Functional
Ecology 2004
18, 125 –129
Variation in rate of nectar production depends on floral
display size: a pollinator manipulation hypothesis
Blackwell Publishing, Ltd.
J. M. BIERNASKIE†‡ and R. V. CARTAR
Department of Biological Sciences, University of Lethbridge, AB, Canada T1K 3M4
Summary
1. Pollinators typically visit more flowers on plants with larger floral displays, which
should present such attractive plants with significant pollen transport losses.
2. Many-flowered plants with hermaphrodite flowers might reduce the costs of attractiveness by encouraging fewer sequential flower visits by pollinators. One mechanism
that accomplishes this is to produce variable nectar rewards, which will cause risk-averse
foragers to leave the plant after visiting fewer flowers.
3. We test the prediction that within-plant variability in nectar production rate increases
with the relative number of open flowers on a plant. A field survey of nine herbaceous
angiosperm species native to Alberta, Canada revealed a significant positive correlation between nectar variability (measured as standard deviation) and the size of the floral
display within species. This relationship existed over and above the null expectation of
a positive correlation between mean and SD.
4. Our results suggest that multiflowered plants might maximize the male fitness
returns associated with a plant’s attraction status (determined by relative display size),
by taking advantage of risk-averse foraging by their pollinators.
Key-words: conditional strategy, geitonogamy, inflorescence size, pollen discounting, risk-sensitive foraging
Functional Ecology (2004) 18, 125 –129
Introduction
Common sense suggests that highly attractive flowering plants should gain an outcrossing advantage; however, one should also expect subtle costs to accompany
pollinator attraction (Klinkhamer, de Jong & Metz
1994; Harder & Barrett 1995). Here we focus on the
costs of attraction to the male fitness (pollen export)
of a multiflowered, hermaphrodite plant, which may
occur when pollinators visit many flowers sequentially
during each approach. Lengthy visitation sequences
will limit the male function of inflorescences, because
the fraction of removed pollen that is available for
export decreases as the number of flowers visited
increases (Klinkhamer & de Jong 1993; Klinkhamer
et al. 1994). This results because pollen may be lost to
other stigmas within the plant (pollen discounting;
Harder et al. 2001); to pollinator grooming (Harder
1990); or to other floral organs within the plant (e.g.
petals, Rademaker, de Jong & Klinkhamer 1997) at
or between each sequential flower visit. Furthermore,
when individual pollinators remove an increasing total
© 2004 British
Ecological Society
†Author to whom correspondence should be addressed.
E-mail: [email protected]
‡Current address: Behavioural Ecology Research Group,
Department of Biological Sciences, Simon Fraser University,
Burnaby, BC, Canada V5A 1S6
amount of pollen from a plant, there may be diminishing returns to realized paternity because of increased
grooming, layering of pollen on the vector’s body, and/
or local mate competition once pollen is deposited
(Harder et al. 2001).
The ideal situation for plants would be when numerous pollinators approach the display, each removing
only small amounts of pollen (Harder & Thomson
1989; Iwasa, de Jong & Klinkhamer 1995). This poses
a ‘dilemma’ for multiflowered plants, as those traits
that increase the pollinator approach rate also tend
to promote lengthy visitation sequences (Klinkhamer
& de Jong 1993). The relative floral display size (daily
number of open flowers) within a population is one
such trait: large floral displays tend to attract frequent
approaches, but also promote many flower visits
within an inflorescence (reviewed by Ohashi & Yahara
2001). Thus plants with the largest floral displays
should also experience the highest pollen-export
costs. Large displays can maximize the benefits of
their attractiveness (maximal pollen export) when
visitation sequences are short, whereas smaller displays maximize pollen export (and partly compensate
for their inevitable disadvantage) when a larger fraction of available flowers are visited (Klinkhamer et al.
1994). The optimal fraction of flowers visited per
approach therefore decreases with the total number of
open flowers available (Iwasa et al. 1995), and this
125
126
J. M. Biernaskie &
R. V. Cartar
relationship is often observed in nature (Ohashi &
Yahara 2001).
Multiflowered plants might mediate the length of
visitation sequences by manipulating the distribution
of nectar within inflorescences (Waser 1983), and one
way of doing so is by altering the nectar production
rates (NPRs) of individual flowers. Although nectar
foragers will tend to reduce the mean and variability of
available nectar volumes, a plant with variable regeneration rates will present a more variable reward distribution to its next visitor than will a plant with constant
regeneration (see also Sakai 1993). We have demonstrated that pollinator patch departure depends on
random variation in nectar rewards: hummingbirds
and bumble bees made fewer sequential flower visits
on high variance inflorescences relative to low variance
inflorescences offering equal (mean) energy returns
(Biernaskie, Cartar & Hurly 2002). We interpreted this
behaviour as aversion to the risk of energy shortfall
(Stephens 1981). Presuming risk-averse departure
behaviour, simple optimization models of nectar allocation (Rathcke 1992) have predicted that plant reproductive success will be maximized at an intermediate
level of within-plant variance in nectar reward, since at
intermediate levels, pollinators should visit fewer flowers
and transfer less self-pollen within the plant, but should
not avoid visitation altogether.
Given the reasoning above, we propose that the optimal level of within-plant variance in NPR should be
conditional on the relative size of the floral display.
Consider the situation in which intraspecific variation
in display size is determined mainly by diffferences in
resource acquisition. An individual’s resource state,
relative to others, will determine its attractiveness and
potential fitness (relative state determines ‘status’;
Gross 1996). We expect plants to respond to their
current status with the nectar distribution tactic that
attains highest possible fitness. If many-flowered plants
can exploit the seemingly risk-averse departure behaviour of their pollinators, then individuals with more
open flowers should vary the nectar production rate
among their flowers more than less showy conspecifics
in the same population. To test the size-dependence
prediction, we observed the nectar production rates
of nine hermaphroditic-flowered species that varied
intraspecifically in floral display size.
Materials and methods
   
© 2004 British
Ecological Society,
Functional Ecology,
18, 125–129
Field work was conducted from May–July 2001 in southwest Alberta, Canada. Sites were located near the University of Lethbridge (UL, 49°4′ N, 112°5′ W); 50 km
west of Fort Macleod (HSI, ≈49°4′ N, 113°3′ W); at
Barrier Lake (BL, 51°0′ N, 115°0′ W); and at the Sheep
River Wildlife Sanctuary (SR, ≈50°4′ N, 114°1′ W).
Nine plant species were surveyed (listed with summary
statistics in Table 1; see Moss 1983 for authorities),
Table 1. Plant species included in the survey, with associated
summary statistics and observed effect size
Species
Study
site
Number
of plants
(days)*
Effect
size†
Delphinium bicolor
Hedysarum boreale
Monarda fistulosa
Oxytropis sericea
Oxytropis splendens
Penstemon nitidus
Penstemon procerus
Thermopsis rhombifolia
Vicia americana
HSI
BL
SR
UL, BL
SR
UL
SR
UL
BL
39 (2)
70 (3)
70 (3)
68 (3)
69 (3)
35 (2)
67 (3)
12 (1)
66 (3)
0·191
0·008
0·120
0·045
0·084
0·011
0·083
0·240
0·188
Mean = 0·094
2 SE = 0·046
*Sample size, plants selected for nectar observations
measured over n days.
†Effect size measures strength of relationship between
display size and within-plant SD in nectar production within
each species; see text for details of this calculation. Estimated
mean effect size is weighted by n plants.
each of which simultaneously display many open flowers
that are frequently visited by nectar-collecting bumble
bees (Bombus spp.).
  
For each species, a sample of 40 plants was first haphazardly selected from throughout the site, and the
number of open flowers on each plant recorded. We
then defined three display size classes based on the
distribution of this sample: small (≤25th percentile);
medium (within one or two flowers of the median
value); and large (≥75th percentile).
To estimate the nectar production rate of flowers,
inflorescences were enclosed in mesh bags (made of bridal
veil) in the evening (≈18.00 h) until nectar rewards were
measured the following day. Each evening we enclosed
10 plants from each display size class for measurement
the next day. Plants were haphazardly selected (independently of the initial sample) from throughout the
site, where size classes grew intermingled. We measured a maximum of 10 flowers per plant; to reach this
limit it was sometimes necessary to bag more than one
inflorescence on multistalked plants. We avoided selecting plants whose small size reflected an early developmental stage (e.g. a plant with many flower buds but
few open flowers), and also selected individuals that
could be clearly identified as a single genet.
The following day (≈09.00 to ≈17.00 h), bagged
inflorescences were picked sequentially and floral
nectar harvested destructively. When the number of open
flowers on a plant exceeded 10, flowers were selected
equally from all inflorescence positions (top, middle,
bottom) and equally from multiple inflorescences, if
necessary. We collected nectar with 2 µl microcapillary
127
Nectar distribution
depends on display
size
Fig. 1. Positive relationship between number (n) of open flowers per plant and within-plant variability in nectar production
(regression line and 95% confidence intervals). Data in the leverage plot are adjusted for all other effects in the  model
(see text). Symbols: +, Delphinium bicolor; ×, Hedysarum boreale; , Monarda fistulosa; Z, Oxytropis sericea; Y, Oxytropis
splendens; , Penstemon nitidus; , Penstemon procerus; , Thermopsis rhombifolia; , Vicia americana.
tubes, and the sugar concentration (mg solute per ml
solution) of each sample was measured with a handheld refractometer (ATAGO, Japan). Each evening, at
the time of inflorescence bagging, we also sampled the
nectar standing crop in six haphazardly chosen inflorescences from the same population (two from each size
class); the nectar standing crop was otherwise measured in the same manner as bagged plants. The same
observer harvested all nectar.
We recorded the time of day when each plant was
picked and the total number of open flowers on the plant
(which may have included multiple inflorescences).

© 2004 British
Ecological Society,
Functional Ecology,
18, 125–129
For each flower measured, we combined nectar volume
and concentration into a measure of available energy
in Joules (J). Each value was then adjusted for time
of day, to a common time of 12.00 h (using the linear
regression equation of J per flower and time for that
species on that day). This correction was necessary
because nectar often accumulates in the flower as the
day progresses.
The intraspecific relationship between display size
(main factor) and within-plant variability (SD, response variable) was analysed in a single general linear
model, while controlling for differences in SD among
the nine species by including ‘species’ as a random
factor. We also included the variable ‘mean NPR
per flower per plant’ in the model as a covariate to
account for an expected positive correlation between
mean nectar production and within-plant variability
(Real & Rathcke 1988). We chose to control for this
potential confound as a covariate rather than by using
a measure of relative variability (the coefficient of variation) in order to avoid the complications of inferring
population parameters for a ratio variable (Lewontin
1966). Interaction terms were not included in our final
 model, as none was significant. We present our
results in a leverage plot (JMP, SAS Institute Inc.,
USA) that accounts statistically for the variance due to
all other effects specified in the model. Where necessary, variables were log-transformed to normalize the
distribution of residuals of the model fit.
In Table 1 we report the strength of the relationship
between display size and within-plant SD as the effect
size for each species. Effect size is the mean daily standardized regression coefficient (herein src) for ‘display
size’ in the model: ‘SD (NPR) = display size + mean
NPR per flower per plant’. The estimated mean effect
size, weighted by the sample size of each species (n
plants), measures the strength of the overall intraspecific relationship between display size and within-plant
SD in nectar production.
Results
We predicted a positive relationship between size of
the floral display (number of open flowers) and variability (SD) in NPR within plants of the same species.
After accounting for significant differences between
species (F8,472 = 22·08, P < 0·0001) and for a strong
128
J. M. Biernaskie &
R. V. Cartar
positive, linear correlation between the mean nectar
production per flower per plant and within-plant SD
in nectar production (F1,472 = 433·96, P < 0·0001), there
was indeed a positive association between the display
size and within-plant SD (src = 0·072; 2 SE = 0·04;
F1,472 = 12·83, P = 0·0004; Fig. 1). Thus the relationship in Fig. 1 exists over and above the null expectation
of a positive correlation between mean and SD. In the
unreported, more saturated models there was no interaction of species and floral display size (F8,454 = 1·48,
P = 0·16), species and mean nectar production per
flower per plant (F8,454 = 1·65, P = 0·11), and also no
three-way interaction (F8,454 = 0·88, P = 0·53). The lack
of interactions means that the species and mean nectar
production are appropriately controlled in the statistical
relationship of interest (Fig. 1).
Similarly, the distribution of the nine species’ effect
sizes in Table 1 had an estimated mean that was greater
than zero (t8 = 3·99, P = 0·004).
We considered whether the correlation between variability and display size is an artefact of our methods
rather than a trait of the plants. Large inflorescences
may have had more variable nectar standing crops at
the time of inflorescence bagging, which was simply
amplified over time and reflected in our estimate of
the NPR. To test this potential confound, we checked
for a correlation between the effect size measured in
bagged plants on each day, and the effect size measured in the nectar standing crop the previous night. No
correlation was detected (r = 0·088, P = 0·69, n = 23
days), hence NPR patterns do not appear to be directly
related to the previous night’s remaining crop.
At the among-species level, no correlation between
mean floral display size and mean SD per plant per
species could be detected (after controlling for mean
NPR per flower per plant per species; F1,6 = 0·25, P =
0·63). With only nine observations, however, we had
little power to detect such an effect, and did not pursue
a proper comparative approach to test this interspecific hypothesis.
Discussion
© 2004 British
Ecological Society,
Functional Ecology,
18, 125–129
As predicted, we found a positive association between
an individual’s relative floral display size and withinplant variability in nectar production that was consistent among all nine species observed (i.e. no species by
inflorescence size interaction). If pollinators in nature
use the variance-averse departure rules demonstrated
in bumble bees and hummingbirds by Biernaskie et al.
(2002), then our results suggest that the adjustment of
nectar variability may be an adaptive plant strategy
used to manipulate the length of pollinator visitation
sequences. This follows theoretical results that demonstrate maximized pollen export when the fraction of
flowers visited per approach decreases with the total
number of open flowers displayed (Iwasa et al. 1995).
We propose that plants may use an environmental
indication of their current attraction status in the popu-
lation (e.g. resource state) to express the nectar distribution tactic that gives highest attainable fitness under
the circumstance. Thus, in addition to morphological
adaptations including heterostyly, dichogamy (Harder
& Barrett 1995), herkogamy, and dioecy (de Jong,
Waser & Klinkhamer 1993; Klinkhamer & de Jong
1993), a highly variable distribution of floral NPRs
may be a mechanism to limit the costs of pollen discounting while maintaining the relative attractiveness
of the inflorescence. This assumes that variance in nectar
distributions does not significantly reduce pollinators’
approach rate to a plant. The rate at which pollinators learn the identity (and location) of plants with
variable nectar rewards, and their possible subsequent
avoidance, demands further attention.
We are careful to recognize that not all variability in
nectar rewards experienced by pollinators is unpredictable; hence not all variability should be considered as
a ‘risk’ for variance-sensitive foragers. Vertical inflorescences are often structured so that the youngest
flowers open at the top of the inflorescence; if NPRs
increase with flower age, then a vertical nectar gradient
is produced, decreasing from bottom to top (e.g. Pyke
1978). Large floral displays of this type may certainly
have a wider range of flower ages, and hence greater
variability in floral NPRs. Nevertheless, our main conclusion holds when considering only those species with
non-structured inflorescence development [excluding
Delphinium bicolor, Hedysarum boreale, Oxytropis sericea,
Oxytropis splendens and Thermopsis rhombifolia:
estimated mean effect size (weighted by n plants) =
0·11 (2 SE = 0·068); see Table 1].
Two additional points are relevant. First, although
our measure of within-plant variability in NPR may, in
some cases, reflect the strength of a vertical nectar gradient, organized variability might manipulate pollinator
departure in the same manner as we expect from
random variation (risk). Pollinators should leave a
nectar gradient as the energy gain decreases to some
threshold rate (as ‘patch depression’ increases; Ohashi
& Yahara 2001). It would be interesting to know if
plants can manipulate patch depression, depending
on relative display size, to mediate the length of visitation sequences. Second, the fact that flowers may vary
nectar production with age does not necessarily confound the relationship in Fig. 1. The maintenance of
age-specific nectar production at the flower level may
simply be a useful proximate mechanism to produce
high levels of NPR variability, whether spatially organized or not, in the largest floral displays.
It is possible that another third variable correlates
with both display size and nectar variability. Harder
et al. (2001) suggested that plants might maintain a
fraction of flowers that produce little or no nectar, so
that pollinators leave the plant early after probing a
seemingly revisited flower. This implies that pollinators
do not respond to variance per se, but to near-empty
flowers; the optimized tactic for plants with large floral
displays may therefore be to maintain a greater fraction
129
Nectar distribution
depends on display
size
of non-secreting flowers. If the hypothesis is true,
then it might be expected that the positive relationship
between display size and within-plant variability in
NPR (Fig. 1) would fail after excluding all plants with
near-empty flowers. We repeated the analysis described
in the Results section (after checking for non-significant
random effect by covariate interaction terms) with all
plants having at least one flower that produced <0·125 µl
excluded from the analysis. (This value just exceeds the
minimal volume of nectar that could be detected by our
extraction methods.) The positive relationship between
display size and within-plant variability in NPR was
maintained (F1,167 = 7·95, P = 0·0054). Hence our conclusions are not attributable to non-secreting or nearempty flowers.
What are the consequences of the observed correlation between mean and variability in nectar rewards
within plants? This positive association is consistent
with other studies of within-plant patterns in nectar
production (Real & Rathcke 1988). If these traits are
causally linked (although they may not be), then the
mean amount of nectar produced within a plant
should present a significant constraint on selection for
a specific level of within-plant variability in nectar production. The optimal level of nectar variability would
then be a trade-off between the costs of producing
more nectar and the combined effects (potential costs
and benefits) of a given combination of mean and
variability on the probability of pollinator visitation
and the number of flowers visited on each approach. We
require additional knowledge of how animals tradeoff the mean and variability in food resources (but cf.
Shafir 2000).
The positive association between variability in
nectar production and a plant’s display size, demonstrated here, is consistent with the expectation of a conditional strategy to maximize the male fitness returns
associated with a plant’s current attraction status in the
population (determined by relative display size). Further
investigation is necessary to elucidate the details of the
relationship between nectar production and pollen discounting. Nevertheless, our conclusions here are based
on the simplified but unequivocal supposition that
pollen losses increase with the length of the visitation
sequence. We hope that this study provokes additional
interest in risk-sensitive foraging, and in the mechanisms which plant phenotypes, especially those that
alter attractiveness during a foraging sequence, are
designed to manipulate the visitation behaviour of
animal pollinators.
Acknowledgements
© 2004 British
Ecological Society,
Functional Ecology,
18, 125–129
We thank E. Elle, A. Parachnowitsch, R. D. Sargent
and M. Schuetz for helpful comments on the manuscript, B. J. Crespi for discussions, and I. Bercovitz for
statistical advice. Research was funded by NSERC of
Canada with a research grant to R.V.C. and an Undergraduate Student Research Award to J.M.B. We thank
the University of Calgary’s Kananaskis Field Stations
for accommodation at the R. B. Miller Field Station.
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Received 16 April 2003; revised 28 September 2003; accepted
8 October 2003