardle 1978),
although very few studies have actually examined pollination in the New Zealand alpine (Garnock-Jones
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M . B I S C H O F F ET AL.
1976; Primack 1983; Schlessman 1986). Whereas
distinct flower preferences of insect flower visitor in
alpine New Zealand have recently been documented
(Campbell et al. 2010), there is no information on the
pollinator effectiveness of common alpine flower visitors such as solitary bees and syrphid and tachinid
flies.
In this study, we measured pollinator importance
in terms of the contribution to deposition of compatible pollen on the stigma (pollination success sensu
Ne’eman et al. 2010). In accord with common usage,
we examined two multiplicative components of pollinator importance: (i) number of conspecific pollen
grains deposited in a single flower visit (hereafter
single-visit pollinator effectiveness); and (ii) frequency of visits by that particular type of pollinator.
Quantifying single-visit pollinator effectiveness as
well as visitation rate distinguishes pollinators from
mere flower visitors, providing a more reliable assessment of their importance for plant reproductive
success and as potential agents of natural selection
on floral traits.
We investigated the relative importance of syrphid
flies (Allograpta spp., Platycheirus spp. (Diptera: Syrphidae)) and native solitary bees (Hylaeus matamoko
(Hymenoptera: Colletidae)) as pollinators of two
common alpine herbs in New Zealand, O. glandulosa
Hook. f. (Plantaginaceae) and Wahlenbergia albomarginata Hook. (Campanulaceae). We (i) quantified the
relative frequencies of the two insect groups as visitors;
(ii) measured the pollen transferred to stigmas in
single visits to virgin receptive stigmas; and (iii) multiplied these two components together to estimate the
overall relative pollinator importance. To our knowledge, our study presents the first quantitative assessment of the pollinator performance of New Zealand
alpine insects.
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METHODS
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Study system
The study site was at the Rastus Burn Recreation Area within
the Remarkables Range in Otago, New Zealand in an alpine
herbfield community of tussock grasses and a diversity of
small alpine herbs and cushion plants (Mark & Bliss 1970;
Patrick et al. 1992). Experiments were carried out between
1650 m and 1750 m a.s.l. along the trail from the Remarkables Ski Area (45°03′11′′S, 168°48′46′′E) to Lake Alta. Both
O. glandulosa and W. albomarginata were abundant in the
area, with peak flowering occurring in January and late February to early March, respectively.
Ourisia glandulosa (Appendix S1a,b) is an alpine perennial herb found in areas above 1000 m a.s.l. in the mountain ranges of Otago. Each racemose inflorescence produces
one to seven zygomorphic flowers on one to four flowering
doi:10.1111/j.1442-9993.2012.02389.x
nodes (Meudt 2006). Two flowers per node typically open
simultaneously as the inflorescence progresses. The flowers
are strongly protogynous. The stigma in the flowers is typically exerted and receptive while the undehisced anthers
are still folded in the corolla tube. After pollination, the
stigma colour changes from white to purple, and the stigma
usually shrivels before the first pair of anthers unfolds and
dehisces, thus minimizing the potential for autogamy.
Excluding insects by bagging and hand-self pollination both
produced a seed set of less than 1% of that made by handoutcrossed flowers, indicating self-incompatibility (Bischoff
2008).
Wahlenbergia albomarginata (Appendix S1c,d) is a small
creeping rhizomatous perennial herb with a distribution
across the South Island to Stewart Island. This species
occurs in tussock grasslands ranging from lowland to
alpine habitats. Each ramet of W. albomarginata produces a
single protandrous flower. The anthers dehisce in the bud
stage and deposit the pollen onto retractable stylar hairs so
that pollen is presented along the side of the style, which
functions as a secondary pollen presenter (Lloyd & Yates
1982) – an arrangement that is common within the Campanulaceae (Endress 2011). After the pollen has been
removed by insect visitors, the stigmatic lobes expand and
the stigma becomes receptive. Autogamous selfing does
not occur, and flowers in hand-self pollination experiments
make less than 5% of the seeds of flowers that are outcrossed, suggesting the species is also largely selfincompatible (Bischoff 2008).
The New Zealand alpine insect fauna is highly unusual
compared to other alpine areas around the world due to its
lack of social bees, bee flies and hawk moths (Primack
1978). The most common flower visitors in alpine New
Zealand are tachinid and syrphid flies, short-tongued bees
and diurnal moths (Primack 1983). We focused on the roles
of the syrphid fly Allograpta spp. and the native solitary bee
H. matamoko as pollinators, both of which were abundant
flower visitors at our field site throughout most of the flowering season (Bischoff 2008). Flies of the genus Allograpta
are also common flower visitors elsewhere in the New
Zealand alpine (Primack 1983). The New Zealand endemic
bee H. matamoko is known from very few specimens in collections, but appears to be confined to montane and alpine
areas of the mid- to southern South Island (Donovan
2007). At our site, it frequently visited other outcrossing
plant species (including Euphrasia zelandica and Gentianella
corymbifera; Bischoff 2008) besides the focal species studied
here.
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(i) Visitation
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Natural field plants
In 2007 and 2008, we observed natural visitation to patches
of 20 flowers each. Observations were carried out in
30-min blocks of time during the 6 h between 10:00 to
13:00 and 14:00 to 17:00, such that each plant species was
observed at least once during each of the eight periods of
45 min available. Before 10:00 and after 17:00 air temperatures were generally too low for any insect activity. Ourisia
© 2012 The Authors
Journal compilation © 2012 Ecological Society of Australia
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N E W Z E A L A N D P O L L I N ATO R E F F E C T I V E N E S S
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glandulosa was observed for a total of 6 h between 17
January to 5 February 2007 and 16–24 January 2008.
Wahlenbergia albomarginata was observed for a total of 7 h
between 15–22 February 2007 and 18–19 February 2008.
For each patch observed, we recorded the number of
insects of each type that entered the patch and visited at
least one flower (hereafter called a foraging bout). Only
visitors that were actively foraging for rewards on the flower
were counted.
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Arrays
Foraging bouts provide only an indirect estimate of visitation frequency, as different insect types can vary in the
number of flowers they visit per bout. For W. albomarginata,
we also obtained direct observations of visitation frequency,
measured as visits per flower per hour. These measurements
were obtained at experimental arrays of 16 numbered
flowers, observed during weather conditions chosen for
peak insect activity (sunny and temperature above 10°C).
Natural visitation rates to W. albomarginata obtained during
representative times were very low compared to O. glandulosa. Use of these arrays allowed us to increase sample sizes
for W. albomarginata. Arrays were set up near (usually
5–10 m away), but not in, patches of natural flowers, and
were generally placed into mats of cushion plants that provided a relatively uniform green background (Campbell
et al. 2010). Flowers were spaced 10 cm apart in four rows
of four flowers, with each flower in a numbered 1.5 mL
micro-centrifuge tube filled with water. We observed 13 different flower arrays, for 1 h each between 19–21 February
2008 and 17–19 February 2009. All observations were
done between 11:30 and 17:00. For each insect that
entered the array, we recorded the sequence of flowers
visited until the insect left and either visited a flower
outside of the array or disappeared from sight. We recorded
the number of foraging bouts by each type of insect, that is,
the number that visited at least one flower in the array, for
comparison with the natural visitation observations. We also
determined the percentage of individual flower visits made
by each type of insect over the entire experiment. Because
all arrays had the same number of flowers and were
observed for the same length of time, these percentages are
equivalent to relative visitation in terms of visits per flower
per hour. For the 12 arrays with more than 10 flower visits,
we compared the number of visits per flower per hour
made by Allograpta spp. and by H. matamoko (the most
common visitors) using a paired t-test.
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Bags were removed from female phase flowers during
observation. Once a visit was received, the flower was
re-bagged for a minimum of 1 h to allow pollen tubes to
germinate. Thereafter the flower was collected and the
stigma excised with forceps without allowing further contamination from pollen on the pollen presenter in the case
of W. albomarginata. Stigmas were stained in a solution of
methylene green-phloxine B following Dafni et al. (2005)
and then squashed in a drop of glycerine prior to counting
the number of germinating pollen grains under a microscope. Only germinating grains were considered to represent effective transfer of pollen. For O. glandulosa we
obtained pollen counts for 27 single visits by Hylaeus bees
and 16 visits by Allograpta flies. These pollen counts were
compared with those for 12 unvisited control stigmas open
inside bags for 48 h on the same days and at the same site.
Control stigmas would have pollen due to any autogamous
self-pollination in the bag or any artificial pollen transfer
during the collection and transport of the flowers. For
W. albomarginata we obtained 30 single visits by Hylaeus
bees, three visits by Leioproctus bees (not included in statistical analysis because of small sample size), 15 single
visits by Allograpta flies, and 23 control flowers that
received no insect visit during observation, all from flowers
observed simultaneously in the same patches. One W. albomarginata control flower was omitted from the final data
set because it was an extreme outlier, likely reflecting contamination; it had 206 pollen grains compared to a range of
0–24 for the other 22 flowers. Because the residuals were
not normally distributed, pollen loads on stigmas were
compared between H. matamoko and Allograpta spp., and
between each type of insect and controls using nonparametric Wilcoxon two-sample tests, with P-values corrected for multiple comparisons using the sequential
Bonferroni method.
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(iii) Pollinator importance
To compare the overall pollinator importance of solitary
bees and syrphid flies, we multiplied the relative visitation
frequencies by relative single-visit pollinator effectiveness, measured as number of pollen grains deposited.
Visitation was assessed as foraging bouts for both
plant species and also as visits per flower per hour for
W. albomarginata.
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RESULTS
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(i) Visitation
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(ii) Single-visit pollinator effectiveness
To estimate the single-visit pollinator effectiveness of different insect visitors, we examined the amount of conspecific
pollen transferred in a single visit to a flower. Single visits
to O. glandulosa were observed in January 2008, and single
visits to W. albomarginata were observed in March 2010 and
2011.
Flowers were bagged while in the bud phase with fine
mesh jewellery bags to provide a supply of virgin stigmas.
© 2012 The Authors
Journal compilation © 2012 Ecological Society of Australia
The colletid bee H. matamoko was the most common
single visitor to both plant species, accounting for
about 46% of foraging bouts on O. glandulosa and
81% of foraging bouts on W. albomarginata (Table 1).
Syrphid flies (mostly of the genera Allograpta and
Platycheirus) all together were about as common as
H. matamoko on O. glandulosa, but were secondary
visitors on W. albomarginata (Table 1). Both visitor
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M . B I S C H O F F ET AL.
Table 1. Percentages of foraging bouts by different insect types to patches of 20 flowers growing in the field in situ and to arrays
of 16 flowers
Ourisia glandulosa
Wahlenbergia albomarginata
Field plants
Field plants
Arrays
45.6
0.0
30.0
15.3
4.9
4.2
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81.4
0.0
7.0
0.0
7.0
4.7
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81.1 (77.8)
5.8 (12.7)
5.8 (3.6)
0.2 (0.2)
3.4 (2.9)
3.9 (2.9)
623 (1563)
Hylaeus (Colletidae)
Leioproctus (Halictidae)
Allograpta (Syrphidae)
Platycheirus (Syrphidae)
Tachinidae
Other
Total n
Percentages of all flower visits are also given in parentheses for the experimental arrays. Total n represents the number of
foraging bouts with the number of flowers visited in parentheses. The ‘Other’ category included flies in the genera Spilogona and
Odontomyia for Ourisia glandulosa, and Spilogona and Eristalis for Wahlenbergia albomarginata, along with one bout by a butterfly.
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types were foraging for pollen as a reward. For
W. albomarginata, the relative visitation by different
insects was similar whether measured in terms of
foraging bouts or flower visits, with the exception
that Leioproctus bees made relatively long foraging
sequences in the arrays and thus accounted for a
higher percentage of visitation based on flower
visits (Table 1). Visits per flower per hour to
W. albomarginata were much higher for H. matamoko
than for Allograpta spp. (means = 6.3 vs. 0.3, paired
t11 = 5.71, P < 0.0001).
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(ii) Single-visit pollinator effectiveness
In single visits to O. glandulosa,Hylaeus bees transferred
more than 10 times as much germinating pollen to the
stigma as did Allograpta flies (mean ⫾ SE = 19.4 ⫾ 7.4
vs. 1.8 ⫾ 0.9 grains, Wilcoxon two-sample test
P < 0.025; Fig. 1A). By comparison, none of the 12
control flowers had any germinating pollen grains.The
relatively small Hylaeus bees typically crawled inside the
corolla (Appendix S1a) and frequently attempted to
open undehisced anthers, whereas syrphid flies
often landed on the lower lip of the zygomorphic
flowers and probed the entrance of the corolla tube
without fully entering the flower (Appendix S1b).
Both types of insects transferred some heterospecific
pollen (mean = 10.0 vs. 3.9 grains for H. matamoko
vs. Allograpta spp.,Wilcoxon two-sample test P > 0.50).
Paired t-tests detected no difference between the
number of germinating conspecific pollen grains
and the number of heterospecific pollen grains deposited in the same visit, for either type of insect (both
P > 0.05).
In single visits to W. albomarginata, Hylaeus bees
transferred nearly three times as much germinating
pollen to the stigma as did Allograpta flies
(mean ⫾ SE = 113.1 ⫾ 17.5 s vs. 40.5 ⫾ 9.4 grains,
doi:10.1111/j.1442-9993.2012.02389.x
Fig. 1. Box plots showing the relative effectiveness of
Allograpta spp. and Hylaeus matamoko at transferring germinating pollen grains on a per visit basis. Lines show median
and mean germinated grains per stigma, the boxes include
the 25th to 75th percentiles, the error bars show the 10th and
90th percentiles, and the outliers indicate 5th and 95th
percentiles. Numbers indicate the sample sizes.
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Wilcoxon two-sample test, P = 0.004, P < 0.05 after
Bonferroni correction; Fig. 1B). Visiting bees typically
entered the corolla and circled around the pollen presenter multiple times. They were frequently observed
walking over the stigmatic surface (Appendix S1c),
whereas Allograpta flies typically landed on a petal and
probed the stigma with an extended proboscis without
actually entering the flower (Appendix S1d). Both
types of visits resulted in more pollen transfer than for
control flowers not visited by an insect (mean = 12
© 2012 The Authors
Journal compilation © 2012 Ecological Society of Australia
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N E W Z E A L A N D P O L L I N ATO R E F F E C T I V E N E S S
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grains, P < 0.05 for both types of insects). Neither type
of insect transferred much heterospecific pollen
(mean < 1 grain for both H. matamoko and Allograpta
spp., Wilcoxon two-sample test comparing the insect
types, P > 0.50). The mean transfer of germinating
pollen by Leioproctus bees was 80 grains (range = 51–
109).Thus, native solitary bees were the most effective
pollinators of both species, although Allograpta flies
did also transport some germinable pollen.
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(iii) Pollinator importance
For O. glandulosa, 45.6% of foraging bouts were by
bees and 50.2% by syrphid or tachinid flies. Assuming that tachinid flies are equally effective as syrphid
flies and weighting these values by effectiveness in
single visits (19.4 vs. 1.8), we estimated that the flies
had a pollinator performance only about 10% as high
as that of the native bee H. matamoko, even though
flies were equally common visitors. Accounting for
variation in single-visit effectiveness represented by
one SE in either direction, flies performed 4–25% as
much pollination as the native bee. For W. albomarginata, 86.9% of foraging bouts were by bees and
11.6% by syrphid or tachinid flies. Weighting these
values by pollen deposition effectiveness (113.1 vs.
40.5), we estimated that the flies performed only
about 5% (3–7% accounting for one SE in effectiveness) as much pollination as the native bees. Calculations based on percentages of flower visits, rather
than foraging bouts (in parentheses in Table 1), gave
an even more extreme result, with flies estimated to
perform only about 3% of the pollination native bees
carry out. The even higher contribution by bees
reflects the relatively long foraging sequences made
by Leioproctus.
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DISCUSSION
Although small short-tongued solitary bees such as
H. matamoko and other members of the Colletidae
and Halictidae are often overlooked as pollinators
(Donovan 2007), H. matamoko can be considered the
primary pollinator of both O. glandulosa and W. albomarginata populations at our field site. Hylaeus
matamoko, an alpine colletid endemic to the South
Island of New Zealand (Donovan 2007), performed
more than 90% of the pollen delivery to receptive
stigmas in both alpine herbs after consideration of
the visitation frequencies and single-visit pollinator
effectiveness. This bee accounted for similarly high
percentages of all visits to W. albomarginata, regardless of whether observations were made during
unusually warm weather at the flower arrays or
during more representative times (Table 1), indicat© 2012 The Authors
Journal compilation © 2012 Ecological Society of Australia
5
ing that the result is robust across a variety of
weather conditions for that plant species. In the
case of O. glandulosa, syrphid flies visited at equal
frequencies as Hylaeus bees, yet transferred only
about 10% of the pollen that H. matamoko deposited.
This result contrasts with previous findings suggesting that pollinator performance is determined
primarily by visitation frequency rather than
pollen deposition effectiveness (Vazquez et al. 2005;
Sahli & Conner 2006, 2007) and indicates the need
for caution when employing visit frequencies as a
proxy for pollinator performance (Ne’eman et al.
2010).
For the purpose of assessing pollinator performance we used single-visit pollen deposition to virgin
stigmas as a measure of pollinator effectiveness rather
than seed set. Post-pollination processes can reduce
fruit or seed set on flowers adequately pollinated with
viable pollen (Cane & Schiffhauer 2001), and the
developing fruit may abort if limited by maternal
resources (e.g. Stephenson 1981; Corbet 1998) or
be lost by stochastic events post-pollination, thus
masking effective pollination. When measuring
single-visit pollen deposition, it cannot be entirely
ruled out that the relative contributions of solitary
bees and flies to seed set would differ if these insects
also varied in the quality of the pollen delivered
beyond that revealed by germination of the pollen.
It seems highly unlikely, however, that any increased
quality of conspecific pollen carried by syrphid
flies could overcome their 10-fold disadvantage in
number of grains delivered compared to solitary
bees.
In theory, contributions to seed set could also be
altered by deposition of heterospecific pollen that
clogs the stigma or interferes with pollen tube growth
by conspecific pollen grains (Shore & Barrett 1984;
Brown & Mitchell 2001; review by Morales &
Traveset 2008). Both the solitary bees and syrphid
flies transferred some heterospecific pollen in addition to conspecific pollen. Heterospecific pollen
transfer did not, however, depend on visitor type, so
the relative pollinator importance for these two types
of insects is unaffected by this process. Whereas
stigma contamination by heterospecific pollen
was generally low in W. albomarginata, O. glandulosa
received amounts approximately equal to the number
of germinating conspecific pollen grains. The difference in stigma contamination between our study
species likely reflects the phenology of co-flowering
species in the alpine plant community. Ourisia
glandulosa blooms at the height of summer with at
least 11 plant species in full bloom at its peak bloom
time, and most insects that visit O. glandulosa also
visit many of these other species (Bischoff 2008). In
contrast, W. albomarginata flowers at the tail end of
the season with five co-flowering species (Dobbie
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M . B I S C H O F F ET AL.
2009). To evaluate fully the relative contributions of
the different insects as selective agents on floral
traits, it would ultimately be desirable also to
compare their success in contributing to seed
set and to number of seeds sired (male function).
The pollen deposition results reported here,
however, provide the most direct first step towards
understanding their ecological contributions to
pollination.
Measuring pollinator performance by multiplying
visitation rate by single-visit pollen deposition
assumes that stigmatic pollen load increases linearly
with successive visits of the same pollinator to the
same flower. Empirical relationships vary from
approximately linear (Galen & Stanton 1989) to a
saturating relationship (Campbell et al. 1994).
Although such non-linear relationships can alter the
absolute performance of a particular insect as a pollinator, they would only alter the relative performance of two species if the two species differed
markedly in the shape of this relationship. Pollinator
effectiveness can also be influenced by insect preferences for male phase or female phase flowers, as
has been reported for some solitary bees in other
systems (Lau & Galloway 2004; Davila & Wardle
2007), as an insect that forages at only one sexual
phase or rarely flies between them would be a poor
pollinator. We observed insects visiting flowers in
both sexual phases at O. glandulosa and W. albomarginata. Although we did not record sexual phase of
the flowers in the arrays, in a study of flower colour
in W. albomarginata we observed visitation at arrays
with a central core of 16 male-phase flowers (both
blue and white) surrounded by 48 female-phase
flowers of one of these colours (Campbell et al.
2012). When only male-phase flowers of the matching colour were included, H. matamoko visited
the male-phase flowers and female-phase flowers
in the array at similar rates (n = 10 arrays,
mean ⫾ SE = 0.13 ⫾ 0.067 vs. 0.12 ⫾ 0.056 visits
per flower per hour), and so did Allograpta spp.
(0.02 ⫾ 0.007 vs. 0.03 ⫾ 0.009 visits per flower per
hour). Furthermore, for foraging bouts of at least
four flowers, bees visited both sexual phases in 78%
of foraging bouts, and flies visited both sexual phases
in 58% of foraging bouts. These data suggest that
relative effectiveness for the two types of insects
would not be markedly affected by preference for a
sexual phase in the case of W. albomarginata. For
O. glandulosa, insects were often observed visiting
flowers in both sexual phases, but we cannot test
directly for preference.
Given these caveats, the very high pollen deposition effectiveness of the Hylaeus bees could help to
explain the maintenance of white flowers in O. glandulosa. In arrays of this plant species with equal
numbers of flowers with petals painted yellow versus
doi:10.1111/j.1442-9993.2012.02389.x
white, the yellow-painted flowers actually received
more overall visits by insects (Campbell et al. 2010).
Hylaeus matamoko, however, preferred flowers
painted white, while the more numerous syrphid flies
preferred flowers painted yellow (Campbell et al.
2010). The white-painted flowers received 0.32 and
0.49 visits per flower per hour by H. matamoko and
syrphid flies, respectively, while yellow-painted
flowers received 0.10 and 1.04 visits per flower per
hour by those same insect types. If we weight those
visit frequencies by the pollinator effectiveness measured in this study (113 vs. 40 pollen grains per visit
for H. matamoko vs. syrphid flies), we predict slightly
higher pollen deposition on the O. glandulosa flowers
painted white to resemble their natural colour
(36.1 + 19.6 = 55.7 pollen grains on a white flower
vs. 11.3 + 41.6 = 52.9 pollen grains on a yellow
flower). For O. glandulosa the higher single-visit
pollinator effectiveness of H. matamoko can tip
the balance towards higher pollination success
for white flowers. On W. albomarginata, however,
H. matamoko visits blue-painted flowers at least as
often as white ones, and so its high pollinator effectiveness does not explain the maintenance of white
petals in that species (Campbell et al. 2012).
Whereas our findings represent the first measure of
pollinator performance in alpine New Zealand, there
is other evidence that short-tongued bees and flies
may often be effective pollinators in New Zealand. At
least one other species of Hylaeus (Hylaeus agilis) is
an effective pollinator of some Peraxilla mistletoes in
New Zealand (Robertson et al. 2005). Solitary bees
of the genus Leioproctus and syrphid flies of the genus
Eristalis have been shown to pollinate Brassica rapa
with the same effectiveness as the introduced honey
bee Apis mellifera in an agricultural setting in lowland
New Zealand (Rader et al. 2009). Pollinator performances of flies and solitary bees have also been
compared outside New Zealand, with some other
cases indicating higher effectiveness for solitary bees
(Larsson 2005), but at least one finding bombyliid
flies to be just as effective (Motten et al. 1981). Such
comparisons have rarely been made however, in
arctic or alpine habitats, where fly pollination is frequently assumed to be important (Larsen et al. 2001;
Körner 2003).
In their review of pollination systems in New
Zealand, Newstrom and Robertson (2005) predicted
that most pollination system in New Zealand corresponded to the ‘small bee syndrome’. Our results
support the importance of small bee pollination for
two plant species from an alpine habitat where little
pollinator dependence was traditionally assumed.
Future studies of pollinator performance focusing on
under-studied pollinator taxa such as short-tongued
bees and most orders of Diptera are needed to evaluate
their contributions to plant reproductive success and
© 2012 The Authors
Journal compilation © 2012 Ecological Society of Australia
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N E W Z E A L A N D P O L L I N ATO R E F F E C T I V E N E S S
evolution of floral traits. Because the majority of alpine
plant species in New Zealand depend on insect pollinators for successful reproduction (Bischoff 2008),
this flora is vulnerable to declines in pollinator
services. Although none of the species in this study are
critically endangered, the bee H. matamoko is considered rare (Donovan 2007). Efforts to protect the New
Zealand alpine can only benefit from future research
on plant–pollinator interactions in this understudied
habitat.
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4
ACKNOWLEDGEMENTS
This research was funded in part by grant 8621-09
from the Committee for Research and Exploration
of the National Geographic Society and contract
CO9X0503 from the New Zealand Public Good
Science Fund as well as a PhD scholarship by the
German Academic Exchange Servive (DAAD) to MB.
Mary Anne Miller and Vickey Tomlinson assisted with
arrangements for supplies. Judith Trunschke helped
with laboratory work. Ian Andrew and John Dugdale
kindly identified insect specimen. NZ Ski Ltd. provided space for housing and laboratory work at the
field site.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in
the online version of this article:
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Appendix S1. Hylaeus matamoko and Platycheirus
spp. on Ourisia glandulosa and H. matamoko and
Allograpta spp. on Wahlenbergia albomarginata.
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© 2012 The Authors
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